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Mollusca: Gastropoda

Chapter · December 2015

DOI: 10.1093/acprof:oso/9780199682201.003.0020

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2 0 M O l lU S c A : G A S t RO P O d A
Elena E. Voronezhskaya and Roger P. Croll
IntROdUctIOn
Snails and slugs crawl through the grass and between the lowers of
backyard gardens in temperate regions around the globe, but are
also commonly encountered when snorkelling over coral reefs in the
tropics. In fact, gastropods have evolved to inhabit a wide variety of
marine, freshwater, and terrestrial habitats distributed between the
two poles and ranging from alpine meadows down to the depths
of the oceans. Finally, in addition to these numerous ecological
niches, where one inds gastropods as free-living organisms, some
species have evolved into parasitic life forms. Along with this tre-
mendous range in the forms and lifestyles of gastropods, they also
vary greatly in adult size from as small as 2–3 mm up to nearly 50
cm for some species of marine snails and slugs. In accordance with
the extraordinary diversity of the Gastropoda, this class is second
in number only to the insects in the entire Animal Kingdom, with
60,000 to 80,000 living species. Estimates refer to 30,000 species of
marine gastropods, 5000 species of fresh and brackish water gastro-
pods, and 24,000 species of terrestrial gastropods. here are 611
families of gastropods, of which 202 families are extinct and appear
only in the fossil record, which goes back to the late cambrian
(Haszprunar 1988, Mc Arthur and tunniclife 1998, Barker 2001,
Brusca and Brusca 2003, Klussmann-Kolb et  al.  2008, Strong
et al. 2008, Appeltans et al. 2010).
he anatomy, behaviour, feeding and reproductive adapta-
tions of gastropods vary signiicantly from one clade or group
to another and it is diicult to state many generalities that are
applicable to all gastropods. In this chapter, we will focus on
major speciications and features of the adult and larval nervous
system which transcend the diversity of gastropods.
GEnERAl MORPHOlOGy
Figure  20.1 shows some of the various body forms of gastro-
pods and details of their anatomy. Most adult gastropods are
bilaterally asymmetrical organisms with common features:
Structure and Evolution of Invertebrate Nervous Systems Edited by Andreas Schmidt-Rhaesa, Stefen Harzsch,
and Günter Purschke © Oxford University Press 2016. Published 2016 by Oxford University Press.
196
(1) a well-developed head, bearing eyes and a variable number
of tentacles; (2) a prominent muscular foot with a ventral sur-
face that forms a lat, creeping sole; (3) a radula (rasp tongue)
used for the procurement of food; (4) an anteriorly and laterally
displaced anus; and (5) a single, often spiral shell with a mantle
lining its last whorl. he shell generally provides protection to
the posterior end of the animal and several internal organs that
are assembled in the dorsal visceral hump. Many aquatic snails
(and a few terrestrial species) carry a hard operculum attached to
the dorsal, posterior surface of the foot that closes the aperture
when the snail withdraws into the shell.
While the preceding description paints a picture of a typical
gastropod, many representatives of this taxon have body plans
that difer signiicantly. For example, adult marine and terres-
trial slugs either have no shell at all or only a greatly reduced and
internalized vestige of this structure. As another example, the
foot of pteropod molluscs has evolved into a wing-like structure,
used not for crawling but rather for swimming within the water
column. Additional general descriptions of the structure of dif-
ferent visceral organs, shell, digestive, and reproduction systems
as well as physiological, behavioural, and evolutionary aspects
of gastropod biology can be found elsewhere (Hyman 1967,
Beklemishev 1969, Haszprunar, 1988, Ruppert et al. 2004).
PHylOGEny
Over the last century, the taxonomy of the Gastropoda has
been repeatedly revised and depicted in various formats. he
taxonomy which can be found in most of the classical sources
was largely based on morphological characters, such as shell
features, and internal anatomy, including the gill and heart
positions, structure of the radula, and details of the reproduct-
ive system (Hyman 1967, Beklemishev 1969). his classiica-
tion includes three major subclasses: Prosobranchia (with gills
in front of the heart), Opisthobranchia (with gills to the right
and behind the heart), and Pulmonata (with a lung instead of

Fig.  20.1. Gastropods with diferent body forms. A: A typical terrestrial
gastropod, Helix, is an asymmetrical animal with a single spiral shell, promi-
nent muscular foot, and a well-developed head bearing tentacles (and eyes at
the tips of the larger posterior set of tentacles). B: like most gastropods, the
freshwater snail, Lymnaea, uses a radula (rasp tongue) to procure its food. C:
he foot of pteropod mollusc Clione has evolved into a wing-like structure,
used for swimming within a water column. D: Sea slugs, like Aplysia, have
gills). his taxonomy was used widely in the historical literature
on the nervous system, but subsequent research has shown that
these traditional subclasses are not monophyletic. More mod-
ern taxonomies of gastropods are based on molecular charac-
teristics (i.e. dnA and RnA sequences) and use clades as taxa.
One widely accepted, modern classiication is a hybrid of trad-
itional linnaean taxonomy and molecular phylogeny (Bouchet
et  al.  2005). A more recent re-evaluation of gastropod phylo-
genetic relationships using genome and transcriptome data
(Zapata et al. 2014) strongly supports monophyly of gastropods
and divides the group into ive main clades: Patellogastropoda,
vetigastropoda, neritimorpha, caenogastropoda, and
Heterobranchia. Heterobranchia comprises the most diverse and
ecologically widespread gastropod clades (Haszprunar 1985),
and a consensus of relationships among heterobranch groups is
emerging (Waegele et al. 2014) suggesting that this clade is sub-
divided into the nudipleura and tectibranchia. he tectipleura
are then in turn subdivided into the Euopisthobranchia and the
Panpulmonata (Jorger et al. 2010, Kocot et al. 2013) (Fig. 20.2).
M O l l U S c A : G A S t RO P O d A
no shell or only a greatly reduced and internalized vestige of this structure.
E: Another aquatic snail, Viviparus, carries a hard operculum on the dorsal,
posterior surface of the foot to close the aperture when the snail withdraws
into the shell. F: Another sea slug, Risbecia, illustrates the bright colouration
often found in these animals. Photographs of Helix, Lymnaea, and Viviparus
were provided by leonid nezlin; Aplysia by Pavel Erokhov; Clione and
Risbecia by Alexander Semenov.
HIStORIcAl InvEStIGAtIOnS
OF tHE nERvOUS SyStEM
Gastropod nervous systems have been the subject of compara-
tive anatomical and physiological investigations for more than
a century and results of numerous early experimental works
were summarized in classical volumes (Bouvier 1887, Bütschli
1912, Bullock and Horridge 1965, Hyman 1967, Beklemishev
1969). Work at the end of the nineteenth and beginning of the
twentieth centuries largely examined the gross anatomy of the
nervous system, especially regarding evolutionary trends toward
centralization and cephalization, as related to torsion—a unique
ontogenic process in gastropods. Spengel (1881, according to
Hyman (Hyman 1967) was the irst to realize that peculiarities
in the organization of the gastropod body plan (and particularly
their nervous systems) are the consequence of torsion, which is
a 180° rotation (generally counter-clockwise from a dorsal view)
of the visceral mass with relation to the head and foot. hus, the
digestive tract twists as the anus migrates to a position above and
197
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
Fig. 20.2. Phylogenetic relationships of various clades of Gastropoda and their position among Mollusca. Modiied from (Zapata et al., 2014).
generally slightly to the side of the head. Also, as a result of tor-
sion, the pallial organs which were originally on the left side are
brought to the right, where they tend to become reduced in size
and may fail to develop altogether. hese developmental changes
in the larval body are also relected in the structure of the adult
nervous system; commissures and connectives can be twisted
into a igure of eight and the various ganglia exhibit signiicant
asymmetries (chiastoneury or streptoneury, Fig. 20.3).
torsion is a synapomorphy which occurs in gastropods
during larval development (generally around the early veli-
ger stage). However, a degree of secondary detorsion or rota-
tion back towards the original body positions occurs in some
taxa. Accordingly, the adult nervous systems of these latter
animals may show little or no signs of twisting and few asym-
metries (Euthyneury, Fig.  20.3). (details of the morphology
of the gastropod nervous system will be discussed further
below). Several hypotheses suggest possible advantages of tor-
sion for the pelagic larvae, benthic adult form, or both (Ruppert
et al. 2004), and a number of recent papers on the subject have
addressed the ontogeny of torsion, particularly in basal gastro-
pods (Page  1997b, Wanninger et  al.  2000, Page  2003, Kurita
and Wada 2011). he nervous system has long been and will
likely continue to be a major player in debates on the matter
since the efects of torsion are so readily observable there.
A second emphasis of early work on gastropods focused
on the detailed microscopic anatomy of the cells within adult
nervous system. As Golgi (1967) and cajal (1967) devoted
most of their attention at the end of the nineteenth and early
twentieth centuries to understanding neuronal anatomy
198
in diferent regions of the brains of vertebrates, others (e.g.
Retzius) were examining the nervous systems of invertebrates
(see Shepherd (1991) for a historical view). For example,
(veratti 1900) used the Golgi staining technique to provide
exquisite descriptions of neuronal morphology in the garden
slug, Limax. during those early times, de nabias, Gilchrist,
and several others also provided important initial views
of the detailed morphology of neurons in gastropods, with
Hanström, Kunze, and others making signiicant later addi-
tions (see Bullock and Horridge (1965) for a more complete
listing of these early comparative neuroanatomists).
Subsequent years witnessed a continual growth in the litera-
ture on gastropod neuroanatomy, with a common observation
that many Heterobranchia possessed ‘giant’ neurons with soma
diameters that could measure into the hundreds of microns.
Moreover, several of these neurons could be readily identiied
from animal to animal within a species (Arvanitaki and tchou
1942; Sakharov 1994). In the 1950s and 1960s, Arvanitaki, her
husband chalazonitis, and another French neurobiologist, tauc,
ushered in the next important phase of research on the gastropod
nervous system by using microelectrodes to record from these
giant cells, and thereby discovered that the individual neurons
could be distinguished not only by their morphology but also
by physiological characteristics, such as spontaneous activity
(tauc 1954, Arvanitaki and chalazonitis 1955, 1956, 1964).
he identiied neurons of gastropods thus ofered the opportu-
nity to repeatedly collect experimental data about the same cell,
using diferent techniques to provide details about membrane
currents responsible for iring patterns, transmitter contents, and

Fig.  20.3. Schematic representations of diferent modes of gastropod
nervous system asymmetry. chiastoneury (or streptoneury)—the connec-
tives between pleural and parietal ganglia are crossed as a consequence of
torsion. Euthyneury, centralization—in both cases the connectives between
pleural and parietal ganglia are not crossed. centralization—the ganglia are
concentrated around the oesophagus. chiastoneury is characteristic of most
receptor expression. tens of neurons could be identiied individ-
ually in species such as Aplysia, Helix, and Lymnaea. Many other
neurons could be identiied as members of tightly clustered and
relatively homogeneous cells sharing anatomical, physiological,
and biochemical features. catalogues could therefore be com-
piled of the deining features of the neurons which constitute
the ganglia of a variety of species (coggeshall 1967). With the
realization that identiied neurons make consistent patterns of
connections with other identiied neurons, an opportunity was
recognized for the analysis of neural circuits underlying cen-
tral pattern generators (cPGs) that mediate behaviours such
as feeding (Benjamin and Rose 1979, Rose and Benjamin
1979, 1981, Elliott and Benjamin 1985), swimming (Getting
1983, Arshavsky et al. 1985a, b, Satterlie et al. 1985, Satterlie
and Spencer 1985) and respiration (Syed et al. 1990, Syed and
Winlow 1991). Much of the work from the late 1960s through
the 1990s was led or inluenced by Kandel, who exploited the
unique features of the gastropod nervous system to examine not
only how circuits underlie behaviour, but how those circuits
change during learning (Kandel 1976, 1979, 2001).
In summary, the gastropod nervous system has allowed a
conluence of powerful biological approaches (classical histol-
ogy at the beginning of the twentieth century, electron micros-
copy, electrophysiology, and immunocytochemistry at the
middle and end of the century, followed in the new millennium
M O l l U S c A : G A S t RO P O d A
Patellogastropoda and vetigastropoda. Among heterobranch species all three
modes of nervous system asymmetry can be found. cerebral ganglia are
coloured red, buccal ganglia are coloured yellow, pedal ganglia are coloured
blue, and the visceral loop ganglia (visceral, parietal, pleural, subintestinal,
supraintestinal) are coloured green; oesophagus are grey. Art drawing by Olga
Kharchenko.
by modern molecular biological approaches) to provide a deep
understanding of the role of single neurons, nerve circuits, neu-
roactive substances, as well as intracellular signalling and genetic
mechanisms in physiology and behaviour. he importance of
gastropod nervous systems in modern neuroscience is marked
by such notable accomplishments as early substantial evidence
for serotonin and dopamine as neurotransmitters (Gerschenfeld
and Stefani 1965,; Berry and cottrell 1973), investigations of
the neuronal basis of behaviour and memory (Kandel 1976,
1979, Willows 1985, 1986), discovery of new types of ionic
channels (neher and lux 1969, 1971, lux et al. 1981), recon-
structions of cPG circuitry in culture (Syed et al. 1990), and
many others.
hese many advances were facilitated by focusing on certain
gastropods, which attained the status of ‘model organisms’ by
virtue of their possession of relatively few central neurons, many
of which attained individual large sizes. he negative side of this
approach has been that, while we now have good understand-
ings of the neurobiology of certain gastropods, these species
all represent only one branch of gastropod phylogeny. In con-
trast to the heterobranchs, we know relatively little about the
anatomy, physiology, or biochemistry of the nervous systems of
the remaining gastropods. As indicated at the beginning of this
chapter, gastropods are extremely diverse and it may be prob-
lematic to generalize our understanding to gastropods in general.
199
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
ARcHItEctURE OF tHE
nERvOUS SyStEM
Gross anatomy
According to classical descriptions (Bullock and Horridge 1965)
(see also Figs. 20.3, 20.4), the central nervous system of gastro-
pods usually consists of the following: (1) A pair of cerebral gan-
glia, which are interconnected by cerebral commissures dorsal
to the oesophagus and send connectives to buccal, pleural, and
pedal ganglia. As will be discussed below, the cerebral ganglia
can fuse with other ganglia (primarily the pleural ganglia) thus
forming a complex brain, as described by Richter et al. (2010).
he cerebral nerves consist of both eferent and aferent axons
which connect with the eyes, statocysts, cephalic tentacles, skin,
and some muscles of lips, head, and column, and sometimes the
penis and surrounding region. (2) A pair of buccal ganglia, which
have a commissure ventral to the oesophagus. nerves from the
buccal ganglia consist of eferent axons to the pharynx and sali-
vary glands, and aferent axons from receptor neurons located in
the gut. (3) A pair of pleural ganglia, which have no commis-
sure but do have ipsilateral connectives with the cerebral ganglia,
pedal ganglia, and posterior ganglia, that form a visceral loop.
he pleural ganglia are often fused with the cerebral ganglia and/
or located close to the pedal ganglia. nerves from the pleural
ganglia mostly run to the mantle and contain both eferent and
aferent axons. (4) A pair of pedal ganglia connected by one or
Fig. 20.4. dissections of the freshwater snail, Lymnaea, showing organs
within the opened body cavity after a mid-dorsal incision. A: location
of the central ganglia relative to other anterior organs in the body cav-
ity. B: central ganglia lying in situ behind buccal mass after removal of
most other organs. C: Lymnaea central ganglia after removal from animal
and with cerebral ganglia retracted laterally after the commissure was cut.
his is a typical coniguration used for electrophysiology and wholemount
200
more commissures (Fig 20.3). In basal forms (e.g. in
Patellogastropoda and vetigastropoda), the ganglia are represented
as elongated medullary cords. he nerves of the pedal ganglia pri-
marily have eferent axons to the muscles and aferent axons from
the skin of the foot. (5) Single supraintestinal and subintestinal
ganglia, which vary widely in position, manifest the presence of
chiastoneury or euthyneury and have tendencies to fuse with other
ganglia of the visceral loop. he ancestral connectives course from
the right pleural to supraintestinal ganglia and from the left pleu-
ral to subintestinal ganglia (Fig. 20.3). In forms with chiastoneury,
secondary connectives often occur between supraintestinal and
the nearby left pleural, and between the subintestinal and nearby
right pleural ganglia, thus exhibiting what is referred to as zygon-
eury. Zygoneury can be also expressed as a connection between the
main mantle nerve and the intestinal ganglionic nerves and pal-
lial nerves, from the pleural ganglia. (6) A pair of parietal ganglia
(in Heterobranchia, though not in more basal gastropods such as
the caenogastropoda), which often fuse with intestinal and pleu-
ral ganglia and connect with peripheral osphradial ganglia. he
nerves of the parietal ganglia consist of both eferent and afer-
ent axons, connecting with the lateral body wall, gills (ctenidia),
and mantle. (7) A visceral ganglion, which is usually unpaired and
completes the posterior segment of the visceral loop. he nerves
of the visceral ganglion run to the caudal region of the gut, anus,
and adjacent parts of the skin and body wall, reproductive organs,
kidney, liver, and heart, and also consist of both eferent and
aferent axons.
immunohistochemistry. D: Schematic representation of Lymnaea central
ganglia. cerebral ganglia (cG) red, buccal ganglia, (BG) yellow, pedal gan-
glia (PeG) blue, visceral loop ganglia (vG, PaG, PlG) green. l left side gan-
glia, R right side ganglia. E: Position of some identiiable neurons within
ganglia in Lymnaea. Photos of Lymnaea by leonid nezlin. Schematic draw-
ings adapted by Olga Kharchenko from (croll and chiasson 1989) and
(Syed et al. 1990).

It is a generally accepted speculation that the nervous sys-
tem found in existing gastropods is derived from a hypotheti-
cal, bilaterally symmetrical ancestor which possessed a pair of
long pedal cords and four or ive pairs of ganglia connected by
connectives and commissures. With torsion, a main feature of
basal gastropods is the crossing of pleural–visceral connectives,
making a igure of eight of the visceral loop (chiastoneury or
streptoneury, Fig. 20.3). In groups thought to be more derived
(Heterobranchia), there is a general tendency toward cephaliza-
tion and centralization of the ganglia (Fig. 20.3). hus, posterior
ganglia of the visceral loop move forward, shortening their con-
nectives with the pleural ganglia. Among Euopisthobranchia all
degrees of concentration are seen, but long connectives tend to
be an exception. he Panpulmonata, in general, are character-
ized by shortening of the visceral loop (Bullock and Horridge
1965). Presumably, because of these processes of cephalization
and centralization, there is often no crossing of central connec-
tives and only a slight crossing of peripheral nerves (euthyneury
or orthoneury) (Fig.  20.3). Based largely on this characteris-
tic, lindberg et al. (lindberg et al. 2004) grouped gastropods,
which are subsumed under the Heterobranchia, as Euthyneura.
As outlined by Schmekel (Schmekel 1985) (see also Haszprunar
1988), these animals characteristically have ive ganglia in their
visceral loop, although these ganglia often fuse during develop-
ment. Frequently, asymmetric fusion results in cells which were
initially bilaterally symmetric becoming asymmetrically posi-
tioned in the visceral loop (Hughes and tauc 1963, Kriegstein
1977, Munoz et al. 1983).
In addition to having well-described central nervous sys-
tems, gastropods also possess extensive peripheral nervous sys-
tems which contain not only the axons emerging from central
neurons, but also large numbers of peripheral neurons located
within diferent organs of the body. Several types of putative
receptor neurons of mixed modalities, including mechano-,
photo-, and chemoreceptors (Hanström 1925, 1928, Bullock
and Horridge 1965, Zaitseva and Bocharova 1981), have long
been recognized to be numerous and to probably play impor-
tant functions. However, they remain relatively poorly investi-
gated, although existing evidence suggests that the peripheral
division of the nervous system rivals or perhaps surpasses the
central ganglia in terms of both its complexity and importance.
For instance, it has recently been estimated that the peripheral
neurons in the tentacles and lips alone in the pond snail Lymnaea
outnumber those in the entire central nervous system (Wyeth
and croll 2011). numerous other peripheral cells, which do not
appear to be receptor neurons (e.g. those without apical den-
drites in the body wall) have been found clustered along periph-
eral nerves, particularly at nerve branches or where they merge
into peripheral plexi. Other peripheral neurons are embedded
deep in the body wall or inner organs of gastropods (e.g. female
and male reproductive organs) and appear to contribute to neu-
ral plexi along various ducts (for example, the alimentary tract).
he roles of these neurons are not known, but they may mediate,
at least in part, motor functions associated with mechanosen-
sory stretch receptors, and their activity probably underlies local
peripheral relexes responsible for mucus secretion and peristal-
tic contractions of the ducts.
M O l l U S c A : G A S t RO P O d A
Microanatomy
Gastropod ganglia have a structure that is typical of other
invertebrates. he cortex is composed of several layers of the
somata of primarily unipolar neurons. hose cells project
their neurites into the central region of the ganglion which
is composed of neuropil. tracts of axons also enter or leave
the neuropil via the commissures and connectives to other
ganglia or via nerves to the periphery. In most gastropods
(Patellogastropoda, vetigastropoda, caenogastropoda) the
neuronal somata are relatively uniform in size and rarely
exceed 30–40 µm in diameter. In Heterobranchia, how-
ever, the somata range widely in size. In Aplysia, some neu-
rons measure up to nearly 1 mm in diameter although many
other neurons are 30–40 µm in diameter in adults. However,
the somata diameters are also scaled to animal body size. As
animals grow during development, the neurons also grow in
size, although not at the same rate as the body (croll and
chiasson 1989, croll et al. 1999). he size of the somata also
varies greatly between species, with animal size being a major
determinant of cell size (Klussmann-Kolb et al. 2013). Hence,
the giant neurons of Lymnaea (with maximum body lengths
of about 5 cm) attain diameters of only a couple of hundred
microns, and are a fraction the size of the neurons found in
fully grown Aplysia, which grow to much larger body sizes.
Moreover, as emphasized in the introduction to this chapter,
gastropods constitute an extremely diverse group of animals,
and there are notable exceptions to all rules. For example,
while land snails and slugs, like Helix, Limax, and Achatina,
are typical of other pulmonates with many giant neurons
within the brain; they also possess procerebrums, which are
regions of the cerebral ganglia specialized for processing infor-
mation about air-borne odours, and contain thousands (per-
haps more than in the whole of the rest of the central nervous
system) of uniformly small neurons which are only 5–7 µm in
diameter (Zs-nagy and Sakharov 1970, chase 2000, Zaitseva
2000, longley 2011, Elekes et al. 2013).
he central neurons of Heterobranchia are especially notable
for the size of the nucleus, which is commonly two-thirds of the
diameter of the cell (see Fig. 20.5), and the large sizes of both the
neuronal somata and their nuclei correlate with an abundance
of dnA in these cells. For example, it has been estimated that
large neurons in Aplysia and Lymnaea have dnA contents which
would be the equivalent to 11–16 whole genome duplications
(up to many thousands of times the haploid content (lasek and
dower 1971, Boer et  al.  1977)). chase and tollockzo (1987)
reported that all cells greater than 9 µm in diameter appeared
to be polyploid, although they cautioned against the use of this
commonly employed term, since evidence suggested that difer-
ential ampliication of only selected segments of genome cause
the increased dnA content. Gillette (1991) discussed possible
evolutionary origins and advantages of the giant neurons and
their ampliied genomes in gastropods.
Another characteristic of gastropod neurons is the ‘trophos-
pongium’, where the somata and the initial segments of axons
are often invaginated by glial cells processes. his structure has
been hypothesized to be involved in trophic support of the large
201
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
Fig.  20.5. Immunohistochemical staining of neurons in Biomphalaria
(A–C), histamine in Lymnaea (D–F) and FMRFamide in Aplysia (G–I).
A: tyrosine hydroxylase immunoreactivity labels a prominent cell,
lPed1, on the posterior margin of the left pedal ganglion. he single
axon from this cell projects through the left pleural and parietal ganglia
(lPlG, lPaG). B: numerous catecholamine-containing neurons (small
arrows) in the buccal ganglion. non-reactive cells (hollow arrows) have
slightly autoluorescent cytoplasm, which outlines the large nuclei that
are characteristic of gastropod neurons. C: he skin of gastropods con-
tains numerous tightly packed tyrosine hydroxylase immunoreactive cells.
he dendrites of these cells project to the skin surface and indicate that
they are likely receptor neurons. D: A multipolar histamine immuno-
reactive neuron in the pedal ganglion of Lymnaea. E: Other histamine
immunoreactive neurons form clusters (larger arrows) on the lateral mar-
gin of the pedal ganglion. he neurites from each cluster form separate
tight bundles (smaller arrows) that either enter the neuropil or project
posteriorly to leave the ganglion. F: he sensory hair cells (larger arrows)
of the statocyst of Lymnaea are also histamine immunoreactive and their
axons project to the cerebral ganglion via the static nerve (small arrow).
202
G: FMRFamide-like immunoreactivity on the ventral surface of the fused
parietovisceral (abdominal) ganglion of Aplysia. labelled cells include
a prominent medial neuron with axons (small arrows) that ascend the
pleural–abdominal connective (PlAc) on each side. Another large neuron
tentatively identiied as l12 is located more posteriorly in the ganglion, as
is a more dimly labelled cluster of neurons (bracket). H: Higher magniica-
tion view of axon (small arrows) of the medial, FMRFamide-like immu-
noreactive soma (larger arrow) as it projects through the left connective.
Inset shows numerous small branches from the main axon, which appear
to terminate in the region of the developing bag cells, which produce egg
laying hormone. I: More lateral cells on the ventral surface of the left
abdominal hemiganglion showing both the neuron (solid arrow) shown
in parts G and H and also other neurons tentatively identiied as l12 and
l13. neurites from an unidentiied neuron(s) make basket-like projections
which surround another soma located along the lateral edge of the ven-
tral surface of the left hemiganglion. Inset shows another example of such
projections surrounding that neuron in another animal. Photographs of
tyrosine hydroxylase immunoreactivity were provided by Mohamed Habib
while others were taken by Roger croll.

neurons (dos Santos et al. 2005a, verkhratsky and Butt 2013).
In fact, glial cells form a major component of the nervous sys-
tems in gastropods and are found throughout ganglia amongst
neuronal somata and within the neuropil. Glial cells may out-
number the neurons by several-fold and comprise 50% or more
of the volume of the tissue.
Anatomically, glia comprises a vast array of cell types, with
marked variations at diferent locations and at diferent stages
of development amongst groups, species, and individuals. Glial
cells that possess a nucleus with peripheral heterochromatin,
scant or no intermediate ilaments, a well-developed Golgi com-
plex, rough and smooth endoplasmic reticula, mitochondria,
and polymorphic lysosomes, have been referred to as protoplas-
mic glial cells. heir morphology suggested phagocytic activ-
ity of debris from the extracellular space and they are probably
involved in such physiological processes as (i) regulation of ionic
composition of neuronal environment, (ii) transmitter uptake,
inactivation, or release, (iii) metabolic interactions with neurons.
Another type showed numerous glial ibrillary acidic protein
(GFAP) and vimentin immunoreactive intermediate ilament
bundles (cardone and Roots 1990), a discrete Golgi complex,
mitochondria, endoplasmic reticulum, lipid droplets and lys-
osomes. hese cells have been referred to as ibrous glial cells
and most probably provide support and protection for nervous
tissue against deformation (Pentreath et  al.  1985, dos Santos
et al. 2005b). he protoplasmic glial cells prevail in the cortical
region, while the ibrous glial cells prevail in the medullar region.
Axon endings have been observed among the somata of
neurons within ganglia (veratti 1900, Elekes 1991, Moroz 2006)
(see also Fig. 20.5I), but most electron microscopy (coggeshall
1967, Bailey et al. 1979, 1982, Bailey and chen 1983, Elekes
and Rozsa 1984, Elekes and Ude 1993), immunocytochem-
istry (see examples in Fig. 20.5A, d, E, G, and references cited
below), and electrophysiological (Arvanitaki and chalazonitis
1949; tauc 1957) studies indicate that the majority of synapses
are located within the neuropil. he procerebrum of terrestrial
gastropods, however, possess a particularly complex system of
synaptic and non-synaptic connections with the somata richly
surrounded by varicosities while the axons also establish contacts
with each other (Elekes et al. 2013).
Surrounding the ganglia and larger nerves is a multilayered
connective tissue sheath, the thickness and composition of which
vary signiicantly between species. he supericial region con-
tains masses of globular cells intermingled with smooth muscle
cells and nerve ibres, all embedded in a connective tissue matrix.
he muscle cells often weave around the globular cells with no
direct contact. nerve ibres innervate at least some of the muscle
cells. he connective tissue consists of large and small diameter
ibres, suggesting that maturation of the ibrous components of
the intercellular matrix is taking place in the supericial regions
of the epineural sheath (Rogers 1969).
nerve tracts, connectives, and commissures have similar struc-
tures. A thick outer sheath surrounds the nerve and consists of
connective layers alternating with ibrous extracellular bundles
embedded into a ground substance. directly under the connect-
ive tissue, a 5–10 µm perineural layer covers the nerve. It is made
up of the closely packed plasma membranes of the invaginated
M O l l U S c A : G A S t RO P O d A
processes of peripheral glial cells and the ibrous matrix secreted
by them. Bodies of glial cells are located beyond the peripheral
glial projections, in the separation area between the axonal bun-
dles (longley 1984, Musio and Bedini 1990). Within the main
nerves, axons can be segregated in groups by glia processes. his
arrangement probably relects a segregation of functional types
of axons, as well as their origin from distinct peripheral areas.
As will be discussed below, certain neurons release their
neurotransmitters/hormones into the blood stream at speciic
sites that act as neurohaemal organs in the outer portions of
nerves, and commissures of the cerebral and visceral ganglia.
neurohaemal zones can also include connective tissue adja-
cent to the ganglia cortical layer. hese areas contain many tiny
nerves which consist mainly of neurosecretory axons, ending
non-synaptically near parts of the vascular system (Bonga 1970,
Joosse 1984). For other neurotransmitters/hormones, there
appear to be no speciic neurohaemal organs, and release into
the blood appears to occur more generally from difuse nerve
terminals or varicose ibres in the connective sheath surrounding
the central ganglia. For example, electron microscopy revealed
serotonin-immunoreactive varicosities within the neural sheath.
varicosities can be also engulfed by glial processes in both the
cell body region and neural sheath, or embedded in the connect-
ive tissue free of glial processes (Elekes 1991).
nEUROtRAnSMIttER
dIStRIBUtIOn
Gastropod nervous systems contain only tens of thousands of
neurons within the central ganglia; a number that stands in bold
contrast to the billions of neurons found in the brains of higher
vertebrates. And yet, in spite of this huge diference in the num-
bers of neurons and presumably in the numbers of connections
between them, there is no proportional diference in the num-
bers of known transmitters between the two groups of animals
(Sakharov 1970, 1974, 1990). Almost all of the classical, small
molecule transmitters, such as glutamate, GABA, acetylcholine,
serotonin, dopamine, norepinephrine, and histamine, have been
detected in the nervous systems of gastropods and appear to be
used for synaptic communication, as does the gaseous transmit-
ter, nO. While gastropods may also share certain peptide trans-
mitters (e.g. some endogenous opiates) with vertebrates, they
generally appear to use an equally large number of neuropep-
tides, such as the FMRFamide-related peptides, which are more
commonly encountered in other invertebrates.
Early work on the distribution of transmitters relied upon
histochemical techniques such as aldehyde/glyoxylate-induced
luorescence of monoamines (Sakharova and Sakharov 1971,
Furness et al. 1977, tritt et al. 1983, Goldstein 1984, Goldstein
and Schwartz 1989). While these techniques still play a role in
conirming the localization of certain transmitters (Elofsson
et  al.  1993, Moroz et  al.  1996, croll et  al.  1999, Wyeth and
croll 2011, vallejo et al. 2014), they have largely been replaced
with immunocytochemical techniques, which are generally
more speciic and sensitive (Fig.  20.5, 20.6). It is beyond the
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S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
scope of this chapter to provide full descriptions of the distribu-
tion patterns for each of the known and/or putative neuroactive
substances found across the gastropods, but a brief description of
the distribution of some of the best studied transmitters can be
used to illustrate general principles in these animals.
Serotonin has long been known to be an important and abun-
dant transmitter in gastropods and has been implicated in the
control of a wide range of behavioural and physiological func-
tions. It is therefore not surprising that when antibodies against
serotonin irst became available, gastropods were among the irst
subjects of study (Goldstein et  al.  1984, Ono and Mccaman
1984, Kistler et al. 1985). In the gastropods examined to date,
serotonin is widely distributed in all ganglia and in all or most
nerves to the periphery where many organs, muscles, and regions
of the body wall are richly innervated with serotonin-containing
eferents (croll and lo 1986, longley and longley 1986, croll
1987a, 1988, croll and chiasson 1989, Elekes et  al.  1989,
Satterlie et  al.  1995, Moroz et  al.  1997, Sudlow et  al.  1998,
Hernadi and Elekes 1999). large neurons in the visceral and/or
parietal ganglia appear to send axons to the heart and generally
have a cardioexcitatory efect (Koester et al. 1979, Rosza 1979,
Buckett et al. 1990, Skelton et al. 1992). Serotonergic neurons in
pedal ganglia send axons to the foot and are involved in locomo-
tion arising from both ciliary activity and muscular contractions
(Audesirk et  al.  1979, Hening et  al.  1979, Syed and Winlow
1989). Another group of serotonergic neurons innervates the
penis (croll and chiasson 1989, deBoer et al. 1997, de lange
et al. 1998). One particularly noteworthy serotonergic neuron,
known as c1 (or alternatively the metacerebral giant cell), is
found within the cerebral ganglion of heterobranch gastropods
and provides all of the serotonin to the buccal ganglia and mus-
cles (Weiss and Kupfermann 1976, Pentreath et  al.  1982). In
vivo recordings in freely behaving, intact snails, as well as record-
ings in the isolated ganglionic preparations, demonstrated that
certain levels of serotonin, correlated with iring activity of c1,
are essential for expression of the feeding motor programme
(Weiss et  al.  1978, yeoman et  al.  1994). Another group of
smaller and more posterior serotonergic neurons trigger and/or
modulate escape and withdrawal responses in a variety of gastro-
pods (Klein et al. 1982, longley and longley 1986, Mc clellan
et al. 1994, Kandel 2001; newcomb and Katz 2007b, 2009).
numerous catecholamine-containing cells have also been
described in gastropods (Fig. 20.5B). Analyses have repeatedly
demonstrated that dopamine is the most common catecho-
lamine present in gastropods, but signiicant levels of norepi-
nephrine can also be detected (Mc caman et al. 1979, Ottaviani
et al. 1988, voronezhskaya et al. 1999). While the majority of
these neurons are found in the periphery (see below), their afer-
ent axons terminate in the central ganglia. In addition, several
catecholamine-containing neurons also reside within the central
ganglia and their distributions have been described in several
species (croll 1987a, 1988, croll et al. 1999, croll 2001, croll
et al. 2001b, vallejo et al. 2014). he best studied of these cat-
echolaminergic neurons are the RPed1 cells of the dextral snail,
Lymnaea, and the lPed1 cells of the sinistral snails, Helisoma,
Planorbis, and Biomphalaria (see below for discussion of these
apparently homologous cells). hese neurons are known to
204
contain and use dopamine as their transmitter and make synaptic
connections with numerous neurons in the visceral and parietal
ganglia (Benjamin and Winlow 1981). hey presumably have
numerous functions, the best studied of which is involvement
in generating the rhythmic activity underlying respiration (Syed
and Winlow 1991). Other well-studied dopaminergic neurons
are involved in the control of feeding (Kemenes et  al.  1990,
Kabotyanski et al. 1998, 2000, diaz-Rios et al. 2002).
Histamine is another biogenic amine that is found in relative
abundance in the nervous systems of gastropods. Histamine-like
immunoreactivity is located in a number of neurons found in
the central ganglia (Weinreich 1977, Ono and Mc caman 1980,
Osborne and Patel 1984, Elste et al. 1990, Soinila et al. 1990,
Hegedus et  al.  2004) (Fig.  20.5d, E, F), and this transmit-
ter appears to be involved in a number of functions, includ-
ing the control of feeding behaviour (Weiss et al. 1986, chiel
et al. 1988, 1990). Histamine also appears to be located in the
hair cells of the statocysts, which are located on the pedal ganglia
(Oshuga et al. 2000). hese organs mediate the sense of balance
in molluscs and disruption of histaminergic neurotransmission
afects the normal orientation of snails to gravity (Braubach and
croll 2004).
demonstrations of potential glutamatergic neurons have
been hindered by the fact that many cells appear to contain
signiicant concentrations of glutamate and are therefore
reactive, to varying degrees, to antibodies raised against this
non-essential amino acid. Furthermore, commonly avail-
able antibodies against proteins, such as vesicular glutamate
transporter (vGlut) from mammals, appear to have limited
cross reactivity in molluscs (but see levenson et  al.  2000).
nevertheless, immunohistochemical studies have identi-
ied potential glutamatergic cells in Lymnaea (Hatakeyama
et  al.  2007), while other studies have added supportive evi-
dence that speciic central neurons use glutamate as their trans-
mitter (levenson et  al.  2000, collado et  al.  2009). he best
cases for the use of glutamate as a transmitter involve synapses
between receptor and motor neurons, mediating escape and
withdrawal behaviours (dale and Kandel 1993, Bravarenko
et al. 2003, Megalou et al. 2009) and synapses involved in the
generation of feeding behaviours (nesic et  al.  1996, Brierley
et al. 1997).
he presence of gamma (γ) amino butyric acid (GABA) and
the efects of its application on neurons were well established in
gastropods by the 1970s (Gerschenfeld and tauc 1961, Osborne
et al. 1971, Gerschenfeld, 1973). corroborating evidence for its
use as a synaptic transmitter followed (Richmond et al. 1991)
and its localization has now been described in several species
of Heterobranchia (cooke and Gelperin 1988, Hernadi 1994,
dyakonova et  al.  1995, diaz-Rios et  al.  1999, Hatakeyama
and Ito 2000, Ierusalimsky and Balaban 2001, Gunaratne
et al. 2014). cells containing GABA are located primarily in the
cerebral, buccal, and pedal ganglia and very similar distribution
patterns can often be recognized between species (Gunaratne
et al. 2014). While axons containing GABA are plentiful in the
commissure and connectives of the central nervous system, few
have been reported in the nerves connecting the central ganglia
with the periphery. GABA has been implicated most strongly

in the control of feeding (Arshavsky et  al.  1993, diaz-Rios
et al. 1999, Bravarenko et al. 2001) and the processing of sen-
sory information (Alkon et al. 1993, Jin et al. 2009, Kobayashi
et al. 2012).
A large body of evidence has indicated that acetylcholine acts
as an important transmitter in the nervous systems of gastro-
pods (tauc and Gerschenfeld 1961, Kehoe 1972, Gerschenfeld
1973, Eisenstadt and Schwartz 1975, treistman and Schwartz
1977, tauc et  al.  1992, Smit et  al.  2001). Some of the best
studied roles of this transmitter involve neurons that control
the heart, feeding, mucus secretion, and processing of olfac-
tory information (King et  al.  1987, vilim et  al.  1996, Elliott
and vehovszky 2000, Ito et al. 2004). However, as in the case
with glutamate, little progress has been made through the use
of immunocytochemistry to generate comprehensive maps of
potential cholinergic neurons. Evidently, acetylcholine is not
rendered suiciently antigenic or immunoreactive by common
ixation procedures, and work in other animals has therefore
turned to choline acetyltransferase-like immunoreactivity as a
reliable indicator of neurons that synthesize, and therefore likely
contain, acetylcholine. Unfortunately, commonly available anti-
bodies raised against choline acetyltransferase from mammals
and insects have generally not cross reacted with the molluscan
proteins, although a recent report has described numerous cho-
line acetyltransferase-like immunoreactive neurons in the central
nervous system of the slug, Limax (d’ Este et al. 2011).
nitric oxide (nO) has a well-documented function as a gas-
eous transmitter in gastropods, and these animals have provided
some of the earliest and best examples of identiied neurons that
are capable of producing nO (as evidenced, for example, by the
expression of the message for nO syntase (nOS)), and with
actions on follower cells that can be suppressed by nOS inhibi-
tors and/or nO scavengers (Jacklet 1995, 1997, Park et al. 1998).
Moreover, precursors and metabolites of the nO pathway and
nOS cofactors can be assayed in the large individual neurons
by means of capillary electrophoresis (Moroz et al. 1999, Moroz
2000). he nitrergic nature of identiied synapses can therefore
be irmly established in gastropods. While antibodies against
nOS have been used to label nitrergic cells, the results have
been inconsistent and much of the work on the localization of
these cells has therefore relied upon nAdPH diaphorase histo-
chemistry (cooke et al. 1994, Moroz 2000). While the central
ganglia generally contain relatively few labelled cells bodies, they
have reliably been reported to contain numerous axons, many of
which appear to originate from chemoreceptor neurons in the
periphery (cooke et  al.  1994, Moroz 2006). he best-studied
functions of nO are related to control of feeding and in the pro-
cessing of chemosensory information (Gelperin 1994, Elphick
et al. 1995, Moroz 2006, Wyeth and croll 2011).
In addition to the classical, small molecule and gaseous trans-
mitters, various neuropeptides have also been studied widely in
gastropods, and data from molecular mapping studies on the
adult Lymnaea brain indicate that at least 12.5% of the estimated
brain total neuronal population is peptidergic (Benjamin 2008).
he family of FMRFamide-related peptides is by far the
best studied in gastropods. Originally discovered in a bivalve
(Price and Greenberg 1977), FMRFamide has now been found
M O l l U S c A : G A S t RO P O d A
throughout the molluscs (loi and tublitz 1997, Wollesen
et  al.  2010)(Fig.  20.5.G, H, I) and beyond (Krajniak 2013,
Orchard and lange 2013). Schaefer et  al.  (1985) irst cloned
and sequenced the FMRFamide gene in Aplysia and showed that
the precursor protein is not only cleaved into several copies of
FMRFamide, but also into numerous other peptides, which gen-
erally end with RFamide at the c terminus, but are elongated
at the n-terminus from the four amino acids of FMRFamide
itself, or alternatively, from the related peptide, FlRFamide.
Santama et  al. (Santama et  al.  1995a, Santama and Benjamin
2000) cloned the FMRFamide gene in Lymnaea, but also found
that the broader family of FMRFamide-related peptides is actu-
ally derived from two, alternatively spliced transcripts from the
encoding dnA. two transcripts encoding FMRFamide related
peptides have also been found in the basal gastropod Haliotis
(cummins et al. 2011), thus suggesting that this organizational
characteristic of the FMRFamide gene is an ancestral trait of the
gastropods.
table  20.1 lists evidence for several additional peptides
in gastropods. he list, however, is intended only to provide
examples and is by no means exhaustive. A fuller list of additional
peptides and their widespread distribution in the gastropods can
be seen from nervous system transcriptome and whole genome
studies of diverse gastropods (Moroz et al. 2006, veenstra 2010).
A major complication for the study of transmission arises from
the inding that the classic separation of neuroactive substances
into transmitters and hormones is blurred in gastropods. Many
of the neuroactive substances that are used for synaptic transmis-
sion are also released into the blood and reach their targets via
the cardiovascular system. A good example of this comes from an
examination of the Lymnaea caudodorsal cell peptides, which act
as transmitters in the central ganglia to orchestrate the sequence
of movements that underlie egg laying behaviour, but also act
as hormones to stimulate ovulation. While the dual use of sub-
stances as both transmitters and hormones is best studied in the
peptides, monoamines may also act as hormones. Evidence for
dopamine and serotonin, acting as neurohormones is generally
attributed to gastropod larval development, but such roles have
been suggested in adult bivalve molluscs (Fong et al. 1993, Pani
and croll 2000, carroll and catapane 2007) and demonstrated
resently for adult gastropods (Ivashkin et al, 2015).
Another complication in the study of neurotransmission
involves the localization of more than a single potential trans-
mitter within a neuron. Evidence suggests that both GABA and
dopamine may be used by certain neurons involved in the con-
trol of feeding in Aplysia (diaz-Rios et al. 2002), while histamine
and nO may be co-released by other neurons (chiel et al. 1986,
Jacklet 1995). Much work has also been devoted to the study of
co-transmission by peptides and classical, small molecule trans-
mitters, such as acetylcholine (Weiss et  al.  1992, dyakonova
et al. 1995, vilim et al. 1996). Finally, alternate splicing of gene
transcripts and the production of multiple neuropeptides from
single precursor proteins means that complex cocktails of neuro-
peptides can be released from single neurons (Sossin et al. 1990,
Santama et al. 1996, Santama and Benjamin 2000, cummins
et al. 2011). hus, even synaptic connections between individual
neurons can involve numerous transmitters and receptors, and
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S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S

Table 20.1: Examples of assorted peptides found in Gastropoda.

Peptides Species References

Achatin peptides (including GFFd/GdFFd) Achatina, Aplysia
APGWamide Lymnaea, Aplysia,
Helix
Buccalin Aplysia, Lymnaea
Ovulation hormones (including Egg laying Aplysia, Lymnaea,
Hormone, caudodorsal cell hormone and diverse species
related peptides)
FMRFamide related peptides (including Aplysia, Lymnaea,
FlRFamide, extended RFamide peptides, Helix, Haliotis
SEEPly, acidic peptide)
Fulicin Achatina
Gonadotropin-releasing hormone related Aplysia, Helisoma,
peptides Lymnaea
Insulin related peptides Lymnaea, Aplysia
Myomodulin Aplysia, Lymnaea
Mytilus inhibitory peptides Aplysia, Achatina,
Helix, Lymnaea
Opioid related peptides (e.g. enkephalins) Lymnaea, Aplysia,
Ilyanassa
Pedal peptides Aplysia, Tritonia,
diverse nudibranchs
R15 and vd1/RPd2 peptides Aplysia, Lymnaea,
diverse species
R3–R14 peptides Aplysia
Small cardioactive peptides (ScP-A, ScP-B) Aplysia, Helix
Sensorin Aplysia
vasopressin/oxytocin peptides Lymnaea
(Satake et al. 1999, Bai et al. 2013)
(croll and van Minnen 1992, Smit et al. 1992a,
li and chase 1995, Fan et al. 1997)
(Miller et al. 1993a, Santama et al. 1994)
(Kupfermann 1970, Scheller et al. 1983, van
Minnen et al. 1988, vreugdenhil et al. 1988,
Ram et al. 1998)
(Schaefer et al. 1985, Price and Greenberg
1989, Price et al. 1990, Santama et al. 1995a, b,
cummins et al. 2011)
(Ohta et al. 1991)
(Goldberg et al. 1993, young et al. 1999, Zhang
et al. 2008)
(Smit et al. 1988, 1991, 1992b, Smit
et al. 1996, Floyd et al. 1999)
(Miller et al. 1993b, Santama et al. 1994)
(Ikeda et al. 1992, Fujisawa et al. 1999, Elekes
et al. 2000)
(Kemenes et al. 1992, carpenter et al. 1995,
Ewadinger et al. 1996, Braubach et al. 2006)
(lloyd and connolly 1989, Beck et al. 2000,
Baltzley et al. 2011)
(Weiss et al. 1989, Kerkhoven et al. 1991,
Bogerd et al. 1993)
(nambu et al. 1983, Knock et al. 1989)
(lloyd et al. 1987, Price et al. 1990, church
and lloyd 1991, Santama et al. 1994, lloyd
et al. 1996)
(Brunet et al. 1991)
(van Kesteren et al. 1995)

histochemical studies of single transmitters ofer only incom-
plete views of the means by which the labelled neurons can inlu-
ence postsynaptic efectors.
he localization of neuroactive substances in speciic, iden-
tiied neurons within central ganglia has played an important
role in analyses of synaptic transmission, intracellular signalling
pathways, and neural circuits that mediate a variety of physio-
logical and behavioural functions. In particular, central Pattern
Generators (cPGs) that play the fundamental role in the pro-
duction of motor programmes underlying speciic behaviours
can be analysed in terms of physiological connections between
individual neurons using synapses, often with known transmit-
ters and receptors. However, as also discussed above, the release
of neuroactive substances is not always localized to closely
apposed postsynaptic membranes; endocrine and perhaps par-
acrine release of neuroactive substances into the neuropil region
and into the blood also appears to occur. he activity of individ-
ual neurons in a cPG might therefore depend, not only on dis-
crete synaptic inputs, but also on a rich and dynamic chemical
microenvironment which relects the physiological state of the
organism (Sakharov 1990, 2012). changes in ‘mediator cock-
tails’ surrounding the cells of the cPG might help to explain
the often noted lexible nature of many cPG circuits, whereby
a single neuronal circuit can produce a variety of diferent out-
puts (croll et  al.  1985, Benjamin 2012, Sakharov 2012, Ito
et al. 2013).

206

transmitter-speciic markers not only yield insights into the
morphology and physiology of central neurons, but also provide
an efective tool for studying the peripheral nervous systems of
gastropods. Although numerous peripheral neurons have long
been known to exist in these animals, they are generally small
and embedded deeply in the body wall. he peripheral nervous
system was therefore largely resistant to the types of electrophysi-
ological analyses that dominated work on gastropods in recent
decades. In fact, work on peripheral neurons often appeared to
be treated as a distraction from studies focused on the organi-
zation of the central circuitry that underlies behaviour and
the central sites of synaptic plasticity that underlie experience-
dependent changes in behaviour (carew et  al.  1979, leonard
et  al.  1989, croll 2003). Immunocytochemistry has begun to
make the study of peripheral neurons much more accessible.
large numbers of peripheral neurons have been revealed by
their reactivity to antibodies raised against tyrosine hydroxylase,
the rate-limiting enzyme in the synthesis of catecholamines. he
catecholamine-containing neurons have subepithelial somata
which bear apical dendrites that penetrate to the outer surface
of the body wall and end in pronounced swellings at the tips.
An axon exits the basal side of each neuronal soma. Many of
these axons converge into peripheral nerve bundles and termin-
ate in the neuropil of central ganglia. hese putative receptor
neurons have now been described in a variety of gastropods
(croll et  al.  1999, croll 2001, Faller et  al.  2008, Wyeth and
croll 2011, vallejo et  al.  2014), and even in bivalves (Smith
et al. 1998) and cephalopods (Buresi et al. 2014). hey appear
early in development (dickinson et  al.  1999, voronezhskaya
et al. 1999, dickinson et al. 2000, dickinson and croll 2003)
and are often packed so tightly that it is diicult to view individ-
ual cells in detail. Hence, it has not yet been determined whether
diferent subtypes of catecholamine-containing neurons exist or
whether all of their axons project exclusively to the central ner-
vous system; peripheral connections may mediate local relexes
which occur in the absence of central input (croll 2003). he
catecholamine-containing neurons are located throughout the
skin but are particularly abundant in cephalic sensory organs
(e.g. tentacles, rhinophores, lips) and along the front edge of the
foot and mantle (Fig. 20.5c), and it has been suggested that they
may mediate mechanoreception and/or a generalized chemosen-
sory function (croll 2003, Wyeth and croll 2011). Putative sen-
sory neurons exhibiting glutamate-like immunoreactivity have
also been reported to be widely distributed in the periphery of
Lymnaea (Hatakeyama et al. 2007).
Additional populations of putative receptor neurons have also
been labelled with antibodies raised against histamine and nitric
oxide syntase (nOS; nOS-positive cells are also often labelled
histochemically by nAdPH diaphorase activity). hese neurons
are concentrated around the mouth and anterior regions of the
head that are specialized for chemoreception (cooke et al. 1994,
Hegedus et  al.  2004, Moroz 2006, Wyeth and croll 2011).
Indeed nO has been implicated in chemosensory control of
feeding (Elphick et al. 1995) and processing of olfaction infor-
mation in gastropods, as mentioned above. Other, potential che-
mosensory cells exhibit FMRFamide-like immunoreactivity at
the tips of the tentacle of terrestrial slugs (Suzuki et al. 1997),
M O l l U S c A : G A S t RO P O d A
while the chemosensory osphradium of pond snails contains
cells reactive to antibodies against FMRFamide, enkephalin, and
GABA (nezlin et al. 1994, nezlin and voronezhskaya 1997).
Homologous cells
Many of the neurons and neuronal clusters noted above are
not only recognizable from animal to animal within a species
but also within genera (e.g. between diferent species of Aplysia
(Blankenship and coggeshall 1976, dickinson 1980) and
within broader taxa of Heterobranchia e.g. between diferent
families of pond snails (delgado et al. 2012, vallejo et al. 2014),
or between diferent sea slugs (newcomb et al. 2006, Gunaratne
et al. 2014). Sakharov (1976, 1990) was early in discussing such
putative neuronal homologies more broadly within the gastro-
pods, and immunocytochemistry now permits a rapid visualiza-
tion of the size, position, morphology, and transmitter content
of individual neurons, and thus ofers an important character
set for the evaluation of homologies (croll 1987b, newcomb
et al. 2006; Gunaratne et al. 2014). For example, c1 neurons are
found in most Heterobranchia and can be readily distinguished
from other neurons within the brain in terms of the relative
size and position of their somata and their axonal projections
to the buccal ganglia and muscles, and also in terms of their
serotonergic nature (Weiss and Kupfermann 1976, Pentreath
et al. 1982, croll 1987b). Other putatively homologous neurons
were irst recognized, not only in terms of their size and posi-
tion, but also their characteristic activity. he single peptidergic
R15 cell in Aplysia ires action potentials in a regular pattern of
bursts (Adams and Benson 1985). Panpulmonata appear to con-
tain, rather than a single cell, a bilateral pair of neurons (one of
which shows comparable anatomical features to R15) with simi-
lar bursting activity (Gainer 1972, chase and Goodman 1977)
and which express homologous peptides (Kerkhoven et al. 1991,
1992). Another group of ive serotonergic cells found posteriorly
on the dorsal surface of the cerebral ganglia has also been studied
as an example of homology. Similar cells have been reported in
Panpulmonata (croll 1988, croll and chiasson 1989, delgado
et al. 2012) and widely in nudipleura (newcomb et al. 2006).
In fact, very similar cells have also been reported as one of the
few instances of identiied individual neurons found in adult
caenogastropoda (croll and lo 1986). he functions of these
cells have been examined most thoroughly in nudipleura and
related Heterobanchia (newcomb et al. 2012), and at least some
of the members of the cluster appear to control locomotion and/
or muscular and ciliary activity on the foot. he subgroup of
dSI cells of Tritonia are especially well studied in this regard
and have long been known to be part of the cPG for escape
swimming (newcomb and Katz 2007a). diferent members of
this cluster are involved in other defensive behaviours (Mackey
et al. 1989).
Another particularly noteworthy and informative set of puta-
tively homologous cells involves the RPed1 and lPed1 neu-
rons of pond snails. hese cells are larger than their neighbours,
reside in similar positions along the posterior margin of the
pedal ganglia, and have roughly mirror image axonal projections
into the ipsilateral, pleural, and parietal ganglia. While these
207
Fig. 20.6. Early neuros appearance in gastropod larvae. A: diferent stages
of development in freshwater pond snail Lymnaea stagnalis: from fertilized
egg within egg mass until hatching of adult-like juvenile. (B–E) Photographs
and diagrams of early posterior FMRFamide-immunoreactive neurons (pio-
neer) in L. stagnalis. Axons of posterior cells establish a scafold upon which
the central neurons appear at later stages. (F, G) Early posterior FMRamide-
immunoreactive neurons in Aplysia and Tritonia trochophore larvae. All
these cells have axons projecting anteriorly to the developing apical organ.
(H, I) diagram of changing position by posterior (pioneer) FMRFamide-
immunoreactive neurons from trochophore to veliger stage in Aplysia. (J–M)
Serotonin-immunoreactive apical neurons in Helisoma trivolvis. K: Each apical
208
serotonin-immunoreactive neuron has a long axon and small dendrite bearing
short sensory cilia. Front L: and side M: view on axons from serotonin-immu-
noreactive apical neurons projecting to the foot locomotor ciliary band at early
veliger stage. Serotonin-immunoreactive varicose ramiications of apical cell
long axon underneath the foot cilia. N: diagram of serotonin-immunoreactive
apical neurons in H. trivolvis. cG: cerebral ganglion; BG: buccal ganglion;
PeG: pedal ganglion; RPaG: right parietal ganglion; vG: visceral ganglion; cc:
cerebral commissures; Photograph in F was made by Roger croll and Elena
voronezhskaya, while others were taken by Elena voronezhskaya and leonid
nezlin. Schematic diagrams adapted from voronezhskaya and Elekes 1996,
dickinson et al. 2000, voronezhskaya et al. 2008.

cells thus appear to be bilaterally symmetric in many regards,
they difer in transmitter phenotype. In the dextral snail
Lymnaea, the left lPed1 is serotonergic and the right RPed1 is
dopaminergic (cottrell et al. 1979, lapainis et al. 2007). In sin-
istral species like Helisoma and Biomphalaria (Fig. 20.5A), the
lPed1 is dopaminergic and RPed1 is serotonergic (delgado
et al. 2012, vallejo et al. 2014). hus, while the several examples
given above suggest that the transmitter phenotype of identiied
neurons is well conserved, these cells provide an example where
contralateral cells within a single species may have switched
transmitter phenotypes. Interestingly, comparable, asymmet-
ric serotonergic cells have also been reported in the left pedal
ganglia of land snails, and more broadly in Heterobranchia;
occasionally a large unpaired catecholamine-containing cell has
been reported in a corresponding position of the right pedal
ganglia, but at other times, no obvious comparable neuron has
been found on the right side (croll 1987a, 1988, newcomb
et al. 2006). Further study of these cells is likely to be particu-
larly illuminating regarding how and why diferent features of
neurons change with the evolution of new behaviours and phys-
iological mechanisms.
As will be discussed below, strikingly similar neurons are
found in the apical organs of the larvae from across the gastro-
pods, and into the bivalves as well. hese putatively homologous,
individual neurons thus appear to have been conserved for over
half a billion years of evolution. Presumably, their conservation
within the larval nervous system is because of equally conserved
functions, such as the neural control of the ciliary bands as well
as neuro-hormonal control of axonal navigation and develop-
mental tempo (see below), which is probably an ancestral feature
of Mollusca, and more broadly lophotrochozoa.
nERvOUS SyStEM
dEvElOPMEnt
Gastropod development is characterized by a complex life
cycle which begins with (1) the internal or external fertilization
(depending on species) of the egg and then proceeds through (2)
embryonic and/or larval phases of development, (3) metamor-
phosis (observed in most marine species, while often modiied in
terrestrial and freshwater species), (4) growth, which can increase
total body size by several orders of magnitude, and inally (5)
courtship, mating, and production of the next cycle of eggs.
Gastropods, like many other molluscs, typically exhibit
two distinct stages of larval development, as trochophores and
veligers, although there are large variations in the timing of
when they irst become free-living and feeding organisms. For
example, broadcast spawners, like abalone, hatch as free swim-
ming trochophores within hours of fertilization, transform
into veligers (feeding or non-feeding in diferent species), and
then settle and metamorphose into juveniles within a few days
of life (Sawatpeera et  al.  2001). At the other end of the spec-
trum, Panpulmonata typically develop through trochophore
and veliger stages while encapsulated, and only later hatch as
postmetamorphic juvenile snails Morrill (1982), Mescheriakov
(1990) (Fig. 20.6A). Many other gastropods adopt intermediate
M O l l U S c A : G A S t RO P O d A
modes of development by hatching as early veligers, but may live
planktonically for several weeks before metamorphosis. In spite
of these variations in ontogeny, it is during the early larval stages
that the irst neural elements appear in gastropods.
he apical organ with its receptor cells, interneurons, and
characteristic tuft of cilia irst appears at the anterior extreme
of the larvae, shortly after gastrulation. typically, three
serotonin-containing, lask-shaped receptor cells irst appear as
the larvae enter the trochophore stage (croll et al. 1997, Kempf
et al. 1997, Marois and carew 1997a, b, Page and Parries 2000)
(Fig. 20.6.G, K, n, and Fig. 20.7). Basal axons from these cells
contribute to the neuropil of the apical organ. Many gastropods
have additional lask-shaped cells which contain catecholamines,
neuropeptides, and nitric oxide syntase (Kempf et  al.  1992,
croll and voronezhskaya 1996, voronezhskaya et  al.  1999,
dickinson and croll 2003, voronezhskaya and Elekes 2003,
croll 2006, Hens et al. 2006). At later stages of development,
serotonin-containing neurites, which appear to have origin-
ated from apical cells, have been reported in close proximity to
ciliated cells of the velum or foot (voronezhskaya and Elekes
1993, croll et  al.  1997, Marois and carew 1997c, dickinson
and croll 2003, croll, 2006)(Fig. 20.6 l, M). Apical neurons
appear to coordinate ciliary activity for swimming and feeding at
early larval stages (diefenbach et al. 1991, Page 2002, Braubach
et al. 2006).
In addition to their efector roles, the apical neurons also sense
abiotic stimuli, such as oxygen concentration or temperature, or
biotic stimuli, such as chemical signals emitted from conspeciic
juveniles and adults or potential food. For example, serotonergic
Fig.  20.7. Schemes of early neuronal development in Gastropoda. A:
Highly simplified scheme of central ganglia appearance along the scafold-
ing made by axons of pioneer neurons (Figure adapted from voronezhskaya
et al. 2002). B: Rudiments of the ganglia are derived from speciic epithelial
proliferative zones (stippled regions) (Figure adapted from Raven 1966).
Generally the central ganglia are formed in the anterior-to-posterior direc-
tion, starting from the cerebral ganglia (red) and followed by pedal (blue)
and visceral loop (green) ganglia.
209
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
and dopaminergic apical cells of freshwater snails (Helisoma and
Lymnaea) function as sensory-motor neurons increasing loco-
motor rotation of the larvae in response to hypoxia. Such behav-
iour is necessary for mixing the egg capsule luid and enhancing
delivery of environmental oxygen to the embryo (Marois and
croll 1991, Kuang et  al.  2002, Goldberg et  al.  2008). It has
also been found that adult gastropods can modulate the devel-
opmental timing of their progeny, and apical neurons appear
to provide a link between environmental signals and this devel-
opmental regulation (voronezhskaya et al. 2004, 2008; Glebov
et al. 2014).
At later stages, when larvae became competent to undergo
metamorphosis, the apical organ has a critical function in the
detection of environmental signals leading to metamorphic
transition (Hirata and Hadield 1986, couper and leise 1996,
Froggett and leise 1999, Hadield et al. 2000, leise and Hadield
2000, Hens et  al.  2006). Apical cilia contain membrane-
associated sensory system for inductive cues (Baxter and Morse
1992). Interestingly, the receptors and transducers controlling
settlement and metamorphosis in marine invertebrate larvae
appear to be closely related to components controlling neuronal
activity, cellular proliferation, and diferentiation in mammals.
various neuroactive substances such as serotonin, GABA, and
nO act separately or in combination to initiate metamorphic
changes. he physiological and molecular mechanisms of these
processes are, however, still the subject of speculation.
A second group of neurons that are immunoreactive for the
peptide FMRFamide appears in the early trochophore larvae of
gastropods (Fig. 20.6B-I). he somata of these cells are usually
located posteriorly in the larvae and neurites project anteriorly
to the apical organ (croll and voronezhskaya 1996, dickinson
et  al.  1999, 2000, dickinson and croll 2003). he extensive
scafolding laid down by the neurites of these posterior cells,
and the fact that processes of many cells that diferentiate later
follow those early neurites suggest that the early peptidergic
neurons pioneer pathways upon which the adult nervous sys-
tem subsequently develops (croll and voronezhskaya 1996,
voronezhskaya and Elekes 1996, 2003, voronezhskaya and
Ivashkin 2010) (Fig.  20.7). he mechanisms underlying the
pathfinding by the posterior peptidergic cells and how they
might determine the structure of the later central nervous sys-
tem of gastropods, however, need experimental examination.
Similar peptigergic cells have now been found in a variety of
molluscan species and the pathways of their neurites exhibit
torsion, chiastoneury, and detorsion during development,
thus providing visualization of the ontogenetic and phyloge-
netic history of the group (voronezhskaya and Elekes 2003).
he anatomy of the posterior neurons also suggests that they
may function to coordinate activity at the anterior and poste-
rior ends of the larvae. Another possible role of such neurons
could be to innervate larval muscles (Page  1997a, Wanninger
et al. 1999, dyachuk and Odintsova 2009, Evans et al. 2009)
and bath applications of FMRFamide increased the frequency
of contractions of muscles in the velum (Braubach et al. 2006).
during subsequent development posterior peptigergic neurons
do not appear to join the ganglia that later form the adult central
nervous system. Instead, they cease to express immunoreactivity
210
after hatching, and likely disappear altogether (voronezhskaya
and Elekes 1996, 2003).
A inal category of neurons, which develop very early in gastro-
pod ontogeny, includes catecholamine- and peptide-containing
cells, most of which are bipolar, with what appear to be a short
dendrite penetrating the overlying epithelium and an axon exit-
ing the basal surface of the soma. he morphology of these cells
thus suggest that they are receptor neurons and their cluster-
ing, particularly of the catecholamine-containing cells, around
the mouth and along the ciliary bands on the velum, suggest
involvement in control of diferent aspects of feeding and pos-
sibly locomotion (croll et al. 1997, voronezhskaya et al. 1999,
dickinson et al. 2000, croll et al. 2001a, dickinson and croll
2003, voronezhskaya and Elekes 2003, Braubach et al. 2006).
he mid-larval stage marks the appearance of nervous struc-
tures that persist into adulthood. he above mentioned receptor
neurons are joined by large numbers of catecholamine-containing
cells located on the tentacles, anterior margin of the growing
foot, and mantle edge. he eyes also appear at this time and the
axons from these sensory structures project to the newly forming
central ganglia (voronezhskaya et  al.  1999; voronezhskaya and
Elekes 2003; dickinson and croll 2003). new sets of retractor
muscles also form and presumably receive innervation from the
central ganglia. Several previous investigations have focused on
the development of these ganglia to understand the origins of the
identiiable neurons of the adult central nervous system described
above. Such studies used electron microscopy and radioactive
birth-dating techniques (Schacher et al. 1979, Kandel et al. 1981,
Jacob 1984) to conirm previous work (Raven 1966), indicating
that the rudiments of the ganglia are derived by invagination and/
or delamination from speciic proliferative zones in the body wall.
After the initial rudiments of the ganglia separate from the prolif-
erative zones, these zones continue to generate inwardly migrat-
ing, post-mitotic neurons (McAllister et al. 1983). Generally the
ganglia develop in an anterior-to-posterior direction starting from
the cerebral ganglia, followed by the pedal and visceral loop gan-
glia. he inal diferentiation of neurons appears to occur within
the ganglia and their outward growing axons form the intercon-
necting commissures and connectives (Kriegstein 1977). he
mechanisms of how migrating progenitors ind their appropri-
ate positions in the ganglionic anlagen and further diferentiate
remain unknown.
he mid and late larval periods thus represent a time when
both the early larval nervous system and the later developing
adult nervous system coexist. A generally accepted point of view
is that mid-larval life marks a time when the early larval and
the developing adult nervous systems cooperate to produce the
integrated, inal output upon which the organism depends for
survival (croll 2009). However, it has also recently been sug-
gested (voronezhskaya and Ivashkin 2010) that larval behaviour
may primarily be under neuro-hormonal control from the larval
nervous system, while the circuits of the central pattern gen-
erators are maturing quiescently within the developing central
ganglia. After they mature during late larval stages, these cir-
cuits can rapidly activate at the time of metamorphosis to drive
juvenile and adult behaviours. According to this hypothesis the
switch from the overall neuro-hormonal control of development

and behaviour to the more precise neuronal control via circuits
of the central pattern generators happens during metamorphosis.
during metamorphosis, the bands of cilia used for larval
feeding and planktonic locomotion, and the neurons that
innervate them, are lost as the juvenile and adult gastropod
typically assumes a benthic lifestyle. he posterior peptidergic
neurons and the apical organ both disappear during or soon
after metamorphosis (voronezhskaya and Elekes 1993, croll
and voronezhskaya 1996, lin and leise 1996, voronezhskaya
and Elekes 1996, Marois and carew 1997b, dickinson and
croll 2003), apparently via programmed cell death (Marois and
carew 1997b, voronezhskaya and Elekes 2003, Gifondorwa
and leise 2006). However, metamorphosis involves not only
the loss of neurons and their targets, but also the gain of other
neurons, and structures such as the buccal muscles and gan-
glia that are used for feeding in adult gastropods (Balog at
al., 2012). Finally, in addition to dramatic losses and gains
of entire organs and their innervation, metamorphosis also
involves numerous changes in the forms and functions of
other organs. he foot, for example, initially functions largely
as an anchor for the operculum and the insertion point for
retractor muscles. With the completion of metamorphosis, the
foot also becomes the primary organ for locomotion in gastro-
pods. hese modiications must be accompanied, not only by
changes to its innervation, but also by activation of central cir-
cuitry used to integrate developing sensory inputs and generate
novel motor outputs.
A particularly noteworthy aspect of neural development in
molluscs involves their dramatic postlarval growth. Gastropod
veligers typically measure less than 1 mm as they approach
metamorphosis, and yet as noted earlier in this chapter, the
adults can attain large body sizes. Obviously, the nervous sys-
tem must change to accommodate such large variations in
body size. Gastropods that possess large, identiiable neuronal
somata appear to have a nearly full complement of such cells
early in their juvenile phase, but these neurons grow dispro-
portionately in size to become increasingly diferentiated from
neighbouring somata (Arvanitaki and tchou 1942, croll and
chiasson 1989). he large size of these neurons presumably
supports the metabolic machinery necessary for the larger
and longer axons that must innervate expanding target ields
(Gillette 1991). In addition, the nervous systems of gastro-
pods also possess clusters of smaller neurons which grow
more modestly during development, but which also increase
in numbers (croll and chiasson 1989). he degree to which
changes in neuronal size and cell number contribute to the
growth of the nervous system of gastropods, which lie out-
side the Heterobranchia and do not possess giant identiiable
neurons, is currently unknown. Additionally, the post-larval
nervous system must not only increase in size to accommo-
date growing target tissues, but as the gastropod reaches sex-
ual maturity, new organs appear and new behaviours must be
generated, often with the addition of new neurons (McAllister
et  al.  1983, croll and chiasson 1989; voronezhskaya and
Elekes, 1996). he gastropod is thus prepared to initiate the
courtship, mating, and producing of gametes which mark the
commencement of a new cycle of life.
M O l l U S c A : G A S t RO P O d A
SUMMARy And cOnclUSIOnS
Gastropods are familiar to most readers as common snails and
slugs, found in a wide variety of aquatic and terrestrial niches
around the world. he central nervous systems of these animals
consist of a set of about 8–12 ganglia linked by connectives and
commissures. While most of the ganglia are paired bilaterally,
they can show a large degree of asymmetry and the intercon-
necting pathways can appear twisted due to a process known
as torsion, which occurs early in larval development. diferent
ganglia also fuse with the varying degrees of cephalization that
can be observed across the gastropods. hus, the positions and
morphologies of the ganglia relect both the evolutionary his-
tory and the particular lifestyle of each member of this extremely
diverse group of animals. Furthermore, in addition to their
complex central nervous systems, gastropods also have extensive
peripheral nervous systems that appear to contain many more
neurons than the central ganglia. hese cells include an array
of receptor neurons in the various organs of the body, but also
appear to mediate motor functions underlying local relexes and
coordinated muscular contractions of diferent organs.
A major force shaping the history of scientiic investigations
of the gastropod nervous system came from the recognition
that some of these animals possessed giant neurons that can
be identiied from specimen to specimen; individual neurons
and members of neuronal clusters are characterized by their
locations within ganglia, axonal morphologies, neurotransmit-
ter contents, and physiological properties. In addition, because
individual neurons also form consistent patterns of synaptic
interactions with other individual neurons, gastropods have
also been used widely in attempts to understand how details of
neural circuitry explain diferent aspects of behaviour, learning,
and memory at a level of resolution that is unapproachable in
the intact brain of vertebrates. Moreover, since such neurons
appear to have homologues within genera, orders, or even more
broadly within the phylum, gastropods have presented oppor-
tunities for studying the evolution of the nervous system and
behaviour at the level of individual neurons. Such special char-
acteristics of the nervous systems of gastropods have allowed
certain species to become ‘model organisms’, used to advance
our understanding of fundamental principles of neuroscience.
However, these species represent only a single phylogenetic
branch. Further studies are needed to understand the adaptive
radiation of the nervous system within the extremely diverse
Gastropoda.
Gastropods, like many other molluscs, generally transition
through trochophore and veliger larval stages before meta-
morphosis to the juvenile and adult stages. here are, however,
large variations among species in the time until the larvae irst
become free-living and feeding organisms. he irst neural elem-
ents appear in gastropods during the early larval stages and they
include: neurons of the apical organ, early posterior, peptide-
containing neurons that appear to pioneer later neural pathways,
peripheral receptor neurons, and neurons within rudiments of
adult ganglia.
Because of their ready availability and special advantages for
neurophysiology (e.g. giant, electrically active, and identiiable
211
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
somata), gastropods have been exploited widely in the quest to
understand basic principles of neuroscience. hey have, in turn,
also become one of the best studied animal groups in terms of
the anatomy, physiology, and biochemistry of their nervous sys-
tems. nor have those advantages become obsolete. For example,
large cell size also lends favour to these animals for the analysis
of single cell transcriptomes as a promising future direction of
research (Moroz et  al.  2006). But in the theme of this book,
the gastropods also ofer perhaps their greatest advantage. hey
provide a solid base of knowledge about the form, function, and
development of the nervous systems from a strongly lophotro-
chozoan perspective. Furthermore, as a particularly diverse and
species-rich group, they also ofer the opportunity to ask how the
nervous system evolves to serve the wide range of body morph-
ologies and behaviours characteristic of this taxon.
A c K n OW l E d G E M E n t S
We wish to express great appreciation to leonid nezlin, Pavel
Erokhov, Alexander Semenov, and Mohamed Habib for use of
their photographs in the igures for this chapter and to Olga
Kharchenko for the art drawings and schematic diagrams. EEv
would like to thank the Russian Foundation for Basic Research for
their permanent inancial support of her work with invertebrates.
REFEREncES
Adams, W.B. and Benson, J.A. (1985). he generation and modula-
tion of endogenous rhythmicity in the Aplysia bursting pacemaker
neurone R15. Progress in Biophysics and Molecular Biology, 46, 1–49.
Alkon, d.l., Anderson, M.J., Kuzirian, A.J., et  al. (1993). GABA-
mediated synaptic interaction between the visual and vestibular
pathways of Hermissenda. Journal of Neurochemistry, 61, 556–566.
Appeltans, W., Bouchet, P., Boxshall, G.A., et  al. (eds.)(2010). World
Register of Marine Species. Accessed at <http://www.marinespecies.org>.
Arshavsky, y.I., Beloozerova, I., Orlovsky, G., Panchin, y.v., and
Pavlova, G. (1985a). control of locomotion in marine mollusc
Clione limacina I. Eferent activity during actual and ictitious swim-
ming. Experimental Brain Research, 58, 255–262.
Arshavsky, y.I., Beloozerova, I., Orlovsky, G., Panchin, y.v., and
Pavlova, G. (1985b). control of locomotion in marine mollusc
Clione limacina II. Rhythmic neurons of pedal ganglia. Experimental
Brain Research, 58, 263–272.
Arshavsky, y.I., deliagina, t.G., Gamkrelidze, G.n., et  al. (1993).
Pharmacologically induced elements of the hunting and feeding
behavior in the pteropod mollusk Clione limacina. I. Efects of
GABA. Journal of Neurophysiology, 69, 512–521.
Arvanitaki, A. and chalazonitis, n. (1949). Prototypes d’interactions
neuronique et transmissions synaptiques: donnees bioelectriques de
preparations cellulaires. Archives des Sciences Physiologiques (Paris),
3, 547–565.
Arvanitaki, A. and chalazonitis, n. (1955). Potentiels d’activite du
soma neuronique geant (Aplysia). Archives des Sciences Physiologiques
(Paris), 9, 115–144.
Arvanitaki, A. and chalazonitis, n. (1956). Activations du soma geant
d’Aplysia par voie orthodrome et par voie antidrome; derivation
endocytaire. Archives des Sciences Physiologiques (Paris), 10, 95–128.
Arvanitaki, A. and chalazonitis, n. (1964). Processus d’excitaion d’un
neurone autoactif sur ondes lentes. Comptes rendus des séances de la
Société de biologie et de ses iliales, 158, 1119–1122.
212
Arvanitaki, A. and tchou, S.H. (1942). les lois de la croissance relative
individuelle des cellules nerveuves chez l’aplysie. Bulletin d’histologie
appliquée à la physiologie et à la pathologie et de technique micro-
scopique, 19, 244–256.
Audesirk, G., Mccaman, R.E., and Willows, A.O.d. (1979). he
role of serotonin in the control of pedal ciliary activity by identi-
ied neurons in Tritonia diomedea. Comparative Biochemistry and
Physiology, 62, 87–91.
Bai, l., livnat, I., Romanova, E.v., et al. (2013). characterization of
GdFFd, a d-amino acid-containing neuropeptide that functions
as an extrinsic modulator of the Aplysia feeding circuit. Journal of
Biological Chemistry, 288, 32837–32851.
Bailey, c.H. and chen, M. (1983). Morphological basis of long-term
habituation and sensitization in Aplysia. Science, 220, 91–93.
Bailey, c.H., chen, M.c., Weiss, K.R., and Kupfermann, I. (1982).
Ultrastructure of a histaminergic synapses in Aplysia. Brain Research,
238, 205–210.
Bailey, c.H., hompson, E.B., castellucci, v.F., and Kandel, E.R.
(1979). Ultrastructure of the synapses of sensory neurons that medi-
ate the gill-withdrawal relex in Aplysia. Journal of Neurocytology, 8,
415–444.
Balog, G., voronezhskaya, E.E., Hiripi, l., and Elekes, K. (2012)
Organization of the serotonergic innervation of the feeding (buccal)
musculature during the maturation of the pond snail Lymnaea stag-
nalis: a morphological and biochemical study. Journal of Comparative
Neurology, 520(2), 315–329.
Baltzley, M.J., Sherman, A., cain, S.d., and lohmann, K.J. (2011).
conservation of a Tritonia Pedal peptides network in gastropods.
Invertebrate Biology, 130, 313–324.
Barker, G.M. (2001). he Biology of Terrestrial Molluscs. cABI
Publishing, new york.
Baxter, G.t. and Morse, d.E. (1992). cilia from abalone larvae contain
a receptor-dependent G-protein transduction system similar to that
in mammals. Biological Bulletin, 183, 147–154.
Beck, J.c., cooper, M.S., and Willows, A.O. (2000).
Immunocytochemical localization of pedal peptide in the central
nervous system of the gastropod mollusc Tritonia diomedea. Journal
of Comparative Neurology, 425, 1–9.
Beklemishev, W.n. (1969). Principles of Comparative Anatomy of
Invertebrates. University of chicago, chicago.
Benjamin, P. (2008). Lymnaea. Scholarpedia, 3, 4124.
Benjamin, P.R. (2012). distributed network organization underlying
feeding behavior in the mollusk Lymnaea. Neural Systems and
Circuits, 2, 4.
Benjamin, P. and Rose, R. (1979). central generation of bursting
in the feeding system of the snail, Lymnaea stagnalis. Journal of
Experimental Biology, 80, 93–118.
Benjamin, P. and Winlow, W. (1981). he distribution of three wide-
acting synaptic inputs to identiied neurons in the isolated brain
of Lymnaea stagnalis (l.). Comparative Biochemistry and Physiology,
70A, 293–307.
Berry, M.S. and cottrell, G.A. (1973). dopamine—excitatory and
inhibitory transmission from a giant dopamine neuron. Nature-
News Biology, 242, 250–253.
Blankenship, J.E. and coggeshall, R.E. (1976). he abdominal gan-
glion of Aplysia brasiliana: a comparative morphological and elec-
trophysiological study, with notes on A. dactylomela. Journal of
Neurobiology, 7, 383–405.
Boer, H.H., Groot, c., de Jong Brink, M., and cornelisse, c.J. (1977).
Polyploidy in freshwater snail Lymnaea stagnalis (Gastropoda,
Pulmonata)—cytophotometric analysis of dnA in neurons and
some other cell-types. Netherlands Journal of Zoology, 27, 245–252.

Bogerd, J., van Kesteren, R.E., van Heerikhuizen, H., et al. (1993).
Alternative splicing generates diversity of vd1/RPd2 alpha pep-
tides in the central nervous system of Lymnaea stagnalis. Cell and
Molecular Neurobiology, 13, 123–136.
Bonga, S.E.W. (1970). Ultrastructure and histochemistry of neurose-
cretory cells and neurohaemal areas in the pond snail Lymnaea stag-
nalis (l.). Zeitschrift für Zellforschung und mikroskopische Anatomie,
108, 190–224.
Bouchet, P., Rocroi, J.P., Fryda, J., et al. (2005). classiication and
nomenclator of gastropod families. Malacologia, 47, 1–368.
Bouvier, E.l. (1887). Systeme nerveux des prosobranches. Annales des
Sciences Naturelles-Zoologie et Biologie Animale, 3, 1–510.
Braubach, O.R. and croll, R.P. (2004). Evidence that histamine acts as
a neurotransmitter in tatocyst hair cells in the snail, Lymnaea stagna-
lis. Journal of Gravitational Physiology, 11, 57–66.
Braubach, O.R., dickinson, A.J., Evans, c.c., and croll, R.P. (2006).
neural control of the velum in larvae of the gastropod, Ilyanassa
obsoleta. Journal of Experimental Biology, 209, 4676–4689.
Bravarenko, n.I., Ierusalimsky, v.n., Korshunova, t.A., Malyshev,
A.y., Zakharov, I.S., and Balaban, P.M. (2001). Participation of
GABA in establishing behavioral hierarchies in the terrestrial snail.
Experimental Brain Research, 141, 340–348.
Bravarenko, n.I., Korshunova, t.A., Malyshev, A.y., and Balaban,
P.M. (2003). Synaptic contact between mechanosensory neu-
ron and withdrawal interneuron in terrestrial snail is mediated by
l-glutamate-like transmitter. Neuroscience Letters, 341, 237–240.
Brierley, M.J., yeoman, M.S., and Benjamin, P.R. (1997). Glutamate
is the transmitter for n2v retraction phase interneurons of the
Lymnaea feeding system. Journal of Neurophysiology, 78, 3408–3414.
Brunet, J.F., Shapiro, E., Foster, S.A., Kandel, E.R., and Iino, y. (1991).
Identiication of a peptide speciic for Aplysia sensory neurons by
PcR-based diferential screening. Science, 252, 856–859.
Brusca, R. and Brusca, G. (2003). Invertebrates. Sinauer Associates,
Inc., Sunderland.
Buckett, K., Peters, M., and Benjamin, P. (1990). Excitation and inhib-
ition of the heart of the snail, Lymnaea, by non-FMRFamidergic
motoneurons. Journal of Neurophysiology, 63, 1436–1447.
Bullock, t.H. and Horridge, G.A. (1965). Structure and Function in
the Nervous Systems of Invertebrates. W.H. Freeman and company,
San Francisco.
Buresi, A., croll, R.P., tiozzo, S., Bonnaud, l., and Baratte, S. (2014).
Emergence of sensory structures in the developing epidermis in Sepia
oicinalis and other coleoid cephalopods. Journal of Comparative
Neurology, 522, 3004–19.
Bütschli, O. (1912). Vorlesungen über vergleichende Anatomie.
Allgemeine Körper- und Bewegungsmuskulatur; elekrische Organe und
Nervensystem. Springer, Berlin.
cajal, S.R.y. (1967). he structure and connexions of neurons. Nobel
Lectures, Physiology or Medicine 1901–1921. Elsevier Amsterdam.
cardone, B. and Roots, B.I. (1990). comparative immunohistochemi-
cal study of glial ilament proteins (glial ibrillary acidic protein and
vimentin) in goldish, octopus, and snail. Glia, 3, 180–192.
carew, t.J., castellucci, v.F., Byrne, J.H., and Kandel, E.R. (1979).
Quantitative analysis of relative contribution of central and periph-
eral neurons to gill-withdrawal relex in Aplysia californica. Journal
of Neurophysiology, 42, 497–509.
carpenter, d.O., Kemenes, G., Elekes, K., et al. (1995). Opioid peptides
in the nervous system of Aplysia: a combined biochemical, immuno-
cytochemical, and electrophysiological study. Cellular and Molecular
Neurobiology, 15, 239–256.
carroll, M.A. and catapane, E.J. (2007). he nervous system con-
trol of lateral ciliary activity of the gill of the bivalve mollusc,
M O l l U S c A : G A S t RO P O d A
Crassostrea virginica. Comparative Biochemistry and Physiology,
148A, 445–450.
chase, R. (2000). Structure and function in the cerebral ganglion.
Microscopy Research and Technique, 49, 511–520.
chase, R. and Goodman, H.E. (1977). Homologous neurosecretory
cell groups in the land snail Achatina fulica and the sea slug Aplysia
californica. Cell & Tissue Research, 176, 109–120.
chase, R. and tolloczko, B. (1987). Evidence for diferential dnA
endoreplication during the development of a molluscan brain.
Journal of Neurobiology, 18, 395–406.
chiel, H.J., Kupfermann, I., and Weiss, K.R. (1988). An identiied
histaminergic neuron can modulate the outputs of buccal-cerebral
interneurons in Aplysia via presynaptic inhibition. Journal of
Neuroscience, 8, 49–63.
chiel, H.J., Weiss, K.R., and Kupfermann, I. (1986). An identiied
histaminergic neuron modulates feeding motor circuitry in Aplysia.
Journal of Neuroscience, 6, 2427–2450.
chiel, H.J., Weiss, K.R., and Kupfermann, I. (1990). Multiple roles of
a histaminergic aferent neuron in the feeding behavior of Aplysia.
Trends in Neuroscience, 13, 223–227.
church, P.J. and lloyd, P.E. (1991). Expression of diverse neuropep-
tide cotransmitters by identiied motor neurons in Aplysia. Journal
of Neuroscience, 11, 618–625.
coggeshall, R. (1967). A light and electron microscope study of the
abdominal ganglion of Aplysia californica. Journal of Neurophysiology,
30, 1263–1287.
collado, M.S., Khabour, O., Fioravante, d., Byrne, J.H., and Eskin, A.
(2009). Post-translational regulation of an Aplysia glutamate trans-
porter during long-term facilitation. Journal of Neurochemistry, 108,
176–189.
cooke, I.R., Edwards, S.l., and Anderson, c.R. (1994). he distribu-
tion of nAdPH diaphorase activity and immunoreactivity to nitric
oxide synthase in the nervous system of the pulmonate mollusc
Helix aspersa. Cell & Tissue Research, 277, 565–572.
cooke, I.R. and Gelperin, A. (1988). distribution of GABA-like
immunoreactive neurons in the slug Limax maximus. Cell & Tissue
Research, 253, 77–81.
cottrell, G., Abernathy, K., and Barrand, M. (1979). large amine-
containing neurones in the central ganglia of Lymnaea stagnalis.
Neuroscience, 4, 685–689.
couper, J.M. and leise, E.M. (1996). Serotonin injections induce
metamorphosis in larvae of the gastropod mollusc Ilyanassa obsoleta.
Biological Bulletin, 191, 178–186.
croll, R.P. (1987a). distribution of monoamines in the central nervous
system of the nudibranch gastropod Hermissenda crassicornis. Brain
Research, 405, 337–347.
croll, R.P. (1987b). Identiied neurons and cellular homologies. In
M.A. Ali, ed. Nervous Systems in Invertebrates. Plenum Press, new
york.
croll, R.P. (1988). distribution of monoamines within the central nerv-
ous system of the pulmonate snail Achatina fulica. Brain Research,
460, 29–49.
croll, R.P. (2001). catecholamine-containing cells in the central
nervous system and periphery of Aplysia californica. Journal of
Comparative Neurology, 441, 91–105.
croll, R.P. (2003). complexities of a simple system: new lessons, old
challenges and peripheral questions for the gill withdrawal relex of
Aplysia. Brain Research Reviews, 43, 266–274.
croll, R.P. (2006). development of embryonic and larval cells contain-
ing serotonin, catecholamines, and FMRFamide-related peptides
in the gastropod mollusc Phestilla sibogae. Biological Bulletin, 211,
232–247.
213
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
croll, R.P. (2009). developing nervous systems in molluscs: navigat-
ing the twists and turns of a complex life cycle. Brain, Behavior &
Evolution, 74, 164–176.
croll, R.P., Boudko, d.y., and Hadield, M.G. (2001a). Histochemical
survey of transmitters in the central ganglia of the gastropod mol-
lusc, Phestilla sibogae. Cell & Tissue Research, 305, 417–432.
croll, R.P. and chiasson, B.J. (1989). Post-embryonic development of
serotonin-like immunoreactivity in the central nervous system of
the snail, Lymnaea stagnalis. Journal of Comparative Neurology, 280,
122–142.
croll, R.P., davis, W.J., and Kovac, M.P. (1985). neural mechanisms of
motor program switching in the mollusc Pleurobranchaea I. central
motor programs underlying ingestion, egestion and the ‘neutral’
rhythm(s). Journal of Neuroscience, 5, 48–55.
croll, R.P., dmitri, y.B., and Hadield, M.G. (2001b). Histochemical
survey of transmitters in the central ganglia of the gastropod mollusc
Phestilla sibogae. Cell & Tissue Research, 305, 417–432.
croll, R.P., Jackson, d.l., and voronezhskaya, E.E. (1997).
catecholamine-containing cells in larval and post-larval bivalve
molluscs. Biological Bulletin, 193, 116–124.
croll, R.P. and lo, R.y.S. (1986). distribution of serotonin-like
immunoreactivity in the central nervous system of the periwinkle,
Littorina littorea (Gastropoda, Prosobranchia, Mesogastropoda).
Biological Bulletin, 171, 426–440.
croll, R.P. and van Minnen, J. (1992). distribution of the neuropep-
tide Ala-Pro-Gly-trp-nH2 (APGWamide) in the nervous system
and periphery of the snail Lymnaea stagnalis as revealed by immuno-
cytochemistry and in situ hybridization. Journal of Comparative
Neurology, 324, 567–574.
croll, R.P. and voronezhskaya, E.E. (1996). Early elements in gastro-
pod neurogenesis. Developmental Biology, 173, 344–347.
croll, R.P., voronezhskaya, E.E., Hiripi, l., and Elekes, K. (1999).
development of catecholaminergic neurons in the pond snail,
Lymnaea stagnalis II: postembryonic development of central and
peripheral cells. Journal of Comparative Neurology, 404, 297–309.
cummins, S.F., tollenaere, A., degnan, B.M., and croll, R.P. (2011).
Molecular analysis of two FMRFamide-encoding transcripts
expressed during the development of the tropical abalone Haliotis
asinina. Journal of Comparative Neurology, 519, 2043–2059.
dale, n. and Kandel, E.R. (1993). l-glutamate may be the fast exci-
tatory transmitter of Aplysia sensory neurons. Proceedings of the
National Academy of Sciences USA, 90, 7163–7167.
deBoer, P.c.M., Jansen, R., Pieneman, A.W., croll, R.P., and ter
Maat, A. (1997). Functional role of right anterior lobe cerebral
neurons in the reproductive behavior of Lymnaea stagnalis. Journal
of Neurophysiology, 78, 2823–2833.
de lange, R.P., de Boer, P.A., ter Maat, A., tensen, c.P., and van
Minnen, J. (1998). transmitter identiication in neurons involved
in male copulation behavior in Lymnaea stagnalis. Journal of
Comparative Neurology, 395, 440–449.
delgado, n., vallejo, d., and Miller, M.W. (2012). localization of
serotonin in the nervous system of Biomphalaria glabrata, an inter-
mediate host for schistosomiasis. Journal of Comparative Neurology,
520, 3236–3255.
d’ Este, l., casini, A., Kimura, S., et al. (2011). Immunohistochemical
demonstration of cholinergic structures in central ganglia of the slug
(Limax maximus, Limax valentianus). Neurochemistry International,
58, 605–611.
diaz-Rios, M., Oyola, E., and Miller, M.W. (2002). colocalization
of gamma-aminobutyric acid-like immunoreactivity and catecho-
lamines in the feeding network of Aplysia californica. Journal of
Comparative Neurology, 445, 29–46.
214
diaz-Rios, M., Suess, E., and Miller, M.W. (1999). localization of
GABA-like immunoreactivity in the central nervous system of
Aplysia californica. Journal of Comparative Neurology, 413, 255–270.
dickinson, P. (1980). neuronal control of gills in diverse Aplysia spe-
cies: conservative evolution. Journal of Comparative Physiology, 139,
17–23.
dickinson, A.J.G. and croll, R.P. (2003). development of the lar-
val nervous system of the gastropod Ilyanassa obsoleta. Journal of
Comparative Neurology, 466, 197–218.
dickinson, A.J., croll, R.P., and voronezhskaya, E.E. (2000).
development of embryonic cells containing serotonin, catechol-
amines, and FMRFamide-related peptides in Aplysia californica.
Biological Bulletin, 199, 305–315.
dickinson, A.J.G., nason, J., and croll, R.P. (1999). Histochemical
localization of FMRFamide, serotonin and catecholamine in
embryonic Crepidula fornicata (Prosobranchia: Gastropoda).
Zoomorphology, 119, 49–62.
diefenbach, t.J., Koehncke, n.K., and Goldberg, J.I. (1991).
characterization and development of rotational behavior in Helisoma
embryos: role of endogenous serotonin. Journal of Neurobiology, 22,
922–934.
dos Santos, P.c., Gottfried, c., Gehlen, G., Goncalves, c.A., and
Achaval, M. (2005a). distribution and ontogeny of glial ibrillary
acidic protein in the snail Megalobulimus abbreviatus. Comparative
Biochemistry and Physiology, 141, 140–145.
dos Santos, P.c., Gottfried, c., Gehlen, G., Goncalves, c.A., and
Achaval, M. (2005b). distribution and ontogeny of glial ibrillary
acidic protein in the snail Megalobulimus abbreviatus. Comparative
Biochemistry and Physiology, 141A, 140–145.
dyachuk, v. and Odintsova, n. (2009). development of the larval
muscle system in the mussel Mytilus trossulus (Mollusca, Bivalvia).
Development, Growth, & Diferentiation, 51, 69–79.
dyakonova, v., carlberg, M., Sakharov, d., and Elofsson, R. (1995).
Anatomical basis for interactions of enkephalins with other trans-
mitters in the cnS of a snail. Journal of Comparative Neurology,
361, 38–47.
Eisenstadt, M.l. and Schwartz, J.H. (1975). Metabolism of acetyl-
choline in the nervous system of Aplysia californica. III. Studies of
an identiied cholinergic neuron. Journal of General Physiology, 65,
293–313.
Elekes, K. (1991). Serotonin-immunoreactive varicosities in the cell
body region and neural sheath of the snail, Helix pomatia, ganglia:
an electron microscopic immunocytochemical study. Neuroscience,
42, 583–591.
Elekes, K., Battonyai, I., Kobayashi, S., and Ito, E. (2013). Organization
of the procerebrum in terrestrial pulmonates reconsidered: cell mass
layer synaptology and its serotonergic input system. Brain Structure
and Function, 218, 477–490.
Elekes, K., Hiripi, l., and Benjamin, P. (1989). A comparison of four
techniques for mapping the distribution of serotonin and serotonin-
containing neurons in ixed and living ganglia of the snail, Lymnaea.
Journal of Neurocytology, 18, 193–208.
Elekes, K., Kiss, t., Fujisawa, y., Hernadi, l., Erdelyi, l., and Muneoka,
y. (2000). Mytilus inhibitory peptides (MIP) in the central and
peripheral nervous system of the pulmonate gastropods, Lymnaea
stagnalis and Helix pomatia: distribution and physiological actions.
Cell & Tissue Research, 302, 115–134.
Elekes, K. and Rosza, K.S. (1984). Synaptic organization of a multi-
functional interneuron in the central nervous system of Helix poma-
tia l. Cell & Tissue Research, 236, 677–683.
Elekes, K. and Ude, J. (1993). An immunogold electron microscopic
analysis of FMRFamide-like immunoreactive neurons in the cnS

of Helix pomatia: ultrastructure and synaptic connections. Journal of
Neurocytology, 22, 1–13.
Elliott, c. and Benjamin, P. (1985). Interactions of pattern-generating
interneurons controlling feeding in Lymnaea stagnalis. Journal of
Neurophysiology, 54, 1396–1411.
Elliott, c.J. and vehovszky, A. (2000). comparative pharmacology of
feeding in molluscs. Acta Biologica Hungarica, 51, 153–163.
Elofsson, R., carlberg, M., Moroz, l., nezlin, l., and Sakharov, d.
(1993). Is nitric oxide (nO) produced by invertebrate neurons?
Neuroreport, 4, 279–282.
Elphick, M.R., Kemenes, G., Staras, K., and O’ Shea, M. (1995).
Behavioral role for nitric oxide in chemosensory activation of feed-
ing in a mollusc. Journal of Neuroscience, 15, 7653–7664.
Elste, A., Koester, J., Shapiro, E., Pertti, P., and Schwartz, J. (1990).
Identiication of histaminergic neurons in Aplysia. Journal of
Neurophysiology, 64, 736–744.
Evans, c.c., dickinson, A.J.G., and croll, R.P. (2009). Major mus-
cle systems in the larval caenogastropod, Ilyanassa obsoleta, display
diferent patterns of development. Journal of Morphology, 270,
1219–1231.
Ewadinger, n.M., Ridgway, R.l., Syed, n.I., lukowiak, K., and
Bulloch, A.G. (1996). Identiication and localization of a [Met5]-
enkephalin-like peptide in the mollusc, Lymnaea stagnalis. Brain
Research, 737, 1–15.
Faller, S., Staubach, S., and Klussmann-Kolb, A. (2008). comparative immu-
nohistochemistry of the cephalic sensory organs in Opisthobranchia
(Mollusca, Gastropoda). Zoomorphology, 127, 227–239.
Fan, X., croll, R.P., Wu, B., et al. (1997). Molecular cloning of a cdnA
encoding the neuropeptides APGWamide and cerebral peptide 1:
localization of APGWamide-like immunoreactivity in the central
nervous system and male reproductive organs of Aplysia. Journal of
Comparative Neurology, 387, 53–62.
Floyd, P.d., li, l., Rubakhin, S.S., et al. (1999). Insulin prohormone
processing, distribution, and relation to metabolism in Aplysia cali-
fornica. Journal of Neuroscience, 19, 7732–7741.
Fong, P.P., noordhuis, R., and Ram, J.l. (1993). dopamine reduces
intensity of serotonin-induced spawning in the zebra mussel,
Dreissena polymorpha (Pallas). Journal of Experimental Zoology, 266,
79–83.
Froggett, S.J. and leise, E.M. (1999). Metamorphosis in the marine
snail Ilyanassa obsoleta, yes or nO? Biological Bulletin, 196, 57–62.
Fujisawa, y., Furukawa, y., Ohta, S., et al. (1999). he Aplysia Mytilus
inhibitory peptide-related peptides: identiication, cloning, pro-
cessing, distribution, and action. Journal of Neuroscience, 19,
9618–9634.
Furness, J.B., costa, M., and Wilson, A.J. (1977). Water-stable luo-
rophores, produced by reaction with aldehyde solutions, for the
histochemical localization of catechol- and indolethylamines.
Histochemistry, 52, 159–170.
Gainer, H. (1972). Electrophysiological behavior of an endogenously
active neurosecretory cell. Brain Research, 39, 403–418.
Gelperin, A. (1994). nitric oxide mediates network oscillations of
olfactory interneurons in a terrestrial mollusc. Nature, 369, 61–63.
Gerschenfeld, H. (1973). chemical transmission in invertebrate central
nervous systems and neuromuscular junctions. Physiological Reviews,
53, 1–119.
Gerschenfeld, H.M. and Stefani, E. (1965). 5-Hydroxytryptamine
receptors and synaptic transmission in molluscan neurones. Nature,
205, 1216–1218.
Gerschenfeld, H. and tauc, l. (1961). Pharmacological speciicities
of neurones in an elementary central nervous system. Nature, 189,
924–925.
M O l l U S c A : G A S t RO P O d A
Getting, P.A. (1983). neural control of swimming in Tritonia. Symposia
of the Society of Experimental Biology, 37, 89–128.
Gifondorwa, d.J. and leise, E.M. (2006). Programmed cell death in
the apical ganglion during larval metamorphosis of the marine mol-
lusc Ilyanassa obsoleta. Biological Bulletin, 210, 109–120.
Gillette, R. (1991) On the signiicance of neuronal giantism in gastro-
pods. Biological Bulletin, 180, 234–240.
Glebov, K., voronezhskaya, E.E., Khabarova, M.y., Ivashkin, E.,
nezlin, l.P., and Ponimaskin, E.G. (2014). Mechanisms underlying
dual efects of serotonin during development of Helisoma trivolvis
(Mollusca). BMC Developmental Biology, 14, 14.
Goldberg, J.I., doran, S.A., Shartau, R.B., et al. (2008). Integrative
biology of an embryonic respiratory behaviour in pond snails: the
‘embryo stir-bar hypothesis’. Journal of Experimental Biology, 211,
1729–1736.
Goldberg, J.I., Garofalo, R., Price, c.J., and chang, J.P. (1993).
Presence and biological activity of a GnRH-like factor in the ner-
vous system of Helisoma trivolvis. Journal of Comparative Neurology,
336, 571–582.
Goldstein, R.S. (1984). Immunocytochemical, histoluorescent and
ultrastructural studies of monoaminergic neurons and their pro-
cesses in Aplysia. Phd hesis, new york, columbia University.
Goldstein, R., Kistler Jr, H., Steinbusch, H., and Schwartz, J. (1984).
distribution of serotonin-immunoreactivity in juvenile Aplysia.
Neuroscience, 11, 535–547.
Goldstein, R.S. and Schwartz, J.H. (1989). catecholamine neurons in
Aplysia: improved light-microscopic resolution and ultrastructural
study using paraformaldehyde and glutaraldehyde (FaGlu) cyto-
chemistry. Journal of Neurobiology, 20, 203–218.
Golgi, c. (1967). he neuron doctrine—theory and facts. Nobel
Lectures, Physiology or Medicine 1901–1921. Elsevier, Amsterdam.
Gunaratne, c.A., Sakurai, A., and Katz, P.S. (2014). comparative mapping
of GABA-immunoreactive neurons in the central nervous systems of
nudibranch molluscs. Journal of Comparative Neurology, 522, 794–810.
Hadield, M.G., Meleshkevitch, E.A., and Boudko, d.y. (2000). he
apical sensory organ of a gastropod veliger is a receptor for settle-
ment cues. Biological Bulletin, 198, 67–76.
Hanström, B. (1925). Über die sogenannten Intelligenzsphären des
Molluskengehirns und die Innervation des tentakels von Helix. Acta
Zoologica (Stockholm), 6, 183–215.
Hanström, B. (1928). Some points on the phylogeny of nerve cells and
of the central nervous system of invertebrates. Journal of Comparative
Neurology, 46, 475–494.
Haszprunar, G. (1985). he Heterobranchia—a new concept of the
Phylogeny of the Higher Gastropoda. Zeitschrift für Zoologische
Systematik und Evolutionsforschung, 23, 15–37.
Haszprunar, G. (1988). On the origin and evolution of major gastro-
pod groups, with special reference to the streptoneura. Journal of
Molluscan Studies, 54, 367–441.
Hatakeyama, d., Aonuma, H., Ito, E., and Elekes, K. (2007).
localization of glutamate-like immunoreactive neurons in the cen-
tral and peripheral nervous system of the adult and developing pond
snail, Lymnaea stagnalis. Biological Bulletin, 213, 172–186.
Hatakeyama, d. and Ito, E. (2000). distribution and developmental
changes in GABA-like immunoreactive neurons in the central nerv-
ous system of pond snail, Lymnaea stagnalis. Journal of Comparative
Neurology, 418, 310–322.
Hegedus, E., Kaslin, J., Hiripi, l., Kiss, t., Panula, P., and Elekes, K.
(2004). Histaminergic neurons in the central and peripheral nerv-
ous system of gastropods (Helix, Lymnaea): an immunocytochemi-
cal, biochemical, and electrophysiological approach. Journal of
Comparative Neurology, 475, 391–405.
215
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
Hening, W.A., Walters, E.t., carew, t.J., and Kandel, E.R. (1979).
Motorneuronal control of locomotion in Aplysia. Brain Research,
179, 231–253.
Hens, M.d., Fowler, K.A., and leise, E.M. (2006). Induction of meta-
morphosis decreases nitric oxide synthase gene expression in larvae
of the marine mollusc Ilyanassa obsoleta (Say). Biological Bulletin,
211, 208–211.
Hernadi, l. (1994). distribution and anatomy of GABA-like immuno-
reactive neurons in the central and peripheral nervous system of the
snail Helix pomatia. Cell & Tissue Research, 277, 189–198.
Hernadi, l. and Elekes, K. (1999). topographic organization of sero-
tonergic and dopaminergic neurons in the cerebral ganglia and their
peripheral projection patterns in the head areas of the snail Helix
pomatia. Journal of Comparative Neurology, 411, 274–287.
Hirata, K.y. and Hadield, M.G. (1986). he role of choline in meta-
morphic induction of Phestilla (Gastropoda, nudibranchia).
Comparative Biochemistry and Physiology, 84, 15–21.
Hughes, G.M. and tauc, l. (1963). An electrophysiological study of
anatomical relations of 2 giant nerve cells in Aplysia depilans. Journal
of Experimental Biology, 40, 469–486.
Hyman, l.H. (1967). he Invertebrates: Mollusca I. McGraw-Hill,
new york.
Ierusalimsky, v.n. and Balaban, P.M. (2001). Ontogenesis of the snail,
Helix aspersa: embryogenesis timetable and ontogenesis of GABA-
like immunoreactive neurons in the central nervous system. Journal
of Neurocytology, 30, 73–91.
Ikeda, t., yasuda-Kamatani, y., Minakata, H., Kenny, P.t., nomoto,
K., and Muneoka, y. (1992). Mytilus-inhibitory peptide analogues
isolated from the ganglia of a pulmonate mollusc, Achatina fulica.
Comparative Biochemistry and Physiology C, 101, 245–249.
Ivashkin, E., Khabarova, M.yu., Melnikova, v., et al. (2015). Serotonin
mediates maternal efects and directs developmental and behavioral
changes in snail progeny. Cell Reports, 12, 1144–1158.
Ito, I., Kimura, t., Watanabe, S., Kirino, y., and Ito, E. (2004).
Modulation of two oscillatory networks in the peripheral olfactory
system by γ-aminobutyric acid, glutamate, and acetylcholine in
the terrestrial slug Limax marginatus. Journal of Neurobiology, 59,
304–318.
Ito, E., Kojima, S., lukowiak, K., and Sakakibara, M. (2013).
From likes to dislikes: conditioned taste aversion in the great
pond snail (Lymnaea stagnalis). Canadian Journal of Zoology, 91,
405–412.
Jacklet, J.W. (1995). nitric oxide is used as an orthograde cotransmitter
at identiied histaminergic synapses. Journal of Neurophysiology, 74,
891–895.
Jacklet, J.W. (1997). nitric oxide signaling in invertebrates. Invertebrate
Neuroscience, 3, 1–14.
Jacob, M.H. (1984). neurogenesis in Aplysia californica resembles ner-
vous system formation in vertebrates. Journal of Neuroscience, 4,
1225–1239.
Jin, n.G., tian, l.-M., and crow, t. (2009). 5-Ht and GABA modu-
late intrinsic excitability of type I interneurons in Hermissenda.
Journal of Neurophysiology, 102, 2825–2833.
Joosse, J. (1984). Recent progress in endocrinology of molluscs. In J.
Hofmann and J. Porchet, eds. Biosynthesis, Metabolism and Mode of
Action of Invertebrate Hormones. Springer, Berlin.
Jorger, K.M., Stöger, I., Kano, y., Fukuda, H., Knebelsberger, t., and
Schrödl, M. (2010). On the origin of Acochlidia and other enig-
matic euthyneuran gastropods, with implications for the systematics
of Heterobranchia. BMC Evolutionary Biology, 10, 323.
Kabotyanski, E.A., Baxter, d.A., and Byrne, J.H. (1998). Identiication
and characterization of catecholaminergic neuron B65, which
216
initiates and modiies patterned activity in the buccal ganglia of
Aplysia. Journal of Neurophysiology, 79, 605–621.
Kabotyanski, E.A., Baxter, d.A., cushman, S.J., and Byrne, J.H.
(2000). Modulation of ictive feeding by dopamine and serotonin
in Aplysia. Journal of Neurophysiology, 83, 374–392.
Kandel, E.R. (1976). Cellular Basis of Behavior. W.H. Freeman and
company, San Francisco.
Kandel, E.R. (1979). Behavioral Biology of Aplysia. Freeman, San
Francisco.
Kandel, E.R. (2001). he molecular biology of memory storage: a dia-
logue between genes and synapses. Science, 294, 1030–1038.
Kandel, E.R., Kriegstein, A., and Schacher, S. (1981). development of
the central nervous system of Aplysia in terms of the diferentiation
of its speciic identiiable cells. Neuroscience, 5, 2033–2063.
Kehoe, J. (1972). hree acetylcholine receptors in Aplysia neurones.
Journal of Physiology, 225, 115–146.
Kemenes, G., Hiripi, l., and Benjamin, P.R. (1990). Behavioural and
biochemical changes in the feeding system of Lymnaea induced by
the dopamine and serotonin neurotoxins 6-hydroxydopamine and
5,6-dixydroxytryptamine. Philosophical Transactions of the Royal
Society of London B Biological Sciences, 329, 243–255.
Kemenes, G., Rozsa, K.S., Stefano, G., and carpenter, d.O. (1992).
distinct receptors for leu- and Met-enkephalin on the metacer-
ebral giant cell of Aplysia. Cellular and Molecular Neurobiology, 12,
107–119.
Kempf, S.c., chun, G.v., and Hadield, M.G. (1992). An immuno-
cytochemical search for potential neurotransmitters in larvae of
Phestilla sibogae (Gastropoda, Opisthobranchia). Comparative
Biochemistry and Physiology, 101 c, 299–305.
Kempf, S.c., Page, l.R., and Pires, A. (1997). development of serotonin-like
immunoreactivity in the embryos and larvae of nudibranch mollusks
with emphasis on the structure and possible function of the apical sen-
sory organ. Journal of Comparative Neurology, 386, 507–528.
Kerkhoven, R.M., croll, R.P., van Minnen, J., Bogerd, J., Ramkema,
M.d., and Boer, H.H. (1991). he vd1/RPd2 neuronal system
in the cnS of Lymnaea stagnalis and homologous systems in other
molluscs with particular reference to the innervation of the auricle
of the heart. In K.S. Kits, H.H. Boer, and J. Joose eds. Molluscan
Neurobiology. north Holland, Amsterdam.
Kerkhoven, R.M., croll, R.P., van Minnen, J., Bogerd, J., Ramkema,
M.d., and Boer, H.H. (1992). Morphological determination of the
vd1/RPd2 neuronal system in the cnS of the pond snail lymnaea
stagnalis using in situ hybridization and immunocytochemistry. Cell
& Tissue Research, 267, 551–559.
King, M.S., delaney, K., and Gelperin, A. (1987). Acetylcholine acti-
vates cerebral interneurons and feeding motor program in Limax
maximus. Journal of Neurobiology, 18, 509–530.
Kistler, H.B., Hawkins, R.d., Koester, J., Steinbusch, H.W., Kandel,
E.R., and Schwartz, J.H. (1985). distribution of serotonin-
immunoreactive cell bodies and processes in the abdominal gan-
glion of mature Aplysia. Journal of Neuroscience, 5, 72–80.
Klein, M., camardo, J., and Kandel, E. (1982). Serotonin modulates
a speciic potassium current in the sensory neurons that show pre-
synaptic facilitation in Aplysia. Proceedings of the National Academy
of Sciences USA, 79, 5713–5717.
Klussmann-Kolb, A., croll, R.P., and Staubach, S. (2013). Use of
axonal projection patterns for the homologisation of cerebral nerves
in Opisthobranchia. Frontiers in Zoology, 10, 20.
Klussmann-Kolb, A., dinapoli, A., Kuhn, K., Streit, B., and Albrecht,
c. (2008). From sea to land and beyond—new insights into the
evolution of euthyneuran Gastropoda (Mollusca). BMC Evolutionary
Biology, 8, 57.

Knock, S.l., nagle, G.t., lin, c.y., Mcadoo, d.J., and Kurosky, A.
(1989). Aplysia brasiliana neurons R3-R14: primary structure of the
myoactive histidine-rich basic peptide and its prohormone. Peptides,
10, 859–867.
Kobayashi, S., Matsuo, R., Sadamoto, H., Watanabe, S., and Ito, E.
(2012). Excitatory efects of GABA on procerebrum neurons in a
slug. Journal of Neurophysiology, 108, 989–998.
Kocot, K.M., Halanych, K.M., and Krug, P.J. (2013). Phylogenomics
supports Panpulmonata: Opisthobranch paraphyly and key evolu-
tionary steps in a major radiation of gastropod molluscs. Molecular
Phylogenetics and Evolution, 69, 764–771.
Koester, J., dieringer, n., and Mandelbaum, d. (1979). cellular
neuronal control of molluscan heart. he American Zoologist, 19,
103–116.
Krajniak, K.G. (2013). Invertebrate FMRFamide related peptides.
Protein and Peptide Letters, 20, 647–670.
Kriegstein, A.R. (1977). development of the nervous system of Aplysia
californica. Proceedings of the National Academy of Sciences USA, 74,
375–378.
Kuang, S., doran, S.A., Wilson, R.J., Goss, G.G., and Goldberg, J.I.
(2002). Serotonergic sensory-motor neurons mediate a behavioral
response to hypoxia in pond snail embryos. Journal of Neurobiology,
52, 73–83.
Kupfermann, I. (1970). Stimulation of egg laying by extracts of neuro-
endocrine cells (bag cells) of abdominal ganglion of Aplysia. Journal
of Neurophysiology, 33, 877–881.
Kurita, y. and Wada, H. (2011). Evidence that gastropod torsion is
driven by asymmetric cell proliferation activated by tGF-beta sig-
nalling. Biology Letters, 7, 759–762.
lapainis, t., Scanlan, c., Rubakhin, S.S., and Sweedler, J.v. (2007).
A multichannel native luorescence detection system for capillary
electrophoretic analysis of neurotransmitters in single neurons.
Analytical and Bioanalytical Chemistry, 387, 97–105.
lasek, R.J. and dower, W.J. (1971). Aplysia californica—analysis of
nuclear dnA in individual nuclei of giant neurons. Science, 172,
278–279.
leise, E.M. and Hadield, M.G. (2000). An inducer of molluscan meta-
morphosis transforms activity patterns in a larval nervous system.
Biological Bulletin, 199, 241–250.
leonard, J.l., Edstrom, J., and lukowiak, K. (1989). Reexamination of
the gill withdrawal relex of Aplysia californica cooper (Gastropoda;
Opisthobranchia). Behavioral Neuroscience, 103, 585–604.
levenson, J., Sherry, d.M., dryer, l., chin, J., Byrne, J.H., and Eskin,
A. (2000). localization of glutamate and glutamate transporters in
the sensory neurons of Aplysia. Journal of Comparative Neurology,
423, 121–131.
li, G. and chase, R. (1995). correlation of axon projections and pep-
tide immunoreactivity in mesocerebral neurons of the snail Helix
aspersa. Journal of Comparative Neurology, 353, 9–17.
lin, M.F. and leise, E.M. (1996). Gangliogenesis in the prosobranch
gastropod Ilyanassa obsoleta. Journal of Comparative Neurology, 374,
180–193.
lindberg, d.R., Ponder, W.F., and Haszprunar, G. (2004). he
Mollusca: relationships and patterns from their irst half-billion
years. In J. cracraft and M.J. donoghue, eds. Assembling the Tree of
Life, pp. 252–278. Oxford University Press, new york.
lloyd, P.E. and connolly, c.M. (1989). Sequence of pedal peptide:
a novel neuropeptide from the central nervous system of Aplysia.
Journal of Neuroscience, 9, 312–317.
lloyd, P.E., Kupfermann, I., and Weiss, K.R. (1987). Sequence of small
cardioactive peptide A: a second member of a class of neuropeptides
in Aplysia. Peptides, 8, 179–184.
M O l l U S c A : G A S t RO P O d A
lloyd, P.E., Phares, G.A., Phillips, n.E., and Willows, A.O.d.
(1996). Puriication and sequencing of neuropeptides from identi-
ied neurons in the marine mollusc, Tritonia. Peptides, 17, 17–23.
loi, P.K. and tublitz, n. (1997). Molecular analysis of FMRFamide-
and FMRFamide-related peptides (FaRPS) in the cuttleish Sepia
oicinalis. Journal of Experimental Biology, 200, 1483–1489.
longley, R.d. (1984). Axon surface infolding and axon size can be
quantitatively related in gastropod molluscs. Journal of Experimental
Biology, 108, 163–177.
longley, R.d. (2011). neurogenesis in the procerebrum of the snail
Helix aspersa: a quantitative analysis. Biological Bulletin, 221,
215–226.
longley, R.d. and longley, A.J. (1986). Serotonin-like immunoreac-
tivity in gastropod Aplysia californica. Journal of Neurobiology, 17,
339–358.
lux, H.d., neher, E., and Marty, A. (1981). Single channel activity
associated with the calcium dependent outward current in Helix
pomatia. Plugers Archiv, 389, 293–295.
Mackey, S., Kandel, E., and Hawkins, R. (1989). Identiied serotoner-
gic interneurons lcB1 and RcB1 in the cerebral ganglia of Aplysia
produce presynaptic facilitation of siphon sensory neurons. Journal
of Neuroscience, 9, 4227–4235.
Marois, R. and carew, t.J. (1997a). Fine structure of the apical gan-
glion and its serotonergic cells in the larva of Aplysia californica.
Biological Bulletin, 192, 388–398.
Marois, R. and carew, t.J. (1997b). Ontogeny of serotonergic neurons in
Aplysia californica. Journal of Comparative Neurology, 386, 477–490.
Marois, R. and carew, t.J. (1997c). Projection patterns and target
tissues of serotonergic cells in larval Aplysia californica. Journal of
Comparative Neurology, 386, 491–506.
Marois, R. and croll, R.P. (1991). Factors inluencing hatching syn-
chrony within the egg mass of the pond snail, Lymnaea stagnalis.
Invertebrate Reproduction and Development, 19, 139–146.
McArthur, A.G. and tunniclife, v. (1998). Relics and antiquity revis-
ited in the modern vent fauna. Geological Society of London Special
Publications, 148, 271–291.
Mccaman, M.W., Ono, J.K., and Mc caman, R.E. (1979). dopamine
measurements in molluscan ganglia and neurons using a new, sensi-
tive assay. Journal of Neurochemistry, 32, 1111–1113.
Mcclellan, A.d., Brown, G.d., and Getting, P.A. (1994). Modulation
of swimming in Tritonia: excitatory and inhibitory efects of seroto-
nin. Journal of Comparative Physiology A, 174, 257–266.
McAllister, l.B., Scheller, R.H., Kandel, E.R., and Axel, R. (1983). In
situ hybridization to study the origin and fate of identiied neurons.
Science, 222, 800–808.
Megalou, E.v., Brandon, c.J., and Frost, W.n. (2009). Evidence that
the swim aferent neurons of tritonia diomedea are glutamatergic.
Biological Bulletin, 216, 103–112.
Mescheriakov, v.n. (1990) he common pond snail lymnaea stag-
nalis l. In t. detlaf, and S.G. vassetzky eds. Animal Species for
Developmental Studies. Plenum, new york.
Miller, M.W., Beushausen, S., cropper, E.c. et  al. (1993a). he
buccalin-related neuropeptides: isolation and characterization of an
Aplysia cdnA clone encoding a family of peptide cotransmitters.
Journal of Neuroscience, 13, 3346–3357.
Miller, M.W., Beushausen, S., vitek, A., et al. (1993b). he myomodulin-
related neuropeptides: characterization of a gene encoding a family
of peptide cotransmitters in Aplysia. Journal of Neuroscience, 13,
3358–3367.
Moroz, l.l. (2000). Giant identiied nO-releasing neurons and com-
parative histochemistry of putative nitrergic systems in gastropod
molluscs. Microscopy Research and Technique, 49, 557–569.
217
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
Moroz, l.l. (2006). localization of putative nitrergic neurons in per-
ipheral chemosensory areas and the central nervous system of Aplysia
californica. Journal of Comparative Neurology, 495, 10–20.
Moroz, l.l., chen, d., Gillette, M.U., and Gillette, R. (1996).
nitric oxide synthase activity in the molluscan cnS. Journal of
Neurochemistry, 66, 873–876.
Moroz, l.l., Edwards, J.R., Puthanveettil, S.v., et al. (2006). neuronal
transcriptome of Aplysia: neuronal compartments and circuitry.
Cell, 127, 1453–1467.
Moroz, l.l., Gillette, R., and Sweedler, J.v. (1999). Single-cell ana-
lyses of nitrergic neurons in simple nervous systems. Journal of
Experimental Biology, 202, 333–341.
Moroz, l.l., Sudlow, l.c., Jing, J., and Gillette, R. (1997). Serotonin-
immunoreactivity in peripheral tissues of the opisthobranch mol-
luscs Pleurobranchaea californica and Tritonia diomedea. Journal of
Comparative Neurology, 382, 176–188.
Morrill, J.B. (1982). development of the pulmonate gastropod,
Lymnaea. In F.W. Harrison and R.R. cowden, eds. Developmental
Biology of the Freshwater Invertebrates. Alan P. liss, new york.
Munoz, d.P., Pawson, P.A., and chase, R. (1983). Symmetrical giant
neurons in asymmetrical ganglia—implications for evolution of
the nervous system in pulmonate mollusks. Journal of Experimental
Biology, 107, 147–148.
Musio, c. and Bedini, c. (1990). Fine structure and axonal organiza-
tion in the buccal ganglia nerves of Aplysia (Mollusca, Gastropoda).
Zoomorphology, 110, 17–26.
nambu, J.R., taussig, R., Mahon, A.c., and Scheller, R.H. (1983).
Gene isolation with cdnA probes from identiied Aplysia neurons:
neuropeptide modulators of cardiovascular physiology. Cell, 35,
47–56.
neher, E. and lux, H.d. (1969). voltage clamp on Helix pomatia neur-
onal membrane; current measurement over a limited area of the
soma surface. Plugers Archiv, 311, 272–277.
neher, E. and lux, H.d. (1971). Properties of somatic membrane
patches of snail neurons under voltage clamp. Plügers Archiv-
European Journal of Physiology, 322, 35–38.
nesic, B., Magoski, n.S., Mckenney, K.K., Syed, n.I., lukowiak, K.,
and Bulloch, A.G.M. (1996). Glutamate as a putative neurotrans-
mitter in the mollusc, Lymnaea stagnalis. Journal of Neuroscience, 9,
1255–1269.
newcomb, J.M., Fickbohm, d.J., and Katz, P.S. (2006). comparative
mapping of serotonin-immunoreactive neurons in the central
nervous systems of nudibranch molluscs. Journal of Comparative
Neurology, 499, 485–505.
newcomb, J.M. and Katz, P.l. (2007a). Homologues of serotonergic
central pattern generator neurons in related nudibranch molluscs
with divergent behaviors. Journal of Comparative Physiology A, 193,
425–443.
newcomb, J.M. and Katz, P.S. (2007b). Homologues of serotonergic cen-
tral pattern generator neurons in related nudibranch molluscs with
divergent behaviors. Journal of Comparative Physiology A, 193, 425–443.
newcomb, J.M. and Katz, P.S. (2009). diferent functions for
homologous serotonergic interneurons and serotonin in species-
speciic rhythmic behaviours. Proceedings of Biological Sciences, 276,
99–108.
newcomb, J.M., Sakurai, A., lillvis, J.l., Gunaratne, c.A., and Katz,
P.S. (2012). Homology and homoplasy of swimming behaviors
and neural circuits in the nudipleura (Mollusca, Gastropoda,
Opisthobranchia). Proceedings of the National Academy of Sciences
USA, 109, 10669–10676.
nezlin, l., Moroz, l., Elofsson, R., and Sakharov, d. (1994).
Immunolabeled neuroactive substances in the osphradium of
218
the pond snail Lymnaea stagnalis. Cell & Tissue Research, 275,
269–275.
nezlin, l. and voronezhskaya, E. (1997). GABA-immunoreactive neu-
rones and interactions of GABA with serotonin and FMRFamide in
a peripheral sensory ganglion of the pond snail Lymnaea stagnalis.
Brain Research, 772, 217–225.
Ohta, n., Kubota, I., takao, t., et al. (1991). Fulicin, a novel neuro-
peptide containing a d-amino acid residue isolated from the
ganglia of Achatina fulica. Biochemical and Biophysical Research
Communications, 178, 486–493.
Ono, J.K. and Mc caman, R.E. (1980). Identiication of additional
histaminergic neurons in Aplysia: improvement of single cell isola-
tion techniques for in tandem physiological and chemical studies.
Neuroscience, 5, 835–840.
Ono, J.K. and Mc caman, R.E. (1984). Immunocytochemical local-
ization and direct assays of serotonin-containing neurons in Aplysia.
Neuroscience, 11, 549–560.
Orchard, I. and lange, A. (2013). FMRFamide-like peptides (FlPs).
In A.J. Kastin, ed. Handbook of Biologically Active Peptides. Elsevier,
Amsterdam.
Osborne, n.n., Briel, G., and neuhof, v. (1971). distribution of
GABA and other amino acids in diferent tissues of the gastropod
mollusc Helix pomatia, including in vitro experiments with 14 c glu-
cose and 14 c glutamic acid. International Journal of Neuroscience,
1, 265–272.
Osborne, n.n. and Patel, S. (1984). localisation of histamine-
immunoreactivity in speciic neurones of the gastropod cnS includ-
ing a cell which has been identiied as histaminergic. Histochemistry,
81, 207–208.
Oshuga, K., Kurokawa, M., and Kuwasawa, K. (2000). Mosaic arrange-
ment of ScPB-, FMRFamide-, and histamine-like immunore-
active sensory hair cells in the statocyst of the gastropod mollusc
Pleurobranchaea japonica. Cell & Tissue Research, 300, 165–172.
Ottaviani, E., caselgrandi, E., and Franchini, A. (1988). Epinephrine
investigation in the snail brain of Helicella virgata (Gastropoda, pul-
monata). Comparative Biochemistry and Physiology C, 89, 267–269.
Page, l.R. (1997a). larval shell muscles in the abalone Haliotis kamts-
chatkana. Biological Bulletin, 193, 30–46.
Page, l.R. (1997b). Ontogenetic torsion and protoconch form in the
archaeogastropod Haliotis kamtschatkana: evolutionary implica-
tions. Acta Zoologica (Stockholm), 78, 227–245.
Page, l.R. (2002). Apical sensory organ in larvae of the patellogastro-
pod Tectura scutum. Biological Bulletin, 202, 6–22.
Page, l.R. (2003). Gastropod ontogenetic torsion: developmental rem-
nants of an ancient evolutionary change in body plan. Journal of
Experimental Zoology B, 297, 11–26.
Page, l.R. and Parries, S.c. (2000). comparative study of the apical
ganglion in planktotrophic caenogastropod larvae: ultrastruc-
ture and immunoreactivity to serotonin. Journal of Comparative
Neurology, 418, 383–401.
Pani, A.K. and croll, R.P. (2000). catechol concentrations in the
haemolymph of the scallop Placopecten magellanicus. General and
Comparative Endocrinology, 118, 48–56.
Park, J.H., Straub, v.A., and O’Shea, M. (1998). Anterograde signaling
by nitric oxide: characterization and in vitro reconstitution of an
identiied nitrergic synapse. Journal of Neuroscience, 18, 5463–5476.
Pentreath, v.W., Berry, M.S., and Osborne, n.n. (1982). he seroton-
ergic cerebral cells in gastropods. In n.n. Osborne, ed. Biology of
Serotonergic Transmission. John Wiley, chichester, new york.
Pentreath, v.W., Radojcic, t., Seal, l.H., and Winstanley, E.K. (1985).
he glial cells and glia-neuron relations in the buccal ganglia of
Planorbis corneus (l.): cytological, qualitative and quantitative

changes during growth and ageing. Philosophical Transactions of the
Royal Society of London B Biological Sciences, 307, 399–455.
Price, d.A. and Greenberg, M.J. (1977). Structure of a molluscan car-
dioexcitatory neuropeptide. Science, 197, 670–671.
Price, d.A. and Greenberg, A.E. (1989). he hunting of FaRPs: the dis-
tribution of FMRFamide-related peptides. Biological Bulletin, 177,
198–205.
Price, d.A., lesser, W., lee, t.d., doble, K.E., and Greenberg, M.J.
(1990). Seven FMRFamide-related and two ScP-related cardioactive
peptides from Helix. Journal of Experimental Biology, 154, 421–437.
Ram, J.l., Gallardo, c.S., Ram, M.I., and croll, R.P. (1998).
Reproduction-associated immunoreactivities in the nervous systems
of prosobranch gastropods. Biological Bulletin, 195, 308–318.
Raven, c.P. (1966) Morphogenesis: he Analysis of Molluscan
Development, Pergamon, Oxford.
Richmond, J., Bulloch, A., Bauce, l., and lukowiak, K. (1991).
Evidence for the presence, synthesis, immunoreactivity, and uptake
of GABA in the nervous system of the snail Helisoma trivolvis.
Journal of Comparative Neurology, 307, 131–143.
Richter, S., loesel, R., Purschke, G., et al. (2010). Invertebrate neuro-
phylogeny: suggested terms and deinitions for a neuroanatomical
glossary. Frontiers in Zoology, 7, 29.
Rogers, d.c. (1969). Fine structure of the epineural connective tissue
sheath of the subesophageal ganglion in Helix aspersa. Zeitschrift für
Zellforschung und Mikroskopische Anatomie, 102, 99–112.
Rose, R.M. and Benjamin, P.R. (1979). he relationship of the central
motor pattern to the feeding cycle of Lymnaea stagnalis. Journal of
Experimental Biology, 80, 137–163.
Rose, R. and Benjamin, P. (1981). Interneuronal control of feeding in
the pond snail Lymnaea stagnalis: II. he interneuronal mechan-
ism generating feeding cycles. Journal of Experimental Biology, 92,
203–228.
Rosza, K.S. (1979). Analysis of the neural network regulating the
cardio-renal system in the central nervous system of Helix pomatia
l. American Zoologist, 19, 117–128.
Ruppert, E.E., Fox, R.S., and Barnes, R.d. (2004). Invertebrate
Zoology: A Functional Evolutionary Approach. homson-Brooks/
cole, Belmont.
Sakharov, d. (1970). cellular aspects of invertebrate neuropharmacol-
ogy. Annual Reviews in Pharmacology, 10, 335–352.
Sakharov, d. (1974). Evolutionary aspects of transmitter heterogeneity.
Neurovegetative Transmission Mechanisms. Springer, Berlin.
Sakharov, d.A. (1976). nerve cell homologies in gastropods. In
J. Salanki, ed. Neurobiology of Invertebrates: Gastropod Brain.
Akademiai Kiado, Budapest.
Sakharov, d.A. (1990). he multiplicity of neurotransmitters: the func-
tional signiicance. Zhurnal Evoliutsionnoi Biokhimii i Fiziologii, 26,
733–741.
Sakharov, d.A. (1994). he long path of the snail. Neuroscience,
Behavior and Physiology, 4, 1–4.
Sakharov, d.A. (2012). he biological substrate for the generation of
behavioral acts. Zhurnal Obshchei Biologii, 73, 334–348.
Sakharova, A.v. and Sakharov, d.A. (1971). visualization of intraneu-
ronal monoamines by treatment with formalin solutions. Progress in
Brain Research, 34, 11–25.
Santama, n. and Benjamin, P.R. (2000). Gene expression and func-
tion of FMRFamide-related neuropeptides in the snail Lymnaea.
Microscopy Research and Technique, 49, 547–556.
Santama, n., Benjamin, P.R., and Burke, J.F. (1995a). Alternative RnA
splicing generates diversity of neuropeptide expression in the brain of
the snail Lymnaea: in situ analysis of mutually exclusive transcripts of
the FMRFamide gene. European Journal of Neuroscience, 7, 65–76.
M O l l U S c A : G A S t RO P O d A
Santama, n., li, K.W., Geraerts, W.P.M., Benjamin, P.R., and Burke,
J.F. (1996). Post-translational processing of alternative neuropeptide
precursor encoded by the FMRFamide gene in the pulmonate snail,
Lymnaea stagnalis. European Journal of Neuroscience, 8, 968–977.
Santama, n., Wheeler, c.H., Burke, J.F., and Benjamin, P.R. (1994).
neuropeptides myomodulin, small cardioactive peptide, and bucca-
lin in the central nervous system of Lymnaea stagnalis: puriication,
immunoreactivity, and artifacts. Journal of Comparative Neurology,
342, 335–351.
Santama, n., Wheeler, c.H., Skingsley, d.R., et  al. (1995b).
Identiication, distribution and physiological activity of three
novel neuropeptides of Lymnaea: EFlRIamide and pQFyRIamide
encoded by the FMRFamide gene, and a related peptide. European
Journal of Neuroscience, 7, 234–246.
Satake, H., yasuda-Kamatani, y., takuwa, K., et  al. (1999).
characterization of a cdnA encoding a precursor polypeptide
of a d-amino acid-containing peptide, achatin-I and localized
expression of the achatin-I and fulicin genes. European Journal of
Biochemistry/FEBS, 261, 130–136.
Satterlie, R.A., labarbera, M., and Spencer, A.n. (1985). Swimming
in the pteropod mollusc, Clione umacina: I. Behaviour and morph-
ology. Journal of Experimental Biology, 116, 189–204.
Satterlie, R.A., norekian, t.P., Jordan, S., and Kazilek, c.J. (1995).
Serotonergic modulation of swimming speed in the pteropod mol-
lusc Clione limacina: I. Serotonin immunoreactivity in the central
nervous system and wings. Journal of Experimental Biology, 198,
895–904.
Satterlie, R.A. and Spencer, A.n. (1985). Swimming in the pteropod
mollusc, Clione limacina: II. Physiology. Journal of Experimental
Biology, 116, 205–222.
Sawatpeera, S., Upatham, E.S., Kruatrachue, M., et al. (2001). larval
development in Haliotis asinina linnaeus. Journal of Shellish
Research, 20, 593–601.
Schacher, S., Kandel, E.R., and Woolley, R. (1979). development
of neurons in the abdominal ganglion of Aplysia calfornica
I. Axosomatic synaptic contacts. Developmental Biology, 71,
176–190.
Schaefer, M., Picciotto, M.R., Kreiner, t., Kaldany, R.R., taussig, R.,
and Scheller, R.H. (1985). Aplysia neurons express a gene encoding
multiple FMRFamide neuropeptides. Cell, 41, 457–467.
Scheller, R.H., Jackson, J.F., Mcallister, l.B., Rothman, B.S., Mayeri,
E., and Axel, R. (1983). A single gene encodes multiple neuropep-
tides mediating a stereotyped behavior. Cell, 32, 7–22.
Schmekel, l. (1985) Aspects of evolution within the opisthobranchs.
In E.R. trueman and M.R. clarke, eds. he Mollusca. Academic,
Orlando.
Shepherd, G.M. (1991). Foundations of the Neuron Doctrine. Oxford
University, new york.
Skelton, M., Alevizos, A., and Koester, J. (1992). control of the car-
diovascular system of Aplysia by identiied neurons. Experientia, 48,
809–817.
Smit, A.B., Geraerts, P.M., Meester, I., van Heerikhuizen, H., and
Joosse, J. (1991). characterization of a cdnA clone encoding mol-
luscan insulin-related peptide II of Lymnaea stagnalis. European
Journal of Biochemistry/FEBS, 199, 699–703.
Smit, A.B., Jimenez, c.R., dirks, R., croll, R.P., and Geraerts, W.P.M.
(1992a). characterization of a cdnA clone encoding multiple cop-
ies of the neuropeptide APGWamide in the mollusc Lymnaea stag-
nalis. Journal of Neuroscience, 12, 1709–1715.
Smit, A.B., Spijker, S., van Minnen, J., et al. (1996). Expression and
characterization of molluscan insulin-related peptide vII from the
mollusc Lymnaea stagnalis. Neuroscience, 70, 589–596.
219
S t RU c t U R E A n d E vO l U t I O n O F I n v E Rt E B R At E n E Rv O U S S y S t E M S
Smit, A.B., Syed, n.I., Schaap, d., et  al. (2001). A glia-derived
acetylcholine-binding protein that modulates synaptic transmission.
Nature, 411, 261–268.
Smit, A.B., hijsen, S.F., Geraerts, W.P., Meester, I., van Heerikhuizen,
H., and Joosse, J. (1992b). characterization of a cdnA clone
encoding molluscan insulin-related peptide v of Lymnaea stagnalis.
Molecular Brain Research, 14, 7–12.
Smit, A.B., vreugdenhil, E., Ebberink, R.H., Geraerts, W.P., Klootwijk,
J., and Joosse, J. (1988). Growth-controlling molluscan neurons
produce the precursor of an insulin-related peptide. Nature, 331,
535–538.
Smith, S.A., nason, J., and croll, R.P. (1998). distribution of catechol-
amines in the sea scallop, Placopecten magellanicus. Canadian Journal
of Zoology, 76, 1254–1262.
Soinila, S., Mptisos, G.l., and Panula, P. (1990). comparative study
of histamine immunoreactivity in nervous system of Aplysia
and Pleurobranchaea. Journal of Comparative Neurology, 298,
83–96.
Sossin, W.S., Sweet-cordero, A., and Scheller, R.H. (1990). dale’s
hypothesis revisited: diferent neuropeptides derived from a com-
mon prohormone are targeted to diferent processes. Proceedings of
the National Academy of Sciences USA, 87, 4845–4848.
Spengel, J. (1881). die Geruchsorgane und das nervensystem der
Mollusken. Zeitschrift fur wissenschaftliche Zoologie. 35.
Strong, E.E., Gargominy, O., Ponder, W.F., and Bouchet, P. (2008).
Global diversity of gastropods (Gastropoda; Mollusca) in freshwater.
Hydrobiologia, 595, 149–166.
Sudlow, l.c., Jing, J., Moroz, l.l., and Gillette, R. (1998). Serotonin
immunoreactivity in the central nervous system of the marine mol-
luscs Pleurobranchaea californica and Tritonia diomedea. Journal of
Comparative Neurology, 395, 466–480.
Suzuki, H., Kimura, t., Sekiguchi, t., and Mizukami, A. (1997).
FMRFamide-like-immunoreactive primary sensory neurons in the
olfactory system of the terrestrial mollusc, Limax marginatus. Cell &
Tissue Research, 289, 339–345.
Syed, n.I., lukowiak, K., and Bulloch, A.G.M. (1990). In vitro recon-
struction of the respiratory central pattern generator of the mollusk
Lymnaea. Science, 250, 282–285.
Syed, n.I. and Winlow, W. (1989). Morphology and electrophysi-
ology of neurons innervating the ciliated locomotor epithelium in
Lymnaea stagnalis (L.). Comparative Biochemistry and Physiology,
93A, 633–644.
Syed, n.I. and Winlow, W. (1991). Respiratory behavior in the pond
snail Lymnaea stagnalis. II. neural elements of the central pattern
generator. Journal of Comparative Physiology, 169A, 557–568.
tauc, l. (1954). Reponse de la cellule nerveuse du ganglion abdominal
de Aplysia depilans a la stimulation directe intra-cellulaire. Comptes
Rendus de l’Académie des Sciences, 239, 1537–1539.
tauc, l. (1957). Stimulation du soma neuronique de l’aplysie par voie
antidromique. Journal de Physiologie (Paris), 49, 973–986.
tauc, l., Fossier, P., and Baux, G. (1992). Regulation of transmitter
release by presynaptic receptors at a cholinergic neuro-neuronal syn-
apse. Acta Biologica Hungarica, 43, 49–58.
tauc, l. and Gerschenfeld, H.M. (1961). cholinergic transmission
mechanisms for both excitation and inhibition in molluscan central
synapses. Nature, 192, 366–367.
treistman, S.n. and Schwartz, J.H. (1977). Metabolism of acetyl-
choline in the nervous system of Aplysia californica. Iv. Studies of
an identiied cholinergic axon. Journal of General Physiology, 69,
725–741.
tritt, S.H., lowe, I.P., and Byrne, J.H. (1983). A modiication of the gly-
oxylic acid induced histoluorescence technique for demonstration
220
of catecholamines and serotonin in tissues of Aplysia californica.
Brain Research, 259, 159–162.
vallejo, d., Habib, M.R., delgado, n., vaasjo, l.O., croll, R.P., and
Miller, M.W. (2014). localization of tyrosine hydroxylase-like
immunoreactivity in the nervous systems of Biomphalaria glabrata
and Biomphalaria alexandrina, intermediate hosts for schistosomia-
sis. Journal of Comparative Neurology, 522, 2532–2552.
van Kesteren, R., Smit, A., de lange, R., et  al. (1995). Structural
and functional evolution of the vasopressin/oxytocin superfam-
ily: vasopressin-related conopressin is the only member present in
Lymnaea, and is involved in the control of sexual behavior. Journal
of Neuroscience, 15, 5989–5998.
van Minnen, J., van der Haar, c., Raap, A.K., and vreugdenhil, E.
(1988). localization of ovulation hormone-like neuropeptide in
the central nervous system of the snail Lymnaea stagnalis by means
of immunocytochemistry and in situ hybridization. Cell & Tissue
Research, 251, 477–484.
veenstra, J.A. (2010). neurohormones and neuropeptides encoded by
the genome of Lottia gigantea, with reference to other mollusks and
insects. General and Comparative Endocrinology, 167, 86–103.
veratti, E. (1900). Richerche sul sistema nervoso dei Limax. tip. B. di
C. Rebeschini, 18.
verkhratsky, A. and Butt, A. (2013). neuroglia: deinition, classii-
cation, evolution, numbers, development. Glial Physiology and
Pathophysiology. John Wiley & Sons, Hoboken.
vilim, F.S., cropper, E.c., Price, d.A., Kupfermann, I., and Weiss,
K.R. (1996). Release of peptide cotransmitters in Aplysia: regu-
lation and functional implications. Journal of Neuroscience, 16,
8105–8114.
voronezhskaya, E.E. and Elekes, K. (1993). distribution of serotonin-
like immunoreactive neurones in the embryonic nervous system of
lymnaeid and planorbid snails. Neurobiology (Bp), 1, 371–383.
voronezhskaya, E.E. and Elekes, K. (1996). transient and sustained
expression of FMRFamide-like immunoreactivity in the develop-
ing nervous system of Lymnaea stagnalis (Mollusca, Pulmonata).
Cellular and Molecular Neurobiology, 16, 661–676.
voronezhskaya, E.E. and Elekes, K. (2003). Expression of FMRFamide
gene encoded peptides by identiied neurons in embryos and
juveniles of the pulmonate snail Lymnaea stagnalis. Cell & Tissue
Research, 314, 297–313.
voronezhskaya, E.E., Glebov, K.I., Khabarova, M.y., Ponimaskin,
E.G., and nezlin, l.P. (2008). Adult-to-embryo chemical signal-
ing in the regulation of larval development in trochophore animals:
cellular and molecular mechanisms. Acta Biologica Hungarica, 59
(Suppl.), 117–122.
voronezhskaya, E.E., Hiripi, l., Elekes, K., and croll, R.P. (1999).
development of catecholaminergic neurons in the pond snail,
Lymnaea stagnalis: I. Embryonic development of dopamine-
containing neurons and dopamine-dependent behaviors. Journal of
Comparative Neurology, 404, 285–296.
voronezhskaya, E.E. and Ivashkin, E.G. (2010). Pioneer neurons: abasis
or limiting factor of lophotrochozoa nervous system diversity?
Russian Journal of Developmental Biology, 41, 337–346.
voronezhskaya, E.E., Khabarova, M.y., and nezlin, l.. (2004). Apical
sensory neurones mediate developmental retardation induced by
conspeciic environmental stimuli in freshwater pulmonate snails.
Development, 131, 3671–3680.
voronezhskaya E.E., tyurin S.A., and nezlin l.P. (2002). neuronal
development in larval chiton Ischnochiton hakodadensis (Mollusca:
Polyplacophora). Journal of Comparative Neurology, 444, 25–38.
vreugdenhil, E., Jackson, J.F., Bouwmeester, t., et al. (1988). Isolation,
characterization, and evolutionary aspects of a cdnA clone

encoding multiple neuropeptides involved in the stereotyped egg-
laying behavior of the freshwater snail Lymnaea stagnalis. Journal of
Neuroscience, 8, 4184–4191.
Waegele, H., Klussmann-Kolb, A., verbeek, E., and Schrodl, M.
(2014). Flashback and foreshadowing–a review of the taxon
Opisthobranchia. Organisms Diversity & Evolution, 14, 133–149.
Wanninger, A., Ruthensteiner, B., and Haszprunar, G. (2000).
torsion in Patella caerulea (Mollusca, Patellogastropoda): ontoge-
netic process, timing, and mechanisms. Invertebrate Biology, 119,
177–187.
Wanninger, A., Ruthensteiner, B., loebnwein, S., Salvenmoser, W.,
dictus, W.J.A.G., and Haszpruner, G. (1999). development of the
musculature in the limpet Patella (Mollusca, Patellogastropoda).
Development, Genes & Evolution, 209, 226–238.
Weinreich, d. (1977). Histamine-containing neurons in Aplysia. In
n.n. Osborne, ed. Biochemistry of Characterised Neurons. Pergamon,
Oxford.
Weiss, K.R., Bayley, H., lloyd, P.E., et  al. (1989). Puriication and
sequencing of neuropeptides contained in neuron R15 of Aplysia
californica. Proceedings of the National Academy of Sciences USA, 86,
2913–2917.
Weiss, K.R., Brezina, v., cropper, E.c., et al. (1992). Peptidergic co-
transmission in Aplysia: functional implications for rhythmic behav-
iors. Experientia, 48, 456–463.
Weiss, K.R., chiel, H.J., Koch, U., and Kupfermann, I. (1986). Activity
of an identiied histaminergic neuron, and its possible role in arousal
of feeding behavior in semi-intact Aplysia. Journal of Neuroscience,
6, 2403–2415.
Weiss, K.R., cohen, J.l., and Kupfermann, I. (1978). Modulatory con-
trol of buccal musculature by a serotonergic neuron (metacerebral
cell) in Aplysia. Journal of Neurophysiology, 41, 181–203.
Weiss, K.R. and Kupfermann, I. (1976). Homology of the giant sero-
tonergic neurons (metacerebral cells) in Aplysia and pulmonate mol-
luscs. Brain Research, 117, 33–49.
Willows, A.O.d. (ed.) (1985). Neurobiology and Behavior, Part I.
Academic, Orlando.
View publication stats
M O l l U S c A : G A S t RO P O d A
Willows, A.O.d. (ed.) (1986). Neurobiology and Behavior, Part II.
Academic, Orlando.
Wollesen, t., cummins, S.F., degnan, B.M., and Wanninger, A.
(2010). FMRFamide gene and peptide expression during central
nervous system development of the cephalopod mollusk, Idiosepius
notoides. Evolutionary Development, 12, 113–130.
Wyeth, R.c. and croll, R.P. (2011). Peripheral sensory cells in the
cephalic sensory organs of Lymnaea stagnalis. Journal of Comparative
Neurology, 519, 1894–1913.
yeoman, M.S., Pieneman, A.W., Ferguson, G.P., ter Maat, A., and
Benjamin, P.R. (1994). Modulatory role for the serotonergic cer-
ebral giant cells in the feeding system of the snail, Lymnaea. I. Fine
wire recording in the intact animal and pharmacology. Journal of
Neurophysiology, 72, 1357–1371.
young, K.G., chang, J.P., and Goldberg, J.I. (1999). Gonadotropin-
releasing hormone neuronal system of the freshwater snails Helisoma
trivolvis and Lymnaea stagnalis: possible involvement in reproduc-
tion. Journal of Comparative Neurology, 404, 427–437.
Zaitseva, O. (2000). Structural organization of procerebrums of ter-
restrial molluscs: characteristics of neuronal pattern, plasticity, and
age peculiarities. Journal of Evolutionary Biochemistry Physiology, 36,
324–333.
Zaitseva, O.v. and Bocharova, l.S. (1981). Sensory cells in the head
skin of pond snails. Cell & Tissue Research, 220, 797–807.
Zapata, F., Wilson, n.G., Howison, M., et al. (2014). Phylogenomic
analyses of deep gastropod relationships reject Orthogastropoda.
Proceedings of the Royal Society of London B Biological Sciences, 281,
20141739. http://dx.doi.org/10.1098/rspb.2014.1739.
Zhang, l., tello, J.A., Zhang, W., and tsai, P.S. (2008). Molecular
cloning, expression pattern, and immunocytochemical localization
of a gonadotropin-releasing hormone-like molecule in the gastropod
mollusk, Aplysia californica. General and Comparative Endocrinology,
156, 201–209.
Zs-nagy, I. and Sakharov, d. (1970). he ine structure of the procer-
ebrum of pulmonate molluscs, Helix and Limax. Tissue & Cell, 2,
399–411.
221