Journal of Chemical Neuroanatomy 48–49 (2013) 1–13

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Journal of Chemical Neuroanatomy

journal homepage: www.elsevier.com/locate/jchemneu

Review

‘‘Limbic associative’’ and ‘‘autonomic’’ amygdala in teleosts: A review of the

evidence
Caio Maximino a,b,*, Monica Gomes Lima a, Karen Renata Matos Oliveira a,
Evander de Jesus Oliveira Batista a, Anderson Manoel Herculano a,b
a
Laboratório de Neuroendocrinologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Brazil
b
Zebrafish Neuroscience Research Consortium, New Orleans, United States

A R T I C L E I N F O A B S T R A C T

Article history: The amygdaloid nuclei form an important hub of structures associated with diverse aspects of cognition
Received 29 March 2012 and emotional behavior. Homologous structures have been determined in tetrapods, but homology of
Received in revised form 4 October 2012 amygdala-like regions in bony fishes is presently unclear. Based on connectivity patterns,
Accepted 5 October 2012
genoarchitecture, chemical neuroanatomy, and functional studies, we suggest that the dorsomedial
Available online 6 November 2012
portion of the pallium of Actinopterygii is the homolog of the basolateral/lateral amygdala
(‘‘frontotemporal amygdaloid system’’), while the supracommissural and postcommissural portions
Keywords:
of the subpallium are homologous to the extended central amygdala (central amygdaloid nucleus and
Amygdala
Actinopterygii
bed nucleus of the stria terminalis). Nonetheless, the differentiation between these nuclei is not as clear-
Fish cut as in mammals, and there is no clear evidence for the existence of an ‘‘olfactory’’ medial amygdala in
Genoarchitecture Actinopterygii, suggesting that the parcellation of one or two amygdaloid nuclei into many subnuclei
Pallium occurred with the appearance of a true vomeronasal system.
Subpallium ß 2012 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. The problem of topography. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
3. The amniote amygdaloid complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3
4. The dorsomedial pallium as frontotemporal amygdaloid system . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.1. Topography and topology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.2. Cytoarchitectonics and neurochemistry. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.3. Hodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
4.4. Expression of developmental regulatory genes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
4.5. Neurophysiology and behavior. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
5. The sub- and postcommissural subpallia as striatal amygdalae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5.1. Topography and topology. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5.2. Cytoarchitectonics and neurochemistry. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5.3. Hodology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5.4. Expression of developmental regulatory genes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
5.5. Neurophysiology and behavior. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
6. Is there a medial amygdala in bony fishes? . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
7. Evolutionary perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
8. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

* Corresponding author at: Laboratório de Neuroendocrinologia, Instituto de Ciências Biológicas, Universidade Federal do Pará, Brazil.

0891-0618/$ – see front matter ß 2012 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.jchemneu.2012.10.001
2 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
1. Introduction
Interest in the teleostean central nervous system is increasing
among neuroscientists in general, leaving the relatively confined
field of comparative neurobiology to influence other areas such as
neuropsychopharmacology (Maximino and Herculano, 2010),
behavioral genetics (Norton and Bally-Cuif, 2010), neuroendocri-
nology (Löhr and Hammerschmidt, 2011), and neurobehavioral
disorders (Stewart et al., 2010). Of special interest in these cases is
the introduction of novel model organisms, such as zebrafish and
medaka (Zhiyuan and Korzh, 2004), and recently, the sequencing of
the guppy transcriptome (Löhr and Hammerschmidt, 2011). From
the 1990s, species such as zebrafish, medaka and goldfish are
increasingly being used in the field of neuroscience.
In recent years, these species are gradually being introduced as
model organisms for the study of the neurobiological and
molecular underpinnings of complex behavior, including fear
and anxiety (Broglio et al., 2005; Braithwaite and Boulcott, 2007;
Maximino et al., 2010a; Jesuthasan, 2012; Levin, 2011; Stewart
et al., 2011). These functions can be understood as highly adaptive
action tendencies which protect an animal from discrete, diffuse or
potential threats from the environment. Among behavioral
neuroscientists, there is a widespread belief that, to some degree,
these functions are controlled by a network of structures of which
some of the amygdaloid nuclei are a hub (LeDoux, 1998, 2003;
Davis, 2004; Canteras and Blanchard, 2008).
Based on electrolytic lesions (Marino-Neto and Sabbatini,
1983; Portavella et al., 2004a,b; Portavella and Vargas, 2005;
Martı́n et al., 2011) and drug microinjection (Xu et al., 2003, 2009)
experiments, it has been suggested that a subregion of the
telencephalic pallium of teleosts, the dorsomedial (Dm) telen-
cephalon, is an amygdala-like structure. This hypothesis is not
without precedent; the idea that Dm is of ventral pallial origin
and, therefore, homologous to the mammalian pallial amygdaloid
nuclei, was proposed on topographical and developmental
grounds (Braford, 1995, 2009).
Comparative studies in tetrapods led to the perception that
the amygdala is neither a structural nor a functional unit
(Swanson and Petrovich, 1998). Furthermore, in amniotes,
derivatives from the lateral (LP) and ventral pallia (VP) and from
the subpallium (SP) constitute fundamental parts of the
amygdaloid complex (Fernandez et al., 1998; Puelles et al.,
2000; Puelles, 2001). Lungfishes, which diverged from the
vertebrate lineage after the divergence of most other fish
lineages but prior to the divergence of amphibians, and anurans,
show three amygdalar subdivisions (Moreno and González,
2007a; Northcutt, 2008; González et al., 2010). Is there any
evidence for the existence of more than one amygdaloid nucleus
(if any, at all) in ray-finned fishes? The present review will
attempt to organize developmental, topological (i.e., positional
and cytoarchitectonic), hodological, and functional data to argue
that the dorsomedial pallium, or part of it, is homologous to the
frontotemporal amygdaloid system, while the commissural and
postcommissural nuclei of the ventral pallium represent the
autonomic amygdaloid system. Whenever possible, we will refer
to Simpson’s (1961) criteria for historical homology (topological
similarity; topographical similarity; hodological similarity;
similarity of morphogenetic field; similarity in the morphologi-
cal features of individual neurons that form the structure;
neurochemical similarity; neurophysiological similarity; and
similarity in the behavioral results of neuronal activity). The
criteria of continuous history and linear modification of
characters are also considered. We will begin by briefly reviewing
the eversion vs. evagination problem, then lay out a structural
and functional organization of the amygdaloid complex, and
finally gather evidence for our argument.
2. The problem of topography
The main difficulty in establishing homologies between
telencephalic structures among ray-finned fishes and other
vertebrates is that the telencephalic hemispheres develop in
different modes in these taxa. In ray-finned fishes, a process of
eversion of the hemispheres (Nieuwenhuys, 1962a,b, 1969)
implies reversal of the medial-to-lateral topography that is
observed in the evaginated telencephali of other vertebrates
(Fig. 1A). In all vertebrates, four pallial subregions (medial, dorsal,
lateral and ventral pallia) are recognized as homologues in
embryonic and adult vertebrates (Smith-Fernandez et al., 1998;
Puelles et al., 2000, 2004; Puelles, 2001). In evagination, the central
lumen of the neural tube enlarges to form the telencephalic
ventricles; the part of the pallium that was originally in the most
dorsomedial position (medial pallium, MP) comes to lie in the most
medial part of the telencephalon. The originally intermediate
pallial area (dorsal pallium, DP) will lie dorsally, and the pallial area
which originally rested in the ventrolateral portion of the neural
tube will lie most laterally, giving rise to the lateral pallium (LP). A
fourth pallial area, the ventral pallium (VP), will lie ventrally
(Fig. 1A).
In non-teleost ray-finned fishes, the eversion process leads the
part of the roof of the neural tube to thin and enlongate, and the
pallial parts of the hemispheres bend outward (Nieuwenhuys,
1962a,b, 1964, 1969). Thus, after eversion, MP will lie at the most
laterally distal portion of the telencephalon, DP will lie most
dorsally (as in other vertebrates), LP will lie in a medial position,
and VP will lie in the most proximal (medial) position. This process
of simple eversion reverses the topography of the pallial areas
while maintaining the topology (Wullimann and Mueller, 2004;
Butler and Hodos, 2005; Northcutt, 2006, 2008; Braford, 2009).
A simple eversion, however, is difficult to sustain for teleost
fishes, since the major pallial targets of the olfactory bulb in this
group, the posterior zone of area dorsalis (Dp) and the nucleus
taenia (NT), are located in a ventrolateral position (Levine and
Dethier, 1985; Folgueira et al., 2004a; Northcutt, 2006) – in which a
medial pallium should be expected. The problem of eversion in
teleosts produced many different models of how this process
occurs. Braford (2009) reviewed those available at the time, and
listed models of partial eversion (Wullimann and Rink, 2002;
Wullimann and Mueller, 2004; Mueller and Wullimann, 2009;
Wullimann, 2009), caudolateral eversion plus displacement
(Yamamoto et al., 2007), and simple eversion with displaced
olfactory projections (Butler, 2000; Nieuwenhuys, 1962a, 1962b,
1963, 1969, 2009a, 2009b, 2011). The resulting homologies which
have been proposed can be found in Table 1.
The medial zone of area dorsalis (Dm) is the pallial zone most
proximal to the (non-everted) subpallium in teleosts, being almost
continual with the subcommissural subpallium (Vs) at the level of
the anterior commissure. At caudal pallial levels, Dp is adjacent to
Dm, but it appears to be absent at more rostral levels. Braford
(1995, 2009), based on cytoarchitectonics and on the presence of
olfactory bulb inputs and outputs within it, considered that a
expansion of the Dm in teleosts led to a lateral displacement of Dp.
Thus, if we follow a flat map of the ventricular surface of the
telencephalon of a teleost, pallial zones are arranged from the
subpallium (SP) in the following order: Dm, Dp, Dd, and Dl
(Figure 1B).
Support for these observations also arose from experiments on
the embryonic expression of the basic loop-helix-loop genes
neurogenin1 and neuroD and proliferation studies in Danio rerio
(Adolf et al., 2006; Mueller and Wullimann, 2003; Mueller et al.,
2011), which suggest that Dp is a rostrolaterally dislocated portion of
the (embryonic) lateral pallium. Using bromo-deoxy-uridine (BrdU),
a marker for proliferative cells, in zebrafish embryos, Mueller and
 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13 3

Fig. 1. Evagination and eversion processes result in different topologies of telencephalic histogenetic domains in ray-finned fishes and in tetrapods. (A) Topology of medial
pallium (MP, dark green), dorsal pallium (DP, light green), lateral and/or ventral pallium (LP/VP, yellow) and subpallium (SP, blue) from the neural tube towards the two
developmental trajectories, resulting in their adult position. (B) Flat map of the ventricular surface of the central portion of a teleostean telencephalon. Colors represent the
proposed embryonic origin of each region (Yellow: VP; Blue: subpallium; Dark green: SP; Beige: LP). Notice that the embryonic origin of Dd and Dp are still under debate.
Modified from Braford (1995). (For interpretation of the color information in this figure legend, the reader is referred to the web version of the article.)

Table 1
Proposed pallial homologies in different ray-finned fish clades, according to different models of the developmental trajectory of eversion.

References Ventral Lateral Dorsal Medial

pallium (VP) pallium (LP) pallium (DP) pallium (MP)

Polypteriformes Bruce and Braford (2008) P1v P1d P2? P3

Sturgeon Huesa et al. (2000) Dm Dl? Dd Dl
Gars Braford (1980), Northcutt (2009) Dm Dp Dd Dl

Teleosts Butler (2000) – Dm Dd, Dld Dp, Dlv, Dlp

Northcutt (2006, 2008) Dm Dp Dd? Dl
Bruce and Braford (2008) Dm Dp Dd? Dl
Wullimann and Mueller (2004) Dmv Dp Dmd, Dd, Dld Dlv
Yamamoto et al. (2007) NT Dp Dm, Dd, Dld Dld
Nieuwenhuys (2009) – Dm Dd Dl, Dp
Braford (2009) Dm Dp Dd Dl
Mueller et al. (2011) Dm Dp, lateral Dc Dl
border of Dm

colleagues (2011) demonstrated a chain of enlongated BrdU-

positive cells originated in a lateral field of Dm and moving towards
a cell-poor area of what will become Dp. When these migrating cells
arrive at their destination, they do not readily mature into neurons,
while cells from the nearby proliferative matrix of the lateral zone of
area dorsalis (Dl) co-express the neuronal marker HuC/D (Mueller
et al., 2011). This later finding reinforces the idea that Dp originates
from this migratory stream, and not from the proliferative zones of
the Dl as suggested by other authors.
The question of which model better explains the topology and
topography of the teleostean telencephalon is still very much open.
In this article, we will assume Dm as homologous to VP and Dp as
homologous to LP (Fig. 2). The question of whether or not a dorsal
pallium exists or how it forms is not of direct interest, but
nonetheless we will assume that Dd and Dc are homologous to DP
(Fig. 2).

3. The amniote amygdaloid complex

Functionally, the amygdaloid complex (AC) can be divided in

olfactory, autonomic and frontotemporal systems (Swanson and
Petrovich, 1998). The first division can be subdivided in an
accessory olfactory (or vomeronasal) component, dominated (in
lungfishes and tetrapods) by the medial amygdala (MeA), one of
the major targets from projections from the accessory olfactory
bulb (Martı́nez-Garcı́a et al., 2002, 2007; Moreno and González,
2007a; González et al., 2010; Medina et al., 2011). This region is
involved in the perception of pheromonal stimuli, including social
recognition (Newman, 1999) and detection of predators or their
Fig. 2. Proposed topography and homologies for telencephalic structures in this
article. (A) Saggital view. (B) Coronal view at a subcommissural level. (C) Coronal
view at a postcommissural level. The homologies are color-coded, so that
yellow = VP, beige = LP, light green = DP, and dark green = MP. Modified from
Mueller et al. (2006) and Mueller (2012). (For interpretation of the color
information in this figure legend, the reader is referred to the web version of
the article.)
4 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
Fig. 3. Ventral pallial (yellow) and subpallial (blue) amygdalae in lampreys, teleosts, lungfishes, and in the coelacanth. Adapted from Northcutt (2008), Northcutt and
González (2011), and Pombal et al. (2011). (For interpretation of the color information in this figure legend, the reader is referred to the web version of the article.)
odors (Canteras, 2008). The second subdivision is the main
olfactory component, dominated in mammals by the basomedial
and posterior amygdalae as well as the posterior portion of the
basolateral amygdala (Swanson and Petrovich, 1998). The acces-
sory and main olfactory components arise from different
histogenetic fields, with the first being subpallial in origin and
the second being ventropallial (Medina et al., 2004; Garcia-Lopez
et al., 2008; Waclaw et al., 2010; Bupesh et al., 2011a). Although
bony fishes do not show a complete vomeronasal system,
pathways from different receptors have been described that detect
social cues, sex pheromones, food odors, and (in Ostariophysan
fish) skin extract from conspecifics (Ubeda-Bañon et al., 2011); a
complete vomeronasal system appears only in lungfish (González
et al., 2010), but it has been argued that the segregated olfactory
system of Osteichthyes is a primitive form of the olfactory-
vomeronasal distinction (Ubeda-Bañon et al., 2011).
The second multisensorial system proposed by Swanson and
Petrovich (1998) is the frontotemporal amygdaloid system, of
ventropallial origin (Medina et al., 2004; Waclaw et al., 2010). The
concept of ventral pallium (VP) has been introduced by Puelles and
colleagues (1999, 2000), and a VP homolog has been proposed even
in lampreys in the ventral part of the evaginated portion of the
telencephalon, while a structure called sub-hippocampal lobe has
been interpreted as the pallial extended amygdala (Pombal et al.,
2009, 2011) (Fig. 3). This system is composed mainly of the
anterior portion of the basolateral amygdala (BLA) and the lateral
amygdala (LA). These areas have long been proposed to be the
‘‘sensory interface’’ of the ‘‘amygdala fear system’’ (LeDoux, 1998,
2003), and synaptic plasticity in both nuclei have been proposed to
underlie fear conditioning (Blair et al., 2001; Fanselow and LeDoux,
1999). In amphibians and fish, a differentiation between the
frontotemporal and the olfactory amygdaloid systems has not
generally been recognized and thus it makes more sense to
consider the pallial amygdalae as a single ‘‘multisensorial
amygdala’’ which receives major olfactory information, but also
polymodal inputs from the thalamus and brainstem (Martı́nez-
Garcı́a et al., 2002, 2007; Moreno and González, 2006; Moreno and
González, 2007a; Medina et al., 2011).
The last component we will consider is the ‘‘autonomic
amygdala’’, composed mainly of the central extended amygdala
(CEXA, composed of central amygdala (CeA) and bed nucleus of the
stria terminalis (BNST)). This component is subpallial in origin,
being a ventromedial expansion of the striatum which has
characteristic brainstem projections to regions of the central
autonomic nervous system, including the dorsal motor nucleus of
the vagus nerve, the nucleus of the solitary tract, and the
parabrachial nucleus, as well as to regions of the lateral
hypothalamic area and periaqueductal gray (Swanson and
Petrovich, 1998).
The amygdaloid complex, thus, has pallial and subpallial
components. The pallial amygdala is composed of developmental
derivatives of the lateral and ventral pallial histogenetic domains,
while the subpallial amygdala consists of developmental deriva-
tives of the lateral and medial ganglionic eminences (Puelles et al.,
1999, 2000; Martı́nez-Garcı́a et al., 2002; Medina et al., 2005;
Moreno and González, 2006, 2007a). The lateral pallial domain has
so far been clearly recognized in mammals, but attempts to
identify it in other taxa exist (Table 1). The pallial amygdala of
mammals is a heterogeneous region, with some nuclei (nucleus of
the lateral olfactory tract, cortical nucleus, and postpiriform and
piriform amygdalar areas) being a caudal expansion of the
olfactory cortex (cortical amygdaloid nuclei, derived from the
lateral pallium) and the some part (lateral, basal and posterior
nuclei) being a ventromedial expansion of the claustrum (claustral
amygdaloid nuclei, derived from the ventral pallium) (Swanson
and Petrovich, 1998). Pallial amygdaloid nuclei use glutamate as a
neurotransmitter in its projection neurons. The subpallial amyg-
dala (central and medial nuclei, and anterior area), however, is
more heterogeneous developmentally. The central and a dorsal
part of the anterior amygdala should be considered striatal-like
 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
(deriving from the lateral ganglionic eminence (LGE); Swanson and
Petrovich, 1998; Garcı́a-López et al., 2008; Waclaw et al., 2010;
Bupesh et al., 2011a,b). On the other hand, the medial amygdala
and the bed nucleus of the stria terminalis includes different cell
subpopulations derived from the ventral pallium, caudoventral
medial ganglionic eminence (MGE), preoptic area and supraopto-
paraventricular subdivision of the hypothalamus (Michaud et al.,
1998; Garcı́a-López et al., 2008; Hirata et al., 2009; Soma et al.,
2009; Carney et al., 2010; Garcı́a-Moreno et al., 2010; Bupesh et al.,
2011a,b; Medina et al., 2011).
The major divisions of the telencephalon show distinct
expression of several developmental regulatory genes, giving
rise to different cell groups (Puelles et al., 2004). Cell groups
derived from the lateral pallium express Emx and Tbr1; cells
derived from the ventral pallium express Tbr1, Dbx-1, and Lhx9;
and the cell groups derived from the subpallium express Dlx1,
Dlx2, and GAD67 (Medina et al., 2004, 2005, 2011; Moreno and
González, 2007a; Puelles et al., 2000, 2004) (Fig. 4). Thus, from a
genoarchitectural and developmental point of view, the amygdala
of amniotes can be divided in at least four components: a ventral
pallial part (including the basal amygdalar complex and a
subpopulation of the medial amygdala), which expresses Lhx2
and Lhx9; a striatal part (including the central amygdala),
expressing Pax6 and Islet1; a pallidal part (including portions
of the medial amygdala), expressing Nkx2.1 and Lhx6; a
Fig. 4. (A) Pallial and subpallial progenitor pools, identified in teleosts and rodents, which give rise to adult amygdalar populations. (B) Adult expression of pallial and
subpallial amygdalar markers in the teleost brain. Adapted from Medina et al. (2011).
5
hypothalamic part, expressing Otp, Sim1 and Lhx5; and a preoptic
part, expressing Shh. The LGE, MGE and diencephalic sources of
future amygdalar cells are in fact a shared source for other brain
regions (Nery et al., 2002; Remédios et al., 2007; Garcı́a-Moreno
et al., 2010; Bupesh et al., 2011a,b; Cocas et al., 2011; Sokolowski
and Corbin, 2012).
Besides these shared progenitor pools, other pools appear to be
dedicated primarily for the amygdala (Sokolowski and Corbin,
2012)–such as the populations which are present at the pallial-
subpallial border (PSB), which is determined by the interaction
between pax6 and the nuclear receptor tlx (Stenman et al., 2003).
These populations express combinations of homeodomain genes
such as pax6, emx1, gsx2 and dbx1. These cells will supply the
excitatory neurons of the AC and the intercalated cell masses
(Puelles et al., 2000; Garcı́a-López et al., 2008; Xu et al., 2008;
Hirata et al., 2009; Soma et al., 2009; Carney et al., 2010; Kaoru
et al., 2010; Cocas et al., 2011). The fate of emx-1-expressing cells is
determined by other transcription factors: cells expressing pax6
will integrate the excitatory neuronal populations of the amygdala,
while cells expressing gsx2 and dlx2 are fated as inhibitory neurons
(Cocas et al., 2011).
In the embryonic zebrafish (Danio rerio) telencephalon, as in
mice, pax6 marks the PSB (Wullimann and Rink, 2001); posteriorly,
Pax6-positive cells extend increasingly more into the pallium, the
area where the developing lateral and ventral pallia are located
6 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
(Wullimann and Rink, 2002). Concomitantly, the expression of
eomesa (tbr-2) is observed only above the PSB in zebrafish larvae
(Mueller et al., 2008). This expression domain is homologous to the
migrating stream of the PSB of amniotes (Smith-Fernandez et al.,
1998; Puelles et al., 2000; Brox et al., 2004).
The murine MGE expresses a combination of markers–Mash1,
Dlx1/2, Lhx1, Lhx2, Lhx6, Lhx7 and isoforms of gad. In contrast, the
LGE lacks Lhx6/7, but expresses Lhx1/2 (Rétaux et al., 1999). In
zebrafish embryos, Dlx1/2 isoforms are expressed in the sub-
pallium in a rostrocaudal and ventrodorsal gradient, with strong
expression of dlx2a in the ventral subdvision of the dorsal
subpallium (Sdv) and weaker expression in the dorsal subdivision
(Sdd) (Zerucha et al., 2000; Ganz et al., 2012); dlx2b is expressed in
all subdivisions of the dorsal subpallium, while lhx1b expression is
restricted to the Sdv (Ganz et al., 2012). In medaka and zebrafish
embryos, lhx7 is expressed in both subdivisions (Alunni et al.,
2004; Mueller et al., 2008). This expression pattern suggests that
the embryonic Sdd is homologous to the mammalian MGE, while
the embryonic Sdv is homologous to the mammalian LGE.
The diencephalic progenitor pool is harder to identify. Two Otp
isoforms were identified in zebrafish, otp1 and otp2 (Del Giacco
et al., 2006). Embryonic expression of both isoforms is limited by
the tract of the anterior commissure and does not enter the
telencephalon, being restricted to the preoptic area and ventral
hypothalamus (Del Giacco et al., 2006; Blechman et al., 2007; Eaton
et al., 2008; Ryu et al., 2007; Amir-Zilberstein et al., 2012); lhx5, on
the other hand is expressed in a stream starting in the preoptic area
and reaching the more caudal portions of the dorsal telencephalon
(Peng and Westerfield, 2006). While sim1 expression is found in
the ventralmost portions of the telencephalon in early develop-
ment, at 53 hpf it is limited by the anterior commissure (Eaton and
Glasgow, 2007). Unfortunately, adult expression data is not
available, which hinders the definition of amygdalar cells derived
from the diencephalon in fish.
4. The dorsomedial pallium as frontotemporal amygdaloid
system
4.1. Topography and topology
As previously mentioned, the adult teleostean telencephalon is
the result of an eversion process and thus the teleostean medial
zone of area dorsalis, or dorsomedial pallium (Dm), topographi-
cally corresponds to the lateroventral pallium of ‘‘evaginated
brains’’ (Fig. 1). Topologically, thus corresponds to the amniote
pallial amygdala. Dm is delimited by the subcommissural nucleus
of the subpallium (Vs) at its caudal extent and by the posterior
zone of area dorsalis (Dp) at its caudal and lateral extent (Fig. 2A–
C).
4.2. Cytoarchitectonics and neurochemistry
In adult zebrafish, astroglial cells have been reported in the
dorsal and medial portions of the telencephalon, and these cells
have long processes extending towards the center of the
telencephalon (Grupp et al., 2010). The Dm of adult goldfish
(Carassius auratus) is composed of a superficial layer of densely
packed granule-like neurons that overlay a core of larger cells
which increase in diameter in a rostrocaudal and dorsoventral
gradients (Northcutt, 2006), a gradient that is inverse to that
observed in rats (de Olmos et al., 2004). The cells from the Dm are
the largest found in the goldfish pallium (Northcutt, 2006); cells
from the rodent BLA also have very large perykaria (de Olmos et al.,
2004). Choline acetyltransferase immunoreactive fibers are
observed in the Dm of zebrafish (Clemente et al., 2004) in
anterodorsal (high density) to posteroventromedial (low density)
gradient that agrees with the gradient observed in the lateral
amygdala of rats (Hellendall et al., 1986).
In both the rostral and caudal portions of the Dm, a moderate
concentration of calretinin-positive cells is found (Northcutt,
2006). On the basis of calretinin-like immunoreactivity, Castro
et al. (2003) differentiated at least four zones in the Dm of trouts
along the rostrocaudal axis. About half of the GABAergic
interneurons of the mammalian basolateral and lateral amygdala
express parvalbumin, while the other half express either calbindin
or calretinin (Kemppainen and Pitkanen, 2000); however, in
zebrafish, parvalbumin-positive neurons are virtually absent in the
Dm (Mueller et al., 2011).
From a neurochemical point of view, some important marker
molecules are expressed in the Dm. While CRF expression is
lacking in this region (consistent with homology with frontotem-
poral amygdala), urotensin I is moderately expressed in the rostral,
but not caudal, portion of the Dm of zebrafish (Alderman and
Bernier, 2007). Likewise, in goldfish, vasotocin immunoreactive
fibers terminate in the Dm at a level just rostral to the anterior
commissure (Thompson and Walton, 2009). In the catfish
telencephalon, low levels of cocaine- and amphetamine-regulated
transcript peptide (CART), a peptide enriched in the medial
amygdala of rodents (de Olmos et al., 2004), are found in the Dm
(Subhedar et al., 2011). These peptides are expressed or secreted at
neurons of the vomeronasal amygdala of mammals, but are also
present in the BLA (Koylu et al., 1998; Sofroniew, 1980).
4.3. Hodology
In trouts, the ventralmost part of the precommissural Dm, Dmv,
receives a direct input from the olfactory bulb via the medial
olfactory tract (mot) (Folgueira et al., 2004a). The olfactory bulb
cells which project to the Dmv are calretinin-positive cells from the
medial portions of the olfactory bulb (Gayoso et al., 2011), a region
which, in crucian carps (Carassius carassius) have neurons which
are selective and sensitive for skin extracts (‘‘Shreckstoff’’) from
conspecifics (Hamdani and Døving, 2003; Lastein et al., 2008)–a
potent stimulus inducing fear-like behavior in Ostartyophysan fish
(Pfeiffer, 1977). These hodological data argue for the Dmv being
part of a ‘‘vomeronasal’’ system; however, as we will see below,
subpallial components receive much more extensive projections
from the Schreckstoff-sensitive medial olfactory bulb.
In Carassius auratus, the Dm receives projections from the
central zone of area dorsalis (Dc), the dorsal zone of area dorsalis
(Dd), and from the dorsal portion of the lateral zone of area dorsalis
(Dld). Subpallial projections come from the dorsal, ventral, lateral,
subcommissural, postcommissural, and intermediate zones of area
ventralis (Vd, Vv, Vl, Vs and Vi). At the diencephalic level,
projections to the Dm come from the anterior parvocellular
preoptic nucleus, dorsal and ventral zones of the periventricular
hypothalamus, all nuclei of the preglomerular complex, central
posterior thalamic nucleus, anterior tuber, posterior tuberal
nucleus, subglomerular nucleus, and posterior thalamic nucleus
(Northcutt, 2006). The preglomerular nuclei that show the densest
projection to the Dm receive auditory (nucleus preglomerulosus
anterior and caudal zone of nucleus preglomerulosus lateralis) and
chemosensory (nucleus preglomerulosus medialis and subglo-
merular nucleus) inputs (Butler and Hodos, 2005).
In the rainbow trout and goldfish, projections from the anterior
portion of the Dm (Dmr, or Dm1) terminate caudally in the
precommissural and postcommissural portions of Dm (Folgueira
et al., 2004b; Northcutt, 2006). Interestingly, this region expresses
transcription factors which are markers of the intercalated masses
(see below), which include interneurons that mediate signaling
between the basolateral complex and the central amygdala (Royer
et al., 1999). Projections from the Dmr can also be found in the
 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
preoptic nucleus and ventrolateral part of the anterior preglo-
merular nucleus, and course caudally through a dense fascicle as
part of the lateral forebrain bundle (lfb), reaching the anterior
tuberal nucleus (Folgueira et al., 2004b). In goldfish, the lfb courses
caudally, with a small number of fibers continuing dorsally,
terminating in the deep white zone of the optic tectum
immediately dorsal to the periventricular gray zone (Northcutt,
2006). The fibers which course caudally will terminate in the dorsal
hypothalamic neuropil (Northcutt, 2006; Rink and Wullimann,
1998). These efferents differ from those of the frontotemporal
system of mammals, but are reminiscent of the projections of the
striatal amygdala (Swanson and Petrovich, 1998), suggesting that
no differentiation between accessory and olfactory amygdaloid
systems exist in teleosts.
Projections from the precommissural Dm of the rainbow trout
cross through the anterior commissure to the neighboring
postcommissural Dm, and in the ventral, dorsal, and supracom-
missural nucleus of area ventralis telencephalis, as well as the
preoptic region (Folgueira et al., 2004b). In goldfish, the terminals
in Vs are dense, and a laterally situated ring of cells and a central
neuropil within Vs receive the densest projection (Northcutt,
2006). A small projection is observed in the ventrolateral region of
the habenula (Folgueira et al., 2004b), a region that projects
selectively to central and intermediate subnuclei of the inter-
peduncular nucleus and ventrorostral part of the raphe nucleus
(Tomizawa et al., 2001).
In trout, the postcommissural Dm projects to some cells in the
lateral zone of area ventralis (Vl) and to a group of cells in the
central zone of area dorsalis (Dc) adjacent to Dm and the preoptic
nucleus, as well as to several regions of the inferior hypothalamic
lobe (preglomerular complex, torus lateralis, diffuse nucleus,
lateral recess nucleus, and nucleus subglomerulosus) (Folgueira
et al., 2004b).
4.4. Expression of developmental regulatory genes
In mice and chick embryos, the expression of pallial genes such
as emx1 is limited by the domain of migrated pax6 cells, leaving a
gap between dlx and tbr1 gene expression that was identified as the
VP (Smith-Fernandez et al., 1998; Puelles et al., 2000). Similarly, in
zebrafish, cells moving from the proliferative zone to the VP
express, sequentially, dlx1a/2a, dlx5a/6a and gad1 (MacDonald
et al., 2010; Robles et al., 2011), which will presumably compose
GABAergic interneurons in the adult Dm (Fig. 4A). Interestingly,
adult expression of dlx5a is not found in the Dm, but scattered
expression is found at the commisural level in the border between
Dm and Dc, as well as in the Dp (Ganz et al., 2012). A similar pattern
is observed in the piriform cortex and in the paracapsular
intercalated cell masses (ITC) of the amygdala of mice (Waclaw
et al., 2010), a cluster of inhibitory neurons which envelops the
basolateral and lateral amygdalae and interface its connections
with the CeA (Royer et al., 1999). Likewise, the forkhead
transcription factor FoxP2 is expressed in the caudal portion of
the zebrafish Dm, and is conspicuously absent in any other region
of the telencephalon (Shah et al., 2006). Some of the foxp2-positive
cells also express emx1. Although its expression in adult animals is
unknown, the homeobox gene meis2.1 is expressed in the
telencephalon in larval zebrafish (24 hpf) (Zerucha and Prince,
2000), suggesting the presence of at least two markers for the ITC
(Waclaw et al., 2010) in this region. Together with the hodological
data pointing to the caudal Dm as the interface between the
rostralmost portions and the subpallial amygdalar nuclei, these
expression data suggest that this region is homologous to the ITC.
However, there are evidences that this cell group is GABAergic in
mammals (Millhouse, 1986; Royer et al., 1999; Marowsky et al.,
2005), while there is no evidence that GAD67 is more densely
7
expressed in the caudal Dm than in other portions of it (Mueller
and Guo, 2009). Moreover, while the Dm is of ventropallial origin
(Braford, 2009), the mammalian ITC is derived from a dorsal
subdivision of the LGE (Kaoru et al., 2010; Waclaw et al., 2010;
Bupesh et al., 2011b). This poses a problem for homologizing the
ITC in teleosts, and future research is necessary to solve the
difficulty.
eomesa (tbr2)-positive cells migrate from the midline pallium
toward the lateral and ventral periphery (Mueller et al., 2008). The
dorsomedial expression of emx paralogs (Viktorin et al., 2009) is
also consistent with the proposal of field homology between Dm
and VP (Fig. 4B). In disagreement, however, lhx9, is expressed in the
dorsal pallium of medaka embryos (Oryzias latipes) (Alunni et al.,
2004) instead of in its expected expression in the ventral pallium.
4.5. Neurophysiology and behavior
So far, very few neurophysiological experiments were made in
the medial zone of area dorsalis telencephalis in teleost fish. Dm of
goldfish show a slow frequency (4–8 Hz) electrocorticographical
rhythm that is significantly accelerated (9–14 Hz) after noise- or
light-induced arousal (Schadé and Weiler, 1959). In the isolated
telencephalon of adult zebrafish, application of current in the
anterior Dm produces a negative peak in the posterior Dm, an
effect which is blocked by the non-specific ionotropic glutamate
receptor antagonist CNQX and potentiated by the GABAA receptor
antagonist BMI (Kim et al., 2004). Perfusion of KCl for 20 min
during current administration induces long-term potentiation
(LTP), an effect which is blocked by the NMDA receptor antagonist
APV and the broad spectrum inhibitor of protein kinases H-7, but
not the L-type calcium channel blocker nifedipine (Nam et al.,
2004). NMDA-dependent plasticity in the frontotemporal amyg-
daloid system has been proposed as characteristic mechanism for
the induction of fear conditioning in mammals (Blair et al., 2001;
Fanselow and LeDoux, 1999).
Among all sensory modalities conveyed to Dm (Wullimann and
Rink, 2002), an important nociceptive information also arrives. In
salmons, galvanic stimulation of the tail at noxious intensities
produce potentials in the Dm, with longer latency components
being introduced with increasing stimulus intensities (Nordgreen
et al., 2007). Thus, nociceptive information is also conveyed to the
dorsomedial telencephalon, suggesting the existence of a spino-
parabrachial-amygdalar pathway in teleosts that is involved in the
autonomic and affective aspects of nociception (Bernard et al.,
1996).
In Chinese mudskippers (Periophtalmus cantonensis), animals
which have been agitated for 1 h by stirring the water show
increased c-Fos-like immunoreactivity, a marker of stimulus-
induced neuronal activity, in the Dm (Wai et al., 2006). An
important result is the increased expression of c-fos mRNA in the
Dm after exposure of adult zebrafish to a light/dark box (Lau
et al., 2012), a manipulation thought to induce anxiety-like
responses (Maximino et al., 2010b). Interestingly, when animals
were handled before exposure to the apparatus (a manipulation
which increases whole-body cortisol levels (Ramsay et al., 2009)
albeit not changing behavior in this particular version of the test
(Lau et al., 2012)), c-fos mRNA expression was dramatically
increased.
The c-fos expression experiments above suggest that the Dm is
activated during exposure to an anxiogenic situation. Lesion
experiments, conversely, also suggest a role for this region on the
acquisition of fear conditioning. Lesions of the posterior Dm were
associated with deficits in habituation of startle responses in
Rutilus rutilus (Laming and Hornby, 1981) and Carassius auratus
(Rooney and Laming, 1986), although an opposite result has been
observed in Betta splendens (Marino-Neto and Sabbatini, 1983).
8 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
More recently, Cosme Salas and colleagues demonstrated that
lesions in Dm, but not in Dl, of goldfish impair the acquisition of
active avoidance (Portavella et al., 2004a,b; Portavella and Vargas,
2005), conditioned emotional bradycardia (Álvarez et al., 2003),
and taste aversion (Martı́n et al., 2011). Likewise, microinjection of
D-AP5, a NMDA receptor antagonist, into Dm of goldfish also
impairs the acquisition of active avoidance (Xu et al., 2003), an
effect which is mimicked by the nitric oxide synthase inhibitor L-
NAME and the cyclic guanosine monophosphate inhibitor LY-
83483 (Xu et al., 2009).
5. The sub- and postcommissural subpallia as striatal
amygdalae
5.1. Topography and topology
The subcommissural nucleus of area ventralis telencephalis
(Vs) occupies most of the caudal dorsomedial wall of the
telencephalon (Fig. 2C). It is located ventrally to the dorsal nucleus
of area ventralis telencephalis (Vd, proposed as the homolog for the
striatum), dorsally to the anterior commissure (CANT), and
ventrolaterally to the caudal portion of Dm (Folgueira et al.,
2004a; Northcutt, 2006). The postcommissural nucleus of area
ventralis telencephalis (Vp) is located posterior to the anterior
commissure at the level of the optic tract (Folgueira et al., 2004a;
Northcutt, 2006). Vp can be distinguished by Vs by a lack of
calretinin-like immunoreactivity (Castro et al., 2003). In mammals,
the medial nucleus of the amygdala is located in a position that is
comparable to that of the teleostean Vp, and the central amygdala
is located in a position that is comparable to that of the teleostean
Vs (Sah et al., 2003).
5.2. Cytoarchitectonics and neurochemistry
A description of the cytoarchitectonics of Vs is found in goldfish
(Northcutt, 2006). This region is characterized by a moderate
number of tyrosine hydroxylase 1 (TH1)-positive, TH2-negative
cells and fibers (Northcutt, 2006; Yamamoto et al., 2010); this
immunoreactivity is probably due to a band of cells and fibers
emerging from the anterior and posterior A16 group (olfactory
bulbs and Vd) and ending in the caudal margin of Vp (Kaslin and
Panula, 2001). The density of serotonergic fibers is moderate
(Kaslin and Panula, 2001) and probably originated from the
superior raphe (Lillesaar et al., 2009; Lillesaar, 2011). Both Vs and
Vp are heavily labeled for GAD67, consistent with a GABAergic
output in these regions (Mueller and Guo, 2009). gad67 mRNA
expression appears in many areas of the subpallium of zebrafish at
3 days postfertilization (Mueller et al., 2006); the GAD67-positive
cells which will compose the adult Vs and Vp migrate from the
ventral division of the dorsal subpallium of larvae (Sdv),
homologous to the medial ganglionic eminence of tetrapods
(Mueller et al., 2006; Mueller and Guo, 2009).
The main trait that characterizes the centromedial or striatal
amygdaloid system is the extensive presence of neuropeptides (de
Olmos et al., 2004; Sah et al., 2003; Swanson and Petrovich, 1998).
For example, the CeA and BNST are the major source of
corticotropin-releasing factor (CRF) in the central nervous system,
outside of the hypothalamus (de Olmos et al., 2004); CART is
densely expressed in the medial amygdala (de Olmos et al., 2004);
and vasopressinergic and oxitonergic projections innervate the
central amygdala (Huber et al., 2005). In the catfish Clarias
gariepinus, CART is expressed at high levels in the rostral portion of
Vs, with decreasing expression at more caudal levels (Subhedar
et al., 2011). In the goldfish telencephalon, sparse but thick
vasotocinergic fibers terminate in the Vs and Vd, as well as in a Dm
zone just rostral to the CANT (Thompson and Walton, 2009). In
zebrafish, CRF and CRF binding protein (CRF-BP) are highly
expressed in Vs (Alderman and Bernier, 2007), and CRF is also
expressed in the Vs of tilapia (Oreochromis mossambicus) in which,
nonetheless, the highest CRF concentration is found in the Vl
(Pepels et al., 2002a,b). However, as stated before, CART is also
expressed at Dm.
5.3. Hodology
The Vs makes reciprocal connections with the olfactory bulbs,
Dm, Vv, Vd, preoptic area, ventral thalamus, preglomerular
complex, anterior and lateral tuberal nuclei, and periventricular
hypothalamus. Projections to the Vs come from the dorsal
thalamus, suprachiasmatic nucleus, tertiary gustatory nucleus,
torus semicircularis and locus coeruleus (Folgueira et al., 2004a;
Northcutt, 2006). A dense projection comes from calretinin-
positive cells from the medial portions of the olfactory bulb
(Gayoso et al., 2011), the region which is sensitive to ‘‘Schreckstoff’’
(Hamdani and Døving, 2003; Lastein et al., 2008). While thalamic
projections are dense in Vs, they altogether avoid the specialized
cell ring and neuropil (Cr), which receives a substantial projection
from the anterior preglomerular nucleus in goldfish (Northcutt,
2006). A secondary trigeminal projection has also been observed in
Cyprinus carpio, relayed from the ventral thalamus (Xue et al.,
2006); this projection could correspond to the spino-trigemino-
parabrachio-amygdaloid pathway of mammals, which is involved
in the emotional aspects of pain (Bernard et al., 1996). In Nile
tilapia, a very important projection to Vs comes from the
commissural nucleus of Cajal (NCC) and area postrema (AP), the
targets of general visceral afferents of the vagal nerve (Yoshimoto
and Yamamoto, 2010), strongly suggesting that the Vs is part of the
central autonomic nervous system. Projections from Vs terminate
in Vp, Dm, dorsal and ventral portions of the Dl, Dc, Dp, habenula,
stratum griseum centrale of the optic tectum (SGC) and nucleus
subglomerulosus (Folgueira et al., 2004a; Rink and Wullimann,
2004; Sloan, 1989). An important projection from the dorsal
portion of Vs terminates in the ventral portion (Folgueira et al.,
2004a), which has been proposed to be homologous to the BNST
(Ganz et al., 2012).
The most extensive study of Vp connections was made in
rainbow trout (Folgueira et al., 2004a). In that species, Vp projects
to the posterior tubercle, and show reciprocal conections with the
preoptic area, anterior and lateral tuberal nuclei, and reticular
formation. In goldfish, a reciprocal connection between Vp and the
rostral portion of Dm (Dmr) has also been described (Northcutt,
2006). Projections to the Vp have been described as originating in
the olfactory bulbs, Vv, Vd, Vs, dorsal thalamus, periventricular
hypothalamic nuclei, lateral reticular tegmentum, torus semicir-
cularis, and superior raphe nucleus (Folgueira et al., 2004a; Rink
and Wullimann, 2004).
5.4. Expression of developmental regulatory genes
Cells from the Vd, Vs and Vp surround the dorsal subpallial
proliferation zone in larval zebrafish (Wullimann and Puelles,
1999), most of them migrating from the medial ganglionic
eminence (Sdv) to its final position as adults (Mueller et al.,
2006; Mueller and Guo, 2009). The zebrafish 5 dpf larva expresses,
in its Sdv, the markers dlx1a, dlx2a, dlx2b, lhx6, lhx7 and gad67, but
not tbr2 (Mueller et al., 2008; MacDonald et al., 2010). In medaka
stage 39 larvae, the expression of dlx2 and lhx7 overlaps with that
of nkx2.1b; the expression of nkx2.1b, however, disappears in adult
medaka (Alunni et al., 2004). In adult zebrafish Vs and Vp, the
expression of part of these genes is retained, with an important
mosaic (Figure 3B): the dorsal portion of Vs is devoid of nkx2.1b and
lhx1b expression; the medial portion is also devoid of these
 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
markers, butis positive for isl; finally, the ventral portion of Vs is
positive for all these markers (Ganz et al., 2012). Most of the
zebrafish adult Vp is devoid of nkx2.1b, lhx1b and isl expression,
but the ventral portion is positive for nkx2.1b and shows moderate
expression of lxh1b (Ganz et al., 2012). Thus, Ganz and colleagues
(2011) suggested that the dorsal and medial Vs and most of the Vp
are homologous to the central amygdala. The expression of
nkx21.b and lhx1b suggest that the ventral portions of Vs and Vp
are homologous to the bed nucleus of the stria terminalis (BNST),
as is observed in tetrapods (Abellán and Medina, 2009; Garcı́a-
López et al., 2008; Moreno et al., 2004; Puelles et al., 2000)
(Fig. 4B).
5.5. Neurophysiology and behavior
Again, very few neurophysiological experiments have been
made regarding Vs and Vp. As mentioned before, increased
expression of c-fos mRNA in the Dm after exposure of adult
zebrafish to a light/dark box; when animals are handled before
exposure, expression is also seem in the Vs and Vp (Lau et al.,
2012), suggesting that stressful manipulations which lead to
increases in anxiety-like behavior activate these regions. More-
over, lesions of the Vs increase fast-starts and decrease defensive
behavior in Macropodus opercularis and goldfish (Davis et al., 1976,
1978; Rooney and Laming, 1986).
6. Is there a medial amygdala in bony fishes?
In rodents, the medial amygdala has a dual prosencephalic
origin, expressing genes that are typical of subpallial components
(Garcı́a-López et al., 2008; Medina et al., 2004; Puelles et al., 2000;
Puelles et al., 2004) but also expressing diencephalic genes such as
otp, sim1, shh and brn2 (Garcı́a-López et al., 2008; Garcı́a-Moreno
et al., 2010; Wang and Lufkin, 2000). The medial amygdala has
multiple subdivisions with different origins–preoptic area, ventral
pallium, medial ganglionic area and anterior peduncular area
(Garcı́a-López et al., 2008; Hirata et al., 2009; Abellán and Medina,
2009; Carney et al., 2010; Bupesh et al., 2011a). In lungfish, the
medial amygdala is characterized by the expression of otp and isl,
but not nkx2.1, as well as the presence of nitric oxide synthase and
substance P (González et al., 2010). These characteristics were also
demonstrated in amphibians (Bardet et al., 2007; González et al.,
2002a; González et al., 2002b; Moreno and González, 2006;
Moreno and González, 2007b; Moreno et al., 2008). In mouse and
chick embryos, otp and dlx5 expression are mutually exclusive in
all regions of the forebrain, including the MeA (Bardet et al., 2007),
and the avian MeA expresses lhx5, lhx6, nkx2.1, shh, Islet1 and
gad67, but not lmo3 (Abellán and Medina, 2009; Abellán et al.,
2010). While otp expression has been described in a region of the
zebrafish larval subpallium that is an extension of the preoptic area
(Del Giacco et al., 2008; Eaton and Glasgow, 2007) and possibly
overlaps brn2 (Hauptmann and Gerster, 2000), Islet1 and nkx2.1b
(Ganz et al., 2012), the expression of otp paralogues in the zebrafish
brain have only been investigated in larvae, and are mainly
restricted to the hypothalamus and preoptic area. The evidence for
the existence of an MeA, thus, is weak.
The most compelling argument for the inexistence of an MeA in
bony fishes, though, is the absence of a discrete vomeronasal organ
in these animals (Ubeda-Bañon et al., 2011). While the number of
genes coding for olfactory receptors is much higher in fishes than
in tetrapods (Niimura and Nei, 2005), and while separate pathways
for social cues, sex pheromones, and food odors (Hamdani and
Doving, 2007), a true vomeronasal system appears only in
lungfishes (González et al., 2010; Ubeda-Bañon et al., 2011) and
the secondary vomeronasal centers (especially the MeA) probably
do not exist in teleosts, are extremely reduced, or are not
9
differentiated from the CeA (Moreno and González, 2007a).
Hodological evidence would support the Vs and Vp as putative
MeA homologues, as these regions receive primary and secondary
olfactory fibers and project to other subpallial regions, hypothala-
mus, and posterior tubercle (Folgueira et al., 2004a; Folgueira et al.,
2004b). These evidences, however, suggest the existence of an
‘‘undifferentiated’’ striatal amygdaloid area in the subpallium of
fish, at least as field homology. Further studies are necessary to
understand whether any portion of the adult Vs and/or Vp show
the genomic ‘‘barcode’’ for a MeA (i.e., otp+/isl+/sim1+/brn2+/
nkx2.1+/dlx5 /lmo3 ).
7. Evolutionary perspective
Based on calretinin immunocytochemistry, Nissl-stained par-
allel serial sections, and on the expression of molecular markers
such as dlx, Pombal and colleagues proposed a segmental
organization of the telencephalon of lampreys which considers
the subhippocampal lobe as part of the telencephalon and
interpreted this region as an unevaginated part of the pallial
extended amygdala (PEA) (Pombal and Puelles, 1999; Pombal et al.,
2009, 2011). The location of the PEA is ventrolateral to the medial
pallium, ventral to the dorsomedial telencephalic neuropil,
ventrolateral to the lateral pallium, lateral to the impar telence-
phalic ventricule, and dorsal to the striatum (Martı́nez-de-la-Torre
et al., 2011; Pombal et al., 2009, 2011). The caudal portion of the
medial pallium (MP) sends GABAergic projections to the optic
tectum (Robertson et al., 2006), hypothalamus and preoptic area
(Northcutt and Wicht, 1997), and to the mesencephalic locomotor
region (Ménard et al., 2007), and receives a massive input from the
olfactory bulb (Northcutt and Wicht, 1997). As in the medial
amygdala of tetrapods, expression of lhx1/5 is strongly detected in
the MP (Osório et al., 2006), and both the MP and the PEA are
devoid of dlx expression (Martı́nez-de-la-Torre et al., 2011). Thus, it
seems that, in lampreys, a MP-PEA continuum represents the
pallial amygdala. These structures, however, show important
characteristics of striatal amygdaloid nuclei, including GABAergic
projections and diencephalic and mesencephalic targets (de Arriba
and Pombal, 2007; Ménard et al., 2007; Northcutt and Wicht, 1997;
Robertson et al., 2006). Since no striatal amygdala has been found
in the lamprey brain, it is likely that a differentiation of amygdaloid
nuclei is a derived trait in vertebrates.
Supporting this interpretation is the analysis of the forebrain of
more derived vertebrates. In the Comoran coelacanth, cytological
and topographical evidence led Northcutt and González (2011) to
propose that the magnocellular preoptic nucleus is actually
homologous to the central amygdala, while the superior preoptic
nucleus is homologous to the medial amygdala. In lungfish,
similarly, a MeA has been identified as a target of the accessory
olfactory bulb in a postcommissural region right above the
preoptic area (González et al., 2010); based on cytoarchitectonical
evidence, the existence of a lateral, a medial, and a central
amygdala has been proposed in the telencephalon of lungfish
(González and Northcutt, 2009; Northcutt, 2009) (Figure 2).
8. Conclusion
The evidence gathered so far points strongly to a homology
between the dorsomedial telencephalon (Dm) of teleost fish and
the ventral pallial components of the tetrapod amygdala (i.e., the
laterobasal complex). Most evidence relies on the presence of
pallial markers, with special attention to Emx paralogs, neurogenin
and dbx1, all markers of the ventral histogenetic division in mice
(Medina et al., 2004); the sparse distribution, in adult fish, of
GAD67-positive cells, which suggest their role as inhibitory
interneurons instead of projection neurons (Mueller and Guo,
10 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
2009); the presence of neurogenin, which is required to specify
glutamatergic projection neurons in the cerebral cortex of mice
and mouse embryonic stem cells (Reyes et al., 2008; Schuurmans
et al., 2004); the expected projection to putative homologues of the
striatum and of the centromedial amygdala (Folgueira et al.,
2004a,b; Northcutt, 2006); and in the functional literature, which
assigns a role for Dm in aversive conditioning (Broglio et al., 2005).
However, some similarities between Dm and subpallial amygda-
loid nuclei (‘‘centromedial’’ or ‘‘striatal’’ nuclei) are also observed,
viz., the connections between Dm and hypothalamic and tectal
targets which, in mammals, are reached only by projections from
the CeA and MeA (Petrovich et al., 2001). This seems to be a
primitive condition, though, since in anuran and urodele amphi-
bians the autonomic and frontotemporal components are inter-
mixed in the telencephalon (Laberge et al., 2006), and an important
projection from the lateral amygdala reaches the ventral hypo-
thalamus via stria terminalis (Moreno and González, 2006, 2007a).
The evidence discussed also points to at least field homology
between the subcommissural and postcommissural regions of the
subpallium with components of the centromedial nucleus. These
regions present subpallial markers (e.g., dlx), and intense staining
for gad67 (MacDonald et al., 2010; Mueller et al., 2008; Mueller and
Guo, 2009), suggesting the presence of GABAergic projection
neurons. The presence of CRFergic cells (Alderman and Bernier,
2007; Pepels et al., 2002b) is also an important marker of the
central amygdala in amniotes. In terms of sensory input, Vs
receives a dense (pseudo-vomeronasal) olfactory projection
(Gayoso et al., 2011), visceral afferents from the autonomic
nervous system (Yoshimoto and Yamamoto, 2010), and a
nociceptive input from the spino-trigemino-parabrachio-amygda-
loid pathway (Xue et al., 2006).
Based on the distribution of molecular markers in adult
zebrafish brains, Ganz and colleagues (2011) suggested that the
dorsal and medial portions of Vs and most of the Vp are
homologous to the central amygdala, while the ventral portions
of Vs and Vp are homologous to the bed nucleus of the stria
terminalis (BNST). This proposal is in agreement with the
information reviewed in the present article.
Acknowledgments
C.M. and M.G.L. are recipients of CAPES/Brazil studentships.
A.M.H. is the recipient of a CNPQ/Brazil productivity grant.
References
Abellán, A., Medina, L., 2009. Subdivisions and derivatives of the chicken subpallium
based on expression of LIM and other regulatory genes and markers of neuron
subpopulations during development. Journal of Comparative Neurology 515,
465–501.
Abellán, A., Vernier, B., Rétaux, S., Medina, L., 2010. Similarities and differences in
the forebrain expression of Lhx1and Lhx5 between chicken and mouse. Insights
for understanding telencephalic development and evolution. Journal of Com-
parative Neurology 518, 3512–3528.
Adolf, B., Chapouton, P., Lam, C.S., Topp, S., Tannhäuser, B., Strähle, U., Götz, M.,
Bally-Cuif, L., 2006. Conserved and acquired features of adult neurogenesis in
the zebrafish telencephalon. Developmental Biology 295, 278–293.
Alderman, S.L., Bernier, N.J., 2007. Localization of corticotropin-releasing factor,
urotensin I, and CRF-binding protein gene expression in the brain of the
zebrafish, Danio rerio. Journal of Comparative Neurology 502, 783–793.
Alunni, A., Blin, M., Deschet, K., Bourratt, F., Vernier, P., Rétaux, S., 2004. Cloning and
developmental expression patterns of Dlx2, Lhx7 and Lhx9 in the medaka fish
(Oryzias latipes). Mechanisms of Development 121, 977–983.
Álvarez, E., Gómez, A., Durán, E., Ocaña, F.M., Jiménez-Moya, F., Broglio, C., Rodrı́-
guez, F., Salas, C., 2003. Brain substrates of eye blink classical conditioning in
goldfish. Acta Neurobiologiae Experimentalis 63, S62.
Amir-Zilberstein, L., Blechman, J., Sztainberg, Y., Norton, W.H.J., Reuveny, A., Bor-
odovsky, N., Tahor, M., Bonkowsky, J.L., Bally-Cuif, L., Chen, A., Levkowitz, G.,
2012. Homeodomain protein Otp and activity-dependent splicing modulate
neuronal adaptation to stress. Neuron 73, 279–291.
Bardet, S.M., Martinez-de-la-Torre, M., Northcutt, R.G., Rubenstein, J.L., Puelles, E.,
2007. Conserved pattern of OTP-positive cells in the paraventricular nucleus
and other hypothalamic sites of tetrapods. Brain Research Bulletin 75, 231–235.
Bernard, J.F., Bester, H., Besson, J.M., 1996. Involvement of the spino-parabrachio-
amygdaloid and -hypothalamic pathways in the autonomic and affective
emotional aspects of pain. Progress in Brain Research 107, 243–255.
Blair, H.T., Schafe, G.E., Bauer, E.P., Rodrigues, S.M., LeDoux, J.E., 2001. Synaptic
plasticity in the lateral amygdala: A cellular hypothesis of fear conditioning.
Learning and Memory 8, 229–242.
Blechman, J., Borodovsky, N., Eisenberg, M., Nabel-Rosen, H., Grimm, J., Levkowitz,
G., 2007. Specification of hypothalamic neurons by dual regulation of the
homeodomain protein Orthopedia. Development 134, 4417–4426.
Braford Jr., M.R., 1995. Comparative aspects of forebrain organization in the ray-
finned fishes: Touchstones or not? Brain, Behavior and Evolution 46, 259–274.
Braford Jr., M.R., 2009. Stalking the everted telencephalon: Comparisons of fore-
brain organization in basal ray-finned fishes and teleosts. Brain, Behavior and
Evolution 74, 56–76.
Braithwaite, V.A., Boulcott, P., 2007. Pain perception, aversion and fear in fish.
Diseases of Aquatic Organisms 75, 131–138.
Broglio, C., Gómez, A., Durán, E., Ocaña, F.M., Jiménez-Moya, F., Rodrı́guez, F., Salas,
C., 2005. Hallmarks of a common forebrain vertebrate plan: Specialized pallial
areas for spatial, temporal and emotional memory in actinopterygian fish. Brain
Research Bulletin 66, 277–281.
Brox, A., Puelles, L., Ferreiro, B., Medina, L., 2004. Expression of the genes Emx1, Tbr1
and Eomes (Tbr2) in the telencephalon of Xenopus laevis confirms the existence
of a ventral pallial division in all tetrapods. Journal of Comparative Neurology
474, 562–577.
Bupesh, M., Legaz, I., Abellán, A., Medina, L., 2011a. Multiple telencephalic and
extratelencephalic embryonic domains contribute neurons to the medial ex-
tended amygdala. Journal of Comparative Neurology 519, 1505–1525.
Bupesh, M., Abellán, A., Medina, L., 2011b. Genetic and experimental evidence
supports the continuum of the central extended amygdala and a multiple
embryonic origin of its principal neurons. Journal of Comparative Neurology
519, 3507–3531.
Butler, A.B., 2000. Topography and topology of the teleost telencephalon: A paradox
resolved. Neuroscience Letters 293, 95–98.
Butler, A.B., Hodos, W., 2005. Comparative vertebrate neuroanatomy. Evolution and
Adaptation, John Wiley & Sons, Hoboken.
Canteras, N.S., 2008. Neural systems activated in response to predators and partial
predator stimuli. In: Blanchard, R.J., Blanchard, D.C., Griebel, G., Nutt, D. (Eds.),
Handbook of Anxiety and Fear, Elsevier B.V., Amsterdam, pp. 125–140.
Canteras, N.S., Blanchard, D.C., 2008. A behavioral and neural systems comparison of
unconditioned and conditioned defensive behaviro. In: Blanchard, R.J., Blan-
chard, D.C., Griebel, G., Nutt, D. (Eds.), Handbook of anxiety and fear, Elsevier
B.V., Amsterdam, pp. 141–153.
Carney, R.S.E., Mangin, J.-M., Hayes, L., Mansfield, K., Sousa, V.H., Fishell, G., Mac-
hold, R.P., Ahn, S., Gallo, V., Corbin, J.G., 2010. Sonic hedgehog expressing and
responding cells generate neuronal diversity in the medial amygdala. Neural
Development 5, 14.
Castro, A., Becerra, M., Manso, M.J., Anadón, R., 2003. Distribution and development
of calretinin-like immunoreactivity in the telencephalon of the brown trout,
Salmo trutta fario. Journal of Comparative Neurology 467, 254–269.
Clemente, D., Porteros, Á., Weruaga, E., Alonso, J.R., Arenzana, F.J., Aijón, J., Arévalo,
R., 2004. Cholinergic elements in the zebrafish central nervous system: Histo-
chemical and immunohistochemical analysis. Journal of Comparative Neurolo-
gy 474, 75–107.
Cocas, L.A., Georgala, P.A., Mangin, J.M., Clegg, J.M., Kessaris, N., Haydar, T.F., Gallo,
V., Price, D.J., Corbin, J.G., 2011. Pax6 is required at the telencephalic pallial-
subpallial boundary for the generation of neuronal diversity in the postnatal
limbic system. Journal of Neuroscience 31, 5313–5324.
Davis, M., 2004. Neural circuitry of anxiety and stress disorders. In: Davis, K.L.,
Charney, D., Coyle, J.T., Nemeroff, C. (Eds.), Neuropsychopharmacology: The
Fifth Generation of Progress, American College of Neuropsychopharmacology,
New York, pp. 931–951.
Davis, R.E., Kassel, J., Schwagmeyer, P., 1976. Telencephalic lesions and behavior in
the teleost, Macropodus opercularis: Reproduction, startle reaction and operant
behavior in the male. Behavioral Biology 18, 165–177.
Davis, R.E., Reynolds, R.C., Ricks, A., 1978. Suppression behavior increased by
telencephalic lesions in the teleost, Macropodus opercularis. Behavioral Biology
24, 32–48.
de Arriba, M. d.C., Pombal, M.A., 2007. Afferent connections of the optic tectum in
lampreys: An experimental study. Brain, Behavior and Evolution 69, 37–68.
de Olmos, J.S., Beltramino, C.A., Alheid, G., 2004. Amygdala and extended amygdala
of the rat - A cytoarchitectonical, fibroarchitectonical and chemoarchitectonical
survey. In: Paxinos, G. (Ed.), The Rat Nervous System, Elsevier, New York, pp.
509–603.
Del Giacco, L., Sordino, P., Pistocchi, A., Andreakis, N., Tarallo, R., Di Benedetto, B.,
Cotelli, F., 2006. Differential regulation of the zebrafish orthopedia1gene during
fate determination of diencephalic neurons. BMC Developmental Biology 6, 50.
Del Giacco, L., Pistocchi, A., Cotelli, F., Fortunato, A.E., Sordino, P., 2008. A peek inside
the neurosecretory brain through Orthopedia lenses. Developmental Dynamics
237, 2295–2303.
Eaton, J.L., Glasgow, E., 2007. Zebrafish orthopedia (otp) is required for isotocin cell
development. Development. Genes and Evolution 217, 149–158.
Eaton, J.L., Holmqvist, B., Glasgow, E., 2008. Ontogeny of vasotocin-expressing cells
in zebrafish: Selective requirement for the transcriptional regulators orthopedia
 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
and single-minded 1 in the preoptic area. Developmental Dynamics 237,
995–1005.
Fanselow, M.S., LeDoux, J.E., 1999. Why we think plasticity underlying Pavlovian
fear conditioning occurs in the basolateral amygdala. Neuron 23, 229–232.
Fernandez, A.S., Pieau, C., Repérant, J., Boncinelli, E., Wassef, M., 1998. Expression of
the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct
domains in the telencephalon of mouse, chicken, turtle and frog embryos:
Implications for the evolution of telencephalic subdivisions in amniotes. De-
velopment 125, 2099–2111.
Folgueira, M., Anadón, R., Yáñez, J., 2004a. An experimental study of the connec-
tions of the telencephalon in the rainbow trout (Oncorhynchus mykiss). I:
Olfactory bulb and ventral area. Journal of Comparative Neurology 480,
180–203.
Folgueira, M., Anadón, R., Yáñez, J., 2004b. Experimental study of the connections of
the telencephalon in the rainbow trout (Oncorhynchus mykiss). II: Dorsal area
and preoptic region. Journal of Comparative Neurology 480, 204–233.
Ganz, J., Kaslin, J., Freudenreich, D., Machate, A., Geffarth, M., Brand, M., 2012.
Subdivisions of the adult zebrafish subpallium by molecular marker analysis.
Journal of Comparative Neurology 520, 633–655.
Garcı́a-López, M., Abellan, A., Legaz, I., Rubenstein, J.L., Puelles, L., Medina, L., 2008.
Histogenetic compartments of the mouse centromedial and extended amygdala
based on gene expression patterns during development. Journal of Comparative
Neurology 506, 46–74.
Garcı́a-Moreno, F., Pedraza, M., Di Giovannantonio, L.G., Di Salvio, M., López-
Mascaraque, L., Simeone, A., De Carlos, J.A., 2010. A neuronal migratory pathway
crossing from diencephalon to telencephalon populates amygdala nuclei. Na-
ture Neuroscience 13, 680–689.
Gayoso, J.Á., Castro, A., Anadón, R., Manso, M.J., 2011. Differential bulbar and
extrabulbar projections of diverse olfactory receptor neuron populations in
the adult zebrafish (Danio rerio). Journal of Comparative Neurology 519,
247–276.
González, A., Northcutt, R.G., 2009. An immunohistochemical approach to lungfish
telencephalic organization. Brain. Behavior and Evolution 74, 43–55.
González, A., López, J.M., Marı́n, O., 2002. Expression pattern of homeobox gene Nkx-
2.1 in the forebrain of Xenopus laveis during development. Gene Expression
Patterns 1, 181–185.
González, A., López, J.M., Sánchez-Camacho, C., Marı́n, O., 2002b. Regional expres-
sion of the homeobox gene NKX2-1 defines pallidal and interneuronal popula-
tions in the basal ganglia of amphibians. Neuroscience 114, 567–575.
González, A., Morona, R., López, J.M., Moreno, N., Northcutt, R.G., 2010. Lungfishes,
like tetrapods, possess a vomeronasal system. Frontiers in Neuroanatomy 4 ,
Article 130.
Grupp, L., Wolburg, H., Mack, A.F., 2010. Astroglial structures in the zebrafish brain.
Journal of Comparative Neurology 518, 4277–4287.
Hamdani, E.H., Doving, K.B., 2007. The functional organization of the fish olfactory
system. Progress in Neurobiology 82, 80–86.
Hamdani, E.H., Døving, K.B., 2003. Sensitivity and selectivity of neurons in the
medial region of the olfactory bulb to skin extract from conspecifics in crucian
carp, Carassius carassius. Chemical Senses 28, 181–189.
Hauptmann, G., Gerster, T., 2000. Regulatory gene expression patterns reveal
transverse and longitudinal subdivisions of the embryonic zebrafish forebrain.
Mechanisms of Development 91, 105–118.
Hellendall, T.R.P., Godfrey, D.A., Ross, C.D., Armstrong, D.M., Price, J.L., 1986. The
distribution of choline-acethyltransferase in the rat amygdaloid complex and
adjacent cortical areas, as determined by quantitative micro-assay and immu-
nohistochemistry. Journal of Comparative Neurology 249, 486–498.
Hirata, T., Li, P., Lanuza, G.M., Cocas, L.A., Huntsman, M.M., Corbin, J.G., 2009.
Identification of distinct telencephalic progenitor pools for neuronal diversity
in the amygdala. Nature Neuroscience 12, 141–149.
Huber, D., Veinante, P., Stoop, R., 2005. Vasopressin and oxytocin excite distinct
neuronal populations in the central amygdala. Science 308, 245–248.
Jesuthasan, S., 2012. Fear, anxiety and control in the zebrafish. Developmental
Neurobiology 72, 395–403.
Kaoru, T., Liu, F.C., Ishida, M., Oishi, T., Hayashi, M., Kitagawa, M., Shimoda, K.,
Takahashi, H., 2010. Molecular characterization of the intercalated cell masses
of the amygdala: Implications for the relationship with the striatum. Neurosci-
ence 166, 220–230.
Kaslin, J., Panula, P., 2001. Comparative anatomy of the histaminergic and other
aminergic systems in zebrafish (Danio rerio). Journal of Comparative Neurology
440, 342–377.
Kemppainen, S., Pitkanen, A., 2000. Distribution of parvalbumin, calretinin, and
calbindin-D(28k) immunoreactivity in the rat amygdaloid complex and colo-
calization with gamma-aminobutyric acid. Journal of Comparative Neurology
426, 441–467.
Kim, Y.-J., Nam, R.-H., Yoo, Y.M., Lee, C.-J., 2004. Identification and functional
evidence of GABAergic neurons in parts of the brain of adult zebrafish (Danio
rerio). Neuroscience Letters 355, 29–32.
Koylu, E.O., Couceyro, P.R., Lambert, P.D., Kuhar, M.J., 1998. Cocaine- and amphet-
amine-regulated transcript peptide immunihistochemical localization in the
rat brain. Journal of Comparative Neurology 391, 115–132.
Laberge, F., Mühlenbrock-Lenter, S., Grunwald, W., Roth, G., 2006. Evolution of the
amygdala. New insights from studies in amphibians. Brain, Behavior and
Evolution 67, 177–187.
Laming, P.R., Hornby, P., 1981. The effect of unilateral telencephalic lesions on
behavioral arousal and its habituation in the roach Rutilus rutilus. Behavioral
and Neural Biology 33, 59–65.
11
Lastein, S., Hamdani, E.H., Døving, K.B., 2008. Single unit responses to skin odorants
from conspecifics and heterospecifics in the olfactory bulb of crucian carp
Carassius carassius. Journal of Experimental Biology 211, 3529–3535.
Lau, B.Y.B., Mathur, P., Gould, G.G., Guo, S., 2012. Identification of a brain center
whose activity discriminates a choice behavior in zebrafish. Proceedings of the
National Academy of Sciences USA 108, 2581–2586.
LeDoux, J., 1998. Fear and the brain: Where have we been, and where are we going?
Biological Psychiatry 44, 1229–1238.
LeDoux, J., 2003. The emotional brain, fear, and the amygdala. Cellular and Molecu-
lar Neurobiology 23, 727–738.
Levin, E.D., 2011. Zebrafish assessment of cognitive improvement and anxiolysis:
Filling the gap between in vitro and rodent models for drug development.
Reviews in the Neurosciences 22, 75–84.
Levine, R.L., Dethier, S., 1985. The connections between the olfactory bulb and the
brain in the goldfish. Journal of Comparative Neurology 237, 427–444.
Lillesaar, C., 2011. The serotonergic system in fish. Journal of Chemical Neuroanat-
omy 41, 294–308.
Lillesaar, C., Stigloher, C., Tannhäuser, B., Wullimann, M.F., Bally-Cuif, L., 2009.
Axonal projections originating from raphe serotonergic neurons in the devel-
oping and adult zebrafish, Danio rerio, using transgenics to visualize raphe-
specific pet1 expression. Journal of Comparative Neurology 512, 158–182.
Löhr, H., Hammerschmidt, M., 2011. Zebrafish in endocrine systems: Recent
advances and implications for human disease. Annual Review of Physiology
73, 183–211.
MacDonald, R.B., Debiais-Thibaud, M., Talbot, J.C., Ekker, M., 2010. The relationship
between dlx and gad1 expression indicates highly conserved genetic pathways
in the zebrafish forebrain. Developmental Dynamics 239, 2298–2306.
Marino-Neto, J., Sabbatini, R.M.E., 1983. Discrete telencephalic lesions accelerate
the habituation rate of behavioral arousal responses in Siamese fighting fish
(Betta splendens). Brazilian Journal of Medical and Biological Research 16.
Marowsky, A., Yanagawa, Y., Obata, K., Vogt, K.E., 2005. A specialized subclass of
interneurons mediates dopaminergic facilitation of amygdala function. Neuron
48, 1025–1037.
Martı́n, I., Gómez, A., Salas, C., Puerto, A., Rodrı́guez, F., 2011. Dorsomedial pallium
lesions impair taste aversion learning in goldfish. Neurobiology of Learning and
Memory 96, 297–305.
Martı́nez-de-la-Torre, M., Pombal, M.A., Puelles, L., 2011. Distal-less-like protein
distribution in the larval lamprey forebrain. Neuroscience 178, 270–284.
Martı́nez-Garcı́a, F., Martı́nez-Marcos, A., Lanuza, E., 2002. The pallial amygdala of
amniote vertebrates: Evolution of the concept, evolution of the structure. Brain
Research Bulletin 57, 463–469.
Martı́nez-Garcı́a, F., Novejarque, A., Lanuza, E., 2007. Evolution of the amygdala in
vertebrates. In: Kaas, J., Bullock, T.H. (Eds.), Evolution of Nervous Systems: A
Comprehensive Reference, Vol. 2. Academic Press, Amsterdam, pp. 255–334.
Maximino, C., Herculano, A.M., 2010. A review of monoaminergic neuropsycho-
pharmacology in zebrafish. Zebrafish 7, 359–378.
Maximino, C., Brito, T.M., Dias, C.A., Gouveia Jr., A., Morato, S., 2010. Scototaxis as
anxiety-like behavior in fish. Nature Protocols 5, 209–216.
Maximino, C., Brito, T.M., Batista, A.W.S., Herculano, A.M., Morato, S., Gouveia Jr., A.,
2010a. Measuring anxiety in zebrafish: A critical review. Behavioural Brain
Research 214, 157–171.
Medina, L., Legaz, I., Gonzalez, G., de Castro, F., Rubenstein, J.L., Puelles, L., 2004.
Expression of Dbx1, Neurogenin 2, Semaphorin 5A, Cadherin 8 and Emx1 distin-
guish ventral and lateral pallial histogenetic divisions in the developing mouse
claustroamygdaloid complex. Journal of Comparative Neurology 474, 504–523.
Medina, L., Brox, A., Legaz, I., Garcı́a-López, M., Puelles, L., 2005. Expression patterns
of developmental regulatory genes show comparable divisions in the telen-
cephalon of Xenopus and mouse: Insights into the evolution of the forebrain.
Brain Research Bulletin 66, 297–302.
Medina, L., Bupesh, M., Abellán, A., 2011. Contribution of genoarchitecture to
understanding forebrain evolution and development, with particular emphasis
on the amygdala. Brain, Behavior and Evolution 3, 216–236.
Ménard, A., Auclair, F., Bourcier-Lucas, C., Grillner, S., Dubuc, R., 2007. Descending
GABAergic projections to the mesencephalic locomotor region in the lamprey
Petromyzon marinus. Journal of Comparative Neurology 501, 260–273.
Michaud, J.L., Rosenquist, T., May, N.R., Fan, C.M., 1998. Development of neuroen-
docrine lineages requires the bHLH-PAS transcription factor SIM1. Genes and
Development 12, 3264–3275.
Millhouse, O.E., 1986. The intercalated cells of the amygdala. Journal of Comparative
Neurology 247, 246–271.
Moreno, N., González, A., 2006. The common organization of the amygdaloid
complex in tetrapods: New concepts based on developmental, hodological
and neurochemical data in anuran amphibians. Progress in Neurobiology 78,
61–90.
Moreno, N., González, A., 2007a. Evolution of the amygdaloid complex in verte-
brates, with special reference to the anamnio-amniotic transition. Journal of
Anatomy 211, 151–163.
Moreno, N., González, A., 2007b. Development of the vomeronasal amygdala in
anuran amphibians: Hodological, neurochemical, and gene expression charac-
terization. Journal of Comparative Neurology 503, 815–831.
Moreno, N., Bachy, I., Retaux, S., González, A., 2004. LIM-homeodomain genes as
developmental and adult genetic markers of Xenopus forebrain functoinal
subdivisions. Journal of Comparative Neurology 472, 52–72.
Moreno, N., Domı́nguez, L., Retaux, S., González, A., 2008. Islet1 as a marker of
subdivisions and cell types in the developing forebrain of Xenopus. Neurosci-
ence 154, 1423–1439.
12 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
Mueller, T., 2012. What is the thalamus in zebrafish? Frontiers in Neuroscience 6,
64.
Mueller, T., Guo, S., 2009. The distribution of GAD67-mRNA in the adult zebrafish
(teleost) forebrain reveals a prosomeric pattern and suggests previously un-
identified homologies to tetrapods. Journal of Comparative Neurology 516,
553–568.
Mueller, T., Wullimann, M.F., 2009. An evolutionary interpretation of teleostean
forebrain anatomy. Brain, Behavior and Evolution 74, 30–42.
Mueller, T., Vernier, P., Guo, S., 2006. A phylotypic stage in vertebrate brain
development: GABA cells patterns in zebrafish compared with mouse. Journal
of Comparative Neurology 494, 620–634.
Mueller, T., Wullimann, M.F., Guo, S., 2008. Early teleostean basal ganglia develop-
ment visualized by zebrafish Dlx2a, Lhx6, Lhx7, Tbr2 (eomesa), and GAD67 gene
expression. Journal of Comparative Neurology 507, 1245–1257.
Mueller, T., Dong, Z., Berberoglu, M.A., Guo, S., 2011. The dorsal pallium in zebrafish,
Danio rerio (Cyprinidae, Teleostei). Brain Research 1381, 95–105.
Nam, R.-H., Kim, W., Lee, C.-J., 2004. NMDA receptor-dependent long-term poten-
tiation in the telencephalon of the zebrafish. Neuroscience Letters 370,
248–251.
Nery, S., Fishell, G., Corbin, J.G., 2002. The caudal ganglionic eminence is a source of
distinct cortical and subcortical cell populations. Nature Neuroscience 5, 1279–
1287.
Newman, S.W., 1999. The medial extended amygdala in male reproductive behav-
ior: A nove in the mammalian social behavior network. Annals of the New York
Academy of Sciences 877, 242–257.
Nieuwenhuys, R., 1962a. Trends in the evolution of the actinopterygian forebrain.
Journal of Morphology 69–88.
Nieuwenhuys, R., 1962b. The morphogenesis and the general structure of the
actinopterygian forebrain. Acta Morphologica Neerlando-Scandinavica 5, 65–78.
Nieuwenhuys, R., 1963. The comparative anatomy of the actinopterygian forebrain.
Journal für Hirnforschung 13, 171–192.
Nieuwenhuys, R., 1964. Further studies on the general structure of the actinopter-
ygian forebrain. Acta Morphologica Neerlando-Scandinavica 6, 65–79.
Nieuwenhuys, R., 1969. A survey of the structure of the forebrain in higher bony
fishes. Annals of the New York Academy of Science 167, 31–64.
Nieuwenhuys, R., 2009a. The actinopterygian forebrain revisited. Brain, Behavior
and Evolution 73, 229–252.
Nieuwenhuys, R., 2009b. On old and new comparative neurological sinners: The
evolutionary importance of the membranous parts of the actinopteryigian
forebrain and their sites of attachment. Journal of Comparative Neurology
516, 87–93.
Nieuwenhuys, R., 2011. The development and general morphology of the telen-
cephalon of actinopterygian fishes: Synopsis, documentation and commentary.
Brain Structure and Function 215, 141–157.
Niimura, Y., Nei, M., 2005. Evolutionary dynamics of olfactory receptor genes in
fishes and tetrapods. Proceedings of the National Academy of Sciences USA 102,
6039–6604.
Nordgreen, J., Horsberg, T.E., Ranheim, B., Chen, A.C.N., 2007. Somatosensory evoked
potentials in the telencephalon of Atlantic salmon (Salmo salar) following
galvanic stimulation of the tail. Journal of Comparative Physiology A 193,
1235–1242.
Northcutt, R.G., 2006. Connections of the lateral and medial divisions of the goldfish
telencephalic pallium. Journal of Comparative Neurology 494, 903–943.
Northcutt, R.G., 2008. Forebrain evolution in bony fishes. Brain Research Bulletin 75,
191–205.
Northcutt, R.G., 2009. Telencephalic organization in the Spotted African lungfish,
Protopterus dolloi: A new cytological model. Brain, Behavior and Evolution 73,
59–80.
Northcutt, R.G., González, A., 2011. A reinterpretation of the cytoarchitectonics of
the telencephalon of the Comoran coelacanth. Frontiers in Neuroanatomy 5 ,
Article 9.
Northcutt, R.G., Wicht, H., 1997. Afferent and efferent connections of the lateral and
medial pallia of the silver lamprey. Brain Behavior and Evolution 49, 1–19.
Norton, W., Bally-Cuif, L., 2010. Adult zebrafish as a model organism for behavioural
genetics. BMC Neuroscience 11, 90.
Osório, J., Megı́as, M., Pombal, M.A., Rétaux, S., 2006. Dynamic expression of the LIM-
homeodomain gene Lhx15 through larval brain development of the sea lamprey
(Petromyzon marinus). Gene Expression Patterns 6, 873–878.
Peng, G., Westerfield, M., 2006. Lhx5 promotes forebrain development and activates
transcription of secreted Wnt antagonists. Development 133, 3191–3200.
Pepels, P.P.L.M., Meek, J., Wendelaar Bonga, S.E., Balm, P.H.M., 2002a. Distribution
and quantification of corticotropin-releasing hormone (CRH) in the brain of the
teleost fish Oreochromis mossambicus (Tilapia). Journal of Comparative Neurol-
ogy 453, 247–268.
Pepels, P.P.L.M., Pesman, G., Korsten, H., Wendelaar Bonga, S.E., Balm, P.H.M., 2002b.
Corticotropin-releasing hormone (CRH) in the teleost fish Oreochromis mos-
sambicus (tilapia): In vitro release and brain distribution determined by a novel
radioimmunoassay. Peptides 23, 1053–1062.
Petrovich, G.D., Canteras, N.S., Swanson, L.W., 2001. Combinatorial amygdalar
inputs to hippocampal domains and hypothalamic behavior systems. Brain
Research Reviews 38, 247–289.
Pfeiffer, W., 1977. The distribution of fright reaction and alarm substance cells in
fishes. Copeia.
Pombal, M.A., Puelles, E., 1999. Prosomeric map of the lamprey forebrain based on
calretinin immunocytochemistry, Nissl stain, and ancillary markers. Journal of
Comparative Neurology 414, 391–422.
Pombal, M.A., Megı́as, M., Bardet, S.M., Puelles, L., 2009. New and old thoughts on
the segmental organization of the forebrain in lampreys. Brain, Behavior and
Evolution 74, 7–19.
Pombal, M.A., Álvarez-Otero, R., Pérez-Fernández, J., Solveira, C., Megı́as, M., 2011.
Development and organization of the lamprey telencephalon with special
reference to the GABAergic system. Frontiers in Neuroanatomy 5 , Article 20.
Portavella, M., Vargas, J.P., 2005. Emotional and spatial learning in goldfish is
dependent on different telencephalic pallial systems. European Journal of
Neuroscience 21, 2800–2806.
Portavella, M., Torres, B., Salas, C., 2004a. Avoidance response in goldfish: Emotional
and temporal involvement of medial and lateral telencephalic pallium. Journal
of Neuroscience 24, 2335–2342.
Portavella, M., Torres, B., Salas, C., Papini, M.R., 2004b. Lesions of the medial pallium,
but not of the lateral pallium, disrupt spaced-trial avoidance learning in goldfish
(Carassius auratus). Neuroscience Letters 362, 75–78.
Puelles, L., 2001. Thoughts on the development, structure and evolution of the
mammalian and avian telencephalic pallium. Philosophical Transactions of the
Royal Society of London B 356, 1538–1598.
Puelles, L., Kuwana, E., Puelles, E., Rubenstein, J.L.R., 1999. Comparison of the
mammalian and avian telencephalon from the perspective of gene expression
data. European Journal of Morphology 37, 139–150.
Puelles, L., Kuwana, E., Puelles, E., Bulfone, A., Shimamura, K., Keleher, J., Smiga, S.,
Rubenstein, J.L.R., 2000. Pallial and subpallial derivatives in the embryonic chick
and mouse telencephalon, traced by the expression of the genes Dlx-2, Emx-1,
Nkx-2.1, Pax-6, and Tbr-1. Journal of Comparative Neurology 424, 409–438.
Puelles, L., Martı́nez, S., Martı́nez-de-la-Torre, M., Rubenstein, J.L.R., 2004. Gene
maps and related histogenetic domains in the forebrain and midbrain. In:
Paxinos, G. (Ed.), The Rat Nervous System, Elsevier, New York, pp. 3–25.
Ramsay, J.M., Feist, G.W., Varga, Z.M., Westerfield, M., Kent, M.L., Schreck, C.B., 2009.
Whole-body cortisol response of zebrafish to acute net handling stress. Aqua-
culture 297, 157–162.
Remédios, R., Huilgol, D., Saha, B., Hari, P., Bhatnagar, L., Kowalczyk Hevner, R.F.,
Suda, Y., Aizawa, S., Ohshima, T., Stoykova, A., Tole, S., 2007. A stream of cells
migrating from the caudal telencephalon reveals a link between the amygdala
and neocortex. Nature Neuroscience 10, 1141–1150.
Rétaux, S., Rogard, M., Bach, I., Failli, V., Besson, M.-J., 1999. Lhx9: A novel LIM-
homeodomain gene expressed in the developing forebrain. Journal of Neuro-
science 19, 783–793.
Reyes, J.H., O’Shea, K.S., Prieskorn, D.M., Wesolowski, K., Miller, J.M., Altschuler, R.A.,
2008. Glutamatergic neuronal differentiation of mouse embryonic stem cells
after transient expression of neurogenin 1 and treatment with BDNF and GDNF:
In vitro and in vivo studies. Journal of Neuroscience 28, 12622–12631.
Rink, E., Wullimann, M.F., 1998. Some forebrain connections of the gustatory system
in the goldfish Carassius auratus visualized by separate DiI application to the
hypothalamic inferior lobe and the torus lateralis. Journal of Comparative
Neurology 394, 152–170.
Rink, E., Wullimann, M.F., 2004. Connections of the ventral telencephalon (sub-
pallium) in the zebrafish (Danio rerio). Brain Research 1011, 206–220.
Robertson, B., Saitoh, K., Ménard, A., Grillner, S., 2006. Afferents of the lamprey optic
tectum with special reference to the GABA input: Combined tracing and
immunohistochemical study. Journal of Comparative Neurology 499, 106–119.
Robles, E., Smith, S.J., Baier, H., 2011. Characterization of genetically targeted neuron
types in the zebrafish optic tectum. Frontiers in Neural Circuits 5 , Article 1.
Rooney, D.J., Laming, P.R., 1986. Localization of telencephalic regions concerned
with habituation of cardiac and ventilatory responses associated with arousal in
the goldfish (Carassius auratus). Behavioral Neuroscience 100, 45–50.
Royer, S., Martina, M., Paré, D., 1999. An inhibitory interface gates impulse traffic
between the input and output stations of the amygdala. Journal of Neuroscience
19, 10575–10583.
Ryu, S., Mahler, J., Acampora, D., Holzschuch, J., Erhardt, S., Omodei, D., Simeone, A.,
Driever, W., 2007. Orthopedia homeodomain protein is essential for dience-
phalic dopaminergic neuron development. Current Biology 17, 873–880.
Sah, P., Faber, E.S.L., Lopez de Armentia, M., Power, J., 2003. The amygdaloid
complex: Anatomy and physiology. Physiological Review 83, 803–834.
Schadé, J.P., Weiler, I.J., 1959. Electroencephalographic patterns of the goldfish
(Carassius auratus L.). Experimental Biology 36, 435–452.
Schuurmans, C., Armant, O., Nieto, M., Stenman, J.M., Britz, O., Klenin, N., Brown, C.,
Langevin, L.-M., Seibt, J., Tang, H., Cunningham, J.M., Dyck, R., Walsh, C., Camp-
bell, K., Polleux, F., Guillemot, F., 2004. Sequential phases of cortical specifica-
tion involve Neurogenin-dependent and -independent pathways. The EMBO
Journal 23, 2892–2902.
Shah, R., Medina-Martinez, O., Chu, L.-F., Samaco, R.C., Jamrich, M., 2006. Expression
of FoxP2 during zebrafish development and in the adult brain. International
Journal of Developmental Biology 50, 435–438.
Simpson, G.G., 1961. Principles of Animal Taxonomy, Columbia University Press,
New York.
Sloan, H.E., 1989. Neuroanatomical substrates of reproductive behavior in goldfish.
Ph.D Thesis, University of Kentucky, Lexington.
Smith-Fernandez, A., Pieau, C., Repérant, J., Boncinelli, E., Wassef, M., 1998. Expres-
sion of the Emx-1 and Dlx-1 homeobox genes define three molecularly distinct
domains in the telencephalon of mouse, chick, turtle and frog embryos:
Implications for the evolution of the telencephalic subdivisions in amniotes.
Development 125, 2099–2111.
Sofroniew, M.V., 1980. Projections from vasopressin, oxytocin, and neurophysin
neurons to neural targets in the rat and human. Journal of Histochemistry and
Cytochemistry 28, 475–478.
 C. Maximino et al. / Journal of Chemical Neuroanatomy 48–49 (2013) 1–13
Sokolowski, K., Corbin, J.G., 2012. Wired for behaviors: From development to function
of innate limbic system circuitry. Frontiers in Molecular Neuroscience 5, 55.
Soma, M., Aizawa, H., Ito, Y., Maekawa, M., Osumi, N., Nakahira, E., Okamoto, H.,
Tanaka, K., Yuasa, S., 2009. Development of the mouse amygdala as revealed by
enhanced green fluorescent protein gene transfer by means of in utero elec-
troporation. Journal of Comparative Neurology 513, 113–128.
Stenman, J., Yu, R.T., Evans, R.M., Campbell, K., 2003. Tlx and Pax6 co-operate
genetically to establish the pallio-subpallial boundary in the embryonic mouse
telencephalon. Development 130, 1113–1122.
Stewart, A., Kadri, F., DiLeo, J., Chung, K., Cachat, J., Goodspeed, J., 2010. The
developing utility of zebrafish in modeling neurobehavioral disorders. Interna-
tional Journal of Comparative Psychology 23, 104–121.
Stewart, A., Gaikwad, S., Kyzar, E., Green, J., Roth, A., Kalueff, A.V., 2011. Modeling
anxiety using adult zebrafish: A conceptual review. Neuropharmacology 62,
135–143.
Subhedar, N., Barsagade, V.G., Singru, P.S., Thim, L., Clausen, J.T., 2011. Cocaine- and
amphetamine-regulated transcript peptide (CART) in the telencephalon of the
catfish, Clarias gariepinus: Distribution and response to fasting, 2-deoxy-D-
glucose, glucose, insulin, and leptin treatments. Journal of Comparative Neu-
rology 519, 1281–1300.
Swanson, L.W., Petrovich, G.D., 1998. What is the amygdala? Trends in Neural
Sciences 21, 323–331.
Thompson, R.R., Walton, J.C., 2009. Vasotocin immunoreactivity in goldfish brains:
Characterizing primitive circuits associated with social regulation. Brain, Be-
havior and Evolution 73, 153–164.
Tomizawa, K., Katayama, H., Nakayasu, H., 2001. A novel monoclonal antibody
recognizes a previously unknown subdivision of the habenulo-interpeduncular
system in zebrafish. Brain Research 117–127.
Ubeda-Bañon, I., Pro-Sistiaga, P., Mohedano-Moriano, A., Saiz-Sanchez, D., de la
Rosa-Prieto, C., Gutierrez-Catellanos, N., Lanuza, E., Martinez-Garcia, F., Marti-
nez-Marcos, A., 2011. Cladistic analysis of olfactory and vomeronasal systems.
Frontiers in Neuroanatomy 5 , Article 3.
Viktorin, G., Chiuchitu, C., Rissler, M., Varga, Z.M., Westerfield, M., 2009. Emx3 is
required for the differentiation of dorsal telencephalic neurons. Developmental
Dynamics 238, 1984–1998.
Waclaw, R.R., Ehrman, L.A., Pierani, A., Campbell, K., 2010. Developmental origin of
the neuronal subtypes that comprise the amygdalar fear circuit in the mouse.
Journal of Neuroscience 30, 6944–6953.
Wai, M.S.M., Lorke, D.E., Webb, S.E., Yew, D.T., 2006. The pattern of c-fos activation
in the CNS is related to behavior in the mudskipper, Periophthalmus canto-
nensis. Behavioural Brain Research 167, 318–327.
Wang, W., Lufkin, T., 2000. The murine Otp homeobox gene plays an essential role in
the specification of neuronal cell lineages in the developing hypothalamus.
Developmental Biology 227, 432–449.
13
Wullimann, M.F., 2009. Secondary neurogenesis and telencephalic organization in
zebrafish and mice: A brief review. Integrative Zoology 4, 123–133.
Wullimann, M.F., Mueller, T., 2004. Teleostean and mammalian forebrains con-
trasted: Evidence from genes to behavior. Journal of Comparative Neurology
475, 143–162.
Wullimann, M.F., Puelles, E., 1999. Postembryonic neural proliferation in the
zebrafish forebrain and its relationship to prosomeric domains. Anatomy
and Embryology 329, 329–348.
Wullimann, M.F., Rink, E., 2001. Detailed immunohistology of Pax6 protein and
tyrosine hydroxylase in the early zebrafish brain suggests role of Pax6 gene in
development of dopaminergic diencephalic neurons. Developmental Brain
Research 131, 173–191.
Wullimann, M.F., Rink, E., 2002. The teleostean forebrain: A comparative and
developmental view based on early proliferation, Pax6 activity and catechol-
aminergic organization. Brain Research Bulletin 57, 363–370.
Xu, X., Bazner, J., Qi, M., Johnson, E., Freidhoff, R., 2003. The role of telencephalic
NMDA receptors in avoidance learning in goldfish (Carassius auratus). Behav-
ioral Neuroscience 117, 548–554.
Xu, Q., Tam, M., Anderson, S.A., 2008. Fate mapping Nkx2.1-lineage cells in the
mouse telencephalon. Journal of Comparative Neurology 506, 16–29.
Xu, X., Bentley, J., Miller, T., Zmolek, K., Kovaleinen, T., Goodman, E., Terri, F., 2009.
The role of telencephalic NO and cGMP in avoidance conditioning in goldfish
(Carassius auratus). Behavioral Neuroscience 123, 614–623.
Xue, H.-G., Yang, C.-Y., Ito, H., Yamamoto, N., Ozawa, H., 2006. Primary and
secondary sensory trigeminal projections in a cyprinid teleost, carp (Cyprinus
carpio). Journal of Comparative Neurology 499, 626–644.
Yamamoto, N., Ishikawa, Y., Yoshimoto, M., Xue, H.-G., Bahaxar, N., Sawai, N., Yang,
C.-H., Ozawa, H., Ito, H., 2007. A new interpretation on the homology of the
teleostean telencephalon based on hodology and a new eversion model. Brain,
Behavior and Evolution 69, 96–104.
Yamamoto, K., Ruuskanen, J.O., Wullimann, M.F., Vernier, P., 2010. Two tyrosine
hydroxylase genes in vertebrates: New dopaminergic territories revelead in the
zebrafish brain. Molecular and Cellular Neuroscience 43, 394–402.
Yoshimoto, M., Yamamoto, N., 2010. Ascending general visceral sensory pathways
from the brainstem to the forebrain in a cichlid fish, Oreochromis (Tilapia)
niloticus. Journal of Comparative Neurology 518, 3570–3603.
Zerucha, T., Prince, V.E., 2000. Cloning and developmental expression of a zebrafish
meis2 homeobox gene. Mechanisms of Development 102, 247–250.
Zerucha, T., Stümehr, T., Hatch, G., Park, B.K., Long, Q., Yu, G., Gambarotta, A., Schultz,
J.R., Rubenstein, J.L.R., Ekker, M., 2000. A highly conserved enhancer in the Dlx5/
Dlx6 intergenic region is the site of cross-regulatory interactions between Dlx
genes in the embryonic forebrain. Journal of Neuroscience 20, 709–721.
Zhiyuan, G., Korzh, V. (Eds.), 2004. Fish Development and Genetics: The Zebrafish
and Medaka Models. World Sicentific Publishing Co. Pte. Ltd, Singapore.