Review
Historical Perspective
Neuroglia: the 150 years after
Helmut Kettenmann1 and Alexei Verkhratsky2,3
1
Max-Delbrück-Center for Molecular Medicine, Robert-Rössle-Straße 10, 13122 Berlin-Buch, Germany
2
Faculty of Life Sciences, The University of Manchester, Manchester, M13 9PT, UK
3
Institute of Experimental Medicine, Academy of Science of Czech Republic, Videnska 1083, 142 20 Prague 4, Czech Republic
The beginning
One hundred and fifty years ago on 3 April 1858, at 37
years of age, Rudolf Virchow (Box 1) promulgated the
concept of neuroglia in a lecture delivered at the New
Pathology Institute of Berlin University. This lecture
was part of a series of 20 lectures for colleagues and
medical practitioners, and the 13th was entitled ‘Spinal
cord and the brain’. In that lecture, Virchow made public
his earlier thoughts [1] on the brain connective tissue, the
‘nervenkitt’ or nerve-cement, which he termed ‘neuroglia’;
he had coined the term already in 1856 in a comment to an
earlier article from 1846 when his collected works were
republished. The lecture series, however, was a landmark
because it was stenographed by one of his students and
published, almost without changes, in the same year. The
resulting book, which appeared under the title Cellular
Pathology [2], is one of the most influential medical pub-
lications in the 19th century. From there, the term neu-
roglia and the concept behind them spread around the
world.
Already in Virchow’s eyes the concept of neuroglia was
set against the concept of nervous elements; he wrote
‘Hitherto, gentlemen, in considering the nervous system,
I have only spoken of the really nervous parts of it. But if
we would study the nervous system in its real relations in
the body, it is extremely important to have a knowledge of
that substance also which lies between the proper nervous
parts, holds them together and gives the whole its form in a
greater or less degree’ [2]. This division between nerve
elements and supportive tissue still persists to a large
degree in the views of many neuroscientists.
For Virchow neuroglia was a connective material,
although he would admit that it ‘also contains a certain
number of cellular elements’ (Figure 1). Nonetheless, glial
elements were recognized even before Virchow’s ideas
appeared when, in 1838, Robert Remak described a sheath
around single nerve fibres (R. Remak, PhD thesis, Univer-
sity of Berlin, 1838) and in 1851 Heinrich Müller [3]
discovered radial fibres in the retina (which later became
known as Müller glial cells). The second part of 19th
century was a golden age of cellular histology, and soon
after initial findings many different forms of glial cells were
described and images published, for example by Otto
Deiters, Jacob Henle, Camillo Golgi, Gustav Retzius
and many others [4–7]. In 1893, Michael von Lenhossek
proposed the term ‘astrocyte’ [8] (astroglial cell), and,
slightly later, Kölliker [9] and Andriezen [10] divided those
Corresponding author: Verkhratsky, A. (alexej.verkhratsky@manchester.ac.uk).
0166-2236/$ – see front matter ß 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.tins.2008.09.003 Available online 20 October 2008
into fibrous and protoplasmic astrocytes. To the anat-
omists and pathologists of that time it was obvious that
the non-neuronal cells were quite diverse in forms
(Figure 2) and also underwent changes in pathology. It
was, however, in 1919 before oligodendrocytes and micro-
glia were recognized as separate cell types and introduced
into the neuroglia concept by Pio del Rio-Hortega [11–13].
It wasn’t until the 1950s that myelin (this term was also
introduced by Virchow) was recognized to be part of the
Schwann cell [14].
The evolution of concept
‘What is the function of glial cells in neural centers? The
answer is still not known, and the problem is even more
serious because it may remain unsolved for many years to
come until physiologists find direct methods to attack it’.
By these prophetic words Santiago Ramon y Cajal began
his treatise on glia in Histology of the Nervous System [15].
The question is still not answered today, although several
concepts have emerged that attribute a variety of roles for
glial cells in brain function.
The first and somewhat negative role of glial cells was
presented by the filling concept originating from Virchow
and elaborated by Karl Weigert [16]. Here, the neuroglia
was given an entirely passive role as an element that fills
‘space not occupied by neurones’. Nonetheless, the second
of Virchow’s ideas – that the neuroglia holds nervous
elements ‘together and gives the whole its form’ – received
a surprising twist. Indeed, the architecture of the grey
matter is defined by the astrocytes because each proto-
plasmic astrocyte occupies its own territory and cantons
the grey matter, covering all neuronal elements within its
domain [17,18]. Loss of this specific organization might,
incidentally, be involved in various forms of brain pathol-
ogy [19]. The astroglial domain is also linked to blood
vessels, a phenomenon initially observed by Golgi, who
was the first to propose the nutritional role for glial cells.
Today, we have arrived at the concept that the astrocyte is
an essential part of a neuronal–glial–vascular unit, and
new studies show that astrocytes control the local blood
flow and supply neurons with energy substrates [20–22].
In fact, the astroglial cell emerges as an important
homeostatic cellular element in the brain because, indeed,
astrocytes control the brain environment by regulating
the volume and composition of extracellular space and
by controlling the barrier that separates the central ner-
vous system from the rest of the body. Evolutionarily, the
initial separation, which subsequently developed into the
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Review
Box 1.
Rudolf Virchow (Figure I) was born on 13 October 1821 in Schivelbein,
part of the Prussian empire, which is now Swidwin in Poland. He
studied medicine in Berlin and worked as a pathologist at the Charité.
After the failed revolution in 1848, in which he had actively
participated, he was urged to leave Berlin and he moved to Würzburg
as a Professor of Pathology. He returned to Berlin in 1856 and stayed
as the chairman of pathology for the rest of his life. He had a broad
interest in science ranging from cancer research, neuroscience to
anthropology and, as the editor-in-chief of Virchows Archiv, he could
oversee it all. Rudolf Virchow was not only a highly influential
scientist but was also actively engaged in different aspects of political
and cultural life. He initiated laws for meat inspection at slaughter-
houses and, as a Member of the German Parliament, he was
instrumental in installing a modern sewage system in the city of
Berlin born out of the recognition that there is a relationship between
infections and hygienic conditions. His interest in anthropology led
him to his friend Heinrich Schliemann’s excavations in Troy and
Virchow convinced him to donate the Priam’s treasure to the city of
Berlin. He assembled a tremendous collection of pathologic speci-
mens and, at the end of his life, he opened a pathologic museum not
only for students and medical practioners but also for the public. He
died in Berlin on 5 September 1902.
Figure I. (a) Rudolf Virchow (1821–1902). (b) The frontispiece of Cellular
Pathology published in 1858 [2]. (c) Lecture 13 (‘Spinal cord and the brain’)
from Cellular Pathology, in which neuroglia were defined.
blood–brain barrier, was entirely made by glial elements;
the more advanced blood–brain barrier is formed by endo-
thelial cells, which nonetheless seem to be controlled by
factors secreted by astrocytes [23]. As far as extracellular
space is concerned, astrocytes control ion environment (in
particular K+), water movements and uptake of many
transmitters (most notably glutamate); the astroglial cell
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Trends in Neurosciences Vol.31 No.12
also acts as a main source for reactive-oxygen-species
scavengers (e. g. glutathione), thus, confronting metabolic
damage [24].
Astroglia are also involved in shaping synaptic connec-
tivity in the brain by controlling the genesis and mainten-
ance of synapses (thus, providing morphological
homeostasis of synaptic connectivity) and by affecting
synaptic strength and plasticity. Initially, the concept of
glia regulating neuronal communications was suggested
by Carl Ludwig Schleich in his landmark book on local
anaesthesia in 1898 [25]. He believed that glial cells could
move between nerve cells and thereby block transmission.
In the extreme case, in general anaesthesia, all neuronal
elements are isolated by glial cells and the activity of the
brain is ceased. We now know that it is not as simple as
Schleich believed, but there might be a piece of truth in his
concept. In particular, microglial cells and also astrocytes
can rapidly move or extend their processes in physiologi-
cally relevant temporal domains [26,27]; whether this form
of plasticity might indeed affect synaptic connectivity
remains, however, unknown. Nevertheless, astrocytes
are legitimate partners in synaptic transmission (the tri-
partite synapse [28]) because their perisynaptic processes
contain an array of neurotransmitter receptors [29,30],
which enables rapid perception of synaptic transmission
events. Astroglia also feed back to neurons, thus, modifying
synaptic transmission; this feedback is accomplished in
many ways, including the release of gliotransmitters (by
exocytosis, transporters or membrane channels [31,32])
and neurotransmitter uptake, which shapes the neuro-
transmitters dynamics in the synaptic cleft [33].
We have also learned that glial cells have intrinsic
signalling systems. Activity among astrocytes can spread
in the form of Ca2+ waves and they can generate spon-
taneous Ca2+ increases that correlate with the release of
glutamate [31,34–37]. The network of astrocytes and oli-
godendrocytes is interconnected in a complex manner by
gap junctions [38]. This syncytium is highly dynamic with
respect to space and time. It might serve to exchange
molecules for signalling and metabolic activity such as
the long-range diffusion of second messengers (e.g. InsP3)
or metabolic substrates (e.g. glucose and ATP) [39,40]. This
network is distinct from the binary signalling of the
neuronal networks in that it offers a new (and completely
unknown) possibility of analogue information processing in
the brain.
Finally, an entirely new concept of the glia as a stem
element of the brain has been developed recently [41]. Not
only does the radial glial cell act a a pluripotent neural
precursor but also some astrocytes can re-enter the cell
cycle and produce all types of neural cells, from neurons to
macroglial cells; identifying the control factors of neuro-
and gliogenesis represents an important challenge.
Oligodendrocytes and Schwann cells have an important
role as isolators, the role initially suggested by Pedro
Ramon y Cajal (the brother of famous Santiago). Both
types of cells produce myelin, which provides for highly
effective electrical isolation of axons, permitting, thus, the
saltatory propagation of action potentials. These cells are,
however, more than simple cable isolators. They are
equipped with transmitter receptors and are able to sense
Review Trends in Neurosciences Vol.31 No.12

Figure 1. Neuroglia as seen by Rudolf Virchow. (a) Ependyma and neuroglia in the floor of the fourth ventricle. Between the ependyma and the nerve fibers is ‘the free
portion of the neuroglia with numerous connective tissue corpuscles and nuclei’. Numerous corpora amylacea are also visible, shown enlarged below the main illustration
(ca). Abbreviations: E, ependymal epithelium; N, nerve fibers; v, blood vessels. (b) Elements of neuroglia from white matter of the human cerebral hemispheres. (i) Free
nuclei with nucleoli. (ii) Nuclei with partially destroyed cell bodies. (iii) Complete cells. Reproduced from Ref. [2].

neuronal activity [42]. This signalling route is thought to The diversification of glia
be involved in controlling oligodendrocytes differentiation The initial division of neuroglia into three types, the
and the state of myelination. astrocytes, the oligodendrocytes and the microglia, was

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Figure 2. Morphological diversity of human glial cells. Neuroglial cells from the human cortex. (a) Vertical slice of one of the gyros of the frontal lobe obtained from 42-year-
old women. (b–e) Vertical slice of the parietal region obtained from a 70-year-old man. In all parts, the upper surface of the cortex is oriented towards the top of the image.
Superficial glial cells send their processes towards the surface of the slice where they spread; glial cells located in the deeper layers are represented by many different types.
In parts (a) and (b) blood vessels with tightly attached glial cells are shown. In (e) a small stained ganglion cell is shown; all other cells are glial elements. All images are
obtained from Golgi-stained preparations. Taken from Ref. [6], Vol. VI, Plate V.

accomplished in the 1920 s and has recently been chal- been characterised. These cells (also termed synantocytes
lenged. An entirely new class of glial cells, the NG2-glia (so from Greek synantv synanto, meaning contact [43]; or
named because of expression of specific marker NG2) has polydendrocytes [44] because of their potential multitude

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of functions) have some neuronal physiological features
and receive synaptic contacts [45]. These cells are highly
reactive and might participate in gliogenesis, myelination
and yet unknown forms of synaptic regulation and
plasticity.
Moreover, it becomes apparent that astrocytes are not a
homogeneous cell population. Astrocytes in different brain
regions have distinct physiological properties and express
various sets of receptors and transporters, most likely
adapting to their immediate environment. This functional
heterogeneity of astroglia can be even more prominent in
the human brain because evolution from mammals to
higher primates resulted in a remarkable increase in both
density and morphological complexity of astrocytes. The
glial to neuron ratio in the frontal cortex has increased
from 0.3 in rodents to 1.65 in humans [46], whereas
protoplasmic astrocytes dimension and volume of their
territorial domains rose by 3 and 30 times, respectively.
As a result, every human astrocyte contacts and enwraps
Figure 3. Activated glial cells associated with neurons. Abbreviations: Gaz, neuron; aglz, glial cell. Taken from Ref. [48].
Trends in Neurosciences Vol.31 No.12
2 million synapses compared with only 100 000
synapses covered by the processes of a rodent astrocyte
[47]. Moreover, in the primate cortex specific types of
astroglial cells have been described: the interlaminar
and polarised astrocytes. The functional properties of
human astroglial cells are virtually unexplored and these
cells might have a greater functional heterogeneity and
regional specificity than astrocytes currently studied in
mouse and rat.
Glia in pathology
The first image of glial cells published by Virchow in
Cellular Pathology resembles neither the morphology of
astrocytes, oligodendrocytes nor microglia of the normal
brain. This image of spherical cells actually comes closest
to an activated microglia in a pathologic brain tissue. So
what he has seen remains in the dust of history. His
followers, however, soon recognized that glial cells undergo
substantial changes in the pathologic brain, and Alois
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Alzheimer edited an entire book devoted to the pathologic
glial cells [48] (Figure 3). Today it is well established that
astrocytes and microglial cells have a complex response
pattern in all known disease states of the brain. Microglia,
very much in line with initial ideas of del Rio Hortega [13],
establish an intrinsic defence system of the brain. Much
has been learned recently about the physiology and proper-
ties of these cells, which seem to be true wardens con-
stantly scanning the brain environment and searching for
the brain damage [26]. The resting (or better termed
‘surveying’) microglial cells are spread throughout the
entire brain parenchyma, each cell occupying its own
territorial domain. The processes of microglia are in con-
stant move, scanning the domain and perceiving either ‘off’
signals (which indicate the normal brain functioning and
prevent microglial activation) or ‘on’ signals (which
indicate brain damage and set up the complex and graded
programme of microglial activation) [49–51].
The integrating glia: what the future holds
One and a half centuries of glial research have had its ebbs
and tides. An initial explosion of research on glial cells,
mainly performed by anatomists and pathologists,
declined to low levels after physiologists discovered that
brain activity was encoded as action potentials in neurons.
Scientists focused on neuronal communications (thereby
identifying synapses and neurotransmitters), on how net-
works of neurons processed information and on how
neuronal circuits define brain areas. The reasons for this
advancement were the newly developed technologies to
record this neuronal activity, first indirectly in the extra-
cellular space and later directly by intracellular electrodes.
The voltage-clamp and the patch-clamp techniques were
further milestones of this technical development. However,
whenever physiologists encountered a glial cell and
recorded with the contemporary techniques, the cells
remained silent and were obviously not integrated into
the network of neurons. Not surprisingly, the researcher
removed his electrode and went on searching for the more
exciting nerve cells. The glial cell kept its stigma as the
passive element that serves to fill the gaps.
The last decades have seen an ascent in glial research
owing to the discovery that glial cells can be excited, but
excited in a way fundamentally distinct from neurones.
The glial form of excitability is encoded in changes in
intracellular Ca2+ that might occur spontaneously, or
are triggered by neuronal activity, and that might spread
in the form of waves. One might wonder how neuroscience
textbooks would look if Ca2+ imaging was developed before
electrophysiology. Our understanding of the glial network
is still rudimentary because the bulk of the experiments
were done in cell culture or in brain slices. The first exciting
results have been recently obtained in vivo and it became
evident that sensory information from the whiskers of the
mouse results in a Ca2+ increase in astrocytes located in
the barrel cortex [52]. There is a fundamental difference
between the action-potential-mediated signalling in
neurons and diffusion-based signalling in astrocytes.
The neuronal response in the form of action potentials is
binary and on a millisecond time scale, whereas the Ca2+
response of the glial cells can be graded and is on a much
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slower time scale, developing within seconds or even min-
utes. Gap junctions amalgamate single glial cells into an
even more complex structure. An increase in numbers and
complexity of astrocytes, which correlates with the
increase in brain cognitive power, can represent the evol-
utionary means for integrating rapid information
exchange provided by neuronal networks with a relatively
slow but longer lasting information processing provided by
glial cells. We might speculate that the combination of
binary and analogue information, handled by the two
cellular networks in the brain, is essential for brain func-
tion in producing thoughts, setting memories and creating
emotions, which, in essence, define our human nature. This
effigy might be heretic, but it cannot be denied without
consideration; only future experiments will produce the
final answer.
References
1 Virchow, R. (1856) Gesammelte Abbildung zur wissenschaftlichen
Medizin, Verlag von Meidinger Sohn & Comp
2 Virchow, R. (1858) Die Cellularpathologie in ihrer Begründung auf
physiologische and pathologische Gewebelehre. Zwanzig Vorlesungen
gehalten während der Monate Februar, März und April 1858 im
pathologischen Institut zu Berlin, August Hirschwald
3 Müller, H. (1851) Zur Histologie der Netzhaut. Z. Wiss. Zool. 3, 234–237
4 Henle, J. and Merkel, F. (1869) Über die sogenannte Bindesubstanz der
Centralorgane des Nervensystems. Z. Med. 34, 49–82
5 Deiters, O. (1865) Untersuchungen über Gehirn und Rückenmark des
Menschen und der Säugethiere, Vieweg
6 Retzius, G. (1894–1916) Biol Untersuchungen. Die Neuroglia des
Gehirns beim Menschen und bei Saeugethieren, Verlag von Gustav
Fischer
7 Golgi, C. (1903) Opera Omnia, Hoepli
8 v Lenhossek, M. (1893) Der feinere Bau des Nervensystems im Lichte
neuester Forschung, Fischer’s Medicinische Buchhandlung H.
Kornfield
9 Kölliker, A. (1889) Handbuch der Gewebelehre des Menschen, Wilhelm
Engelmann
10 Andriezen, W.L. (1893) The neuroglia elements of the brain. BMJ 2,
227–230
11 del Rio-Hortega, P. (1919) El tercer elemento de los centros nerviosos.
Biol. Soc. Esp. Biol. 9, 69–120
12 del Rio-Hortega, P. (1921) Estudios sobre la neuroglia. La glia
de escasas radiaciones oligodendroglia. Biol. Soc. Esp. Biol. 21,
64–92
13 Rio-Hortega, P.d. (1932) Microglia. In Cytology and Cellular Pathology
of the Nervous System (Vol. 2) (Penfield, W., ed.), pp. 483–534, Hafner
14 Geren, B.B. (1954) The formation from the Schwann cell surface of
myelin in the peripheral nerves of chick embryos. Exp. Cell Res. 7, 558–
562
15 Cajal, S. and Ramon, y. (1995) Histology of the Nervous System,
translated by N. Swanson & L. Swanson, Oxford University Press
16 Weigert, K. (1895) Beiträge zur Kenntnis der normalen menschlichen
Neuroglia, Diesterweg
17 Bushong, E.A. et al. (2002) Protoplasmic astrocytes in CA1 stratum
radiatum occupy separate anatomical domains. J. Neurosci. 22, 183–
192
18 Nedergaard, M. et al. (2003) New roles for astrocytes: redefining the
functional architecture of the brain. Trends Neurosci. 26, 523–530
19 Oberheim, N.A. et al. (2008) Loss of astrocytic domain organization in
the epileptic brain. J. Neurosci. 28, 3264–3276
20 Mulligan, S.J. and MacVicar, B.A. (2004) Calcium transients in
astrocyte endfeet cause cerebrovascular constrictions. Nature 431,
195–199
21 Zonta, M. et al. (2003) Neuron-to-astrocyte signaling is central to the
dynamic control of brain microcirculation. Nat. Neurosci. 6, 43–50
22 Magistretti, P.J. (2006) Neuron-glia metabolic coupling and plasticity.
J. Exp. Biol. 209, 2304–2311
23 Bundgaard, M. and Abbott, N.J. (2008) All vertebrates started out with
a glial blood-brain barrier 4-500 million years ago. Glia 56, 699–708
Review
24 Giaume, C. et al. (2007) Glia: the fulcrum of brain diseases. Cell Death
Differ. 14, 1324–1335
25 Schleich, C.L. (1894) Schmerzlose Operationen: Örtliche Betäubung mit
indiffrenten Flüssigkeiten. Psychophysik des natürlichen und
künstlichen Schlafes, Julius Springer
26 Nimmerjahn, A. et al. (2005) Resting microglial cells are highly
dynamic surveillants of brain parenchyma in vivo. Science 308,
1314–1318
27 Hirrlinger, J. et al. (2004) Astroglial processes show spontaneous
motility at active synaptic terminals in situ. Eur. J. Neurosci. 20,
2235–2239
28 Araque, A. et al. (1999) Tripartite synapses: glia, the unacknowledged
partner. Trends Neurosci. 22, 208–215
29 Kettenmann, H. et al. (1984) Aspartate, glutamate and g-aminobutyric
acid depolarize cultured astrocytes. Neurosci. Lett. 52, 25–29
30 Verkhratsky, A. and Steinhauser, C. (2000) Ion channels in glial cells.
Brain Res. Brain Res. Rev. 32, 380–412
31 Volterra, A. and Meldolesi, J. (2005) Astrocytes, from brain glue to
communication elements: the revolution continues. Nat. Rev. Neurosci.
6, 626–640
32 Pankratov, Y. et al. (2006) Vesicular release of ATP at central synapses.
Pflugers Arch. 452, 589–597
33 Tzingounis, A.V. and Wadiche, J.I. (2007) Glutamate transporters:
confining runaway excitation by shaping synaptic transmission. Nat.
Rev. Neurosci. 8, 935–947
34 Cornell Bell, A.H. et al. (1990) Glutamate induces calcium waves in
cultured astrocytes: long- range glial signaling. Science 247, 470–473
35 Verkhratsky, A. and Kettenmann, H. (1996) Calcium signalling in glial
cells. Trends Neurosci. 19, 346–352
36 Verkhratsky, A. et al. (1998) Glial calcium: homeostasis and signaling
function. Physiol. Rev. 78, 99–141
37 Verkhratsky, A. (2006) Calcium ions and integration in neural circuits.
Acta Physiol. (Oxf.) 187, 357–369
38 Giaume, C. and McCarthy, K.D. (1996) Control of gap-junctional
communication in astrocytic networks. Trends Neurosci. 19, 319–325
Trends in Neurosciences Vol.31 No.12
39 Kang, J. et al. (2008) Connexin 43 hemichannels are permeable to ATP.
J. Neurosci. 28, 4702–4711
40 Tabernero, A. et al. (2006) Glucose metabolism and proliferation in glia:
role of astrocytic gap junctions. J. Neurochem. 99, 1049–1061
41 Pinto, L. and Gotz, M. (2007) Radial glial cell heterogeneity–the source
of diverse progeny in the CNS. Prog. Neurobiol. 83, 2–23
42 Bakiri, Y. et al. Glutamatergic signaling in the brain’s white matter.
Neuroscience (in press)
43 Butt, A.M. et al. (2005) Synantocytes: the fifth element. J. Anat. 207,
695–706
44 Nishiyama, A. (2007) Polydendrocytes: NG2 cells with many roles in
development and repair of the CNS. Neuroscientist 13, 62–76
45 Paukert, M. and Bergles, D.E. (2006) Synaptic communication
between neurons and NG2+ cells. Curr. Opin. Neurobiol. 16, 515–
521
46 Sherwood, C.C. et al. (2006) Evolution of increased glia-neuron ratios in
the human frontal cortex. Proc. Natl. Acad. Sci. U. S. A. 103, 13606–
13611
47 Oberheim, N.A. et al. (2006) Astrocytic complexity distinguishes the
human brain. Trends Neurosci. 29, 547–553
48 Alzheimer, A. (1910) Beiträge zur Kenntnis der pathologischen
Neuroglia und ihrer Beziehungen zu den Abbauvorgängen im
Nervengewebe. In Histologische und histopathologische Arbeiten
über die Grosshirnrinde mit besonderer Berücksichtigung der
pathologischen Anatomie der Geisteskrankheiten (Vol. 3) Nissl, F.
and Alzheimer, A.,eds pp. 401–562, Gustav Fischer
49 Biber, K. et al. (2007) Neuronal ‘On’ and ‘Off’ signals control microglia.
Trends Neurosci. 30, 596–602
50 Hanisch, U.K. and Kettenmann, H. (2007) Microglia: active sensor and
versatile effector cells in the normal and pathologic brain. Nat.
Neurosci. 10, 1387–1394
51 Pocock, J.M. and Kettenmann, H. (2007) Neurotransmitter receptors
on microglia. Trends Neurosci. 30, 527–535
52 Wang, X. et al. (2006) Astrocytic Ca2+ signaling evoked by sensory
stimulation in vivo. Nat. Neurosci. 9, 816–823
659