1 GSF, National Research Centre for Environment and Health, Institute for Stem
Cell Research, Neuherberg/Munich and Institute of Physiology, University of
Munich, 80336 Munich, Germany
2 Institute of Cell Biology, Department of Biology, Swiss Federal Institute of
Technology, ETH-Honggerberg, CH-8093 Zurich, Switzerland
* Author for correspondence (e-mail: magdalena.goetz{at}gsf.de)
SUMMARY
The fascinating question of how the enormous diversity of neuronal and glial cells in the cerebral cortex is generated during development was recently discussed at a meeting on cortical development and stem cells in Greece. What emerged from this meeting is an equally fascinating answer, namely that precursor diversity at rather early stages of development anticipates later cell type diversity.
Introduction
The steeply cliffed Aegean island of Santorini was the venue for a recent meeting on neural stem cells and cortical development that was organized by John Parnavelas (University College, London, UK) and Arnold Kriegstein (University of California, San Francisco, CA, USA). The stimulating atmosphere and success of the meeting was fortunately not affected by a pan-Hellenic strike on 11 May, which caused many of the meeting's participants to have their own personal experience of the never-ending travels of Odysseus, as described in ancient Greek mythology.
The ground plan
The cerebral cortex covers almost the entire human brain, owing to its
enormous growth and increase in surface area during mammalian evolution. It
forms from the most rostral region of the neural tube, the prosencephalon,
that later divides into the telencephalon and diencephalon. The dorsal region
of the telencephalon gives rise to the cerebral cortex, which comprises the
neocortex, paleocortex (piriform cortex) and archicortex (hippocampus), while
the ventral telencephalon differentiates into the basal ganglia. These
dorsoventral, and also rostrocaudal, differences are established by diffusible
morphogens, which are released from distinct locations. For example,
fibroblast growth factor 8 (Fgf8) is produced rostrally, while Wnt and bone
morphogenetic proteins are released caudally and dorsally, and sonic hedgehog
(Shh) is released ventrally (Fig.
1A) (Shimogori et al.,
2004). These factors instruct the surrounding tissue to acquire a
`dorsal', `rostral' or `ventral' identity, as is evident when Wnt signalling
is activated or deleted and causes consequent changes in dorsal patterning.
For example, as presented by Corinne Houart (King's College, London, UK),
constitutively activating Wnt signalling in zebrafish leads to a dorsalization
of the telencephalon. Wnt signalling in the caudodorsal region of the
telencephalon does not rely on a single ligand, but rather on several members
of the Wnt family, most of which are expressed in a small region located in
the caudomedial telencephalon called the cortical hem
(Grove et al., 1998
). The
cortical hem is intercalated between the medial cortex, which will later
develop into the hippocampal anlage, and the medial most choroid plexus anlage
(Fig. 1A). Besides the richness
of Wnt gene expression in the cortical hem, its precise role and progeny have
been unknown. However, Liz Grove (University of Chicago, Chicago, IL, USA)
shed new light on this at the meeting from her fate-mapping studies of the hem
and its progeny. When these researchers crossed a Wnt3a-Cre
mouse line to reporter strains, they found that reelin-positive cells spread
over the dorsal telencephalon in the uppermost layer of the cerebral cortex
(layer 1) were labelled as the main progeny of the cortical hem, consistent
with previous data (Takiguchi-Hayashi et
al., 2004
). It is these cells that are largely lost if the hem is
ablated at embryonic day (E) 10 by hem-specific diphtheria toxin expression.
Notably, however, no obvious patterning defects occur upon hem ablation, nor
is cortical layering abnormal, despite the severe reduction of reelin-positive
cells (the absence of reelin in the reeler mouse mutant leads to
defects in cortical layering, as detailed below) (for a review, see
Tissir and Goffinet, 2003
). A
possible explanation for the absence of patterning defects in the dorsal
telencephalon, despite ablation of the cortical hem, may be timing. When
ß-catenin is deleted at E8 in the mouse, the prospective dorsal
telencephalon becomes at least partially ventralized, whereas this is not the
case when ß-catenin is deleted at E11
(Backman et al., 2005
). Thus,
the absence of gross dorsalization defects in the telencephalon upon hem
deletion at E10 might mean that either the crucial time window for Wnt
signalling from the cortical hem takes place prior to E10 or that there are
other sources of Wnt signalling outside the cortical hem that are sufficient
to maintain the dorsal identity of the dorsal telencephalon, at least at these
latter stages. Indeed, signalling centres are often most crucial at the
earliest developmental stages, and lose their importance when a tissue grows
and regional cell identity has been intrinsically fixed by cell autonomous
mechanisms (Li et al., 2005
).
Taken together, at mostly early stages of telencephalic development, local
sources of signalling molecules are crucial in setting up the ground plan of
the telencephalon and are crucially required for its subsequent
differentiation into the cerebral cortex dorsally and the basal ganglia
ventrally. As discussed below, new insights were presented at the meeting as
to how cell biological processes regulate such signalling events.
Spotlight on cilia and microvilli
A mutagenesis screen designed to identify molecular mechanisms that
regulate telencephalic patterning
(Zarbalis et al., 2004)
revealed two mouse mutants with somewhat paradoxical defects in dorsoventral
patterning: an early loss of ventral structures but an apparent ventralization
of the cortex over time. The defects were traced to a loss of the retrograde
motor for intraflagellar transport, and the telencephalon in these mutant mice
had neuroectodermal cells with abnormally thick cilia filled with
intraflagellar transport particles. Andy Peterson (University of California,
San Francisco, CA, USA) presented evidence that it is the intraflagellar
transport directed out of the cilia that fails in these mouse mutants. He
presented additional evidence that the smoothened (Smo) protein, an essential
component of the Shh signal transduction pathway, is normally localized to
cilia. The inability of the mutants to localize Smo to the cilia causes a loss
of both transcriptional activation and transcriptional repression by the Gli
transcription factors (Liu et al.,
2005
). Shh is expressed in the ventral most regions of the
developing telencephalon (Fig.
1A) and acts via Gli activators to regulate Nkx2.1 and specify
ventral regions (Fig. 1B),
while Gli-repressor activity is required for dorsal telencephalic regions to
develop. Thus, intraflagellar transport in apically located cilia is crucial
for a specific signalling pathway, an important demonstration of a role for
these enigmatic organelles.
|
Diversity of cortical precursors
The findings presented above highlight the importance of signalling within
the ventricular fluid and the role of the apical membrane domain in signalling
in cell division and cortical development. Indeed, elegant time-lapse studies
of individual precursors in cortical slice preparations have demonstrated that
an important difference exists between the precursors that divide at the
apical surface (ventricular zone precursors) or within the parenchyma
(abventricular mitoses, basal precursors): only the former divide
asymmetrically; the latter nearly always divide symmetrically and in most
cases only once (Haubensak et al.,
2004; Miyata et al.,
2004
; Noctor et al.,
2004
). Thus, cell fate and the number of cell divisions are rather
limited in the absence of access to apical fate determinants. As the apical
membrane surface is so small (1-2% of the total membrane, see above), its
unequal or equal distribution does not readily correlate with the orientation
of cell division (Kosodo et al.,
2004
). Vertically oriented cell division can either divide the
apical membrane patch equally, in which case both daughters remain as
precursors, or unequally, resulting in the generation of two unequal
daughters: a neuron and a precursor cell. Thus, it is the membrane fusion
mediated by the cleavage furrow, rather than the gross orientation of cell
division, that seems to predict the mode of cell division at least in
the mammalian cerebral cortex (reviewed by
Götz and Huttner, 2005
).
Consistent with this concept, Steven Noctor (University of California, San
Francisco, CA, USA) presented evidence that the basally located precursors
undergo randomly oriented divisions with a bias towards a horizontal plane of
cell division, consistent with previous observations
(Smart, 1973
). Thus, the
orientation of cell division can not serve as an indicator of symmetric or
asymmetric daughter cell fate. A riddle not yet solved, however, is why
abventricular cell divisions are neurogenic in the embryonic cortex, while at
some point, glial precursors also divide at this position. In fact, glial
precursors also divide mostly symmetrically with the notable exception of some
adult neural stem cells that are characterized by access to the ventricle
(Alvarez-Buylla et al., 2001
).
Indeed, signalling from the ventricle also continues to exert crucial
influence during adult neurogenesis. Arturo Alvarez-Buylla (University of
California, San Francisco, CA, USA) presented evidence for a signalling
gradient that is established by the secretion of diffusible molecules from the
choroid plexus into the cerebrospinal fluid and by the directed beating of
ependymal cilia, which influences the directed migration of neuroblasts in the
adult subependymal zone.
As evident from the above discussion, both the location and time of cell
division have to be tightly controlled during cortical development to ensure
the generation of proper neuronal and non-neuronal cell numbers, but how this
is molecularly regulated still remains unknown. The Notch-signalling effectors
Hes1, Hes3 and Hes5 might be crucial players in this process, as nicely
illustrated by Ryoichiro Kageyama (Kyoto University, Kyoto, Japan), who
presented the effects of disrupting Hes genes in mice. Their loss, he showed,
interfered with the capacity of radial glia to undergo asymmetric cell
division, thereby causing radial glia cell depletion and premature
neurogenesis (Hatakeyama et al.,
2004). In addition, both apical intercellular junctions and the
basal lamina are lost in these mutants, resulting in the scattering of
neuronal cells and in the disorganization of brain and spinal cord structures.
These data also raise the intriguing possibility that Notch signalling acts
via, or may require, adherens junction complexes, thereby providing yet
another link between cell fate and apicobasal membrane specializations (as
also evident in the numb and numb-like mutant cortex)
(Li et al., 2003
). According
to this idea, Notch-signalling via Hes maintains neuroepithelial or radial
glia identity (Gaiano et al.,
2000
), while Hes expression is not maintained in abventricular
progenitors, allowing these cells to differentiate into neurons. Hes proteins
have a similar function in maintaining radial glial properties in brain
compartment boundaries and in signalling centres, where Hes1
expression is high and persistent, resulting in the permanent suppression of
neurogenesis. Strikingly, although Hes factors can promote cell proliferation
by repressing cyclin-dependent kinase inhibitors
(Castella et al., 2000
;
Murata et al., 2005
),
persistently high levels of Hes (as found in boundary cells) reduce cell
proliferation, while still preventing neurogenesis. This role is reminiscent
of a general mechanism for maintaining stem cells in a quiescent state
a notion that is supported by the fact that some boundary cells maintain
undifferentiated or stem-cell-like properties into adulthood
(Alvarez-Buylla et al., 2001
;
Geling et al., 2004
).
Specificity in origin relates to subtype diversity
Once a multi- or bi-potent precursor cell has chosen to generate further
differentiated progeny, such as neuronal or glial precursors in the
neuroepithelium, how is neuronal and glial subtype heterogeneity established?
During telencephalon development, GABAergic interneurons and oligodendrocyte
precursors migrate from ventral regions into dorsal territories
(Fig. 1C). However, not all
oligodendrocyte precursors originate at ventral positions, but rather
originate in various telencephalic (and spinal cord) regions. This was
beautifully demonstrated by Nic Kessaris (University College, London, UK), who
used a rich collection of mice expressing the Cre recombinase in specific
regions of the developing brain [and spinal cord, see Fogarty et al.
(Fogarty et al., 2005)].
Kessaris and colleagues' fate-mapping of the progeny of cells from the
Nkx2.1-expressing medial ganglionic eminence
(Fig. 1B) (which they mapped by
crossing a Nkx2.1::Cre line to a reporter line) confirmed
that all oligodendrocyte precursors in the dorsal telencephalon and the
cerebral cortex originally derived from ventral sources at most embryonic
stages. However, their numbers dwindled at late embryonic stages, until only
4% of all oligodendrocytes were labelled in the postnatal and adult brain.
Indeed, the converse fate-mapping experiment, using Emx1 to drive
Cre in the dorsal telencephalon
(Fig. 1B), revealed that
oligodendrocytes originating from dorsal regions take over around birth, when
30% of all oligodendrocytes are derived from dorsal precursors in the cortex,
reaching 50% at later stages. Thus, oligodendrocyte precursors from ventral
regions dominate at embryonic stages throughout the telencephalon, while
regional sources of oligodendrocytes take over postnatally (see also
Ivanova et al., 2003
;
Spassky et al., 2001
). A
similar scenario occurs in the subplate and marginal zone, where transient
sources of neurons function during development, while other neuronal subtypes
take over in the adult cortex. However, by using the Cre-lines to ablate
specific oligodendrocyte precursors, Kessaris showed that each population of
oligodendrocyte precursors can compensate for the other, and, so far, no
oligodendrocyte precursor that has a region-specific origin has been observed
to have a specific function. As ventrally derived precursors generate probably
both interneurons and oligodendrocytes (He
et al., 2001
; Yung et al.,
2002
), the ventrally derived precursors might be bipotent
neuro-oligo precursors, while the dorsally derived oligodendrocyte precursors
may be glial-restricted precursors. This would explain why the number of
bi-potent oligodendrocyte precursors drops postnatally
(Belachew et al., 2003
) and
would predict that most oligodendrocyte precursors maintain their bipotent
fate in the Emx1-Cre-depleted oligodendrocyte precursor pool.
These observations also highlight the need to re-examine with these more
accurate tools whether indeed all GABAergic neurons as currently
thought originate at ventral positions. Many certainly do (reviewed by
Marin and Rubenstein, 2001),
and another focus of the meeting was on how early subtypes of GABAergic
interneurons are specified. Transplantation experiments have directly
demonstrated that the birth date of a cortical interneuron in the ganglionic
eminence predicts which cortical layer it will later occupy, such that
early-born GABAergic neurons settle in the deeper cortical layers, whereas
later-born GABAergic neurons settle largely in the upper cortical layers
(Valcanis and Tan, 2003
). As
heterochronic transplants show a mixed phenotype (i.e. some transplanted cells
behave according to the host environment, while others behave according to
their intrinsic birth date), both intrinsic mechanisms of specification, as
well as extrinsic factors that regulate layer-specific cell migration, seem to
play a role. Seong-Seng Tan (Howard Florey Institute, Melbourne, Australia)
presented intriguing evidence that one of the extrinsic cues regulating
interneuron layer-specific targeting is reelin, the same factor that also
governs the radial migration of cortical projection neurons (reviewed by
Tissir and Goffinet, 2003
).
Interneurons deficient in one of the essential intracellular mediators of
reelin signalling, Dab1, end up in the wrong layer position, just as pyramidal
cells do in reeler mutant mice
(Polleux et al., 1998
). As
late-born interneurons are seen to delve into deeper positions of the cortical
wall where pyramidal neurons are about to commence their radial journey, these
data suggest that both pyramidal and non-pyramidal neurons react to the same
extrinsic signals directing their layer-specific migration. Neuronal migration
is, however, also governed by intrinsic cues, such as the transcription factor
neurogenin 2 (Ngn2). Data from Franck Polleux (University of North Carolina,
Chapel Hill, NC, USA) and Francois Guillemot (National Institute of Medical
Research, London, UK) revealed a novel mechanism by which Ngn2 affects the
radial migration of cortical neurons independently of its DNA-binding domain
but dependent on its phosphorylation state. This mechanism also provides a
basis for integrating extrinsic and intrinsic neuronal migration regulatory
mechanisms an obvious requirement for matching the position of diverse
cell types in the same layer.
In this regard it is amazing how many detailed aspects of the phenotype of a neuron seem to be already prefigured at its birth date. For example, new data from the laboratory of Gord Fishell (Skirball Institute, New York, NY, USA) demonstrate that both the laminar position and the physiological characteristics of an interneuron subtype correlate with the birthday of these interneurons, as beautifully demonstrated by the use of the tamoxifen-inducible form of Cre (CreERT2) under region-specific control elements. The fate-mapping of interneurons by inducing the nuclear localization of Cre in different regions of the ventral telencephalon (using the mouse lines, Olig2-CreERT2, Dlx2-CreERT2 and Dlx5-6-CreERT2, see Fig. 1B) revealed a fascinating degree of specificity. For example, interneurons generated at E10 from the Olig2-expressing domain were almost exclusively interneurons that fire trains of action potentials at high rates (fast-spiking), whereas those generated from the same domain at E15 were mostly of the regular-spiking phenotype. These results show that rather sophisticated electrophysiological features of interneuron subtypes correlate with their much earlier spatial and temporal origin, many weeks before these features develop.
Cortex evolution in mice and humans
Intriguingly, the matching of projection and interneuron numbers has
apparently been maintained during the expansion of the cerebral cortex in
phylogeny even across cortical areas
(Winfield et al., 1980),
despite prominent differences in the total number of neurons residing in
specific layers of distinct cortical areas. In mammals, including in mice and
humans, cortical areas take the form of radial domains within the cortex that
specialize in specific aspects of information processing. For example, the
occipital cortex comprises the visual areas, with the primary visual area V1
receiving direct thalamic input, in contrast to the neighbouring secondary
visual cortex. Importantly, many more neurons reside in the upper cortical
layers of V1 than of V2, and this feature of cortical organization seems to be
specified by early regulatory mechanisms at the precursor cell stage. Colette
Dehay (INSERM, Lyon, France) presented evidence that in primates, upper layer
neurons in V1 are mostly generated by a layer of precursors that seems to have
no analogy in the mouse, the so-called outer subventricular zone (OSVZ)
(Smart et al., 2002
). This
zone contains most of the precursors at the time when upper layer neurons are
generated (see Campbell, 2005
),
while the ventricular zone consists of a cell layer that is just a few cell
diameters thick. Surprisingly, the OSVZ contains cells with a radial glia
morphology, which is notably distinct from the morphology of the precursors in
the SVZ of the mouse cortex that exhibit only short processes with no apparent
contact with the apical surface or basement membrane
(Haubensak et al., 2004
;
Miyata et al., 2004
;
Noctor et al., 2004
).
Importantly for the generation of area-specific differences, precursors in the
OSVZ of V1 in the primate cortex have a 30% faster cell cycle than those
located in V2 [for cell cycle differences in cortical area of the mouse, see
Polleux et al. (Polleux et al.,
1997
)], and the fastest cycling cells are located in close
proximity to thalamic axons that innervate V1 but not V2. These findings
suggest that shortening the cell cycle in G1 by decreasing p27 levels and
increasing cyclin E causes the area-specific increase in upper layer neurons
mediated by the innervating afferents. Thus, regulating cell cycle length
specifies area identity, illustrating just one of several links between cell
cycle regulation and cell fate.
The striking concept to emerge from this work is that the fine-tuned
physiological factors that influence cortical information processing in
distinct areas are set up at amazingly early stages of cortical development.
Besides the early role of Fgf8 in ventralizing the developing telencephalon,
as demonstrated in a beautiful allelic series of Fgf8 mutant mice
(John Rubenstein, University of California, San Francisco, CA, USA) and by
conditional deletions of the Fgf receptors Fgfr1 and Fgfr2
by BF1-Cre (Jean Hébert, Albert Einstein College of Medicine, New York,
USA), the rostral location of Fgf8 (Fig.
1A) also provides the rostral pole that specifies the cortical
area in a rostrodorsal and lateromedial Cartesian grid. Indeed, tinkering with
Fgf8 also influences cortical area specification
(Fukuchi-Shimogori and Grove,
2001), including the appropriate innervation from the thalamus, as
presented by Liz Grove. During cortical development, thalamic fibres first
innervate the subplate layer according to their specification (thalamic fibres
from visual relay stations, the lateral geniculate nucleus, innervate the
subplate of the later visual cortex), and only later extend towards their
final target neurons in layer 4 of the cortex. Grove presented data suggesting
that thalamic fibres can re-orient towards layer 4 of their correct area, if
area identity has been shifted after the generation of subplate neurons. When
area shifts were induced after E11 (by electroporation of additional Fgf8
sources), only neurons generated from then onwards, i.e. those forming
cortical layers 5 to 2, are affected. Consequently, thalamic afferents target
their normal position in the subplate zone, but when they grow into the
later-generated layer 4, they seemingly `realize' that they are in the wrong
cortical area and grow laterally towards layer 4 of the correct area identity.
These observations strengthen the idea that the detailed functional aspects of
neuronal specificity and connectivity are set up at the time of neuronal birth
date. Indeed, Dennis O'Leary (Salk Institute, San Diego, CA, USA) presented
evidence that characteristic system properties of visual information
processing, which were initiated at the precursor cell stage by the mild
overexpression of Emx2, also follow the expansion of visual areas
(Hamasaki et al., 2004
). This
expansion of visual areas, however, comes at a price, as the consequent
reduction in motor areas apparently leads to significant defects in motor
behaviour, suggesting that a specific area size is crucial for appropriate
information processing.
Taken together, these and other findings presented at this meeting show that the functional features of cortical neuronal information processing are established at amazingly early stages of development, such as at the precursor cell level, and that already at these early stages neuronal and glial heterogeneity are prefigured. Thus, systems neuroscience moves to the early stages of development.
ACKNOWLEDGMENTS
We thank the organizers, John Parnavelas and Arnold Kriegstein, for a truly inspiring and wonderful meeting that comprised many more highlights than we could discuss here. We therefore apologize to all colleagues who presented fascinating new data that we could not discuss here owing to space constraints. We are also very grateful to Marie-Theres Schmid for preparing the figure for this review.
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