Decision by division: Making cortical maps

Department of Neurobiology and Kavli Institute of Neuroscience, Yale University School of Medicine, New Haven, CT 06510, USA.
Trends in Neurosciences (Impact Factor: 12.9). 05/2009; 32(5):291-301. DOI: 10.1016/j.tins.2009.01.007
Source: PubMed

ABSTRACT In the past three decades, mounting evidence has revealed that specification of the basic cortical neuronal classes starts at the time of their final mitotic divisions in the embryonic proliferative zones. This early cell determination continues during the migration of the newborn neurons across the widening cerebral wall, and it is in the cortical plate that they attain their final positions and establish species-specific cytoarchitectonic areas. Here, the development and evolutionary expansion of the neocortex is viewed in the context of the radial unit and protomap hypotheses. A broad spectrum of findings gave insight into the pathogenesis of cortical malformations and the biological bases for the evolution of the modern human neocortex. We examine the history and evidence behind the concept of early specification of neurons and provide the latest compendium of genes and signaling molecules involved in neuronal fate determination and specification.

Download full-text


Available from: Albert Ayoub, Aug 31, 2015
  • Source
    • "Eph-ephrin interactions regulate a variety of neurodevelopmental processes, including axonal guidance, migration and apoptosis, in addition to proliferation (Drescher et al., 1997; Flanagan and Vanderhaeghen, 1998; Depaepe et al., 2005; Zimmer et al., 2008; North et al., 2009; Rudolph et al., 2010), and are crucial for establishing thalamocortical projections (Donoghue and Rakic, 1999; Šestan et al., 2001; Bolz et al., 2004). Despite intensive discussion as to whether cortical development is mainly regulated by intrinsic and/or extrinsic cues (Rakic, 1988, 1991; Dehay et al., 2001; Rakic et al., 2009; Zhou et al., 2010; Reillo et al., 2011), the thalamic influence on cortical progenitors and neurogenesis remains debated. Here, we provide further evidence for the extra-cortical regulation of cortical progenitors and hence the final output of neurons by thalamic afferents via the Eph/ephrin system. "
    [Show abstract] [Hide abstract]
    ABSTRACT: The phenotype of excitatory cerebral cortex neurons is specified at the progenitor level, orchestrated by various intrinsic and extrinsic factors. Here, we provide evidence for a subcortical contribution to cortical progenitor regulation by thalamic axons via ephrin A5-EphA4 interactions. Ephrin A5 is expressed by thalamic axons and represents a high-affinity ligand for EphA4 receptors detected in cortical precursors. Recombinant ephrin A5-Fc protein, as well as ephrin A ligand-expressing, thalamic axons affect the output of cortical progenitor division in vitro. Ephrin A5-deficient mice show an altered division mode of radial glial cells (RGCs) accompanied by increased numbers of intermediate progenitor cells (IPCs) and an elevated neuronal production for the deep cortical layers at E13.5. In turn, at E16.5 the pool of IPCs is diminished, accompanied by reduced rates of generated neurons destined for the upper cortical layers. This correlates with extended infragranular layers at the expense of superficial cortical layers in adult ephrin A5-deficient and EphA4-deficient mice. We suggest that ephrin A5 ligands imported by invading thalamic axons interact with EphA4-expressing RGCs, thereby contributing to the fine-tuning of IPC generation and thus the proper neuronal output for cortical layers. © 2015. Published by The Company of Biologists Ltd.
    Development 12/2014; 142(1). DOI:10.1242/dev.104927 · 6.27 Impact Factor
  • Source
    • "Similarly, the highly visual marmoset monkey (Callithrix jacchus) visual cortex comprises more areas and enhanced visual ability but a comparatively smaller brain than the cat. Therefore, the evolutionary expansion of the neocortical surface (Rakic et al., 2009) does not directly correlate with the addition of visual areas in higher species (Kaas, 1997). It has been proposed that the complexity of neural system, corresponding to the number of cortical divisions and subcortical nuclei, increases with the establishment of a new mammalian order (Manger, 2005). "
    [Show abstract] [Hide abstract]
    ABSTRACT: The integration of the visual stimulus takes place at the level of the neocortex, organized in anatomically distinct and functionally unique areas. Primates, including humans, are heavily dependent on vision, with approximately 50% of their neocortical surface dedicated to visual processing and possess many more visual areas than any other mammal, making them the model of choice to study visual cortical arealisation. However, in order to identify the mechanisms responsible for patterning the developing neocortex, specifying area identity as well as elucidate events that have enabled the evolution of the complex primate visual cortex, it is essential to gain access to the cortical maps of alternative species. To this end, species including the mouse have driven the identification of cellular markers, which possess an area-specific expression profile, the development of new tools to label connections and technological advance in imaging techniques enabling monitoring of cortical activity in a behaving animal. In this review we present non-primate species that have contributed to elucidating the evolution and development of the visual cortex. We describe the current understanding of the mechanisms supporting the establishment of areal borders during development, mainly gained in the mouse thanks to the availability of genetically modified lines but also the limitations of the mouse model and the need for alternate species.
    Frontiers in Neural Circuits 07/2014; 8:79. DOI:10.3389/fncir.2014.00079 · 2.95 Impact Factor
  • Source
    • "Our data suggest that, when the timing of neurogenesis is disrupted, ipsilateral and contralateral specification related to chiasmatic decussation is altered. Our findings are also in agreement with analyses of other brain regions and species illustrating that precise patterns of proliferation and neurogenesis regulate cell fate decisions, and that the length of cell cycle phases and time of birth can influence the proper proportion of different cell types [47-50]. Moreover, similar to our findings in the VT retina, it has been shown in the neocortex that variations in cell cycle length and transcription factor expression collaborate during the production of specific cell types and determination of their ultimate position [51]. "
    [Show abstract] [Hide abstract]
    ABSTRACT: Background Proper binocular vision depends on the routing at the optic chiasm of the correct proportion of retinal ganglion cell (RGC) axons that project to the same (ipsilateral) and opposite (contralateral) side of the brain. The ipsilateral RGC projection is reduced in mammals with albinism, a congenital disorder characterized by deficient pigmentation in the skin, hair, and eyes. Compared to the pigmented embryonic mouse retina, the albino embryonic mouse retina has fewer RGCs that express the zinc-finger transcription factor, Zic2, which is transiently expressed by RGCs fated to project ipsilaterally. Here, using Zic2 as a marker of ipsilateral RGCs, Islet2 as a marker of contralateral RGCs, and birthdating, we investigate spatiotemporal dynamics of RGC production as they relate to the phenotype of diminished ipsilateral RGC number in the albino retina. Results At embryonic day (E)15.5, fewer Zic2-positive (Zic2+) RGCs are found in the albino ventrotemporal (VT) retina compared with the pigmented VT retina, as we previously reported. However, the reduction in Zic2+ RGCs in the albino is not accompanied by a compensatory increase in Zic2-negative (Zic2−) RGCs, resulting in fewer RGCs in the VT retina at this time point. At E17.5, however, the number of RGCs in the VT region is similar in pigmented and albino retinae, implicating a shift in the timing of RGC production in the albino. Short-term birthdating assays reveal a delay in RGC production in the albino VT retina between E13 and E15. Specifically, fewer Zic2+ RGCs are born at E13 and more Zic2− RGCs are born at E15. Consistent with an increase in the production of Zic2− RGCs born at later ages, more RGCs at E17.5 express the contralateral marker, Islet2, in the albino VT retina compared with the pigmented retina. Conclusions A delay in neurogenesis in the albino retina is linked to the alteration of RGC subtype specification and consequently leads to the reduced ipsilateral projection that characterizes albinism.
    Neural Development 05/2014; 9(1):11. DOI:10.1186/1749-8104-9-11 · 3.37 Impact Factor
Show more