Modulation of the cell cycle contributes to the parcellation of the primate visual cortex

Dehay, Colette; Giroud, Pascale; Berland, Michel; Smart, I. H. M.; Kennedy, Henry

doi:10.1038/366464a0

Cited by 147 publications

(95 citation statements)

References 22 publications

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“…The mean duration of gestation for M. fascilcularis (used here) and M. mulatta (the species used by Rakic) is 165 d. The ranges of gestation are reported to vary somewhat between these two species (Roonwal and Mohnot, 1977). However, we observed similar timetables and tempos of prenatal visual system development in both species (Rakic, 1974;Dehay et al, 1993). Therefore, we are confident that our results can be directly compared across these two species.…”

Section: Methodsmentioning

confidence: 49%

Early and Rapid Targeting of Eye-Specific Axonal Projections to the Dorsal Lateral Geniculate Nucleus in the Fetal Macaque

Huberman¹,

Dehay²,

Berland³

et al. 2005

J. Neurosci.

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The emergence of eye-specific axonal projections to the dorsal lateral geniculate nucleus (dLGN) is a well established model system for exploring the mechanisms underlying afferent targeting during development. Using modern tract tracing methods, we examined the development of this feature in the macaque, an Old World Primate with a visual system similar to that of humans. Cholera toxin ␤ fragment conjugated to Alexa 488 was injected into the vitreous of one eye, and CT␤ conjugated to Alexa 594 into the other eye of embryos at known gestational ages. On embryonic day 69 (E69), which is ϳ100 d before birth, inputs from the two eyes were extensively intermingled in the dLGN. However, even at this early age, portions of the dLGN were preferentially innervated by the right or left eye, and segregation is complete within the dorsalmost layers 5 and 6. By E78, eye-specific segregation is clearly established throughout the parvocellular division of the dLGN, and substantial ocular segregation is present in the magnocellular division. By E84, segregation of left and right eye axons is essentially complete, and the six eye-specific domains that characterize the mature macaque dLGN are clearly discernable. These findings reveal that targeting of eye-specific axonal projections in the macaque occurs much earlier and more rapidly than previously reported. This segregation process is completed before the reported onset of ganglion cell axon loss and retino-dLGN synapse elimination, suggesting that, in the primate, eye-specific targeting occurs independent of traditional forms of synaptic plasticity.

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Section: Methodsmentioning

confidence: 49%

Early and Rapid Targeting of Eye-Specific Axonal Projections to the Dorsal Lateral Geniculate Nucleus in the Fetal Macaque

Huberman¹,

Dehay²,

Berland³

et al. 2005

J. Neurosci.

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Section: Abstract: Development; Cortex; Proliferation; Areal Specifimentioning

confidence: 99%

“…Environmental signaling during the final round of mitosis has been shown to be a key event in the specification of the future connectivity of cortical neuroblasts (McConnell and Kaznowski, 1991;Eagleson et al, 1997), and modulation of cell-cycle kinetics contributes to determining areal cytoarchitecture (Dehay et al, 1993;Polleux et al, 1997). There is indirect evidence that, in the primate, thalamic afferents contribute toward specifying the identity of cortical areas during very early stages of cortical development by regulating the rates of neurogenesis in the ventricular zone (Dehay et al, 1993. Thalamic afferents could influence rates of neuron production either by influencing cell death, which is prevalent in the ventricular zone (Blaschke et al, 1998;Haydar et al, 1999a), or by acting on cell-cycle parameters, in accordance with findings in lower vertebrates and invertebrates (Kollros, 1953(Kollros, , 1982Williams and Herrup, 1988;Baptista et al, 1990;Selleck and Steller, 1991;Gong and Shipley, 1995).…”

Section: Abstract: Development; Cortex; Proliferation; Areal Specifimentioning

confidence: 99%

Cell-Cycle Kinetics of Neocortical Precursors Are Influenced by Embryonic Thalamic Axons

et al. 2001

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Thalamic afferents are known to exert a control over the differentiation of cortical areas at late stages of development. Here, we show that thalamic afferents also influence early stages of corticogenesis at the level of the ventricular zone. Using an in vitro approach, we show that embryonic day 14 mouse thalamic axons release a diffusable factor that promotes the proliferation of cortical precursors over a restricted developmental window. The thalamic mitogenic effect on cortical precursors (1) shortens the total cell-cycle duration via a reduction of the G 1 phase; (2) facilitates the G 1 /S transition leading to an increase in proliferative divisions; (3) is significantly reduced by antibodies directed against bFGF; and (4) influences the proliferation of both glial and neuronal precursors and does not preclude the action of signals that induce differentiation in these two lineages. We have related these in vitro findings to the in vivo condition: the organotypic culture of cortical explants in which anatomical thalamocortical innervation is preserved shows significantly increased proliferation rates compared with cortical explants devoid of subcortical afferents. These results are in line with a number of studies at subcortical levels showing the control of neurogenesis via afferent fibers in both vertebrates and invertebrates. Specifically, they indicate the mechanisms whereby embryonic thalamic afferents contribute to the known early regionalization of the ventricular zone, which plays a major role in the specification of neocortical areas. Key words: development; cortex; proliferation; areal specification; mouse; ventricular zoneCells of the cerebral cortex originate from the ventricular and subventricular zones of the embryonic telencephalon. The heterogeneous population of precursors lining the ventricular zone divide, migrate, and differentiate to form the cerebral cortex. Although many of the developmental events occurring during corticogenesis have been described (Angevine and Sidman, 1961;Smart, 1973;Smart and Smart, 1982;Rakic, 1988;Bayer and Altman, 1991), the contribution of early mechanisms that determine the phenotypes of cortical neurons and specify the identity of cortical areas still has to be resolved (McConnell, 1995).The sensory periphery exerts an important control over the development of the immature cortical plate via thalamic afferents (O'Leary, 1989). Such afferent specification of cortex (Killackey, 1990) is in line with in vivo and in vitro experiments showing that thalamic afferents influence cell survival and differentiation (Repka and Cunningham, 1987;Windrem and Finlay, 1991;Lotto and Price, 1996;Price and Lotto, 1996;Zhou et al., 1999). However, there is also clear evidence that there is a specification of cortical neuron phenotype at the level of the ventricular zone before migration to the cortical plate (Arimatsu et al., 1992;Cohen-Tannoudji et al., 1994;Soriano et al., 1995;Levitt et al., 1997;Miyashita-Lin et al., 1999, Nakagawa et al., 1999.Given the developmental impa...

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“…The above described results of the precursor pool dynamics from Otani et al have been obtained from observations over a 20-day period, from D20 to D40 in macaque and human cultures. D40 in macaque cultures corresponds to the end of layer V, beginning of layer IV production [circa E65 in the macaque visual cortex (31,32,36)] and to the peak of layer VI production in human [circa E65 in the human visual cortex (32)] (Figure 1). The 20-day culture period (13) and (14) for macaque and human respectively).…”

Section: Species-specific Differences In the Timing Of Precursor Poolmentioning

confidence: 99%

“…The in vitro culture accurately models the early stages of corticogenesis An extensive and reliable database of the macaque cortical precursor proliferation dynamics has been provided by a series of in vivo and ex vivo studies (18,31,(34)(35)(36)(37)(38). Establishing the correspondence between the in vitro and the in vivo tempo of corticogenesis is a prerequisite to fully appraise the relevance of the in vitro findings.…”

Section: Species-specific Differences In the Timing Of Precursor Poolmentioning

confidence: 99%

From stem cells to comparative corticogenesis: a bridge too far?

Betizeau

Dehay

2016

Stem Cell Investig.

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It has been hypothesized that the higher number of neurons in human cortex compared to the chimpanzee and other primate species is key to high cognitive function. Are human cortical precursors endowed with specific properties that drive greater neuronal expansion than in other non-human primates?Otani et al. 2016 addressed this issue taking advantage of comparative in vitro corticogenesis models based on human, chimpanzee and macaque pluripotent stem cells. Clonal analysis revealed a heterochrony of early developmental events possibly leading to a relatively higher expansion of human cortical precursor population. In absence of evidence going beyond putative correlation, the claim that stem cell models of cortical development indicate mechanism of cortical size regulation needs to be further examined notably with respect to in vivo observations of cortical precursor lineages.

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Modulation of the cell cycle contributes to the parcellation of the primate visual cortex

Cited by 147 publications

References 22 publications

Early and Rapid Targeting of Eye-Specific Axonal Projections to the Dorsal Lateral Geniculate Nucleus in the Fetal Macaque

Early and Rapid Targeting of Eye-Specific Axonal Projections to the Dorsal Lateral Geniculate Nucleus in the Fetal Macaque

Cell-Cycle Kinetics of Neocortical Precursors Are Influenced by Embryonic Thalamic Axons

From stem cells to comparative corticogenesis: a bridge too far?

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