Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases

Noctor, Stephen C.; Martínez‐Cerdeño, Verónica; Ivic, Lidija; Kriegstein, Arnold R.

doi:10.1038/nn1172

Cited by 2,012 publications

(2,154 citation statements)

References 48 publications

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“…Transitions occur at mitosis but not along the cell cycle between mitoses, when bRGCs remain stable as a single morphotype. This remarkable lineage plasticity between bRGCs and IPCs, and its apparent reversibility (bRGC‐to‐IPC, and IPC‐to‐bRGC) is in sharp contrast with current observations in mouse where the sequence aRGC‐to‐IPC or aRGC‐to‐bRGC is irreversible (Betizeau et al, 2013; Noctor et al, 2004; Shitamukai et al, 2011; Wang et al, 2011). Given that these transitions are a dynamic feature, it will require using similar videomicroscopy approaches to define if they also occur in other species, and at which frequency.…”

Section: Variations On a Mouse Theme: Toward A Global Understandingcontrasting

confidence: 86%

“…2). In agreement with this notion, the occurrence of direct neurogenesis in the mouse cerebral cortex is remarkably infrequent (Attardo et al, 2008; Haubensak et al, 2004; Kowalczyk et al, 2009; Noctor et al, 2004). Hence, two fundamental changes must have occurred during vertebrate evolution between reptiles/birds and mammals leading to the emergence of the neocortex: (1) abundant generation of a novel type of neurogenic progenitor cell populating and dividing at basal positions in the embryonic cortex and (2) near complete suppression of the direct neurogenic program from aRGCs (Fig.…”

Section: Dawn and Expansion Of The Neocortexmentioning

confidence: 73%

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Coevolution of radial glial cells and the cerebral cortex

Romero

Borrell

2015

Glia

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Radial glia cells play fundamental roles in the development of the cerebral cortex, acting both as the primary stem and progenitor cells, as well as the guides for neuronal migration and lamination. These critical functions of radial glia cells in cortical development have been discovered mostly during the last 15 years and, more recently, seminal studies have demonstrated the existence of a remarkable diversity of additional cortical progenitor cell types, including a variety of basal radial glia cells with key roles in cortical expansion and folding, both in ontogeny and phylogeny. In this review, we summarize the main cellular and molecular mechanisms known to be involved in cerebral cortex development in mouse, as the currently preferred animal model, and then compare these with known mechanisms in other vertebrates, both mammal and nonmammal, including human. This allows us to present a global picture of how radial glia cells and the cerebral cortex seem to have coevolved, from reptiles to primates, leading to the remarkable diversity of vertebrate cortical phenotypes. GLIA 2015;63:1303–1319

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Section: Variations On a Mouse Theme: Toward A Global Understandingcontrasting

confidence: 86%

Section: Dawn and Expansion Of The Neocortexmentioning

confidence: 73%

Coevolution of radial glial cells and the cerebral cortex

Romero

Borrell

2015

Glia

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“…For this study we tested the impact of constraining the directionality of differentiation, so that precursors after each division become progressively more fate constrained. Although this is a common hypothesis concerning the nature of corticogenesis (Qian et al, 1998; Noctor et al, 2004; Tyler and Haydar, 2013), we found that an explicit inclusion of this assumption leads to a model (Fig. 9) that does not match the biological reality as well as fully unconstrained models, suggesting that bidirectional transitions between most (but not all) of the precursor types would be a fundamental property that a model of primate corticogenesis should capture.…”

Section: Discussionmentioning

confidence: 99%

Unsupervised lineage‐based characterization of primate precursors reveals high proliferative and morphological diversity in the OSVZ

Pfeiffer

Betizeau

Waltispurger

et al. 2015

J of Comparative Neurology

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Generation of the primate cortex is characterized by the diversity of cortical precursors and the complexity of their lineage relationships. Recent studies have reported miscellaneous precursor types based on observer classification of cell biology features including morphology, stemness, and proliferative behavior. Here we use an unsupervised machine learning method for Hidden Markov Trees (HMTs), which can be applied to large datasets to classify precursors on the basis of morphology, cell‐cycle length, and behavior during mitosis. The unbiased lineage analysis automatically identifies cell types by applying a lineage‐based clustering and model‐learning algorithm to a macaque corticogenesis dataset. The algorithmic results validate previously reported observer classification of precursor types and show numerous advantages: It predicts a higher diversity of progenitors and numerous potential transitions between precursor types. The HMT model can be initialized to learn a user‐defined number of distinct classes of precursors. This makes it possible to 1) reveal as yet undetected precursor types in view of exploring the significant features of precursors with respect to specific cellular processes; and 2) explore specific lineage features. For example, most precursors in the experimental dataset exhibit bidirectional transitions. Constraining the directionality in the HMT model leads to a reduction in precursor diversity following multiple divisions, thereby suggesting that one impact of bidirectionality in corticogenesis is to maintain precursor diversity. In this way we show that unsupervised lineage analysis provides a valuable methodology for investigating fundamental features of corticogenesis. J. Comp. Neurol. 524:535–563, 2016. © 2015 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

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“…A subpopulation of bIPs with self‐renewing capacity has been reported in the rodent (Noctor et al, 2004) and human neocortex (Hansen et al, 2010; LaMonica et al, 2013). Their abundance has been speculated to be at least partially responsible for the expansion of the neocortex in gyrencephalic species (Lui et al, 2011).…”

mentioning

confidence: 92%

“…Basal intermediate progenitors (bIPs) are multipolar cells with no known polarity cues; they express the transcription factor Tbr2, and in mouse typically undergo a terminal symmetric division, generating two neurons (Englund et al, 2005; Haubensak et al, 2004; Miyata et al, 2004; Noctor et al, 2004). A subpopulation of bIPs with self‐renewing capacity has been reported in the rodent (Noctor et al, 2004) and human neocortex (Hansen et al, 2010; LaMonica et al, 2013).…”

mentioning

confidence: 99%

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

García

Chang

Arai

et al. 2015

J of Comparative Neurology

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The evolutionary expansion of the neocortex primarily reflects increases in abundance and proliferative capacity of cortical progenitors and in the length of the neurogenic period during development. Cell cycle parameters of neocortical progenitors are an important determinant of cortical development. The ferret (Mustela putorius furo), a gyrencephalic mammal, has gained increasing importance as a model for studying corticogenesis. Here, we have studied the abundance, proliferation, and cell cycle parameters of different neural progenitor types, defined by their differential expression of the transcription factors Pax6 and Tbr2, in the various germinal zones of developing ferret neocortex. We focused our analyses on postnatal day 1, a late stage of cortical neurogenesis when upper‐layer neurons are produced. Based on cumulative 5‐ethynyl‐2′‐deoxyuridine (EdU) labeling as well as Ki67 and proliferating cell nuclear antigen (PCNA) immunofluorescence, we determined the duration of the various cell cycle phases of the different neocortical progenitor subpopulations. Ferret neocortical progenitors were found to exhibit longer cell cycles than those of rodents and little variation in the duration of G1 among distinct progenitor types, also in contrast to rodents. Remarkably, the main difference in cell cycle parameters among the various progenitor types was the duration of S‐phase, which became shorter as progenitors progressively changed transcription factor expression from patterns characteristic of self‐renewal to those of neuron production. Hence, S‐phase duration emerges as major target of cell cycle regulation in cortical progenitors of this gyrencephalic mammal. J. Comp. Neurol. 524:456–470, 2016. © 2015 The Authors The Journal of Comparative Neurology Published by Wiley Periodicals, Inc.

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Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases

Cited by 2,012 publications

References 48 publications

Coevolution of radial glial cells and the cerebral cortex

Coevolution of radial glial cells and the cerebral cortex

Unsupervised lineage‐based characterization of primate precursors reveals high proliferative and morphological diversity in the OSVZ

S‐phase duration is the main target of cell cycle regulation in neural progenitors of developing ferret neocortex

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