Abstract
The dramatic evolutionary expansion of the cerebral cortex of Homo sapiens underlies our unique higher cortical functions, and therefore bears on the ultimate issue of what makes us human. Recent insights into developmental events during early proliferative stages of cortical development indicate how neural stem and progenitor cells might interact to produce cortical expansion during development, and could shed light on evolutionary changes in cortical structure.
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References
Lindblad-Toh, K. Genome sequencing: three's company. Nature 428, 475–476 (2004).
Ji, Q. et al. The earliest known eutherian mammal. Nature 416, 816–822 (2002).
Lois, C. & Alvarez-Buylla, A. Proliferating subventricular zone cells in the adult mammalian forebrain can differentiate into neurons and glia. Proc. Natl Acad. Sci. USA 90, 2074–2077 (1993).
Gadisseux, J. F. & Evrard, P. Glial–neuronal relationship in the developing central nervous system. A histochemical–electron microscope study of radial glial cell particulate glycogen in normal and reeler mice and the human fetus. Dev. Neurosci. 7, 12–32 (1985).
Bruckner, G. & Biesold, D. Histochemistry of glycogen deposition in perinatal rat brain: importance of radial glial cells. J. Neurocytol. 10, 749–757 (1981).
Choi, B. H. & Lapham, L. W. Radial glia in the human fetal cerebrum: a combined Golgi, immunofluorescent and electron microscopic study. Brain Res. 148, 295–311 (1978).
Kriegstein, A. R. & Gotz, M. Radial glia diversity: a matter of cell fate. Glia 43, 37–43 (2003).
Noctor, S. C., Flint, A. C., Weissman, T. A., Dammerman, R. S. & Kriegstein, A. R. Neurons derived from radial glial cells establish radial units in neocortex. Nature 409, 714–720 (2001).
Misson, J. P., Edwards, M. A., Yamamoto, M. & Caviness, V. S. Jr. Mitotic cycling of radial glial cells of the fetal murine cerebral wall: a combined autoradiographic and immunohistochemical study. Brain Res. 466, 183–190 (1988).
Levitt, P., Cooper, M. L. & Rakic, P. Coexistence of neuronal and glial precursor cells in the cerebral ventricular zone of the fetal monkey: an ultrastructural immunoperoxidase analysis. J. Neurosci. 1, 27–39 (1981).
Schmechel, D. E. & Rakic, P. Arrested proliferation of radial glial cells during midgestation in rhesus monkey. Nature 277, 303–305 (1979).
Rakic, P. Neuronal migration and contact guidance in the primate telencephalon. Postgrad. Med. J. 1, 25–40 (1978).
Miyata, T., Kawaguchi, A., Okano, H. & Ogawa, M. Asymmetric inheritance of radial glial fibers by cortical neurons. Neuron 31, 727–741 (2001).
Malatesta, P., Hartfuss, E. & Gotz, M. Isolation of radial glial cells by fluorescent-activated cell sorting reveals a neuronal lineage. Development 127, 5253–5263 (2000).
Anthony, T. E. et al. Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41, 881–890 (2004).
Tamamaki, N. et al. Radial glia is a progenitor of neocortical neurons in the developing cerebral cortex. Neurosci. Res. 41, 51–60 (2001).
Noctor, S. C., Martinez-Cerdeno, V., Ivic, L. & Kriegstein, A. R. Cortical neurons arise in symmetric and asymmetric division zones and migrate through specific phases. Nature Neurosci. 7, 136–144 (2004).
Kornack, D. R. & Rakic, P. Radial and horizontal deployment of clonally related cells in the primate neocortex: relationship to distinct mitotic lineages. Neuron 15, 311–321 (1995).
Rakic, P. Radial unit hypothesis of neocortical expansion. Novartis Found. Symp. 228, 30–42; discussion 42–52 (2000).
Chenn, A. & Walsh, C. A. Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297, 365–369 (2002).
Ponting, C. & Jackson, A. P. Evolution of primary microcephaly genes and the enlargement of primate brains. Curr. Opin. Genet. Dev. 15, 241–248 (2005).
Gilbert, S. L., Dobyns, W. B. & Lahn, B. T. Genetic links between brain development and brain evolution. Nature Rev. Genet. 6, 581–590 (2005).
Woods, C. G., Bond, J. & Enard, W. Autosomal recessive primary microcephaly (MCPH): a review of clinical, molecular, and evolutionary findings. Am. J. Hum. Genet. 76, 717–728 (2005).
Bond, J. et al. ASPM is a major determinant of cerebral cortical size. Nature Genet. 32, 316–320 (2002).
Evans, P. D. et al. Adaptive evolution of ASPM, a major determinant of cerebral cortical size in humans. Hum. Mol. Genet. 13, 489–494 (2004).
Evans, P. D. et al. Microcephalin, a gene regulating brain size, continues to evolve adaptively in humans. Science 309, 1717–1720 (2005).
Kouprina, N. et al. Accelerated evolution of the ASPM gene controlling brain size begins prior to human brain expansion. PLoS Biol. 2, E126 (2004).
Zhang, J. Evolution of the human ASPM gene, a major determinant of brain size. Genetics 165, 2063–2070 (2003).
Mekel-Bobrov, N. et al. Ongoing adaptive evolution of ASPM, a brain size determinant in Homo sapiens. Science 309, 1720–1722 (2005).
Ripoll, P., Pimpinelli, S., Valdivia, M. M. & Avila, J. A cell division mutant of Drosophila with a functionally abnormal spindle. Cell 41, 907–912 (1985).
do Carmo Avides, M. & Glover, D. M. Abnormal spindle protein, Asp, and the integrity of mitotic centrosomal microtubule organizing centers. Science 283, 1733–1735 (1999).
Wakefield, J. G., Bonaccorsi, S. & Gatti, M. The Drosophila protein asp is involved in microtubule organization during spindle formation and cytokinesis. J. Cell. Biol. 153, 637–648 (2001).
Ponting, C. P. A novel domain suggests a ciliary function for ASPM, a brain size determining gene. Bioinformatics 22, 1031–1035 (2006).
Groszer, M. et al. Negative regulation of neural stem/progenitor cell proliferation by the Pten tumor suppressor gene in vivo. Science 294, 2186–2189 (2001).
Groszer, M. et al. PTEN negatively regulates neural stem cell self-renewal by modulating G0–G1 cell cycle entry. Proc. Natl Acad. Sci. USA 103, 111–116 (2006).
Nieuwenhuys, R., ten Donkelaar, H. J. & Nicholson, C. The Central Nervous System of Vertebrates Vol. 3, 2219 (Springer, Berlin, 1998).
Striedter, G. F. Principles of Brain Evolution 436 (Sinauer Associates, Sunderland, 2005).
Rakic, P. A small step for the cell, a giant leap for mankind: a hypothesis of neocortical expansion during evolution. Trends Neurosci. 18, 383–388 (1995).
Rakic, P. Developmental and evolutionary adaptations of cortical radial glia. Cereb. Cortex 13, 541–549 (2003).
Roth, K. A. et al. Epistatic and independent functions of caspase-3 and Bcl-XL in developmental programmed cell death. Proc. Natl Acad. Sci. USA 97, 466–471 (2000).
Smart, I. H. & McSherry, G. M. Growth patterns in the lateral wall of the mouse telencephalon. II. Histological changes during and subsequent to the period of isocortical neuron production. J. Anat. 134, 415–442 (1982).
Megason, S. G. & McMahon, A. P. A mitogen gradient of dorsal midline Wnts organizes growth in the CNS. Development 129, 2087–2098 (2002).
Parr, B. A., Shea, M. J., Vassileva, G. & McMahon, A. P. Mouse Wnt genes exhibit discrete domains of expression in the early embryonic CNS and limb buds. Development 119, 247–261 (1993).
Tarabykin, V., Stoykova, A., Usman, N. & Gruss, P. Cortical upper layer neurons derive from the subventricular zone as indicated by Svet1 gene expression. Development 128, 1983–1993 (2001).
Zimmer, C., Tiveron, M. C., Bodmer, R. & Cremer, H. Dynamics of Cux2 expression suggests that an early pool of SVZ precursors is fated to become upper cortical layer neurons. Cereb. Cortex 14, 1408–1420 (2004).
Englund, C. et al. Pax6, Tbr2, and Tbr1 are expressed sequentially by radial glia, intermediate progenitor cells, and postmitotic neurons in developing neocortex. J. Neurosci. 25, 247–251 (2005).
Anderson, S. A. et al. Mutations of the homeobox genes Dlx-1 and Dlx-2 disrupt the striatal subventricular zone and differentiation of late born striatal neurons. Neuron 19, 27–37 (1997).
Krubitzer, L. & Kahn, D. M. Nature versus nurture revisited: an old idea with a new twist. Prog. Neurobiol. 70, 33–52 (2003).
Britanova, O. et al. A novel mode of tangential migration of cortical projection neurons. Dev. Biol. 30 Jun 2006 (doi:10.1016/j.ydbio.2006.06.040).
Reid, C. B., Liang, I. & Walsh, C. Systematic widespread clonal organization in cerebral cortex. Neuron 15, 299–310 (1995).
Walsh, C. & Cepko, C. L. Widespread dispersion of neuronal clones across functional regions of the cerebral cortex. Science 255, 434–440 (1992).
Walsh, C. & Cepko, C. L. Clonally related cortical cells show several migration patterns. Science 241, 1342–1345 (1988).
Haubensak, W., Attardo, A., Denk, W. & Huttner, W. B. Neurons arise in the basal neuroepithelium of the early mammalian telencephalon: a major site of neurogenesis. Proc. Natl Acad. Sci. USA 101, 3196–3201 (2004).
Iacopetti, P. et al. Expression of the antiproliferative gene TIS21 at the onset of neurogenesis identifies single neuroepithelial cells that switch from proliferative to neuron-generating division. Proc. Natl Acad. Sci. USA 96, 4639–4644 (1999).
Martinez-Cerdeno, V., Noctor, S. C. & Kriegstein, A. R. The role of the intermediate progenitor cells in the evolutionary expansion on the cerebral cortex. Cereb. Cortex 16, 152–161 (2006).
Smart, I. H., Dehay, C., Giroud, P., Berland, M. & Kennedy, H. Unique morphological features of the proliferative zones and postmitotic compartments of the neural epithelium giving rise to striate and extrastriate cortex in the monkey. Cereb. Cortex 12, 37–53 (2002).
Zecevic, N., Chen, Y. & Filipovic, R. Contributions of cortical subventricular zone to the development of the human cerebral cortex. J. Comp. Neurol. 491, 109–122 (2005).
Noctor, S. C., Scholnicoff, N. J. & Juliano, S. L. Histogenesis of ferret somatosensory cortex. J. Comp. Neurol. 387, 179–193 (1997).
Kornack, D. R. & Rakic, P. Changes in cell-cycle kinetics during the development and evolution of primate neocortex. Proc. Natl Acad. Sci. USA 95, 1242–1246 (1998).
Takahashi, T., Nowakowski, R. S. and Caviness, V. Jr. The cell cycle of the pseudostratified ventricular epithelium of the embryonic murine cerebral wall. J. Neurosci. 15, 6046–6057 (1995).
DeFelipe, J., Alonso-Nanclares, L. & Arellano, J. I. Microstructure of the neocortex: comparative aspects. J. Neurocytol. 31, 299–316 (2002).
Richman, D. P., Stewart, R. M., Hutchinson, J. W. & Caviness, V. S. Jr. Mechanical model of brain convolutional development. Science 189, 18–21 (1975).
Bayer, S. A. & Altman, J. The Human Brain During the Second Trimester (Taylor & Francis, Boca Raton, 2005).
Nery, S., Fishell, G. & Corbin, J. G. The caudal ganglionic eminence is a source of distinct cortical and subcortical cell populations. Nature Neurosci. 5, 1279–1287 (2002).
de Carlos, J. A., Lopez-Mascaraque, L. & Valverde, F. Dynamics of cell migration from the lateral ganglionic eminence in the rat. J. Neurosci. 16, 6146–6156 (1996).
Lavdas, A. A., Grigoriou, M., Pachnis, V. & Parnavelas, J. G. The medial ganglionic eminence gives rise to a population of early neurons in the developing cerebral cortex. J. Neurosci. 19, 7881–7888 (1999).
Anderson, S. A., Marin, O., Horn, C., Jennings, K. & Rubenstein, J. L. Distinct cortical migrations from the medial and lateral ganglionic eminences. Development 128, 353–363 (2001).
Anderson, S. A., Eisenstat, D. D., Shi, L. & Rubenstein, J. Interneuron migration from basal forebrain to neocortex: dependence on dlx genes. Science 278, 474–476 (1997).
Wichterle, H., Garcia-Verdugo, J. M., Herrera, D. G. & Alvarez-Buylla, A. Young neurons from medial ganglionic eminence disperse in adult and embryonic brain. Nature Neurosci. 2, 461–466 (1999).
Wichterle, H., Turnbull, D. H., Nery, S., Fishell, G. & Alvarez-Buylla, A. In utero fate mapping reveals distinct migratory pathways and fates of neurons born in the mammalian basal forebrain. Development 128, 3759–3771 (2001).
Sussel, L., Marin, O., Kimura, S. & Rubenstein, J. L. Loss of Nkx2.1 homeobox gene function results in a ventral to dorsal molecular respecification within the basal telencephalon: evidence for a transformation of the pallidum into the striatum. Development 126, 3359–3370 (1999).
Tamamaki, N., Fujimori, K. E. & Takauji, R. Origin and route of tangentially migrating neurons in the developing neocortical intermediate zone. J. Neurosci. 17, 8313–8323 (1997).
Halliday, A. L. & Cepko, C. L. Generation and migration of cells in the developing striatum. Neuron 9, 15–26 (1992).
Walsh, C. & Cepko, C. L. Clonal dispersion in proliferative layers of developing cerebral cortex. Nature 362, 632–635 (1993).
Reid, C. B. & Walsh, C. A. Evidence of common progenitors and patterns of dispersion in rat striatum and cerebral cortex. J. Neurosci. 22, 4002–4014 (2002).
Letinic, K., Zoncu, R. & Rakic, P. Origin of GABAergic neurons in the human neocortex. Nature 417, 645–649 (2002).
Brody, T. & Odenwald, W. F. Programmed transformations in neuroblast gene expression during Drosophila CNS lineage development. Dev. Biol. 226, 34–44 (2000).
Kambadur, R. et al. Regulation of POU genes by castor and hunchback establishes layered compartments in the Drosophila CNS. Genes. Dev. 12, 246–260 (1998).
Isshiki, T., Pearson, B., Holbrook, S. & Doe, C. Q. Drosophila neuroblasts sequentially express transcription factors which specify the temporal identity of their neuronal progeny. Cell 106, 511–521 (2001).
Cui, X. & Doe, C. Q. ming is expressed in neuroblast sublineages and regulates gene expression in the Drosophila central nervous system. Development 116, 943–952 (1992).
Mellerick, D. M., Kassis, J. A., Zhang, S. D. & Odenwald, W. F. castor encodes a novel zinc finger protein required for the development of a subset of CNS neurons in Drosophila. Neuron 9, 789–803 (1992).
Novotny, T., Eiselt, R. & Urban, J. Hunchback is required for the specification of the early sublineage of neuroblast 7–3 in the Drosophila central nervous system. Development 129, 1027–1036 (2002).
Zhong, W. Diversifying neural cells through order of birth and asymmetry of division. Neuron 37, 11–14 (2003).
Frantz, G. D., Weimann, J. M., Levin, M. E. & McConnell, S. K. Otx1 and Otx2 define layers and regions in developing cerebral cortex and cerebellum. J. Neurosci. 14, 5725–5740 (1994).
Molyneaux, B. J., Arlotta, P., Hirata, T., Hibi, M. & Macklis, J. D. Fezl is required for the birth and specification of corticospinal motor neurons. Neuron 47, 817–831 (2005).
Nieto, M. et al. Expression of Cux-1 and Cux-2 in the subventricular zone and upper layers II–IV of the cerebral cortex. J. Comp. Neurol. 479, 168–180 (2004).
Hanashima, C., Li, S. C., Shen, L., Lai, E. & Fishell, G. Foxg1 suppresses early cortical cell fate. Science 303, 56–59 (2004).
Shen, Q. et al. The timing of cortical neurogenesis is encoded within lineages of individual progenitor cells. Nature Neurosci. 9, 743–751 (2006).
Lavdas, A. A., Mione, M. C. & Parnavelas, J. G. Neuronal clones in the cerebral cortex show morphological and neurotransmitter heterogeneity during development. Cereb. Cortex 6, 490–497 (1996).
Williams, B. P., Read, J. & Price, J. The generation of neurons and oligodendrocytes from a common precursor cell. Neuron 7, 685–693 (1991).
Luskin, M. B., Parnavelas, J. G. & Barfield, J. A. Neurons, astrocytes, and oligodendrocytes of the rat cerebral cortex originate from separate progenitor cells: an ultrastructural analysis of clonally related cells. J. Neurosci. 13, 1730–1750 (1993).
Walsh, C. & Cepko, C. L. Cell lineage and cell migration in the developing cerebral cortex. Experientia 46, 940–947 (1990).
Temple, S. Division and differentiation of isolated CNS blast cells in microculture. Nature 340, 471–473 (1989).
Bayer, S. A. & Altman, J. Neocortical Development (Raven, New York, 1991).
Acknowledgements
The authors thank A. Alvarez-Bullya and J. L. R. Rubenstein for helpful comments on the manuscript. This work has been supported by grants from the National Institutes of Health to A.R.K., and from the the Ministerio de Educación, Cultura y Deporte, Spain, to V.M.C.
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Glossary
- Asymmetric division
-
A cell division that produces two cells with different fate potential.
- Cladogram
-
A tree-like diagram depicting evolutionary relationships between different species. In these diagrams, branches that share the same node are closely related.
- Cortical plate
-
The cellular layer of the developing cerebral cortex that will become layers II–VI of the adult cortex.
- Gyrencephalic cortex
-
Adult six-layered neocortex that develops a folded surface associated with gyri and sulci.
- Lissencephalic cortex
-
Adult six-layered neocortex without folds created by gyri and sulci, which therefore has a smooth surface.
- Preplate
-
The first cortical layer to develop, containing the earliest-generated cortical neurons. This layer is split by migrating cortical plate neurons that settle here, dividing it into a superficial layer that becomes the marginal zone and a deep layer that becomes the subplate.
- Stem mammal
-
Putative vertebrate species from which all mammals evolved.
- Symmetric division
-
A cell division that produces two cells with identical fate potential.
- Telencephalon
-
The anterior portion of the forebrain, which includes the cerebral hemispheres, basal ganglia and the olfactory bulbs.
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Kriegstein, A., Noctor, S. & Martínez-Cerdeño, V. Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7, 883–890 (2006). https://doi.org/10.1038/nrn2008
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DOI: https://doi.org/10.1038/nrn2008
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