Evolution and Ontogenetic Development of Cortical Structures

The cerebral cortex controls our unique higher cognitive abilities. Modifi cations to gene expression, progenitor behavior, cell lineage, and neural circuitry have accompanied evolution of the cerebral cortex. This chapter considers the progress made over the past thirty years in defi ning potential mechanisms that contribute to cortical development and evolution. It discusses the value of model systems for understanding elaboration of cortical organization in humans, with an emphasis on recent technical and conceptual advances. It then examines our current understanding of the molecular and cellular basis for cortical development and evolution; discusses how neuronal fates are specifi ed and organized in lamina, columns, and areas; and revisits the radial unit and protomap hypotheses. Finally, it considers our current understanding of the development, stability, and plasticity of cortical circuitry. Throughout, it highlights the profound impact that new technological advances have made at the molecular and cellular level, and how this has changed our understanding of cortical development and evolution. The authors conclude by identifying critical and tractable research directions to address gaps in our understanding of cortical development and evolution. Group photos (top left to bottom right) Debra Silver, Pasko Rakic, Christopher Walsh, Takao Hensch, Elizabeth Grove, Michael Stryker, Tarik Haydar, John Rubenstein, Zoltán Molnár, Mriganka Sur, Nenad Sestan, Maria Antonietta Tosches, Wieland Huttner, Debra Silver, Mriganka Sur, Maria Antonietta Tosches, John Rubenstein, Pasko Rakic, Zoltán Molnár, Nenad Sestan, Michael Stryker From “The Neocortex,” edited by W. Singer, T. J. Sejnowski and P. Rakic. Strüngmann Forum Reports, vol. 27, J. R. Lupp, series editor. Cambridge, MA: MIT Press. ISBN 978-0-262-04324-3 62 D. L. Silver et al.

[1]  E. Grove,et al.  Morphogens, patterning centers, and their mechanisms of action , 2020, Patterning and Cell Type Specification in the Developing CNS and PNS.

[2]  W. Huttner,et al.  Brain organoids as models to study human neocortex development and evolution. , 2018, Current opinion in cell biology.

[3]  E. Quinlan,et al.  Critical periods in amblyopia , 2018, Visual Neuroscience.

[4]  D. Geschwind,et al.  The Dynamic Landscape of Open Chromatin during Human Cortical Neurogenesis , 2018, Cell.

[5]  Z. Molnár,et al.  Absence of Tangentially Migrating Glutamatergic Neurons in the Developing Avian Brain , 2018, Cell reports.

[6]  G. Clowry,et al.  Charting the protomap of the human telencephalon. , 2017, Seminars in cell & developmental biology.

[7]  M. Hiller,et al.  Evolution and cell-type specificity of human-specific genes preferentially expressed in progenitors of fetal neocortex , 2017, bioRxiv.

[8]  S. Hippenmeyer,et al.  Cell Polarity in Cerebral Cortex Development—Cellular Architecture Shaped by Biochemical Networks , 2017, Front. Cell. Neurosci..

[9]  Rüdiger Klein,et al.  Regulation of Cerebral Cortex Folding by Controlling Neuronal Migration via FLRT Adhesion Molecules , 2017, Cell.

[10]  C. Dehay,et al.  Division modes and physical asymmetry in cerebral cortex progenitors , 2017, Current Opinion in Neurobiology.

[11]  I. Kostović,et al.  Secondary expansion of the transient subplate zone in the developing cerebrum of human and nonhuman primates , 2016, Proceedings of the National Academy of Sciences.

[12]  Madeline A. Lancaster,et al.  Human cerebral organoids recapitulate gene expression programs of fetal neocortex development , 2015, Proceedings of the National Academy of Sciences.

[13]  A. Kriegstein,et al.  Wide Dispersion and Diversity of Clonally Related Inhibitory Interneurons , 2015, Neuron.

[14]  Z. Molnár,et al.  Subset of early radial glial progenitors that contribute to the development of callosal neurons is absent from avian brain , 2015, Proceedings of the National Academy of Sciences.

[15]  Janet Kelso,et al.  Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion , 2015, Science.

[16]  R. Gordân,et al.  Human-Chimpanzee Differences in a FZD8 Enhancer Alter Cell-Cycle Dynamics in the Developing Neocortex , 2015, Current Biology.

[17]  Sarah M. N. Woolley,et al.  Coding principles of the canonical cortical microcircuit in the avian brain , 2015, Proceedings of the National Academy of Sciences.

[18]  L. Luo,et al.  Deterministic Progenitor Behavior and Unitary Production of Neurons in the Neocortex , 2014, Cell.

[19]  Yoav Gilad,et al.  A panel of induced pluripotent stem cells from chimpanzees: a resource for comparative functional genomics , 2014, bioRxiv.

[20]  Magdalena Götz,et al.  Role of radial glial cells in cerebral cortex folding , 2014, Current Opinion in Neurobiology.

[21]  Steven A. Chance,et al.  The cortical microstructural basis of lateralized cognition: a review , 2014, Front. Psychol..

[22]  E. Grove,et al.  The cortical hem regulates the size and patterning of neocortex , 2014, Development.

[23]  Wieland B Huttner,et al.  Neural progenitors, neurogenesis and the evolution of the neocortex , 2014, Development.

[24]  Katherine S. Pollard,et al.  Many human accelerated regions are developmental enhancers , 2013, Philosophical Transactions of the Royal Society B: Biological Sciences.

[25]  D. Geschwind,et al.  Cortical Evolution: Judge the Brain by Its Cover , 2013, Neuron.

[26]  J. D. Macklis,et al.  Molecular logic of neocortical projection neuron specification, development and diversity , 2013, Nature Reviews Neuroscience.

[27]  D. O'Leary,et al.  Geniculocortical Input Drives Genetic Distinctions Between Primary and Higher-Order Visual Areas , 2013, Science.

[28]  Le Cong,et al.  Multiplex Genome Engineering Using CRISPR/Cas Systems , 2013, Science.

[29]  A. Espinosa,et al.  Fate-Restricted Neural Progenitors in the Mammalian Cerebral Cortex , 2012, Science.

[30]  M. Stryker,et al.  Development and Plasticity of the Primary Visual Cortex , 2012, Neuron.

[31]  Martin Kircher,et al.  Transcriptomes of germinal zones of human and mouse fetal neocortex suggest a role of extracellular matrix in progenitor self-renewal , 2012, Proceedings of the National Academy of Sciences.

[32]  Isabel Reillo,et al.  Emerging roles of neural stem cells in cerebral cortex development and evolution , 2012, Developmental neurobiology.

[33]  Z. Molnár,et al.  Compartmentalization of cerebral cortical germinal zones in a lissencephalic primate and gyrencephalic rodent. , 2012, Cerebral cortex.

[34]  Tarik F Haydar,et al.  The (not necessarily) convoluted role of basal radial glia in cortical neurogenesis. , 2012, Cerebral cortex.

[35]  S. Anderson,et al.  Clonal Production and Organization of Inhibitory Interneurons in the Neocortex , 2011, Science.

[36]  W. Huttner,et al.  Cortical progenitor expansion, self-renewal and neurogenesis—a polarized perspective , 2011, Current Opinion in Neurobiology.

[37]  G. Elston,et al.  Pyramidal Cells in Prefrontal Cortex of Primates: Marked Differences in Neuronal Structure Among Species , 2010, Frontiers in Neuroanatomy.

[38]  Felipe Oroquieta,et al.  The evolution of the brain, the human nature of cortical circuits and intellectual creativity , 2011 .

[39]  J. Kaas,et al.  Connectivity-driven white matter scaling and folding in primate cerebral cortex , 2010, Proceedings of the National Academy of Sciences.

[40]  Pasko Rakic,et al.  Renewed focus on the developing human neocortex , 2010, Journal of anatomy.

[41]  O. Marín,et al.  Generation of interneuron diversity in the mouse cerebral cortex , 2010, The European journal of neuroscience.

[42]  J. Fish,et al.  OSVZ progenitors of human and ferret neocortex are epithelial-like and expand by integrin signaling , 2010, Nature Neuroscience.

[43]  G. Wray,et al.  Contrasts between adaptive coding and noncoding changes during human evolution , 2010, Proceedings of the National Academy of Sciences.

[44]  A. Kriegstein,et al.  Neurogenic radial glia in the outer subventricular zone of human neocortex , 2010, Nature.

[45]  Y. Kawasawa,et al.  Selective depletion of molecularly defined cortical interneurons in human holoprosencephaly with severe striatal hypoplasia. , 2009, Cerebral cortex.

[46]  Yoshiki Sasai,et al.  Self-organized formation of polarized cortical tissues from ESCs and its active manipulation by extrinsic signals. , 2008, Cell stem cell.

[47]  J. Rubenstein,et al.  Frontal cortex subdivision patterning is coordinately regulated by Fgf8, Fgf17, and Emx2 , 2008, The Journal of comparative neurology.

[48]  Colin Blakemore,et al.  Development of the human cerebral cortex: Boulder Committee revisited , 2008, Nature Reviews Neuroscience.

[49]  Henry Kennedy,et al.  Cell-cycle control and cortical development , 2007, Nature Reviews Neuroscience.

[50]  J. Kaas,et al.  Cellular scaling rules for primate brains , 2007, Proceedings of the National Academy of Sciences.

[51]  M. Bear,et al.  Instructive Effect of Visual Experience in Mouse Visual Cortex , 2006, Neuron.

[52]  C. Blakemore,et al.  The first neurons of the human cerebral cortex , 2006, Nature Neuroscience.

[53]  P. Rakic,et al.  Molecular and Morphological Heterogeneity of Neural Precursors in the Mouse Neocortical Proliferative Zones , 2006, The Journal of Neuroscience.

[54]  R. Hevner The cerebral cortex malformation in thanatophoric dysplasia: neuropathology and pathogenesis , 2005, Acta Neuropathologica.

[55]  Tobias M. Fischer,et al.  Short- and Long-Range Attraction of Cortical GABAergic Interneurons by Neuregulin-1 , 2004, Neuron.

[56]  J. Rubenstein,et al.  Intermediate targets in formation of topographic projections: inputs from the thalamocortical system , 2004, Trends in Neurosciences.

[57]  Tadashi Hamasaki,et al.  EMX2 Regulates Sizes and Positioning of the Primary Sensory and Motor Areas in Neocortex by Direct Specification of Cortical Progenitors , 2004, Neuron.

[58]  L. Medina,et al.  Expression of the genes Emx1, Tbr1, and Eomes (Tbr2) in the telencephalon of Xenopus laevis confirms the existence of a ventral pallial division in all tetrapods , 2004, The Journal of comparative neurology.

[59]  R. Nieuwenhuys The neocortex , 1994, Anatomy and Embryology.

[60]  Otto D. Creutzfeldt,et al.  Generality of the functional structure of the neocortex , 1977, Naturwissenschaften.

[61]  E. Grove,et al.  Emx2 patterns the neocortex by regulating FGF positional signaling , 2003, Nature Neuroscience.

[62]  J. Rubenstein,et al.  Molecular regionalization of the neocortex is disrupted in Fgf8 hypomorphic mutants , 2003, Development.

[63]  Anjen Chenn,et al.  Regulation of Cerebral Cortical Size by Control of Cell Cycle Exit in Neural Precursors , 2002, Science.

[64]  A. Butler,et al.  Development and evolution of the collopallium in amniotes: a new hypothesis of field homology , 2002, Brain Research Bulletin.

[65]  Y. Ohkubo,et al.  Coordinate expression of Fgf8, Otx2, Bmp4, and Shh in the rostral prosencephalon during development of the telencephalic and optic vesicles , 2001, Neuroscience.

[66]  I. Cobos,et al.  The avian telencephalic subpallium originates inhibitory neurons that invade tangentially the pallium (dorsal ventricular ridge and cortical areas). , 2001, Developmental biology.

[67]  H. Kennedy,et al.  Cell-Cycle Kinetics of Neocortical Precursors Are Influenced by Embryonic Thalamic Axons , 2001, The Journal of Neuroscience.

[68]  P S Goldman-Rakic,et al.  Synaptogenesis in the prefrontal cortex of rhesus monkeys. , 1994, Cerebral cortex.

[69]  A. Kriegstein,et al.  Morphological differentiation of distinct neuronal classes in embryonic turtle cerebral cortex , 1991, The Journal of comparative neurology.

[70]  P. Rakić,et al.  Synaptogenesis in visual cortex of normal and preterm monkeys: evidence for intrinsic regulation of synaptic overproduction. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[71]  P. Goldman-Rakic Motor control function of the prefrontal cortex. , 1987, Ciba Foundation symposium.

[72]  L. Lapham,et al.  Radial glia in the human fetal cerebrum: A combined golgi, immunofluorescent and electron microscopic study , 1978, Brain Research.