Development and Arealization of the Cerebral Cortex

Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-ce...

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Published in	Neuron (Cambridge, Mass.) Vol. 103; no. 6; pp. 980 - 1004
Main Authors	Cadwell, Cathryn R., Bhaduri, Aparna, Mostajo-Radji, Mohammed A., Keefe, Matthew G., Nowakowski, Tomasz J.
Format	Journal Article
Language	English
Published	United States Elsevier Inc 25.09.2019 Elsevier Limited
Subjects	Animals autism brain development Cerebral cortex Cerebral Cortex - embryology Cognitive ability Deep Learning Gene expression Gene Expression Regulation, Developmental Genotype & phenotype Homology human brain Humans Interneurons - cytology Interneurons - metabolism machine learning Neural Inhibition Neural networks Neurodevelopmental disorders neurogenesis Neurogenesis - genetics Neurogenesis - physiology Neurons Neurons - cytology Neurons - metabolism protocortex protomap serial homology Single-Cell Analysis Thalamus - embryology brain development cerebral cortex human brain protocortex neural networks neurogenesis machine learning autism protomap serial homology
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Abstract	Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-cell transcriptomics, provide a new perspective on area-specific molecular diversity. Here, we review the early developmental processes that underlie cortical arealization, including both cortex intrinsic and extrinsic mechanisms as embodied by the protomap and protocortex hypotheses, respectively. We propose an integrated model of serial homology whereby intrinsic genetic programs and local factors establish early transcriptomic differences between excitatory neurons destined to give rise to broad “proto-regions,” and activity-dependent mechanisms lead to progressive refinement and formation of sharp boundaries between functional areas. Finally, we explore the potential of these basic developmental processes to inform our understanding of the emergence of functional neural networks and circuit abnormalities in neurodevelopmental disorders. Cadwell et al. review the early developmental processes that underlie arealization of the cerebral cortex, with a focus on recent single-cell transcriptomic studies, the interplay of intrinsic genetic programs and extrinsic signals, and implications for developmental of functional circuits.
AbstractList	Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-cell transcriptomics, provide a new perspective on area-specific molecular diversity. Here, we review the early developmental processes that underlie cortical arealization, including both cortex intrinsic and extrinsic mechanisms as embodied by the protomap and protocortex hypotheses, respectively. We propose an integrated model of serial homology whereby intrinsic genetic programs and local factors establish early transcriptomic differences between excitatory neurons destined to give rise to broad “proto-regions,” and activity-dependent mechanisms lead to progressive refinement and formation of sharp boundaries between functional areas. Finally, we explore the potential of these basic developmental processes to inform our understanding of the emergence of functional neural networks and circuit abnormalities in neurodevelopmental disorders. Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-cell transcriptomics, provide a new perspective on area-specific molecular diversity. Here we review the early developmental processes that underlie cortical arealization, including both cortex intrinsic and extrinsic mechanisms as embodied by the protomap and protocortex hypotheses, respectively. We propose an integrated model of serial homology whereby intrinsic genetic programs and local factors establish early transcriptomic differences between excitatory neurons destined to give rise to broad “proto-regions”, while activity-dependent mechanisms lead to progressive refinement and formation of sharp boundaries between functional areas. Finally, we explore the potential of these basic developmental processes to inform our understanding of the emergence of functional neural networks and circuit abnormalities in neurodevelopmental disorders. Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-cell transcriptomics, provide a new perspective on area-specific molecular diversity. Here, we review the early developmental processes that underlie cortical arealization, including both cortex intrinsic and extrinsic mechanisms as embodied by the protomap and protocortex hypotheses, respectively. We propose an integrated model of serial homology whereby intrinsic genetic programs and local factors establish early transcriptomic differences between excitatory neurons destined to give rise to broad “proto-regions,” and activity-dependent mechanisms lead to progressive refinement and formation of sharp boundaries between functional areas. Finally, we explore the potential of these basic developmental processes to inform our understanding of the emergence of functional neural networks and circuit abnormalities in neurodevelopmental disorders. Cadwell et al. review the early developmental processes that underlie arealization of the cerebral cortex, with a focus on recent single-cell transcriptomic studies, the interplay of intrinsic genetic programs and extrinsic signals, and implications for developmental of functional circuits. Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-cell transcriptomics, provide a new perspective on area-specific molecular diversity. Here, we review the early developmental processes that underlie cortical arealization, including both cortex intrinsic and extrinsic mechanisms as embodied by the protomap and protocortex hypotheses, respectively. We propose an integrated model of serial homology whereby intrinsic genetic programs and local factors establish early transcriptomic differences between excitatory neurons destined to give rise to broad "proto-regions," and activity-dependent mechanisms lead to progressive refinement and formation of sharp boundaries between functional areas. Finally, we explore the potential of these basic developmental processes to inform our understanding of the emergence of functional neural networks and circuit abnormalities in neurodevelopmental disorders.Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops from an initially uniform neuroepithelium has been the subject of decades of seminal research, and emerging technologies, including single-cell transcriptomics, provide a new perspective on area-specific molecular diversity. Here, we review the early developmental processes that underlie cortical arealization, including both cortex intrinsic and extrinsic mechanisms as embodied by the protomap and protocortex hypotheses, respectively. We propose an integrated model of serial homology whereby intrinsic genetic programs and local factors establish early transcriptomic differences between excitatory neurons destined to give rise to broad "proto-regions," and activity-dependent mechanisms lead to progressive refinement and formation of sharp boundaries between functional areas. Finally, we explore the potential of these basic developmental processes to inform our understanding of the emergence of functional neural networks and circuit abnormalities in neurodevelopmental disorders.
Author	Keefe, Matthew G. Mostajo-Radji, Mohammed A. Nowakowski, Tomasz J. Bhaduri, Aparna Cadwell, Cathryn R.
AuthorAffiliation	6 Department of Psychiatry, University of California, San Francisco, San Francisco, CA, 94143, USA 3 The Eli and Edythe Broad Center for Regeneration Medicine and Stem Cell Research at the University of California, San Francisco, San Francisco, CA, 94143, USA 4 Developmental and Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA, 94143, USA 1 Department of Anatomic Pathology, University of California, San Francisco, San Francisco, CA, 94143, USA 5 Department of Anatomy, University of California, San Francisco, San Francisco, CA, 94143, USA 2 Department of Neurology, University of California, San Francisco, San Francisco, CA, 94122, USA
AuthorAffiliation_xml	– name: 2 Department of Neurology, University of California, San Francisco, San Francisco, CA, 94122, USA – name: 3 The Eli and Edythe Broad Center for Regeneration Medicine and Stem Cell Research at the University of California, San Francisco, San Francisco, CA, 94143, USA – name: 4 Developmental and Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA, 94143, USA – name: 5 Department of Anatomy, University of California, San Francisco, San Francisco, CA, 94143, USA – name: 1 Department of Anatomic Pathology, University of California, San Francisco, San Francisco, CA, 94143, USA – name: 6 Department of Psychiatry, University of California, San Francisco, San Francisco, CA, 94143, USA
Author_xml	– sequence: 1 givenname: Cathryn R. surname: Cadwell fullname: Cadwell, Cathryn R. organization: Department of Anatomic Pathology, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 2 givenname: Aparna surname: Bhaduri fullname: Bhaduri, Aparna organization: Department of Neurology, University of California, San Francisco, San Francisco, CA 94122, USA – sequence: 3 givenname: Mohammed A. surname: Mostajo-Radji fullname: Mostajo-Radji, Mohammed A. organization: Department of Neurology, University of California, San Francisco, San Francisco, CA 94122, USA – sequence: 4 givenname: Matthew G. surname: Keefe fullname: Keefe, Matthew G. organization: Developmental and Stem Cell Biology Graduate Program, University of California, San Francisco, San Francisco, CA 94143, USA – sequence: 5 givenname: Tomasz J. surname: Nowakowski fullname: Nowakowski, Tomasz J. email: tomasz.nowakowski@ucsf.edu organization: The Eli and Edythe Broad Center for Regeneration Medicine and Stem Cell Research at the University of California, San Francisco, San Francisco, CA 94143, USA
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31557462$$D View this record in MEDLINE/PubMed
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Snippet	Adult cortical areas consist of specialized cell types and circuits that support unique higher-order cognitive functions. How this regional diversity develops...
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SubjectTerms	Animals autism brain development Cerebral cortex Cerebral Cortex - embryology Cognitive ability Deep Learning Gene expression Gene Expression Regulation, Developmental Genotype & phenotype Homology human brain Humans Interneurons - cytology Interneurons - metabolism machine learning Neural Inhibition Neural networks Neurodevelopmental disorders neurogenesis Neurogenesis - genetics Neurogenesis - physiology Neurons Neurons - cytology Neurons - metabolism protocortex protomap serial homology Single-Cell Analysis Thalamus - embryology
Title	Development and Arealization of the Cerebral Cortex
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