The development of local circuits in the neocortex: recent lessons from the mouse visual cortex

Precise synaptic connections among neurons in the neocortex generate the circuits that underlie a broad repertoire of cortical functions including perception, learning and memory, and complex problem solving. The specific patterns and properties of these synaptic connections are fundamental to the computations cortical neurons perform. How such specificity arises in cortical circuits has remained elusive. Here, we first consider the cell-type, subcellular and synaptic specificity required for generating mature patterns of cortical connectivity and responses. Next, we focus on recent progress in understanding how the synaptic connections among excitatory cortical projection neurons are established during development using the primary visual cortex of the mouse as a model.

[1]  J. Gibson,et al.  Postsynaptic FMRP Promotes the Pruning of Cell-to-Cell Connections among Pyramidal Neurons in the L5A Neocortical Network , 2014, The Journal of Neuroscience.

[2]  D. Feldmeyer,et al.  Dendritic Target Region-Specific Formation of Synapses Between Excitatory Layer 4 Neurons and Layer 6 Pyramidal Cells. , 2016, Cerebral cortex.

[3]  Xiaolong Jiang,et al.  The organization of two new cortical interneuronal circuits , 2013, Nature Neuroscience.

[4]  Jia-Jia Liu,et al.  A Critical Role of Presynaptic Cadherin/Catenin/p140Cap Complexes in Stabilizing Spines and Functional Synapses in the Neocortex , 2017, Neuron.

[5]  Sandra J. Kuhlman,et al.  Fast-spiking interneurons have an initial orientation bias that is lost with vision , 2011, Nature Neuroscience.

[6]  Christian Lohmann,et al.  Spontaneous Activity Drives Local Synaptic Plasticity In Vivo , 2015, Neuron.

[7]  David Fitzpatrick,et al.  Local Order within Global Disorder: Synaptic Architecture of Visual Space , 2017, Neuron.

[8]  Sonja B. Hofer,et al.  Synaptic organization of visual space in primary visual cortex , 2017, Nature.

[9]  Justus M. Kebschull,et al.  The logic of single-cell projections from visual cortex , 2018, Nature.

[10]  B. Cubelos,et al.  Cux1 and Cux2 Regulate Dendritic Branching, Spine Morphology, and Synapses of the Upper Layer Neurons of the Cortex , 2010, Neuron.

[11]  R. Reid,et al.  Homeostatic Regulation of Eye-Specific Responses in Visual Cortex during Ocular Dominance Plasticity , 2007, Neuron.

[12]  P. Arlotta,et al.  Neuronal subtype specification in the cerebral cortex , 2007, Nature Reviews Neuroscience.

[13]  Quanxin Wang,et al.  Modularity in the Organization of Mouse Primary Visual Cortex , 2015, Neuron.

[14]  R. Huganir,et al.  Secreted Semaphorins Control Spine Distribution and Morphogenesis in the Postnatal CNS , 2009, Nature.

[15]  S. Shi,et al.  Preferential electrical coupling regulates neocortical lineage-dependent microcircuit assembly , 2012, Nature.

[16]  Kenichi Ohki,et al.  Neuronal activity is not required for the initial formation and maturation of visual selectivity , 2015, Nature Neuroscience.

[17]  C. Clopath,et al.  The emergence of functional microcircuits in visual cortex , 2013, Nature.

[18]  S. Hestrin,et al.  Intracortical circuits of pyramidal neurons reflect their long-range axonal targets , 2009, Nature.

[19]  Jianhua Cang,et al.  Critical Period Plasticity Matches Binocular Orientation Preference in the Visual Cortex , 2010, Neuron.

[20]  Nathalie L Rochefort,et al.  Sparsification of neuronal activity in the visual cortex at eye-opening , 2009, Proceedings of the National Academy of Sciences.

[21]  T. Hosoya,et al.  Periodic Organization of a Major Subtype of Pyramidal Neurons in Neocortical Layer V , 2011, The Journal of Neuroscience.

[22]  Tania A Seabrook,et al.  Architecture, Function, and Assembly of the Mouse Visual System. , 2017, Annual review of neuroscience.

[23]  D. R. Muir,et al.  Functional organization of excitatory synaptic strength in primary visual cortex , 2015, Nature.

[24]  J. Gibson,et al.  Experience-Dependent and Differential Regulation of Local and Long-Range Excitatory Neocortical Circuits by Postsynaptic Mef2c , 2017, Neuron.

[25]  P. Manis,et al.  Neural Cell Adhesion Molecule NrCAM Regulates Semaphorin 3F-Induced Dendritic Spine Remodeling , 2014, The Journal of Neuroscience.

[26]  B. Connors.  Synchrony and so much more: Diverse roles for electrical synapses in neural circuits , 2017, Developmental neurobiology.

[27]  Anatol C. Kreitzer,et al.  Sonic Hedgehog Expression in Corticofugal Projection Neurons Directs Cortical Microcircuit Formation , 2012, Neuron.

[28]  Z. Nusser.  Creating diverse synapses from the same molecules , 2018, Current Opinion in Neurobiology.

[29]  S. Anderson,et al.  The chandelier cell, form and function , 2014, Current Opinion in Neurobiology.

[30]  Jianhua Cang,et al.  Experience-dependent and independent binocular correspondence of receptive field subregions in mouse visual cortex. , 2014, Cerebral cortex.

[31]  Y. Dan,et al.  Clonally Related Visual Cortical Neurons Show Similar Stimulus Feature Selectivity , 2012, Nature.

[32]  Wenlian Lu,et al.  Neonatal CX26 removal impairs neocortical development and leads to elevated anxiety , 2017, Proceedings of the National Academy of Sciences.

[33]  Ho Ko,et al.  Emergence of Feature-Specific Connectivity in Cortical Microcircuits in the Absence of Visual Experience , 2014, The Journal of Neuroscience.

[34]  Brett J. Graham,et al.  Anatomy and function of an excitatory network in the visual cortex , 2016, Nature.

[35]  Sooyoung Chung,et al.  Functional imaging with cellular resolution reveals precise micro-architecture in visual cortex , 2005, Nature.

[36]  K. Ohki,et al.  Mixed functional microarchitectures for orientation selectivity in the mouse primary visual cortex , 2016, Nature Communications.

[37]  P. J. Sjöström,et al.  Functional specificity of local synaptic connections in neocortical networks , 2011, Nature.

[38]  C. Lohmann,et al.  The developmental stages of synaptic plasticity , 2014, The Journal of physiology.

[39]  Bert Sakmann,et al.  Synaptic Connections between Layer 5B Pyramidal Neurons in Mouse Somatosensory Cortex Are Independent of Apical Dendrite Bundling , 2007, The Journal of Neuroscience.

[40]  Anirvan Ghosh,et al.  Specification of synaptic connectivity by cell surface interactions , 2015, Nature Reviews Neuroscience.

[41]  K. Ohki,et al.  Similarity of Visual Selectivity among Clonally Related Neurons in Visual Cortex , 2012, Neuron.

[42]  T. Hosoya,et al.  Lattice system of functionally distinct cell types in the neocortex , 2017, Science.

[43]  S. Shi,et al.  Specific synapses develop preferentially among sister excitatory neurons in the neocortex , 2009, Nature.

[44]  Yumiko Yoshimura,et al.  Experience-Dependent Emergence of Fine-Scale Networks in Visual Cortex , 2014, The Journal of Neuroscience.

[45]  P. J. Sjöström,et al.  A Cooperative Switch Determines the Sign of Synaptic Plasticity in Distal Dendrites of Neocortical Pyramidal Neurons , 2006, Neuron.

[46]  Tobias Bonhoeffer,et al.  Clusters of synaptic inputs on dendrites of layer 5 pyramidal cells in mouse visual cortex , 2016, eLife.

[47]  K. Shen,et al.  Cellular and molecular mechanisms of synaptic specificity. , 2014, Annual review of cell and developmental biology.

[48]  Daniel N. Hill,et al.  Development of Direction Selectivity in Mouse Cortical Neurons , 2011, Neuron.

[49]  P. Rakic.  Specification of cerebral cortical areas. , 1988, Science.

[50]  R. Tremblay,et al.  GABAergic Interneurons in the Neocortex: From Cellular Properties to Circuits , 2016, Neuron.

[51]  Ian R. Wickersham,et al.  Hierarchical Connectivity and Connection-Specific Dynamics in the Corticospinal–Corticostriatal Microcircuit in Mouse Motor Cortex , 2012, The Journal of Neuroscience.

[52]  S. Ge,et al.  Inside-Out Radial Migration Facilitates Lineage-Dependent Neocortical Microcircuit Assembly , 2015, Neuron.

[53]  R. Reid,et al.  Local Diversity and Fine-Scale Organization of Receptive Fields in Mouse Visual Cortex , 2011, The Journal of Neuroscience.

[54]  Z. Qiu,et al.  Coordinated Spine Pruning and Maturation Mediated by Inter-Spine Competition for Cadherin/Catenin Complexes , 2015, Cell.

[55]  Patrick J. Mineault,et al.  Spatial clustering of tuning in mouse primary visual cortex , 2016, Nature Communications.

[56]  K. Svoboda,et al.  The subcellular organization of neocortical excitatory connections , 2009, Nature.

[57]  J. Lübke,et al.  Efficacy and connectivity of intracolumnar pairs of layer 2/3 pyramidal cells in the barrel cortex of juvenile rats , 2006, The Journal of physiology.

[58]  Y. Kawaguchi,et al.  Recurrent Connection Patterns of Corticostriatal Pyramidal Cells in Frontal Cortex , 2006, The Journal of Neuroscience.

[59]  R. Douglas,et al.  Neuronal circuits of the neocortex. , 2004, Annual review of neuroscience.

[60]  G. Shepherd,et al.  The neocortical circuit: themes and variations , 2015, Nature Neuroscience.

[61]  T. Wiesel,et al.  The Sharpey-Schafer lecture. Morphological basis of visual cortical function. , 1983, Quarterly journal of experimental physiology.

[62]  H. Markram,et al.  Physiology and anatomy of synaptic connections between thick tufted pyramidal neurones in the developing rat neocortex. , 1997, The Journal of physiology.

[63]  Balázs Rózsa,et al.  Single-cell–initiated monosynaptic tracing reveals layer-specific cortical network modules , 2015, Science.

[64]  Y. Yoshimura,et al.  Establishment of high reciprocal connectivity between clonal cortical neurons is regulated by the Dnmt3b DNA methyltransferase and clustered protocadherins , 2016, BMC Biology.

[65]  K. Harris,et al.  Cortical connectivity and sensory coding , 2013, Nature.

[66]  H. Markram,et al.  Frequency and Dendritic Distribution of Autapses Established by Layer 5 Pyramidal Neurons in the Developing Rat Neocortex: Comparison with Synaptic Innervation of Adjacent Neurons of the Same Class , 1996, The Journal of Neuroscience.