Scientific Understanding of Consciousness
Visual Cortex Functional Microcircuits
Nature 496, 96–100 (04 April 2013)
The emergence of functional microcircuits in visual cortex
Department of Neuroscience, Physiology and Pharmacology, University College London, 21 University Street, London WC1E 6DE, UK
Ho Ko, Lee Cossell, Chiara Baragli, Jan Antolik, Sonja B. Hofer & Thomas D. Mrsic-Flogel
Center for Theoretical Neuroscience, Columbia University, 1051 Riverside Drive, Unit 87 Kolb Research Annex, New York, New York 10032, USA
Unité de Neuroscience Information et Complexité, UPR 3293 CNRS, 1 Avenue de la Terrasse, 91198 Gif-sur-Yvette, France.
Sensory processing occurs in neocortical microcircuits in which synaptic connectivity is highly structured and excitatory neurons form subnetworks that process related sensory information. However, the developmental mechanisms underlying the formation of functionally organized connectivity in cortical microcircuits remain unknown. Here we directly relate patterns of excitatory synaptic connectivity to visual response properties of neighbouring layer 2/3 pyramidal neurons in mouse visual cortex at different postnatal ages, using two-photon calcium imaging in vivo and multiple whole-cell recordings in vitro. Although neural responses were already highly selective for visual stimuli at eye opening, neurons responding to similar visual features were not yet preferentially connected, indicating that the emergence of feature selectivity does not depend on the precise arrangement of local synaptic connections. After eye opening, local connectivity reorganized extensively: more connections formed selectively between neurons with similar visual responses and connections were eliminated between visually unresponsive neurons, but the overall connectivity rate did not change. We propose a sequential model of cortical microcircuit development based on activity-dependent mechanisms of plasticity whereby neurons first acquire feature preference by selecting feedforward inputs before the onset of sensory experience—a process that may be facilitated by early electrical coupling between neuronal subsets—and then patterned input drives the formation of functional subnetworks through a redistribution of recurrent synaptic connections.
Intrinsic and experiential factors guide the patterning of neural pathways and the establishment of sensory response properties during postnatal development. During this time, neural circuit refinement is thought to depend on the elimination of initially exuberant projections, selective formation of new connections or both. However, the mechanisms governing the emergence of structured connectivity in local cortical microcircuits, where dendrites and axons overlap extensively, remain uncertain. Moreover, it is not clear whether the organization of synaptic connections between nearby neurons is established early and inherently linked to the formation of receptive fields (RFs) before the onset of sensory experience or whether the mature patterns of recurrent connectivity appear only after the formation of RFs as a result of correlated activity induced by feedforward drive from the sensory periphery. Here we investigate these questions in networks of layer 2/3 (L2/3) pyramidal cells in mouse primary visual cortex (V1) — where neighbouring neurons exhibit a diversity of preference for visual features—by determining how local synaptic connectivity relates to visual response properties during development.
In conclusion, the patterning of recurrent cortical connectivity through the feedforward-driven, activity-dependent redistribution of connections may be a fundamental rule by which neurons link together into assemblies that process related information.
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