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Published December 8, 2021 | Published + Accepted Version
Journal Article Open

Balanced Enhancements of Synaptic Excitation and Inhibition Underlie Developmental Maturation of Receptive Fields in the Mouse Visual Cortex

Abstract

Neurons in the developing visual cortex undergo progressive functional maturation as indicated by the refinement of their visual feature selectivity. However, changes of the synaptic architecture underlying the maturation of spatial visual receptive fields (RFs) per se remain largely unclear. Here, loose-patch as well as single-unit recordings in layer 4 of mouse primary visual cortex (V1) of both sexes revealed that RF development following an eye-opening period is marked by an increased proportion of cortical neurons with spatially defined RFs, together with the increased signal-to-noise ratio of spiking responses. By exploring excitatory and inhibitory synaptic RFs with whole-cell voltage-clamp recordings, we observed a balanced enhancement of both synaptic excitation and inhibition, and while the excitatory subfield size remains relatively constant during development, the inhibitory subfield is broadened. This balanced developmental strengthening of excitatory and inhibitory synaptic inputs results in enhanced visual responses, and with a reduction of spontaneous firing rate, contributes to the maturation of visual cortical RFs. Visual deprivation by dark rearing impedes the normal strengthening of excitatory inputs but leaves the apparently normal enhancement of inhibition while preventing the broadening of the inhibitory subfield, leading to weakened RF responses and a reduced fraction of neurons exhibiting a clear RF, compared with normally reared animals. Our data demonstrate that an experience-dependent and coordinated maturation of excitatory and inhibitory circuits underlie the functional development of visual cortical RFs.

Additional Information

© 2021 the authors. Beginning six months after publication the Work will be made freely available to the public on SfN's website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received Mar. 1, 2021; revised Sep. 14, 2021; accepted Oct. 23, 2021. This work was supported by Grants EY-019049 and EY-022478 to H.W.T. and Grant DC-008983 to L.I.Z. from the National Institutes of Health. Author contributions: L.I.Z. and H.W.T. designed research; Q.F., Y.-t.L., B.P., and Z.L. performed research; Q.F. and Y.-t.L. analyzed data; and L.I.Z. and H.W.T. wrote the paper. The authors declare no competing financial interests.

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Additional details

Created:
October 5, 2023
Modified:
October 25, 2023