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

Fang, Qi and Li, Ya-tang and Peng, Bo and Li, Zhong and Zhang, Li I. and Tao, Huizhong W. (2021) Balanced Enhancements of Synaptic Excitation and Inhibition Underlie Developmental Maturation of Receptive Fields in the Mouse Visual Cortex. Journal of Neuroscience, 41 (49). pp. 10065-10079. ISSN 0270-6474. PMCID PMC8660040. doi:10.1523/jneurosci.0442-21.2021. https://resolver.caltech.edu/CaltechAUTHORS:20211201-184621035

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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.


Item Type:Article
Related URLs:
URLURL TypeDescription
https://doi.org/10.1523/jneurosci.0442-21.2021DOIArticle
ORCID:
AuthorORCID
Li, Ya-tang0000-0003-2763-1534
Tao, Huizhong W.0000-0002-3660-0513
Alternate Title:Maturation of Cortical Synaptic Receptive fields
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.
Funders:
Funding AgencyGrant Number
NIHEY-019049
NIHEY-022478
NIHDC-008983
Subject Keywords:development; excitation/inhibition balance; receptive field; synaptic input; visual cortex; whole-cell recording
Issue or Number:49
PubMed Central ID:PMC8660040
DOI:10.1523/jneurosci.0442-21.2021
Record Number:CaltechAUTHORS:20211201-184621035
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20211201-184621035
Official Citation:Balanced Enhancements of Synaptic Excitation and Inhibition Underlie Developmental Maturation of Receptive Fields in the Mouse Visual Cortex. Qi Fang, Ya-tang Li, Bo Peng, Zhong Li, Li I. Zhang, Huizhong W. Tao. Journal of Neuroscience 8 December 2021, 41 (49) 10065-10079; DOI: 10.1523/JNEUROSCI.0442-21.2021
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:112146
Collection:CaltechAUTHORS
Deposited By: Tony Diaz
Deposited On:01 Dec 2021 22:20
Last Modified:15 Dec 2021 23:46

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