Zhang, Deng and Yan, Xingjian and She, Liang and Wen, Yunqing and Poo, Mu-ming (2020) Global enhancement of cortical excitability following coactivation of large neuronal populations. Proceedings of the National Academy of Sciences of the United States of America, 117 (33). pp. 20254-20264. ISSN 0027-8424. doi:10.1073/pnas.1914869117. https://resolver.caltech.edu/CaltechAUTHORS:20200803-144801580
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Abstract
Correlated activation of cortical neurons often occurs in the brain and repetitive correlated neuronal firing could cause long-term modifications of synaptic efficacy and intrinsic excitability. We found that repetitive optogenetic activation of neuronal populations in the mouse cortex caused enhancement of optogenetically evoked firing of local coactivated neurons as well as distant cortical neurons in both ipsilateral and contralateral hemispheres. This global enhancement of evoked responses required coactivation of a sufficiently large population of neurons either within one cortical area or distributed in several areas. Enhancement of neuronal firing was saturable after repeated episodes of coactivation, diminished by inhibition of N-methyl-D-aspartic acid receptors, and accompanied by elevated excitatory postsynaptic potentials, all consistent with activity-induced synaptic potentiation. Chemogenetic inhibition of neuronal activity of the thalamus decreased the enhancement effect, suggesting thalamic involvement. Thus, correlated excitation of large neuronal populations leads to global enhancement of neuronal excitability.
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Additional Information: | © 2020 National Academy of Sciences. Contributed by Mu-ming Poo, July 3, 2020 (sent for review September 16, 2019; reviewed by Sydney S. Cash and Karunesh Ganguly). PNAS first published August 3, 2020. We thank Shengjin Xu, Qingfang Zhang, Chunfeng Shang, Haishan Yao, Wei Huang, Dechen Liu, Tianyi Wang, Wenhui Qiao, and Dinghong Zhang for technical advice and support. This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (Grant XDB32070100), Key Research Program of Frontier Sciences, Chinese Academy of Sciences (QYZDY-SSW-SMCO01), International Partnership Program of Chinese Academy of Sciences (153D31KYSB20170059), the Shanghai Key Basic Research Project (16JC1420201), Shanghai Municipal Science and Technology Major Project (2018SHZDZX05), and the Shanghai Key Basic Research Project (18JC1410100). Data Availability: All study data are included in the article and SI Appendix. D.Z. and X.Y. contributed equally to this work. Author contributions: D.Z., X.Y., and M.-m.P. designed research; D.Z. and X.Y. performed research; D.Z., X.Y., L.S., and Y.W. contributed new reagents/analytic tools; D.Z., X.Y., L.S., and Y.W. analyzed data; and D.Z., X.Y., and M.-m.P. wrote the paper. Reviewers: S.S.C., Massachusetts General Hospital; and K.G., University of California, San Francisco. The authors declare no competing interest. This article contains supporting information online at https://www.pnas.org/lookup/suppl/doi:10.1073/pnas.1914869117/-/DCSupplemental. | ||||||||||||||
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Subject Keywords: | activity-dependent plasticity; synaptic potentiation; global excitability; cortical wave; corticothalamocortical circuit | ||||||||||||||
Issue or Number: | 33 | ||||||||||||||
DOI: | 10.1073/pnas.1914869117 | ||||||||||||||
Record Number: | CaltechAUTHORS:20200803-144801580 | ||||||||||||||
Persistent URL: | https://resolver.caltech.edu/CaltechAUTHORS:20200803-144801580 | ||||||||||||||
Official Citation: | Global enhancement of cortical excitability following coactivation of large neuronal populations. Deng Zhang, Xingjian Yan, Liang She, Yunqing Wen, Mu-ming Poo. Proceedings of the National Academy of Sciences Aug 2020, 117 (33) 20254-20264; DOI: 10.1073/pnas.1914869117 | ||||||||||||||
Usage Policy: | No commercial reproduction, distribution, display or performance rights in this work are provided. | ||||||||||||||
ID Code: | 104709 | ||||||||||||||
Collection: | CaltechAUTHORS | ||||||||||||||
Deposited By: | Tony Diaz | ||||||||||||||
Deposited On: | 03 Aug 2020 21:59 | ||||||||||||||
Last Modified: | 16 Nov 2021 18:34 |
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