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Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex

Research output: Contribution to journalArticlepeer-review

Dustin Hayden, Daniel Montgomery, Samuel Cooke, M.F. Bear

Original languageEnglish
Article numberJN-RM-0391-21
Pages (from-to)6257-6272
Number of pages16
JournalJournal of Neuroscience
Volume41
Issue number29
Early online date8 Jun 2021
DOIs
E-pub ahead of print8 Jun 2021
Published21 Jul 2021

Bibliographical note

Funding Information: Received Feb. 22, 2021; revised May 18, 2021; accepted May 19, 2021. Author contributions: M.F.B., D.J.H., D.P.M., and S.F.C. designed research; D.J.H. and D.P.M. performed research; D.J.H. and D.P.M. analyzed data; M.F.B., D.J.H., and S.F.C. wrote the paper. Support was provided by the National Institutes of Health (R01EY023037), the Picower Institute Innovation Fund, the Picower Young Faculty Support Fund, and a National Science Foundation Graduate Research Fellowship (D.J.H.). S.F.C. was supported by the Wellcome Trust (207727/Z/17/Z) and the Biotechnology and Biological Sciences Research Council (BB/S008276/1).We thank Arnold Heynen, Nina Palisano, Jessica Buckey, Athene Wilson-Glover, Kiki Chu, and Erin Hickey. We also thank Dr. Robert W. Komorowski for initiating and encouraging this project. *D.J.H. and D.P.M. contributed equally to this work. The authors declare no competing financial interests. Correspondence should be addressed to Mark F. Bear at mbear@mit.edu. https://doi.org/10.1523/JNEUROSCI.0391-21.2021 Copyright © 2021 Hayden, Montgomery et al. This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed. Publisher Copyright: Copyright © 2021 Hayden, Montgomery et al. Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

King's Authors

Abstract

Learning to recognize and filter familiar, irrelevant sensory stimuli eases the computational burden on the cerebral cortex. Inhibition is a candidate mechanism in this filtration process, and oscillations in the cortical local field potential (LFP) serve as markers of the engagement of different inhibitory neurons. We show here that LFP oscillatory activity in visual cortex is profoundly altered as male and female mice learn to recognize an oriented grating stimulus—low-frequency (;15 Hz peak) power sharply increases, whereas high-frequency (;65 Hz peak) power decreases. These changes report recognition of the familiar pattern as they disappear when the stimulus is rotated to a novel orientation. Two-photon imaging of neuronal activity reveals that parvalbumin-expressing inhibitory neurons disengage with familiar stimuli and reactivate to novelty, whereas somatostatin-expressing inhibitory neurons show opposing activity patterns. We propose a model in which the balance of two interacting interneuron circuits shifts as novel stimuli become familiar.

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