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

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 in...

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Main Authors: Hayden, Dustin J, Montgomery, Daniel P, Cooke, Samuel F, Bear, Mark F
Other Authors: Picower Institute for Learning and Memory
Format: Article
Language:English
Published: Society for Neuroscience 2021
Online Access:https://hdl.handle.net/1721.1/138163
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author Hayden, Dustin J
Montgomery, Daniel P
Cooke, Samuel F
Bear, Mark F
author2 Picower Institute for Learning and Memory
author_facet Picower Institute for Learning and Memory
Hayden, Dustin J
Montgomery, Daniel P
Cooke, Samuel F
Bear, Mark F
author_sort Hayden, Dustin J
collection MIT
description 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 while 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.SIGNIFICANCE STATEMENT:Habituation, familiarity and novelty detection are fundamental cognitive processes that enable organisms to adaptively filter meaningless stimuli and focus attention on potentially important elements of their environment. We have shown that this process can be studied fruitfully in the mouse primary visual cortex by using simple grating stimuli for which novelty and familiarity are defined by orientation, and by measuring stimulus-evoked and continuous local field potentials. Altered event-related and spontaneous potentials, and deficient habituation, are well-documented features of several neurodevelopmental psychiatric disorders. The paradigm described here will be valuable to interrogate the origins of these signals and the meaning of their disruption more deeply.
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spelling mit-1721.1/1381632023-08-11T18:26:24Z Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex Hayden, Dustin J Montgomery, Daniel P Cooke, Samuel F Bear, Mark F Picower Institute for Learning and Memory Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences 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 while 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.SIGNIFICANCE STATEMENT:Habituation, familiarity and novelty detection are fundamental cognitive processes that enable organisms to adaptively filter meaningless stimuli and focus attention on potentially important elements of their environment. We have shown that this process can be studied fruitfully in the mouse primary visual cortex by using simple grating stimuli for which novelty and familiarity are defined by orientation, and by measuring stimulus-evoked and continuous local field potentials. Altered event-related and spontaneous potentials, and deficient habituation, are well-documented features of several neurodevelopmental psychiatric disorders. The paradigm described here will be valuable to interrogate the origins of these signals and the meaning of their disruption more deeply. 2021-11-19T15:45:10Z 2021-11-19T15:45:10Z 2021 2021-11-19T15:39:45Z Article http://purl.org/eprint/type/JournalArticle https://hdl.handle.net/1721.1/138163 Hayden, Dustin J, Montgomery, Daniel P, Cooke, Samuel F and Bear, Mark F. 2021. "Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex." Journal of Neuroscience, 41 (29). en 10.1523/JNEUROSCI.0391-21.2021 Journal of Neuroscience Creative Commons Attribution 4.0 International license https://creativecommons.org/licenses/by/4.0/ application/pdf Society for Neuroscience Society for Neuroscience
spellingShingle Hayden, Dustin J
Montgomery, Daniel P
Cooke, Samuel F
Bear, Mark F
Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
title Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
title_full Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
title_fullStr Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
title_full_unstemmed Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
title_short Visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
title_sort visual recognition is heralded by shifts in local field potential oscillations and inhibitory networks in primary visual cortex
url https://hdl.handle.net/1721.1/138163
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