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Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex

Contrast gain control is the systematic adjustment of neuronal gain in response to the contrast of sensory input. It is widely observed in sensory cortical areas and has been proposed to be a canonical neuronal computation. Here, we investigated whether shunting inhibition from parvalbumin-positive...

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Autores principales: Cooke, James E., Kahn, Martin C., Mann, Edward O., King, Andrew J., Schnupp, Jan W. H., Willmore, Ben D. B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Physiological Society 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7191518/
https://www.ncbi.nlm.nih.gov/pubmed/32186432
http://dx.doi.org/10.1152/jn.00587.2019
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author Cooke, James E.
Kahn, Martin C.
Mann, Edward O.
King, Andrew J.
Schnupp, Jan W. H.
Willmore, Ben D. B.
author_facet Cooke, James E.
Kahn, Martin C.
Mann, Edward O.
King, Andrew J.
Schnupp, Jan W. H.
Willmore, Ben D. B.
author_sort Cooke, James E.
collection PubMed
description Contrast gain control is the systematic adjustment of neuronal gain in response to the contrast of sensory input. It is widely observed in sensory cortical areas and has been proposed to be a canonical neuronal computation. Here, we investigated whether shunting inhibition from parvalbumin-positive interneurons—a mechanism involved in gain control in visual cortex—also underlies contrast gain control in auditory cortex. First, we performed extracellular recordings in the auditory cortex of anesthetized male mice and optogenetically manipulated the activity of parvalbumin-positive interneurons while varying the contrast of the sensory input. We found that both activation and suppression of parvalbumin interneuron activity altered the overall gain of cortical neurons. However, despite these changes in overall gain, we found that manipulating parvalbumin interneuron activity did not alter the strength of contrast gain control in auditory cortex. Furthermore, parvalbumin-positive interneurons did not show increases in activity in response to high-contrast stimulation, which would be expected if they drive contrast gain control. Finally, we performed in vivo whole-cell recordings in auditory cortical neurons during high- and low-contrast stimulation and found that no increase in membrane conductance was observed during high-contrast stimulation. Taken together, these findings indicate that while parvalbumin-positive interneuron activity modulates the overall gain of auditory cortical responses, other mechanisms are primarily responsible for contrast gain control in this cortical area. NEW & NOTEWORTHY We investigated whether contrast gain control is mediated by shunting inhibition from parvalbumin-positive interneurons in auditory cortex. We performed extracellular and intracellular recordings in mouse auditory cortex while presenting sensory stimuli with varying contrasts and manipulated parvalbumin-positive interneuron activity using optogenetics. We show that while parvalbumin-positive interneuron activity modulates the gain of cortical responses, this activity is not the primary mechanism for contrast gain control in auditory cortex.
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spelling pubmed-71915182020-05-11 Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex Cooke, James E. Kahn, Martin C. Mann, Edward O. King, Andrew J. Schnupp, Jan W. H. Willmore, Ben D. B. J Neurophysiol Research Article Contrast gain control is the systematic adjustment of neuronal gain in response to the contrast of sensory input. It is widely observed in sensory cortical areas and has been proposed to be a canonical neuronal computation. Here, we investigated whether shunting inhibition from parvalbumin-positive interneurons—a mechanism involved in gain control in visual cortex—also underlies contrast gain control in auditory cortex. First, we performed extracellular recordings in the auditory cortex of anesthetized male mice and optogenetically manipulated the activity of parvalbumin-positive interneurons while varying the contrast of the sensory input. We found that both activation and suppression of parvalbumin interneuron activity altered the overall gain of cortical neurons. However, despite these changes in overall gain, we found that manipulating parvalbumin interneuron activity did not alter the strength of contrast gain control in auditory cortex. Furthermore, parvalbumin-positive interneurons did not show increases in activity in response to high-contrast stimulation, which would be expected if they drive contrast gain control. Finally, we performed in vivo whole-cell recordings in auditory cortical neurons during high- and low-contrast stimulation and found that no increase in membrane conductance was observed during high-contrast stimulation. Taken together, these findings indicate that while parvalbumin-positive interneuron activity modulates the overall gain of auditory cortical responses, other mechanisms are primarily responsible for contrast gain control in this cortical area. NEW & NOTEWORTHY We investigated whether contrast gain control is mediated by shunting inhibition from parvalbumin-positive interneurons in auditory cortex. We performed extracellular and intracellular recordings in mouse auditory cortex while presenting sensory stimuli with varying contrasts and manipulated parvalbumin-positive interneuron activity using optogenetics. We show that while parvalbumin-positive interneuron activity modulates the gain of cortical responses, this activity is not the primary mechanism for contrast gain control in auditory cortex. American Physiological Society 2020-04-01 2020-03-18 /pmc/articles/PMC7191518/ /pubmed/32186432 http://dx.doi.org/10.1152/jn.00587.2019 Text en Licensed under Creative Commons Attribution CC-BY 4.0: © the American Physiological Society. ISSN 0022-3077. http://creativecommons.org/licenses/by/4.0/deed.en_US Licensed under Creative Commons Attribution CC-BY 4.0 (http://creativecommons.org/licenses/by/4.0/deed.en_US) : © the American Physiological Society.
spellingShingle Research Article
Cooke, James E.
Kahn, Martin C.
Mann, Edward O.
King, Andrew J.
Schnupp, Jan W. H.
Willmore, Ben D. B.
Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
title Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
title_full Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
title_fullStr Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
title_full_unstemmed Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
title_short Contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
title_sort contrast gain control occurs independently of both parvalbumin-positive interneuron activity and shunting inhibition in auditory cortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7191518/
https://www.ncbi.nlm.nih.gov/pubmed/32186432
http://dx.doi.org/10.1152/jn.00587.2019
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