Alternating sources of perisomatic inhibition during behavior

Barna Dudok; Peter M. Klein; Ernie Hwaun; Brian R. Lee; Zizhen Yao; Olivia Fong; John C. Bowler; Satoshi Terada; Fraser T. Sparks; Gergely G. Szabo; Jordan S. Farrell; Jim Berg; Tanya L. Daigle; Bosiljka Tasic; Jordane Dimidschstein; Gord Fishell; Attila Losonczy; Hongkui Zeng; Ivan Soltesz

doi:10.1016/j.neuron.2021.01.003

Alternating sources of perisomatic inhibition during behavior

Barna Dudok, Peter M. Klein, Ernie Hwaun, Brian R. Lee, Zizhen Yao, Olivia Fong, John C. Bowler, Satoshi Terada, Fraser T. Sparks, Gergely G. Szabo, Jordan S. Farrell, Jim Berg, Tanya L. Daigle, Bosiljka Tasic, Jordane Dimidschstein, Gord Fishell, Attila Losonczy, Hongkui Zeng, Ivan Soltesz

Center for Genomics and Systems Biology

Research output: Contribution to journal › Article › peer-review

Abstract

Interneurons expressing cholecystokinin (CCK) and parvalbumin (PV) constitute two key GABAergic controllers of hippocampal pyramidal cell output. Although the temporally precise and millisecond-scale inhibitory regulation of neuronal ensembles delivered by PV interneurons is well established, the in vivo recruitment patterns of CCK-expressing basket cell (BC) populations has remained unknown. We show in the CA1 of the mouse hippocampus that the activity of CCK BCs inversely scales with both PV and pyramidal cell activity at the behaviorally relevant timescales of seconds. Intervention experiments indicated that the inverse coupling of CCK and PV GABAergic systems arises through a mechanism involving powerful inhibitory control of CCK BCs by PV cells. The tightly coupled complementarity of two key microcircuit regulatory modules demonstrates a novel form of brain-state-specific segregation of inhibition during spontaneous behavior.

Original language	English (US)
Pages (from-to)	997-1012.e9
Journal	Neuron
Volume	109
Issue number	6
DOIs	https://doi.org/10.1016/j.neuron.2021.01.003
State	Published - Mar 17 2021

Keywords

CA1
CB1 receptor
GABA
Sncg
brain state
cholecystokinin
hippocampus
inhibition
interneuron
locomotion
parvalbumin

ASJC Scopus subject areas

General Neuroscience

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10.1016/j.neuron.2021.01.003

Cite this

Dudok, B., Klein, P. M., Hwaun, E., Lee, B. R., Yao, Z., Fong, O., Bowler, J. C., Terada, S., Sparks, F. T., Szabo, G. G., Farrell, J. S., Berg, J., Daigle, T. L., Tasic, B., Dimidschstein, J., Fishell, G., Losonczy, A., Zeng, H., & Soltesz, I. (2021). Alternating sources of perisomatic inhibition during behavior. Neuron, 109(6), 997-1012.e9. https://doi.org/10.1016/j.neuron.2021.01.003

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abstract = "Interneurons expressing cholecystokinin (CCK) and parvalbumin (PV) constitute two key GABAergic controllers of hippocampal pyramidal cell output. Although the temporally precise and millisecond-scale inhibitory regulation of neuronal ensembles delivered by PV interneurons is well established, the in vivo recruitment patterns of CCK-expressing basket cell (BC) populations has remained unknown. We show in the CA1 of the mouse hippocampus that the activity of CCK BCs inversely scales with both PV and pyramidal cell activity at the behaviorally relevant timescales of seconds. Intervention experiments indicated that the inverse coupling of CCK and PV GABAergic systems arises through a mechanism involving powerful inhibitory control of CCK BCs by PV cells. The tightly coupled complementarity of two key microcircuit regulatory modules demonstrates a novel form of brain-state-specific segregation of inhibition during spontaneous behavior.",

keywords = "CA1, CB1 receptor, GABA, Sncg, brain state, cholecystokinin, hippocampus, inhibition, interneuron, locomotion, parvalbumin",

author = "Barna Dudok and Klein, {Peter M.} and Ernie Hwaun and Lee, {Brian R.} and Zizhen Yao and Olivia Fong and Bowler, {John C.} and Satoshi Terada and Sparks, {Fraser T.} and Szabo, {Gergely G.} and Farrell, {Jordan S.} and Jim Berg and Daigle, {Tanya L.} and Bosiljka Tasic and Jordane Dimidschstein and Gord Fishell and Attila Losonczy and Hongkui Zeng and Ivan Soltesz",

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doi = "10.1016/j.neuron.2021.01.003",

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AU - Klein, Peter M.

AU - Hwaun, Ernie

AU - Lee, Brian R.

AU - Yao, Zizhen

AU - Fong, Olivia

AU - Bowler, John C.

AU - Terada, Satoshi

AU - Sparks, Fraser T.

AU - Szabo, Gergely G.

AU - Farrell, Jordan S.

AU - Berg, Jim

AU - Daigle, Tanya L.

AU - Tasic, Bosiljka

AU - Dimidschstein, Jordane

AU - Fishell, Gord

AU - Losonczy, Attila

AU - Zeng, Hongkui

AU - Soltesz, Ivan

PY - 2021/3/17

Y1 - 2021/3/17

N2 - Interneurons expressing cholecystokinin (CCK) and parvalbumin (PV) constitute two key GABAergic controllers of hippocampal pyramidal cell output. Although the temporally precise and millisecond-scale inhibitory regulation of neuronal ensembles delivered by PV interneurons is well established, the in vivo recruitment patterns of CCK-expressing basket cell (BC) populations has remained unknown. We show in the CA1 of the mouse hippocampus that the activity of CCK BCs inversely scales with both PV and pyramidal cell activity at the behaviorally relevant timescales of seconds. Intervention experiments indicated that the inverse coupling of CCK and PV GABAergic systems arises through a mechanism involving powerful inhibitory control of CCK BCs by PV cells. The tightly coupled complementarity of two key microcircuit regulatory modules demonstrates a novel form of brain-state-specific segregation of inhibition during spontaneous behavior.

AB - Interneurons expressing cholecystokinin (CCK) and parvalbumin (PV) constitute two key GABAergic controllers of hippocampal pyramidal cell output. Although the temporally precise and millisecond-scale inhibitory regulation of neuronal ensembles delivered by PV interneurons is well established, the in vivo recruitment patterns of CCK-expressing basket cell (BC) populations has remained unknown. We show in the CA1 of the mouse hippocampus that the activity of CCK BCs inversely scales with both PV and pyramidal cell activity at the behaviorally relevant timescales of seconds. Intervention experiments indicated that the inverse coupling of CCK and PV GABAergic systems arises through a mechanism involving powerful inhibitory control of CCK BCs by PV cells. The tightly coupled complementarity of two key microcircuit regulatory modules demonstrates a novel form of brain-state-specific segregation of inhibition during spontaneous behavior.

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KW - CB1 receptor

KW - GABA

KW - Sncg

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KW - inhibition

KW - interneuron

KW - locomotion

KW - parvalbumin

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Alternating sources of perisomatic inhibition during behavior

Abstract

Keywords

ASJC Scopus subject areas

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