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Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons

Nicotine can diversely affect neural activity and motor learning in animals. However, the impact of chronic nicotine on striatal activity in vivo and motor learning at long‐term sparse timescale remains unknown. Here, we demonstrate that chronic nicotine persistently suppresses the activity of stria...

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Autores principales: Kim, Baeksun, Im, Heh‐In
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8243919/
https://www.ncbi.nlm.nih.gov/pubmed/32767546
http://dx.doi.org/10.1111/adb.12956
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author Kim, Baeksun
Im, Heh‐In
author_facet Kim, Baeksun
Im, Heh‐In
author_sort Kim, Baeksun
collection PubMed
description Nicotine can diversely affect neural activity and motor learning in animals. However, the impact of chronic nicotine on striatal activity in vivo and motor learning at long‐term sparse timescale remains unknown. Here, we demonstrate that chronic nicotine persistently suppresses the activity of striatal fast‐spiking parvalbumin interneurons, which mediate nicotine‐induced deficit in sparse motor learning. Six weeks of longitudinal in vivo single‐unit recording revealed that mice show reduced activity of fast‐spiking interneurons in the dorsal striatum during chronic nicotine exposure and withdrawal. The reduced firing of fast‐spiking interneurons was accompanied by spike broadening, diminished striatal delta oscillation power, and reduced sample entropy in local field potential. In addition, chronic nicotine withdrawal impaired motor learning with a weekly sparse training regimen but did not affect general locomotion and anxiety‐like behavior. Lastly, the excitatory DREADD hM3Dq‐mediated activation of striatal fast‐spiking parvalbumin interneurons reversed the chronic nicotine withdrawal‐induced deficit in sparse motor learning. Taken together, we identified that chronic nicotine withdrawal impairs sparse motor learning via disruption of activity in striatal fast‐spiking parvalbumin interneurons. These findings suggest that sparse motor learning paradigm can reveal the subtle effect of nicotine withdrawal on motor function and that striatal fast‐spiking parvalbumin interneurons are a neural substrate of nicotine's effect on motor learning.
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spelling pubmed-82439192021-07-02 Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons Kim, Baeksun Im, Heh‐In Addict Biol Preclinical Studies Nicotine can diversely affect neural activity and motor learning in animals. However, the impact of chronic nicotine on striatal activity in vivo and motor learning at long‐term sparse timescale remains unknown. Here, we demonstrate that chronic nicotine persistently suppresses the activity of striatal fast‐spiking parvalbumin interneurons, which mediate nicotine‐induced deficit in sparse motor learning. Six weeks of longitudinal in vivo single‐unit recording revealed that mice show reduced activity of fast‐spiking interneurons in the dorsal striatum during chronic nicotine exposure and withdrawal. The reduced firing of fast‐spiking interneurons was accompanied by spike broadening, diminished striatal delta oscillation power, and reduced sample entropy in local field potential. In addition, chronic nicotine withdrawal impaired motor learning with a weekly sparse training regimen but did not affect general locomotion and anxiety‐like behavior. Lastly, the excitatory DREADD hM3Dq‐mediated activation of striatal fast‐spiking parvalbumin interneurons reversed the chronic nicotine withdrawal‐induced deficit in sparse motor learning. Taken together, we identified that chronic nicotine withdrawal impairs sparse motor learning via disruption of activity in striatal fast‐spiking parvalbumin interneurons. These findings suggest that sparse motor learning paradigm can reveal the subtle effect of nicotine withdrawal on motor function and that striatal fast‐spiking parvalbumin interneurons are a neural substrate of nicotine's effect on motor learning. John Wiley and Sons Inc. 2020-08-06 2021-05 /pmc/articles/PMC8243919/ /pubmed/32767546 http://dx.doi.org/10.1111/adb.12956 Text en © 2020 The Authors. Addiction Biology published by John Wiley & Sons Ltd on behalf of Society for the Study of Addiction https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Preclinical Studies
Kim, Baeksun
Im, Heh‐In
Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
title Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
title_full Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
title_fullStr Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
title_full_unstemmed Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
title_short Chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
title_sort chronic nicotine impairs sparse motor learning via striatal fast‐spiking parvalbumin interneurons
topic Preclinical Studies
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8243919/
https://www.ncbi.nlm.nih.gov/pubmed/32767546
http://dx.doi.org/10.1111/adb.12956
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