Cargando…

Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration

Animals can capitalize on invariance in the environment by learning and automating highly consistent actions; however, they must also remain flexible and adapt to environmental changes. It remains unclear how primary motor cortex (M1) can drive precise movements, yet also support behavioral explorat...

Descripción completa

Detalles Bibliográficos
Autores principales: Kondapavulur, Sravani, Lemke, Stefan M., Darevsky, David, Guo, Ling, Khanna, Preeya, Ganguly, Karunesh
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9068924/
https://www.ncbi.nlm.nih.gov/pubmed/35508447
http://dx.doi.org/10.1038/s41467-022-30069-1
_version_ 1784700323203383296
author Kondapavulur, Sravani
Lemke, Stefan M.
Darevsky, David
Guo, Ling
Khanna, Preeya
Ganguly, Karunesh
author_facet Kondapavulur, Sravani
Lemke, Stefan M.
Darevsky, David
Guo, Ling
Khanna, Preeya
Ganguly, Karunesh
author_sort Kondapavulur, Sravani
collection PubMed
description Animals can capitalize on invariance in the environment by learning and automating highly consistent actions; however, they must also remain flexible and adapt to environmental changes. It remains unclear how primary motor cortex (M1) can drive precise movements, yet also support behavioral exploration when faced with consistent errors. Using a reach-to-grasp task in rats, along with simultaneous electrophysiological monitoring in M1 and dorsolateral striatum (DLS), we find that behavioral exploration to overcome consistent task errors is closely associated with tandem increases in M1 and DLS neural variability; subsequently, consistent ensemble patterning returns with convergence to a new successful strategy. We also show that compared to reliably patterned intracranial microstimulation in M1, variable stimulation patterns result in significantly greater movement variability. Our results thus indicate that motor and striatal areas can flexibly transition between two modes, reliable neural pattern generation for automatic and precise movements versus variable neural patterning for behavioral exploration.
format Online
Article
Text
id pubmed-9068924
institution National Center for Biotechnology Information
language English
publishDate 2022
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-90689242022-05-05 Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration Kondapavulur, Sravani Lemke, Stefan M. Darevsky, David Guo, Ling Khanna, Preeya Ganguly, Karunesh Nat Commun Article Animals can capitalize on invariance in the environment by learning and automating highly consistent actions; however, they must also remain flexible and adapt to environmental changes. It remains unclear how primary motor cortex (M1) can drive precise movements, yet also support behavioral exploration when faced with consistent errors. Using a reach-to-grasp task in rats, along with simultaneous electrophysiological monitoring in M1 and dorsolateral striatum (DLS), we find that behavioral exploration to overcome consistent task errors is closely associated with tandem increases in M1 and DLS neural variability; subsequently, consistent ensemble patterning returns with convergence to a new successful strategy. We also show that compared to reliably patterned intracranial microstimulation in M1, variable stimulation patterns result in significantly greater movement variability. Our results thus indicate that motor and striatal areas can flexibly transition between two modes, reliable neural pattern generation for automatic and precise movements versus variable neural patterning for behavioral exploration. Nature Publishing Group UK 2022-05-04 /pmc/articles/PMC9068924/ /pubmed/35508447 http://dx.doi.org/10.1038/s41467-022-30069-1 Text en © This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2022 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Kondapavulur, Sravani
Lemke, Stefan M.
Darevsky, David
Guo, Ling
Khanna, Preeya
Ganguly, Karunesh
Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
title Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
title_full Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
title_fullStr Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
title_full_unstemmed Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
title_short Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
title_sort transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9068924/
https://www.ncbi.nlm.nih.gov/pubmed/35508447
http://dx.doi.org/10.1038/s41467-022-30069-1
work_keys_str_mv AT kondapavulursravani transitionfrompredictabletovariablemotorcortexandstriatalensemblepatterningduringbehavioralexploration
AT lemkestefanm transitionfrompredictabletovariablemotorcortexandstriatalensemblepatterningduringbehavioralexploration
AT darevskydavid transitionfrompredictabletovariablemotorcortexandstriatalensemblepatterningduringbehavioralexploration
AT guoling transitionfrompredictabletovariablemotorcortexandstriatalensemblepatterningduringbehavioralexploration
AT khannapreeya transitionfrompredictabletovariablemotorcortexandstriatalensemblepatterningduringbehavioralexploration
AT gangulykarunesh transitionfrompredictabletovariablemotorcortexandstriatalensemblepatterningduringbehavioralexploration