A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics

Habits are notoriously difficult to break and, if broken, are usually replaced by new routines. To examine the neural basis of these characteristics, we recorded spike activity in cortical and striatal habit sites as rats learned maze tasks. Overtraining induced a shift from purposeful to habitual b...

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Main Authors: Smith, Kyle S., Graybiel, Ann M., Smith, Kyle S., Graybiel, Ann M.
Other Authors: Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Format: Article
Language:en_US
Published: Elsevier 2016
Online Access:http://hdl.handle.net/1721.1/102219
https://orcid.org/0000-0002-4326-7720
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author Smith, Kyle S.
Graybiel, Ann M.
Smith, Kyle S.
Graybiel, Ann M.
author2 Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
author_facet Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences
Smith, Kyle S.
Graybiel, Ann M.
Smith, Kyle S.
Graybiel, Ann M.
author_sort Smith, Kyle S.
collection MIT
description Habits are notoriously difficult to break and, if broken, are usually replaced by new routines. To examine the neural basis of these characteristics, we recorded spike activity in cortical and striatal habit sites as rats learned maze tasks. Overtraining induced a shift from purposeful to habitual behavior. This shift coincided with the activation of neuronal ensembles in the infralimbic neocortex and the sensorimotor striatum, which became engaged simultaneously but developed changes in spike activity with distinct time courses and stability. The striatum rapidly acquired an action-bracketing activity pattern insensitive to reward devaluation but sensitive to running automaticity. A similar pattern developed in the upper layers of the infralimbic cortex, but it formed only late during overtraining and closely tracked habit states. Selective optogenetic disruption of infralimbic activity during overtraining prevented habit formation. We suggest that learning-related spiking dynamics of both striatum and neocortex are necessary, as dual operators, for habit crystallization.
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spelling mit-1721.1/1022192022-09-27T20:04:20Z A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics Smith, Kyle S. Graybiel, Ann M. Smith, Kyle S. Graybiel, Ann M. Massachusetts Institute of Technology. Department of Brain and Cognitive Sciences McGovern Institute for Brain Research at MIT Smith, Kyle S. Graybiel, Ann M. Habits are notoriously difficult to break and, if broken, are usually replaced by new routines. To examine the neural basis of these characteristics, we recorded spike activity in cortical and striatal habit sites as rats learned maze tasks. Overtraining induced a shift from purposeful to habitual behavior. This shift coincided with the activation of neuronal ensembles in the infralimbic neocortex and the sensorimotor striatum, which became engaged simultaneously but developed changes in spike activity with distinct time courses and stability. The striatum rapidly acquired an action-bracketing activity pattern insensitive to reward devaluation but sensitive to running automaticity. A similar pattern developed in the upper layers of the infralimbic cortex, but it formed only late during overtraining and closely tracked habit states. Selective optogenetic disruption of infralimbic activity during overtraining prevented habit formation. We suggest that learning-related spiking dynamics of both striatum and neocortex are necessary, as dual operators, for habit crystallization. National Institutes of Health (U.S.) (Grant R01 MH060379) National Institutes of Health (U.S.) (Grant F32 MH085454) United States. Office of Naval Research (Grant N00014-04-1-0208) Stanley H. and Sheila G. Sydney Fund 2016-04-08T15:58:14Z 2016-04-08T15:58:14Z 2013-06 2013-05 Article http://purl.org/eprint/type/JournalArticle 08966273 1097-4199 http://hdl.handle.net/1721.1/102219 Smith, Kyle S., and Ann M. Graybiel. “A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics.” Neuron 79, no. 2 (July 2013): 361–374. https://orcid.org/0000-0002-4326-7720 en_US http://dx.doi.org/10.1016/j.neuron.2013.05.038 Neuron Creative Commons Attribution-Noncommercial-NoDerivatives http://creativecommons.org/licenses/by-nc-nd/4.0/ application/pdf Elsevier PMC
spellingShingle Smith, Kyle S.
Graybiel, Ann M.
Smith, Kyle S.
Graybiel, Ann M.
A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics
title A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics
title_full A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics
title_fullStr A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics
title_full_unstemmed A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics
title_short A Dual Operator View of Habitual Behavior Reflecting Cortical and Striatal Dynamics
title_sort dual operator view of habitual behavior reflecting cortical and striatal dynamics
url http://hdl.handle.net/1721.1/102219
https://orcid.org/0000-0002-4326-7720
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