Cited by 324Memory and Neural MechanismsNeural and Behavioral Psychology StudiesNeurotransmitter Receptor Influence on Behavior

A dual operator view of habitual behavior reflecting cortical and striatal dynamics

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Smith, Kyle S., Graybiel, Ann M.·2013·Neuron

Abstract

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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Authors
Smith, K. S., & Graybiel, A. M.
Affiliations
McGovern Institute for Brain Research (US)
Corresponding author
  • Smith, Kyle S.
  • Graybiel, Ann M.
Venue
Neuron
Publisher
Elsevier BV
Published
2013-07
Volume
79
Issue
2
Pages
361-374
ISSN
0896-6273 (ISSN-L)
OpenAlex
W2123053862
Cited by
324
References
63
Citations by year
2026: 16 · 2025: 14 · 2024: 38 · 2023: 23 · 2022: 21 · 2021: 35 · 2020: 29 · 2019: 22 · 2018: 24 · 2017: 22 · 2016: 26 · 2015: 31 · 2014: 18 · 2013: 5
FWCI
14.36
Type
journal article
Language
en
Update notices
erratum (2013-08-07)
Open access
Locations
  • Neuron (publishedVersion)
  • PubMed (publishedVersion)
  • Europe PMC (PubMed Central) (acceptedVersion)
  • PubMed Central (acceptedVersion)
  • DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
Funders
National Institute of Mental Health (F32MH085454, R01MH060379)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
habit formation, habitual behavior, infralimbic cortex, sensorimotor striatum, overtraining, neuronal ensembles, reward devaluation, rats
MeSH terms
Action Potentials, Animals, Behavior, Animal, Cerebral Cortex, Corpus Striatum, Habits, Maze Learning, Rats

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