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Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions

Author

Listed:
  • Christina M. Gremel

    (Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health)

  • Rui M. Costa

    (Laboratory for Integrative Neuroscience, National Institute on Alcohol Abuse and Alcoholism, National Institutes of Health
    Champalimaud Neuroscience Programme, Champalimaud Institute for the Unknown)

Abstract

Shifting between goal-directed and habitual actions allows for efficient and flexible decision making. Here we demonstrate a novel, within-subject instrumental lever-pressing paradigm, in which mice shift between goal-directed and habitual actions. We identify a role for orbitofrontal cortex (OFC) in actions following outcome revaluation, and confirm that dorsal medial (DMS) and lateral striatum (DLS) mediate different action strategies. Simultaneous in vivo recordings of OFC, DMS and DLS neuronal ensembles during shifting reveal that the same neurons display different activities depending on whether presses are goal-directed or habitual, with DMS and OFC becoming more and DLS less engaged during goal-directed actions. Importantly, the magnitude of neural activity changes in OFC following changes in outcome value positively correlates with the level of goal-directed behavior. Chemogenetic inhibition of OFC disrupts goal-directed actions, whereas optogenetic activation of OFC specifically increases goal-directed pressing. These results also reveal a role for OFC in action revaluation, which has implications for understanding compulsive behavior.

Suggested Citation

  • Christina M. Gremel & Rui M. Costa, 2013. "Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions," Nature Communications, Nature, vol. 4(1), pages 1-12, October.
    • Handle: RePEc:nat:natcom:v:4:y:2013:i:1:d:10.1038_ncomms3264
    DOI: 10.1038/ncomms3264
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    Cited by:

    1. Francesco Paolo Ulloa Severino & Oluwadamilola O. Lawal & Kristina Sakers & Shiyi Wang & Namsoo Kim & Alexander David Friedman & Sarah Anne Johnson & Chaichontat Sriworarat & Ryan H. Hughes & Scott H., 2023. "Training-induced circuit-specific excitatory synaptogenesis in mice is required for effort control," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    2. Bernard Bloem & Rafiq Huda & Ken-ichi Amemori & Alex S. Abate & Gayathri Krishna & Anna L. Wilson & Cody W. Carter & Mriganka Sur & Ann M. Graybiel, 2022. "Multiplexed action-outcome representation by striatal striosome-matrix compartments detected with a mouse cost-benefit foraging task," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    3. Huixin Lin & Jingfeng Zhou, 2024. "Hippocampal and orbitofrontal neurons contribute to complementary aspects of associative structure," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    4. Sravani Kondapavulur & Stefan M. Lemke & David Darevsky & Ling Guo & Preeya Khanna & Karunesh Ganguly, 2022. "Transition from predictable to variable motor cortex and striatal ensemble patterning during behavioral exploration," Nature Communications, Nature, vol. 13(1), pages 1-17, December.
    5. Nitzan Shahar & Tobias U Hauser & Michael Moutoussis & Rani Moran & Mehdi Keramati & NSPN consortium & Raymond J Dolan, 2019. "Improving the reliability of model-based decision-making estimates in the two-stage decision task with reaction-times and drift-diffusion modeling," PLOS Computational Biology, Public Library of Science, vol. 15(2), pages 1-25, February.
    6. Thomas Akam & Rui Costa & Peter Dayan, 2015. "Simple Plans or Sophisticated Habits? State, Transition and Learning Interactions in the Two-Step Task," PLOS Computational Biology, Public Library of Science, vol. 11(12), pages 1-25, December.

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