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Expectancy-related changes in firing of dopamine neurons depend on hippocampus

Author

Listed:
  • Zhewei Zhang

    (National Institute on Drug Abuse)

  • Yuji K. Takahashi

    (National Institute on Drug Abuse)

  • Marlian Montesinos-Cartegena

    (National Institute on Drug Abuse)

  • Thorsten Kahnt

    (National Institute on Drug Abuse)

  • Angela J. Langdon

    (National Institute on Mental Health)

  • Geoffrey Schoenbaum

    (National Institute on Drug Abuse)

Abstract

The orbitofrontal cortex (OFC) and hippocampus (HC) both contribute to the cognitive maps that support flexible behavior. Previously, we used the dopamine neurons to measure the functional role of OFC. We recorded midbrain dopamine neurons as rats performed an odor-based choice task, in which expected rewards were manipulated across blocks. We found that ipsilateral OFC lesions degraded dopaminergic prediction errors, consistent with reduced resolution of the task states. Here we have repeated this experiment in male rats with ipsilateral HC lesions. The results show HC also shapes the task states, however unlike OFC, which provides information local to the trial, the HC is necessary for estimating upper-level hidden states that distinguish blocks. The results contrast the roles of the OFC and HC in cognitive mapping and suggest that the dopamine neurons access rich information from distributed regions regarding the environment’s structure, potentially enabling this teaching signal to support complex behaviors.

Suggested Citation

  • Zhewei Zhang & Yuji K. Takahashi & Marlian Montesinos-Cartegena & Thorsten Kahnt & Angela J. Langdon & Geoffrey Schoenbaum, 2024. "Expectancy-related changes in firing of dopamine neurons depend on hippocampus," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-53308-z
    DOI: 10.1038/s41467-024-53308-z
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    References listed on IDEAS

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    1. Brad E. Pfeiffer & David J. Foster, 2013. "Hippocampal place-cell sequences depict future paths to remembered goals," Nature, Nature, vol. 497(7447), pages 74-79, May.
    2. Pascale Waelti & Anthony Dickinson & Wolfram Schultz, 2001. "Dopamine responses comply with basic assumptions of formal learning theory," Nature, Nature, vol. 412(6842), pages 43-48, July.
    3. 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.
    4. Masayuki Matsumoto & Okihide Hikosaka, 2009. "Two types of dopamine neuron distinctly convey positive and negative motivational signals," Nature, Nature, vol. 459(7248), pages 837-841, June.
    5. David J. Foster & Matthew A. Wilson, 2006. "Reverse replay of behavioural sequences in hippocampal place cells during the awake state," Nature, Nature, vol. 440(7084), pages 680-683, March.
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