IDEAS home Printed from https://ideas.repec.org/a/nat/nature/v621y2023i7979d10.1038_s41586-023-06492-9.html
   My bibliography  Save this article

Dopamine and glutamate regulate striatal acetylcholine in decision-making

Author

Listed:
  • Lynne Chantranupong

    (Harvard Medical School)

  • Celia C. Beron

    (Harvard Medical School)

  • Joshua A. Zimmer

    (Harvard Medical School)

  • Michelle J. Wen

    (Harvard Medical School)

  • Wengang Wang

    (Harvard Medical School)

  • Bernardo L. Sabatini

    (Harvard Medical School)

Abstract

Striatal dopamine and acetylcholine are essential for the selection and reinforcement of motor actions and decision-making1. In vitro studies have revealed an intrastriatal circuit in which acetylcholine, released by cholinergic interneurons (CINs), drives the release of dopamine, and dopamine, in turn, inhibits the activity of CINs through dopamine D2 receptors (D2Rs). Whether and how this circuit contributes to striatal function in vivo is largely unknown. Here, to define the role of this circuit in a living system, we monitored acetylcholine and dopamine signals in the ventrolateral striatum of mice performing a reward-based decision-making task. We establish that dopamine and acetylcholine exhibit multiphasic and anticorrelated transients that are modulated by decision history and reward outcome. Dopamine dynamics and reward encoding do not require the release of acetylcholine by CINs. However, dopamine inhibits acetylcholine transients in a D2R-dependent manner, and loss of this regulation impairs decision-making. To determine how other striatal inputs shape acetylcholine signals, we assessed the contribution of cortical and thalamic projections, and found that glutamate release from both sources is required for acetylcholine release. Altogether, we uncover a dynamic relationship between dopamine and acetylcholine during decision-making, and reveal multiple modes of CIN regulation. These findings deepen our understanding of the neurochemical basis of decision-making and behaviour.

Suggested Citation

  • Lynne Chantranupong & Celia C. Beron & Joshua A. Zimmer & Michelle J. Wen & Wengang Wang & Bernardo L. Sabatini, 2023. "Dopamine and glutamate regulate striatal acetylcholine in decision-making," Nature, Nature, vol. 621(7979), pages 577-585, September.
  • Handle: RePEc:nat:nature:v:621:y:2023:i:7979:d:10.1038_s41586-023-06492-9
    DOI: 10.1038/s41586-023-06492-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41586-023-06492-9
    File Function: Abstract
    Download Restriction: Access to the full text of the articles in this series is restricted.

    File URL: https://libkey.io/10.1038/s41586-023-06492-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    As the access to this document is restricted, you may want to search for a different version of it.

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Min Jung Kim & Daniel J. Gibson & Dan Hu & Tomoko Yoshida & Emily Hueske & Ayano Matsushima & Ara Mahar & Cynthia J. Schofield & Patlapa Sompolpong & Kathy T. Tran & Lin Tian & Ann M. Graybiel, 2024. "Dopamine release plateau and outcome signals in dorsal striatum contrast with classic reinforcement learning formulations," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    2. Xiaolong Gao & Huan Wei & Wenjie Ma & Wenjie Wu & Wenliang Ji & Junjie Mao & Ping Yu & Lanqun Mao, 2024. "Inflammation-free electrochemical in vivo sensing of dopamine with atomic-level engineered antioxidative single-atom catalyst," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    3. Lior Matityahu & Naomi Gilin & Gideon A. Sarpong & Yara Atamna & Lior Tiroshi & Nicolas X. Tritsch & Jeffery R. Wickens & Joshua A. Goldberg, 2023. "Acetylcholine waves and dopamine release in the striatum," Nature Communications, Nature, vol. 14(1), pages 1-23, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:nature:v:621:y:2023:i:7979:d:10.1038_s41586-023-06492-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    We have no bibliographic references for this item. You can help adding them by using this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.