IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-023-44358-w.html
   My bibliography  Save this article

Dopamine release in human associative striatum during reversal learning

Author

Listed:
  • Filip Grill

    (Umeå University
    Umeå Center for Functional Brain Imaging, Umeå University)

  • Marc Guitart-Masip

    (Karolinska Institutet
    Center for Psychiatry Research, Region Stockholm
    Karolinska Institutet
    University College London)

  • Jarkko Johansson

    (Umeå University
    Umeå Center for Functional Brain Imaging, Umeå University)

  • Lars Stiernman

    (Umeå Center for Functional Brain Imaging, Umeå University
    Umeå University)

  • Jan Axelsson

    (Umeå Center for Functional Brain Imaging, Umeå University
    Umeå University)

  • Lars Nyberg

    (Umeå University
    Umeå Center for Functional Brain Imaging, Umeå University
    Umeå University)

  • Anna Rieckmann

    (Umeå University
    Umeå Center for Functional Brain Imaging, Umeå University
    Umeå University
    University of the Bundeswehr Munich)

Abstract

The dopaminergic system is firmly implicated in reversal learning but human measurements of dopamine release as a correlate of reversal learning success are lacking. Dopamine release and hemodynamic brain activity in response to unexpected changes in action-outcome probabilities are here explored using simultaneous dynamic [11C]Raclopride PET-fMRI and computational modelling of behavior. When participants encounter reversed reward probabilities during a card guessing game, dopamine release is observed in associative striatum. Individual differences in absolute reward prediction error and sensitivity to errors are associated with peak dopamine receptor occupancy. The fMRI response to perseverance errors at the onset of a reversal spatially overlap with the site of dopamine release. Trial-by-trial fMRI correlates of absolute prediction errors show a response in striatum and association cortices, closely overlapping with the location of dopamine release, and separable from a valence signal in ventral striatum. The results converge to implicate striatal dopamine release in associative striatum as a central component of reversal learning, possibly signifying the need for increased cognitive control when new stimuli-responses should be learned.

Suggested Citation

  • Filip Grill & Marc Guitart-Masip & Jarkko Johansson & Lars Stiernman & Jan Axelsson & Lars Nyberg & Anna Rieckmann, 2024. "Dopamine release in human associative striatum during reversal learning," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44358-w
    DOI: 10.1038/s41467-023-44358-w
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-44358-w
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-44358-w?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
    ---><---

    References listed on IDEAS

    as
    1. Mathias Pessiglione & Ben Seymour & Guillaume Flandin & Raymond J. Dolan & Chris D. Frith, 2006. "Dopamine-dependent prediction errors underpin reward-seeking behaviour in humans," Nature, Nature, vol. 442(7106), pages 1042-1045, August.
    2. Ruben Bosch & Britt Lambregts & Jessica Määttä & Lieke Hofmans & Danae Papadopetraki & Andrew Westbrook & Robbert-Jan Verkes & Jan Booij & Roshan Cools, 2022. "Striatal dopamine dissociates methylphenidate effects on value-based versus surprise-based reversal learning," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Hanan Shteingart & Tal Neiman & Yonatan Loewenstein, 2012. "The Role of First Impression in Operant Learning," Discussion Paper Series dp626, The Federmann Center for the Study of Rationality, the Hebrew University, Jerusalem.
    2. Kuhnen, Camelia M. & Miu, Andrei C., 2017. "Socioeconomic status and learning from financial information," Journal of Financial Economics, Elsevier, vol. 124(2), pages 349-372.
    3. Hiroyuki Kawai & Youcef Bouchekioua & Naoya Nishitani & Kazuhei Niitani & Shoma Izumi & Hinako Morishita & Chihiro Andoh & Yuma Nagai & Masashi Koda & Masako Hagiwara & Koji Toda & Hisashi Shirakawa &, 2022. "Median raphe serotonergic neurons projecting to the interpeduncular nucleus control preference and aversion," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    4. Dimitrije Marković & Andrea M F Reiter & Stefan J Kiebel, 2019. "Predicting change: Approximate inference under explicit representation of temporal structure in changing environments," PLOS Computational Biology, Public Library of Science, vol. 15(1), pages 1-31, January.
    5. Reimann, Martin & Bechara, Antoine, 2010. "The somatic marker framework as a neurological theory of decision-making: Review, conceptual comparisons, and future neuroeconomics research," Journal of Economic Psychology, Elsevier, vol. 31(5), pages 767-776, October.
    6. George I. Christopoulos & Xiao-Xiao Liu & Ying-yi Hong, 2017. "Toward an Understanding of Dynamic Moral Decision Making: Model-Free and Model-Based Learning," Journal of Business Ethics, Springer, vol. 144(4), pages 699-715, September.
    7. Maël Lebreton & Karin Bacily & Stefano Palminteri & Jan B Engelmann, 2019. "Contextual influence on confidence judgments in human reinforcement learning," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-27, April.
    8. Yosuke Yawata & Yu Shikano & Jun Ogasawara & Kenichi Makino & Tetsuhiko Kashima & Keiko Ihara & Airi Yoshimoto & Shota Morikawa & Sho Yagishita & Kenji F. Tanaka & Yuji Ikegaya, 2023. "Mesolimbic dopamine release precedes actively sought aversive stimuli in mice," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    9. Kazutaka Maeda & Ken-ichi Inoue & Masahiko Takada & Okihide Hikosaka, 2023. "Environmental context-dependent activation of dopamine neurons via putative amygdala-nigra pathway in macaques," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    10. Torben Ott & Anna Marlina Stein & Andreas Nieder, 2023. "Dopamine receptor activation regulates reward expectancy signals during cognitive control in primate prefrontal neurons," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    11. Kuhnen, Camelia M. & Knutson, Brian, 2011. "The Influence of Affect on Beliefs, Preferences, and Financial Decisions," Journal of Financial and Quantitative Analysis, Cambridge University Press, vol. 46(3), pages 605-626, June.
    12. Bruno B Averbeck, 2015. "Theory of Choice in Bandit, Information Sampling and Foraging Tasks," PLOS Computational Biology, Public Library of Science, vol. 11(3), pages 1-28, March.
    13. Karima Chakroun & Antonius Wiehler & Ben Wagner & David Mathar & Florian Ganzer & Thilo Eimeren & Tobias Sommer & Jan Peters, 2023. "Dopamine regulates decision thresholds in human reinforcement learning in males," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    14. Xin-Yue Wang & Wen-Bin Jia & Xiang Xu & Rui Chen & Liang-Biao Wang & Xiao-Jing Su & Peng-Fei Xu & Xiao-Qing Liu & Jie Wen & Xiao-Yuan Song & Yuan-Yuan Liu & Zhi Zhang & Xin-Feng Liu & Yan Zhang, 2023. "A glutamatergic DRN–VTA pathway modulates neuropathic pain and comorbid anhedonia-like behavior in mice," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    15. Stefano Palminteri & Emma J Kilford & Giorgio Coricelli & Sarah-Jayne Blakemore, 2016. "The Computational Development of Reinforcement Learning during Adolescence," PLOS Computational Biology, Public Library of Science, vol. 12(6), pages 1-25, June.
    16. Ruben Bosch & Britt Lambregts & Jessica Määttä & Lieke Hofmans & Danae Papadopetraki & Andrew Westbrook & Robbert-Jan Verkes & Jan Booij & Roshan Cools, 2022. "Striatal dopamine dissociates methylphenidate effects on value-based versus surprise-based reversal learning," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    17. Paul M Bays & Ben A Dowding, 2017. "Fidelity of the representation of value in decision-making," PLOS Computational Biology, Public Library of Science, vol. 13(3), pages 1-16, March.
    18. Antoine Collomb-Clerc & Maëlle C. M. Gueguen & Lorella Minotti & Philippe Kahane & Vincent Navarro & Fabrice Bartolomei & Romain Carron & Jean Regis & Stephan Chabardès & Stefano Palminteri & Julien B, 2023. "Human thalamic low-frequency oscillations correlate with expected value and outcomes during reinforcement learning," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    19. David Vaquero-Puyuelo & Concepción De-la-Cámara & Beatriz Olaya & Patricia Gracia-García & Antonio Lobo & Raúl López-Antón & Javier Santabárbara, 2021. "Anhedonia as a Potential Risk Factor of Alzheimer’s Disease in a Community-Dwelling Elderly Sample: Results from the ZARADEMP Project," IJERPH, MDPI, vol. 18(4), pages 1-12, February.
    20. Sophie Massin, 2011. "La notion d'addiction en économie : La théorie du choix rationnel à l'épreuve," Revue d'économie politique, Dalloz, vol. 121(5), pages 713-750.

    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:natcom:v:15:y:2024:i:1:d:10.1038_s41467-023-44358-w. 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.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with 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.