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Two types of dopamine neuron distinctly convey positive and negative motivational signals

Author

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  • Masayuki Matsumoto

    (Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435, USA)

  • Okihide Hikosaka

    (Laboratory of Sensorimotor Research, National Eye Institute, National Institutes of Health, Bethesda, Maryland 20892-4435, USA)

Abstract

Dopamine neuron complexity Dopamine neurons at the base of the brain are crucial for normal motor behaviour, and their loss leads to conditions such as Parkinson's disease. Yet the activity of dopamine neurons is not related to body movements, but to reward events. Recent theories suggest that dopamine neurons, as a homogeneous functional group, guide motor learning via reward-related signals. Now a study in monkeys undergoing Pavlovian conditioning to 'positive' and 'negative' stimuli shows that dopamine neurons are more heterogeneous than this model implies. Different groups of dopamine neurons, located in slightly different areas of the brain, have specific responses to pleasant and unpleasant stimuli, as well as to the trigger stimuli associated with these events. This suggests that dopamine neurons have a more complex involvement in learning control, encoding more subtle signals than simple reward.

Suggested Citation

  • 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.
  • Handle: RePEc:nat:nature:v:459:y:2009:i:7248:d:10.1038_nature08028
    DOI: 10.1038/nature08028
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    1. Laura Alice Santos de Oliveira & Luís Aureliano Imbiriba & Maitê Mello Russo & Anaelli A Nogueira-Campos & Erika de C Rodrigues & Mirtes G Pereira & Eliane Volchan & Cláudia Domingues Vargas, 2012. "Preparing to Grasp Emotionally Laden Stimuli," PLOS ONE, Public Library of Science, vol. 7(9), pages 1-7, September.
    2. Colin W. Hoy & David R. Quiroga-Martinez & Eduardo Sandoval & David King-Stephens & Kenneth D. Laxer & Peter Weber & Jack J. Lin & Robert T. Knight, 2023. "Asymmetric coding of reward prediction errors in human insula and dorsomedial prefrontal cortex," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    3. 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.
    4. Ali Ghazizadeh & Okihide Hikosaka, 2022. "Salience memories formed by value, novelty and aversiveness jointly shape object responses in the prefrontal cortex and basal ganglia," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    5. Johannes Rentzsch & Christina Shen & Maria C Jockers-Scherübl & Jürgen Gallinat & Andres H Neuhaus, 2015. "Auditory Mismatch Negativity and Repetition Suppression Deficits in Schizophrenia Explained by Irregular Computation of Prediction Error," PLOS ONE, Public Library of Science, vol. 10(5), pages 1-11, May.
    6. 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.
    7. Huanyuan Zhou & KongFatt Wong-Lin & Da-Hui Wang, 2018. "Parallel Excitatory and Inhibitory Neural Circuit Pathways Underlie Reward-Based Phasic Neural Responses," Complexity, Hindawi, vol. 2018, pages 1-20, April.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. 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.
    13. Paul Leon Brown & Paul D Shepard, 2013. "Lesions of the Fasciculus Retroflexus Alter Footshock-Induced cFos Expression in the Mesopontine Rostromedial Tegmental Area of Rats," PLOS ONE, Public Library of Science, vol. 8(4), pages 1-9, April.
    14. 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.
    15. Abigail Kalmbach & Vanessa Winiger & Nuri Jeong & Arun Asok & Charles R. Gallistel & Peter D. Balsam & Eleanor H. Simpson, 2022. "Dopamine encodes real-time reward availability and transitions between reward availability states on different timescales," Nature Communications, Nature, vol. 13(1), pages 1-13, December.

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