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Dissociable dopamine dynamics for learning and motivation

Author

Listed:
  • Ali Mohebi

    (University of California, San Francisco)

  • Jeffrey R. Pettibone

    (University of California, San Francisco)

  • Arif A. Hamid

    (Brown University)

  • Jenny-Marie T. Wong

    (University of Michigan)

  • Leah T. Vinson

    (University of California, San Francisco)

  • Tommaso Patriarchi

    (University of California, Davis)

  • Lin Tian

    (University of California, Davis)

  • Robert T. Kennedy

    (University of Michigan)

  • Joshua D. Berke

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

Abstract

The dopamine projection from ventral tegmental area (VTA) to nucleus accumbens (NAc) is critical for motivation to work for rewards and reward-driven learning. How dopamine supports both functions is unclear. Dopamine cell spiking can encode prediction errors, which are vital learning signals in computational theories of adaptive behaviour. By contrast, dopamine release ramps up as animals approach rewards, mirroring reward expectation. This mismatch might reflect differences in behavioural tasks, slower changes in dopamine cell spiking or spike-independent modulation of dopamine release. Here we compare spiking of identified VTA dopamine cells with NAc dopamine release in the same decision-making task. Cues that indicate an upcoming reward increased both spiking and release. However, NAc core dopamine release also covaried with dynamically evolving reward expectations, without corresponding changes in VTA dopamine cell spiking. Our results suggest a fundamental difference in how dopamine release is regulated to achieve distinct functions: broadcast burst signals promote learning, whereas local control drives motivation.

Suggested Citation

  • Ali Mohebi & Jeffrey R. Pettibone & Arif A. Hamid & Jenny-Marie T. Wong & Leah T. Vinson & Tommaso Patriarchi & Lin Tian & Robert T. Kennedy & Joshua D. Berke, 2019. "Dissociable dopamine dynamics for learning and motivation," Nature, Nature, vol. 570(7759), pages 65-70, June.
  • Handle: RePEc:nat:nature:v:570:y:2019:i:7759:d:10.1038_s41586-019-1235-y
    DOI: 10.1038/s41586-019-1235-y
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    Cited by:

    1. Seetha Krishnan & Chad Heer & Chery Cherian & Mark E. J. Sheffield, 2022. "Reward expectation extinction restructures and degrades CA1 spatial maps through loss of a dopaminergic reward proximity signal," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    2. Zengpeng Han & Nengsong Luo & Wenyu Ma & Xiaodong Liu & Yuxiang Cai & Jiaxin Kou & Jie Wang & Lei Li & Siqi Peng & Zihong Xu & Wen Zhang & Yuxiang Qiu & Yang Wu & Chaohui Ye & Kunzhang Lin & Fuqiang X, 2023. "AAV11 enables efficient retrograde targeting of projection neurons and enhances astrocyte-directed transduction," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Susanne Prokop & Péter Ábrányi-Balogh & Benjámin Barti & Márton Vámosi & Miklós Zöldi & László Barna & Gabriella M. Urbán & András Dávid Tóth & Barna Dudok & Attila Egyed & Hui Deng & Gian Marco Leggi, 2021. "PharmacoSTORM nanoscale pharmacology reveals cariprazine binding on Islands of Calleja granule cells," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    4. Carole Morel & Sarah E. Montgomery & Long Li & Romain Durand-de Cuttoli & Emily M. Teichman & Barbara Juarez & Nikos Tzavaras & Stacy M. Ku & Meghan E. Flanigan & Min Cai & Jessica J. Walsh & Scott J., 2022. "Midbrain projection to the basolateral amygdala encodes anxiety-like but not depression-like behaviors," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    5. Marie A. Labouesse & Maria Wilhelm & Zacharoula Kagiampaki & Andrew G. Yee & Raphaelle Denis & Masaya Harada & Andrea Gresch & Alina-Măriuca Marinescu & Kanako Otomo & Sebastiano Curreli & Laia Serrat, 2024. "A chemogenetic approach for dopamine imaging with tunable sensitivity," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    6. Johannes Algermissen & Jennifer C. Swart & René Scheeringa & Roshan Cools & Hanneke E. M. den Ouden, 2024. "Prefrontal signals precede striatal signals for biased credit assignment in motivational learning biases," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    7. 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.
    8. Allen P. F. Chen & Jeffrey M. Malgady & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Joshua L. Plotkin & Shaoyu Ge & Qiaojie Xiong, 2022. "Nigrostriatal dopamine pathway regulates auditory discrimination behavior," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. 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.
    10. Miguel Skirzewski & Oren Princz-Lebel & Liliana German-Castelan & Alycia M. Crooks & Gerard Kyungwook Kim & Sophie Henke Tarnow & Amy Reichelt & Sara Memar & Daniel Palmer & Yulong Li & R. Jane Rylett, 2022. "Continuous cholinergic-dopaminergic updating in the nucleus accumbens underlies approaches to reward-predicting cues," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    11. Han Guo & Jian-Bo Jiang & Wei Xu & Mu-Tian Zhang & Hui Chen & Huan-Ying Shi & Lu Wang & Miao He & Michael Lazarus & Shan-Qun Li & Zhi-Li Huang & Wei-Min Qu, 2023. "Parasubthalamic calretinin neurons modulate wakefulness associated with exploration in male mice," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Angela M. Ianni & Daniel P. Eisenberg & Erie D. Boorman & Sara M. Constantino & Catherine E. Hegarty & Michael D. Gregory & Joseph C. Masdeu & Philip D. Kohn & Timothy E. Behrens & Karen F. Berman, 2023. "PET-measured human dopamine synthesis capacity and receptor availability predict trading rewards and time-costs during foraging," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. Lauren Faget & Lucie Oriol & Wen-Chun Lee & Vivien Zell & Cody Sargent & Andrew Flores & Nick G. Hollon & Dhakshin Ramanathan & Thomas S. Hnasko, 2024. "Ventral pallidum GABA and glutamate neurons drive approach and avoidance through distinct modulation of VTA cell types," Nature Communications, Nature, vol. 15(1), pages 1-18, 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. Armando G. Salinas & Jeong Oen Lee & Shana M. Augustin & Shiliang Zhang & Tommaso Patriarchi & Lin Tian & Marisela Morales & Yolanda Mateo & David M. Lovinger, 2023. "Distinct sub-second dopamine signaling in dorsolateral striatum measured by a genetically-encoded fluorescent sensor," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    16. Laurens Winkelmeier & Carla Filosa & Renée Hartig & Max Scheller & Markus Sack & Jonathan R. Reinwald & Robert Becker & David Wolf & Martin Fungisai Gerchen & Alexander Sartorius & Andreas Meyer-Linde, 2022. "Striatal hub of dynamic and stabilized prediction coding in forebrain networks for olfactory reinforcement learning," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    17. 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.
    18. Allen P. F. Chen & Lu Chen & Kaiyo W. Shi & Eileen Cheng & Shaoyu Ge & Qiaojie Xiong, 2023. "Nigrostriatal dopamine modulates the striatal-amygdala pathway in auditory fear conditioning," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    19. 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.

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