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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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    2. 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.
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    9. 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.
    10. Harris E. Blankenship & Kelsey A. Carter & Kevin D. Pham & Nina T. Cassidy & Andrea N. Markiewicz & Michael I. Thellmann & Amanda L. Sharpe & Willard M. Freeman & Michael J. Beckstead, 2024. "VTA dopamine neurons are hyperexcitable in 3xTg-AD mice due to casein kinase 2-dependent SK channel dysfunction," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. 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.
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    14. 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.
    15. 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.
    16. 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.
    17. 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.
    18. 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.
    19. 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.
    20. 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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