Dopamine release plateau and outcome signals in dorsal striatum contrast with classic reinforcement learning formulations

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 and Ann M. Graybiel ()
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Min Jung Kim: Massachusetts Institute of Technology
Daniel J. Gibson: Massachusetts Institute of Technology
Dan Hu: Massachusetts Institute of Technology
Tomoko Yoshida: Massachusetts Institute of Technology
Emily Hueske: Massachusetts Institute of Technology
Ayano Matsushima: Massachusetts Institute of Technology
Ara Mahar: Massachusetts Institute of Technology
Cynthia J. Schofield: Massachusetts Institute of Technology
Patlapa Sompolpong: Massachusetts Institute of Technology
Kathy T. Tran: Massachusetts Institute of Technology
Lin Tian: Max Planck Florida Institute for Neuroscience
Ann M. Graybiel: Massachusetts Institute of Technology

Nature Communications, 2024, vol. 15, issue 1, 1-20

Abstract: Abstract We recorded dopamine release signals in centromedial and centrolateral sectors of the striatum as mice learned consecutive versions of visual cue-outcome conditioning tasks. Dopamine release responses differed for the centromedial and centrolateral sites. In neither sector could these be accounted for by classic reinforcement learning alone as classically applied to the activity of nigral dopamine-containing neurons. Medially, cue responses ranged from initial sharp peaks to modulated plateau responses; outcome (reward) responses during cue conditioning were minimal or, initially, negative. At centrolateral sites, by contrast, strong, transient dopamine release responses occurred at both cue and outcome. Prolonged, plateau release responses to cues emerged in both regions when discriminative behavioral responses became required. At most sites, we found no evidence for a transition from outcome signaling to cue signaling, a hallmark of temporal difference reinforcement learning as applied to midbrain dopaminergic neuronal activity. These findings delineate a reshaping of striatal dopamine release activity during learning and suggest that current views of reward prediction error encoding need review to accommodate distinct learning-related spatial and temporal patterns of striatal dopamine release in the dorsal striatum.

Date: 2024
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DOI: 10.1038/s41467-024-53176-7

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