From Prediction to Action: Dissociable Roles of Ventral Tegmental Area and Substantia Nigra Dopamine Neurons in Instrumental Reinforcement

Kurt M. Fraser, Heather J. Pribut, Patricia H. Janak, Ronald Keiflin

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

Reward seeking requires the coordination of motor programs to achieve goals. Midbrain dopamine neurons are critical for reinforcement, and their activation is sufficient for learning about cues, actions, and outcomes. Here we examine in detail the mechanisms underlying the ability of ventral tegmental area (VTA) and substantia nigra (SNc) dopamine neurons to support instrumental learning. By exploiting numerous behavioral tasks in combination with time-limited optogenetic manipulations in male and female rats, we reveal that VTA and SNc dopamine neurons generate reinforcement through separable psychological processes. VTA dopamine neurons imbue actions and their associated cues with motivational value that allows flexible and persistent pursuit, whereas SNc dopamine neurons support time-limited, precise, action-specific learning that is nonscalable and inflexible. This architecture is reminiscent of actor–critic reinforcement learning models with VTA and SNc instructing the critic and actor, respectively. Our findings indicate that heterogeneous dopamine systems support unique forms of instrumental learning that ultimately result in disparate reward-seeking strategies.

Original languageEnglish (US)
Pages (from-to)3895-3908
Number of pages14
JournalJournal of Neuroscience
Volume43
Issue number21
DOIs
StatePublished - May 24 2023
Externally publishedYes

Bibliographical note

Publisher Copyright:
Copyright © 2023 the authors.

Keywords

  • ICSS
  • dopamine
  • motivation
  • operant conditioning
  • reinforcement
  • reward

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