Reward expectations direct learning and drive operant matching in Drosophila

Adithya E. Rajagopalan, Ran Darshan, Karen L. Hibbard, James E. Fitzgerald, Glenn C. Turner*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Foraging animals must use decision-making strategies that dynamically adapt to the changing availability of rewards in the environment. A wide diversity of animals do this by distributing their choices in proportion to the rewards received from each option, Herrnstein’s operant matching law. Theoretical work suggests an elegant mechanistic explanation for this ubiquitous behavior, as operant matching follows automatically from simple synaptic plasticity rules acting within behaviorally relevant neural circuits. However, no past work has mapped operant matching onto plasticity mechanisms in the brain, leaving the biological relevance of the theory unclear. Here, we discovered operant matching in Drosophila and showed that it requires synaptic plasticity that acts in the mushroom body and incorporates the expectation of reward. We began by developing a dynamic foraging paradigm to measure choices from individual flies as they learn to associate odor cues with probabilistic rewards. We then built a model of the fly mushroom body to explain each fly’s sequential choice behavior using a family of biologically realistic synaptic plasticity rules. As predicted by past theoretical work, we found that synaptic plasticity rules could explain fly matching behavior by incorporating stimulus expectations, reward expectations, or both. However, by optogenetically bypassing the representation of reward expectation, we abolished matching behavior and showed that the plasticity rule must specifically incorporate reward expectations. Altogether, these results reveal the first synapse-level mechanisms of operant matching and provide compelling evidence for the role of reward expectation signals in the fly brain.

Original languageEnglish (US)
Article numbere2221415120
JournalProceedings of the National Academy of Sciences of the United States of America
Volume120
Issue number39
DOIs
StatePublished - 2023

Keywords

  • decision-making
  • dopamine
  • foraging
  • learning-rules
  • mushroom body

ASJC Scopus subject areas

  • General

Fingerprint

Dive into the research topics of 'Reward expectations direct learning and drive operant matching in Drosophila'. Together they form a unique fingerprint.

Cite this