Enhanced olfactory memory performance in trap-design Y-mazes allows the study of novel memory phenotypes in<i>Drosophila</i>

Mohandasan, Radhika; Fm, Iqbal; Thakare, Manikrao; Sridharan, Madhav; Das, Gopal

doi:10.1101/2020.11.18.386128

Cited by 2 publications

(1 citation statement)

References 83 publications

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“…1). The design of this assay was inspired by an earlier behavior assay for flies (77)(78)(79)(80)(81) and foraging related 2AFC tasks in vertebrates (13)(14)(15)18). In our Y-arena, a single fly begins a trial in an arm filled with clean air and can choose between two odor cues that are randomly assigned to the other two arms (see Supp.…”

Section: Flies Can Learn Multiple Probabilistic Cue-reward Associationsmentioning

confidence: 99%

Reward expectations direct learning and drive operant matching inDrosophila

Rajagopalan

Darshan

Fitzgerald

et al. 2022

Preprint

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Foraging animals must use decision-making strategies that dynamically account for uncertainty in the world. To cope with this uncertainty, animals have developed strikingly convergent strategies that use information about multiple past choices and reward to learn representations of the current state of the world. However, the underlying learning rules that drive the required learning have remained unclear. Here, working in the relatively simple nervous system of Drosophila, we combine behavioral measurements, mathematical modeling, and neural circuit perturbations to show that dynamic foraging depends on a learning rule incorporating reward expectation. Using a novel olfactory dynamic foraging task, we characterize the behavioral strategies used by individual flies when faced with unpredictable rewards and show, for the first time, that they perform operant matching. We build on past theoretical work and demonstrate that this strategy requires the existence of a covariance-based learning rule in the mushroom body - a hub for learning in the fly. In particular, the behavioral consequences of optogenetic perturbation experiments suggest that this learning rule incorporates reward expectation. Our results identify a key element of the algorithm underlying dynamic foraging in flies and suggest a comprehensive mechanism that could be fundamental to these behaviors across species.

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Section: Flies Can Learn Multiple Probabilistic Cue-reward Associationsmentioning

confidence: 99%

Reward expectations direct learning and drive operant matching inDrosophila

Rajagopalan

Darshan

Fitzgerald

et al. 2022

Preprint

View full text Add to dashboard Cite

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Reward expectations direct learning and drive operant matching in Drosophila

Rajagopalan,

Darshan,

Hibbard

et al. 2023

Proc. Natl. Acad. Sci. U.S.A.

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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.

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Enhanced olfactory memory performance in trap-design Y-mazes allows the study of novel memory phenotypes inDrosophila

Cited by 2 publications

References 83 publications

Reward expectations direct learning and drive operant matching inDrosophila

Reward expectations direct learning and drive operant matching inDrosophila

Reward expectations direct learning and drive operant matching in Drosophila

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