Dopaminergic systems create reward seeking despite adverse consequences

Kristijan D. Jovanoski (), Lucille Duquenoy, Jessica Mitchell, Ishaan Kapoor, Christoph D. Treiber, Vincent Croset, Georgia Dempsey, Sai Parepalli, Paola Cognigni, Nils Otto, Johannes Felsenberg and Scott Waddell ()
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Kristijan D. Jovanoski: University of Oxford
Lucille Duquenoy: University of Oxford
Jessica Mitchell: University of Oxford
Ishaan Kapoor: University of Oxford
Christoph D. Treiber: University of Oxford
Vincent Croset: University of Oxford
Georgia Dempsey: University of Oxford
Sai Parepalli: University of Oxford
Paola Cognigni: University of Oxford
Nils Otto: University of Oxford
Johannes Felsenberg: University of Oxford
Scott Waddell: University of Oxford

Nature, 2023, vol. 623, issue 7986, 356-365

Abstract: Abstract Resource-seeking behaviours are ordinarily constrained by physiological needs and threats of danger, and the loss of these controls is associated with pathological reward seeking1. Although dysfunction of the dopaminergic valuation system of the brain is known to contribute towards unconstrained reward seeking2,3, the underlying reasons for this behaviour are unclear. Here we describe dopaminergic neural mechanisms that produce reward seeking despite adverse consequences in Drosophila melanogaster. Odours paired with optogenetic activation of a defined subset of reward-encoding dopaminergic neurons become cues that starved flies seek while neglecting food and enduring electric shock punishment. Unconstrained seeking of reward is not observed after learning with sugar or synthetic engagement of other dopaminergic neuron populations. Antagonism between reward-encoding and punishment-encoding dopaminergic neurons accounts for the perseverance of reward seeking despite punishment, whereas synthetic engagement of the reward-encoding dopaminergic neurons also impairs the ordinary need-dependent dopaminergic valuation of available food. Connectome analyses reveal that the population of reward-encoding dopaminergic neurons receives highly heterogeneous input, consistent with parallel representation of diverse rewards, and recordings demonstrate state-specific gating and satiety-related signals. We propose that a similar dopaminergic valuation system dysfunction is likely to contribute to maladaptive seeking of rewards by mammals.

Date: 2023
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DOI: 10.1038/s41586-023-06671-8

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