Dopaminergic mechanism underlying reward-encoding of punishment omission during reversal learning in Drosophila

Li Yan McCurdy, Preeti Sareen, Pasha A. Davoudian and Michael N. Nitabach ()
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Li Yan McCurdy: Yale University
Preeti Sareen: Yale University
Pasha A. Davoudian: Yale University
Michael N. Nitabach: Yale University

Nature Communications, 2021, vol. 12, issue 1, 1-17

Abstract: Abstract Animals form and update learned associations between otherwise neutral sensory cues and aversive outcomes (i.e., punishment) to predict and avoid danger in changing environments. When a cue later occurs without punishment, this unexpected omission of aversive outcome is encoded as reward via activation of reward-encoding dopaminergic neurons. How such activation occurs remains unknown. Using real-time in vivo functional imaging, optogenetics, behavioral analysis and synaptic reconstruction from electron microscopy data, we identify the neural circuit mechanism through which Drosophila reward-encoding dopaminergic neurons are activated when an olfactory cue is unexpectedly no longer paired with electric shock punishment. Reduced activation of punishment-encoding dopaminergic neurons relieves depression of olfactory synaptic inputs to cholinergic neurons. Synaptic excitation by these cholinergic neurons of reward-encoding dopaminergic neurons increases their odor response, thus decreasing aversiveness of the odor. These studies reveal how an excitatory cholinergic relay from punishment- to reward-encoding dopaminergic neurons encodes the absence of punishment as reward, revealing a general circuit motif for updating aversive memories that could be present in mammals.

Date: 2021
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DOI: 10.1038/s41467-021-21388-w

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