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

By Li Yan McCurdy, Preeti Sareen, Pasha A Davoudian, M. Nitabach. 2021

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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. Unexpected omission of aversive outcome is encoded as reward via activation of reward-encoding dopaminergic neurons in animals. The authors identify the Drosophila neural circuit through which reward-encoding dopaminergic neurons are activated when an olfactory cue is no longer paired with punishment.

Subfields: Cellular and Molecular Neuroscience, Ecology, Evolution, Behavior and Systematics, Genetics