Conflict during learning reconfigures the neural representation of positive valence and approach behaviour

Abstract

Punishing and rewarding experiences can change the valence of sensory stimuli and guide animal behaviour in opposite directions, resulting in avoidance or approach. Often, however, a stimulus is encountered with both positive and negative experiences. How is such conflicting information represented in the brain and resolved into a behavioural decision? We address this question by dissecting a circuit for sexual conditioning in C. elegans. In this learning paradigm, an odour is conditioned with both a punishment (starvation) and a reward (mates) resulting in odour approach. We find that negative and positive experiences are both encoded by the neuropeptide PDF-1 being released from and acting on different neurons. Each experience creates a separate, parallel memory in the circuit for odour processing. This results in the sensorimotor representation of odour being different in naive and sexually conditioned animals despite both displaying approach. Our results reveal that the positive valence of a stimulus is not represented in the activity of any single neuron class but flexibly represented within the circuit according to the experiences and predictions associated with the stimulus.