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

Punishing and rewarding experiences can change the valence of sensory stimuli and guide animal behavior 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 behavioral decision? We address this question by dissecting a circuit for sexual conditioning in C. elegans. In this learning paradigm, an odor is conditioned with both a punishment (starvation) and a reward (mates), resulting in odor approach. We find that negative and positive experiences are both encoded by the neuropeptide pigment dispersing factor 1 (PDF-1) being released from, and acting on, different neurons. Each experience creates a distinct memory in the circuit for odor processing. This results in the sensorimotor representation of the odor 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. [Display omitted] •Aversive and rewarding experiences are both encoded by PDF-1 neuromodulation•When presented together, each experience generates a distinct memory•Positive valence can be encoded by more than one pattern of neural activity•Stimulus valence is represented according to stimulus prediction How are positive and negative experiences integrated during learning? Here, Molina-García, Colinas-Fischer, et al. find that the neuropeptide PDF-1 encodes both experiences by being released from and acting on different cells. Each experience generates a co-existing memory, and this changes the neural representation of positive valence.