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

Molina-García, Laura, Colinas-Fischer, Susana, Benavides-Laconcha, Sergio, Lin, Lucy, Clark, Emma, Treloar, Neythen J., García-Minaur-Ortíz, Blanca, Butts, Milly, Barnes, Chris P. and Barrios, Arantza 2024. Conflict during learning reconfigures the neural representation of positive valence and approach behavior. Current Biology 34 (23) , pp. 5470-5483. 10.1016/j.cub.2024.10.024

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Abstract

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.

Item Type:	Article
Date Type:	Publication
Status:	Published
Schools:	Psychology
Publisher:	Elsevier
ISSN:	0960-9822
Date of First Compliant Deposit:	3 February 2025
Date of Acceptance:	8 October 2024
Last Modified:	03 Feb 2025 16:59
URI:	https://orca.cardiff.ac.uk/id/eprint/175856

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