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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; ... Barrios, Arantza; + view all (2024) Conflict during learning reconfigures the neural representation of positive valence and approach behavior. Current Biology , 34 (23) 5470-5483.e7. 10.1016/j.cub.2024.10.024. Green open access

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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.

Type: Article
Title: Conflict during learning reconfigures the neural representation of positive valence and approach behavior
Location: England
Open access status: An open access version is available from UCL Discovery
DOI: 10.1016/j.cub.2024.10.024
Publisher version: https://doi.org/10.1016/j.cub.2024.10.024
Language: English
Additional information: Copyright © 2024 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
Keywords: Valence; neuromodulation; neuropeptide; learning; reward; aversion; conditioning; C. elegans; PDF; memory; engram
UCL classification: UCL
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences
UCL > Provost and Vice Provost Offices > School of Life and Medical Sciences > Faculty of Life Sciences > Div of Biosciences > Cell and Developmental Biology
URI: https://discovery.ucl.ac.uk/id/eprint/10201541
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