Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons

Abstract The nucleus accumbens (NAc) is a key brain region for motivated behaviors, yet how distinct neuronal populations encode appetitive or aversive stimuli remains undetermined. Using microendoscopic calcium imaging in mice, we tracked NAc shell D1- or D2-medium spiny neurons’ (MSNs) activity du...

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Main Authors: Ana Verónica Domingues, Tawan T. A. Carvalho, Gabriela J. Martins, Raquel Correia, Bárbara Coimbra, Ricardo Bastos-Gonçalves, Marcelina Wezik, Rita Gaspar, Luísa Pinto, Nuno Sousa, Rui M. Costa, Carina Soares-Cunha, Ana João Rodrigues
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55269-9
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author Ana Verónica Domingues
Tawan T. A. Carvalho
Gabriela J. Martins
Raquel Correia
Bárbara Coimbra
Ricardo Bastos-Gonçalves
Marcelina Wezik
Rita Gaspar
Luísa Pinto
Nuno Sousa
Rui M. Costa
Carina Soares-Cunha
Ana João Rodrigues
author_facet Ana Verónica Domingues
Tawan T. A. Carvalho
Gabriela J. Martins
Raquel Correia
Bárbara Coimbra
Ricardo Bastos-Gonçalves
Marcelina Wezik
Rita Gaspar
Luísa Pinto
Nuno Sousa
Rui M. Costa
Carina Soares-Cunha
Ana João Rodrigues
author_sort Ana Verónica Domingues
collection DOAJ
description Abstract The nucleus accumbens (NAc) is a key brain region for motivated behaviors, yet how distinct neuronal populations encode appetitive or aversive stimuli remains undetermined. Using microendoscopic calcium imaging in mice, we tracked NAc shell D1- or D2-medium spiny neurons’ (MSNs) activity during exposure to stimuli of opposing valence and associative learning. Despite drift in individual neurons’ coding, both D1- and D2-population activity was sufficient to discriminate opposing valence unconditioned stimuli, but not predictive cues. Notably, D1- and D2-MSNs were similarly co-recruited during appetitive and aversive conditioning, supporting a concurrent role in associative learning. Conversely, when contingencies changed, there was an asymmetric response in the NAc, with more pronounced changes in the activity of D2-MSNs. Optogenetic manipulation of D2-MSNs provided causal evidence of the necessity of this population in the extinction of aversive associations. Our results reveal how NAc shell neurons encode valence, Pavlovian associations and their extinction, and unveil mechanisms underlying motivated behaviors.
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spelling doaj-art-3de549da099b4954be16fa8c1bd0f99d2025-01-05T12:40:08ZengNature PortfolioNature Communications2041-17232025-01-0116112010.1038/s41467-024-55269-9Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neuronsAna Verónica Domingues0Tawan T. A. Carvalho1Gabriela J. Martins2Raquel Correia3Bárbara Coimbra4Ricardo Bastos-Gonçalves5Marcelina Wezik6Rita Gaspar7Luísa Pinto8Nuno Sousa9Rui M. Costa10Carina Soares-Cunha11Ana João Rodrigues12Life and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoZuckerman Mind Brain Behavior Institute at Columbia UniversityLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoZuckerman Mind Brain Behavior Institute at Columbia UniversityLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoLife and Health Sciences Research Institute (ICVS), School of Medicine, University of MinhoAbstract The nucleus accumbens (NAc) is a key brain region for motivated behaviors, yet how distinct neuronal populations encode appetitive or aversive stimuli remains undetermined. Using microendoscopic calcium imaging in mice, we tracked NAc shell D1- or D2-medium spiny neurons’ (MSNs) activity during exposure to stimuli of opposing valence and associative learning. Despite drift in individual neurons’ coding, both D1- and D2-population activity was sufficient to discriminate opposing valence unconditioned stimuli, but not predictive cues. Notably, D1- and D2-MSNs were similarly co-recruited during appetitive and aversive conditioning, supporting a concurrent role in associative learning. Conversely, when contingencies changed, there was an asymmetric response in the NAc, with more pronounced changes in the activity of D2-MSNs. Optogenetic manipulation of D2-MSNs provided causal evidence of the necessity of this population in the extinction of aversive associations. Our results reveal how NAc shell neurons encode valence, Pavlovian associations and their extinction, and unveil mechanisms underlying motivated behaviors.https://doi.org/10.1038/s41467-024-55269-9
spellingShingle Ana Verónica Domingues
Tawan T. A. Carvalho
Gabriela J. Martins
Raquel Correia
Bárbara Coimbra
Ricardo Bastos-Gonçalves
Marcelina Wezik
Rita Gaspar
Luísa Pinto
Nuno Sousa
Rui M. Costa
Carina Soares-Cunha
Ana João Rodrigues
Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons
Nature Communications
title Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons
title_full Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons
title_fullStr Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons
title_full_unstemmed Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons
title_short Dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell D1- and D2-medium spiny neurons
title_sort dynamic representation of appetitive and aversive stimuli in nucleus accumbens shell d1 and d2 medium spiny neurons
url https://doi.org/10.1038/s41467-024-55269-9
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