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

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 () and Ana João Rodrigues ()
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Ana Verónica Domingues: School of Medicine, University of Minho
Tawan T. A. Carvalho: School of Medicine, University of Minho
Gabriela J. Martins: Zuckerman Mind Brain Behavior Institute at Columbia University
Raquel Correia: School of Medicine, University of Minho
Bárbara Coimbra: School of Medicine, University of Minho
Ricardo Bastos-Gonçalves: School of Medicine, University of Minho
Marcelina Wezik: School of Medicine, University of Minho
Rita Gaspar: School of Medicine, University of Minho
Luísa Pinto: School of Medicine, University of Minho
Nuno Sousa: School of Medicine, University of Minho
Rui M. Costa: Zuckerman Mind Brain Behavior Institute at Columbia University
Carina Soares-Cunha: School of Medicine, University of Minho
Ana João Rodrigues: School of Medicine, University of Minho

Nature Communications, 2025, vol. 16, issue 1, 1-20

Abstract: 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.

Date: 2025
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DOI: 10.1038/s41467-024-55269-9

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