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Engagement of basal amygdala-nucleus accumbens glutamate neurons in the processing of rewarding or aversive social stimuli
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  • Giulia Poggi,
  • Giorgio Bergamini,
  • Redas Dulinskas,
  • Lorraine Madur,
  • Alexandra Greter,
  • Christian Ineichen,
  • Amael Dagostino,
  • Diana Kukelova,
  • Hannes Sigrist,
  • Klaus Bornemann,
  • Bastian Hengerer,
  • Christopher Pryce
Giulia Poggi
University of Zurich
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Giorgio Bergamini
University of Zurich
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Redas Dulinskas
University of Zurich
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Lorraine Madur
University of Zurich
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Alexandra Greter
University of Zurich
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Christian Ineichen
University of Zurich
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Amael Dagostino
University of Zurich
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Diana Kukelova
University of Zurich
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Hannes Sigrist
University of Zurich
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Klaus Bornemann
Boehringer Ingelheim Pharma GmbH & Co KG
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Bastian Hengerer
Boehringer Ingelheim Pharma GmbH und Co. KG
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Christopher Pryce
University of Zurich

Corresponding Author:christopher.pryce@bli.uzh.ch

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Abstract

Basal amygdala (BA) neurons projecting to nucleus accumbens core/shell (NAc) are primarily glutamatergic and are integral to the circuitry of emotional processing. Several recent mouse studies have addressed whether neurons in this population(s) respond to reward, aversion, or both emotional valences. The focus has been on processing of physical emotional stimuli and here we extend this to salient social stimuli. In male mice, an iterative study was conducted into engagement of BA-NAc neurons in response to estrous female (social reward, SR) and/or aggressive-dominant male (social aversion, SA). In BL/6J mice, SR and SA activated c-Fos expression in a high and similar number/density of BA-NAc neurons in the anteroposterior intermediate BA (int-BA), whereas activation was predominantly by SA in posterior (post-)BA. In Fos-TRAP2 mice, compared with SR-SR or SA-SA controls, exposure to successive presentation of SR-SA or SA-SR, followed by assessment of tdTomato reporter and/or c-Fos expression, demonstrated that many int-BA-NAc neurons were activated by only one of SR and SA; these SR/SA monovalent neurons were similar in number and present in magnocellular and parvocellular int-BA subregions. In freely moving BL/6J mice exposed to SR, bulk GCaMP6 fibre photometry provided confirmatory in vivo evidence for engagement of int-BA-NAc neurons during social and sexual interactions. Therefore, populations of BA-NAc glutamate neurons are engaged by salient rewarding and aversive social stimuli in a topographic and valence-specific manner; this novel evidence is important to the overall understanding of the roles of this pathway in the circuitry of socio-emotional processing.
22 Aug 2023Submitted to European Journal of Neuroscience
23 Aug 2023Submission Checks Completed
23 Aug 2023Assigned to Editor
23 Aug 2023Review(s) Completed, Editorial Evaluation Pending
19 Sep 2023Reviewer(s) Assigned