Engagement of basal amygdala‐nucleus accumbens glutamate neurons in the processing of rewarding or aversive social stimuli

Author:

Poggi Giulia1,Bergamini Giorgio1,Dulinskas Redas1,Madur Lorraine12,Greter Alexandra1,Ineichen Christian1,Dagostino Amael1,Kúkeľová Diana1,Sigrist Hannes1,Bornemann Klaus D.3,Hengerer Bastian3,Pryce Christopher R.12ORCID

Affiliation:

1. Preclinical Laboratory for Translational Research into Affective Disorders, Department of Psychiatry, Psychotherapy and Psychosomatics Psychiatric University Hospital Zürich (PUK) and University of Zurich (UZH) Zurich Switzerland

2. Zurich Neuroscience Center University of Zurich and Swiss Federal Institute of Technology Zurich Zurich Switzerland

3. CNS Diseases Research, Boehringer Ingelheim Pharma GmbH & Co. KG Biberach Germany

Abstract

AbstractBasal amygdala (BA) neurons projecting to nucleus accumbens (NAc) core/shell 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 both 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.

Funder

Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung

Publisher

Wiley

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