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