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. 2022 Apr 8;25(5):104230.
doi: 10.1016/j.isci.2022.104230. eCollection 2022 May 20.

Species-typical group size differentially influences social reward neural circuitry during nonreproductive social interactions

Jose A Gonzalez Abreu  1 , Ashley E Rosenberg  1 , Brandon A Fricker  1 , Kelly J Wallace  1 , Ashley W Seifert  2 , Aubrey M Kelly  1
Affiliations

Species-typical group size differentially influences social reward neural circuitry during nonreproductive social interactions

Jose A Gonzalez Abreu et al. iScience. .

Abstract

We investigated whether nonreproductive social interactions may be rewarding for colonial but not non-colonial species. We found that the colonial spiny mouse (Acomys cahirinus) is significantly more gregarious, more prosocial, and less aggressive than its non-colonial relative, the Mongolian gerbil (Meriones unguiculatus). In an immediate-early gene study, we examined oxytocin (OT) and tyrosine hydroxylase (TH) neural responses to interactions with a novel, same-sex conspecific or a novel object. The paraventricular nucleus of the hypothalamus (PVN) OT cell group was more responsive to interactions with a conspecific compared to a novel object in both species. However, the ventral tegmental area (VTA) TH cell group showed differential responses only in spiny mice. Further, PVN OT and VTA TH neural responses positively correlated in spiny mice, suggesting functional connectivity. These results suggest that colonial species may have evolved neural mechanisms associated with reward in novel, nonreproductive social contexts to promote large group-living.

Keywords: Biological sciences; Cellular neuroscience; Ethology.

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Conflict of interest statement

The authors declare no competing interests.

Figures

None
Graphical abstract
Figure 1
Figure 1
Group size preference test (A) Mean (±SEM) time spent (s) affiliating with the large group minus the small group. Spiny mice (light beige) exhibited higher degrees of gregariousness than gerbils (blue). (B) Mean (±SEM) time spent (s) in the middle of the arena not affiliating with any stimulus animals. Male (light beige) and female (dark beige) spiny mice spent less time not affiliating with stimuli than male (light blue) and female (dark blue) gerbils. Dots represent individual data points. ∗ indicates statistical significance (p < 0.05). Letters (A,B,C) denote significant post hoc comparisons (p ≤ 0.05), with shared letters indicating statistical similarity between groups; bars that do not share a letter were significantly different.
Figure 2
Figure 2
Prosocial interaction test (A) Mean (±SEM) time spent (s) exhibiting prosocial behavior. Spiny mice (beige) exhibited more prosocial behavior than gerbils (blue). (B) Mean (±SEM) time spent (s) exhibiting aggressive behavior. Spiny mice (beige) exhibited less aggression than gerbils (blue). Dots represent individual data points. ∗ indicates statistical significance (p < 0.05).
Figure 3
Figure 3
Representative images for PVN OT-Fos cell counts Representative photomicrographs (10x magnification) of rostral and caudal brain sections containing the PVN. Regions of interest were not used for cell counts and instead all OT + cells in the PVN were quantified. Images were pseudocolored light blue for OT and red for Fos. Images shown are from a female gerbil. Scale bar represents 100um.
Figure 4
Figure 4
PVN OT neural responses Spiny mice and gerbils exposed to a novel, same-sex conspecific (dark green) exhibited a higher percentage of rostral (A) and caudal (B) PVN OT-Fos colocalized cells than animals exposed to a novel object (light green). Data are represented as mean (±SEM). Dots represent individual data points. ∗ indicates statistical significance (p < 0.05).
Figure 5
Figure 5
Regions of interest for VTA TH-Fos cell counts Representative photomicrographs (5x magnification) of rostral and caudal brain sections containing the VTA. Regions of interest for cell counts are shown as a dashed white box. Images were pseudocolored green for TH and red for Fos. Images shown are from a male spiny mouse. Scale bar represents 200um.
Figure 6
Figure 6
VTA TH neural responses Spiny mice exposed to a novel, same-sex conspecific (dark green) exhibited a higher percentage of VTA TH-Fos colocalized cells than spiny mice exposed to a novel object (light green). Spiny mice exposed to a novel, same-sex conspecific also had greater VTA TH-Fos colocalization compared to gerbils. Data are represented as mean (±SEM). Dots represent individual data points. ∗ indicates statistical significance (p < 0.05).
Figure 7
Figure 7
PVN OT – behavior correlations In gerbils exposed to a novel, same-sex conspecific (A) aggressive behavior positively correlated with the percentage of rostral PVN OT-Fos colocalization and (B) prosocial behavior negatively correlated with the percentage of rostral PVN OT-Fos colocalization. (C) Spiny mice exposed to a novel, same-sex conspecific exhibited no relationship between aggression and caudal PVN OT-Fos colocalization, but (D) did exhibit a positive relationship between prosocial behavior and the percentage of caudal PVN OT-Fos colocalization.
Figure 8
Figure 8
VTA TH – behavior correlations (A) Spiny mice exposed to a novel, same-sex conspecific exhibited a positive correlation between the percentage of VTA TH-Fos colocalization and prosocial behavior, whereas (B) no significant correlation was observed for gerbils.
Figure 9
Figure 9
Caudal PVN OT – VTA TH correlations in spiny mice (A) In spiny mice exposed to a novel, same-sex conspecific, the percentage of VTA TH-Fos colocalization positively correlated with the percentage of caudal PVN OT-Fos colocalization, whereas (B) no significant correlation was observed for gerbils.
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