The Influence of Social Isolation on Social Orientation, Sociability, Social Novelty Preference, and Hippocampal Parvalbumin-Expressing Interneurons in Peripubertal Rats – Understanding the Importance of Meeting Social Needs in Adolescence

Abstract

The fulfillment of belonging needs underlies a variety of behaviors. In order to understand how social needs unmet during maturation shape everyday life, we examined social motivation and cognition in peripubertal rats, as a rodent model of adolescence, subjected to social isolation (SI) during early and early-to-mid adolescence. The behavioral correlates of social orientation (social space preference), sociability (preference for social over non-social novelty), and social novelty preference (SNP) were examined in group-housed (GH) and single-housed (SH) rats in a 3-chamber test. The response to social odors was examined to gain insights into the developmental role of social odors in motivated social behavior. Differentiation between appetitive (number of visits/approaches) and consummatory (exploratory time) aspects of motivated social behavior was done to determine which facet of social motivation characterizes maturation when social needs are met and which aspect dominates when social needs are unsatisfied. The SI-sensitive parvalbumin-expressing interneurons (PVI) in the hippocampus were examined using immunohistochemistry. The main findings are the following: (1) in GH rats, the preference for social space is not evident regardless of animals’ age, while sociability becomes apparent in mid-adolescence strictly through consummatory behavior, along with complete SNP (appetitive, consummatory); (2) SH promotes staying in a social chamber/space regardless of animals’ age and produces an appetitive preference for it only in early-adolescent animals; (3) SH promotes sociability (appetitive, consummatory) regardless of the animals’ age and prevents the SNP; (4) the preference for a social odor is displayed in all the groups through consummatory behavior, while appetitive behavior is evident only in SH rats; (5) the response to social odors does not commensurate directly to the response to conspecifics; (6) SH does not influence PVI in the hippocampus, except in the case of early-adolescence when a transient decrease in the dentate gyrus is observed. These results accentuate the developmental complexity of social motivation and cognition, and the power of SI in adolescence to infringe social maturation at different functional levels, promoting appetitive behavior toward peers overall but harming the interest for social novelty. The findings emphasize the importance of the fulfillment of basic social needs in the navigation through the social world.

Adolescent parvalbumin expression in the left orbitofrontal cortex shapes sociability in female mice

“…In humans, social isolation during adolescence can increase the occurrence of neurological disorders and cause defects in brain function (Almeida et al, 2021). Similarly, depriving rodents of social experience during adolescence caused defects in the maturation of their brains and alterations in social and cognitive behaviors (Cooke et al, 2000; Schubert et al, 2009; Makinodan et al, 2012; Hinton et al, 2019; Potrebic et al, 2022). Furthermore, behavioral and physiological changes caused by adolescent social isolation were often sex-specific (Pisu et al, 2016; Bicks et al, 2020; Tan et al, 2021).…”

“…Mammalian social behavior is important for maintaining a conspecific society. Social interaction during adolescence is critical for shaping social and cognitive behaviors in both humans and rodents (Spear, 2000; Makinodan et al, 2012; Hinton et al, 2019; Almeida et al, 2021; Potrebic et al, 2022). Interestingly, the mammalian brain shows hemispheric asymmetry and lateralization in executing social behaviors (Marlin et al, 2015).…”

Morphine exposure during adolescence induces enduring social changes dependent on adolescent stage of exposure, sex, and social test.

“…In rodents, social behavior milestones during adolescence include a reduction in juvenile social play behavior and an increase in copulatory behavior, both of which need to occur for normal adult social behaviors to be achieved (Chu et al, 2021; Kopec et al, 2018). Critical periods mark developmental periods of increased vulnerability to adverse experiences such as substance use (Hunt et al, 2017; Pierce et al, 2022; Potrebić et al, 2022). We previously demonstrated that developmental changes in the nucleus accumbens reward region regulate social play in rats during sex-specific adolescent periods: early to mid-adolescence in males (postnatal days, P30–40) and preearly adolescence in females (P20–30; Kopec et al, 2018).…”