Establishment of a social conditioned place preference paradigm for the study of social reward in female mice

Abstract

Social interactions can be and often are rewarding. The effect of social contact strongly depends on circumstances, and the reward may be driven by varied motivational processes, ranging from parental or affiliative behaviors to investigation or aggression. Reward associated with nonreproductive interactions in rodents is measured using the social conditioned place preference (sCPP) paradigm, where a change in preference for an initially neutral context confirms reinforcing effects of social contact. Here, we revised the sCPP method and reexamined social reward in adult female mice. Contrary to earlier studies, we found that robust rewarding effects of social contact could be detected in adult (14-week-old) female C57BL/6 mice when the sCPP task was refined to remove confounding factors. Strikingly, the rewarding effects of social interaction were only observed among female siblings who remained together from birth. Contact with same-age nonsiblings was not rewarding even after 8 weeks of cohousing. Other factors critical for the social reward effect in the sCPP paradigm included the number of conditioning sessions and the inherent preference for contextual cues. Thus, we show that social interaction is rewarding in adult female mice, but this effect strictly depends on the familiarity of the interaction partners. Furthermore, by identifying confounding factors, we provide a behavioral model to study the mechanisms underlying the rewarding effects of nonreproductive social interaction in adult mice.

Prosocial behavior, social reward and affective state discrimination in adult male and female mice

“…No preference for the prosocial choices in male mice could potentially be attributed to a generally lower sensitivity to the rewarding effects of social interaction. To assess this possibility, we tested adult mice of both sexes in the social conditioned place preference task (sCPP), with a 6-day conditioning protocol 37 . In this test, experience of social contact during conditioning causes an increase in time spent in the previously neutral context from pretest to posttest.…”

“…sCPP was performed as previously described (Harda et al, 2022(Harda et al, , 2020. The procedure consisted of three phases: pretest, conditioning phase, and posttest.…”

“…Social conditioned place preference (sCPP) sCPP was performed as previously described 37,46 . The procedure consisted of three phases:…”

“…To assess prosocial behavior, we have developed a food-motivated prosocial choice task based on the rat task described by Hernandez-Lallement and collaborators (Hernandez-Lallement et al, 2014), with a custom-designed apparatus and schedule adapted for mice. Empathy was tested in a paradigm where sensitivity to the emotional state of interaction partners was assayed, modified from Scheggia et al (2020a), and social reward was tested in the social conditioned place preference task (Harda et al, 2022). We found that, similar to the case in humans, sex had a significant effect on the propensity for prosocial choices; however, females and males did not differ with respect to levels of social reward and empathy.…”

“…Thus, we first investigated prosocial choices in adult male and female C57BL/6 laboratory mice, towards a familiar partner (sibling) using model based on the general outline the rat task described by Hernandez-Lallement and collaborators 10 . Affective state discrimination was tested in a mice paradigm modified from Scheggia et al in 2020, where sensitivity to the emotional state of interaction partners was assayed 26 and social reward was tested in the social conditioned place preference task 37 . We found that, similar to humans, sex had a significant effect on the propensity for prosocial choices; however, females and males did not differ with respect to levels of social reward and affective state discrimination.…”