Abstract
Mammalian social relationships, such as mother–offspring attachments and pair bonds, can directly affect reproductive output. However, conspecifics approach one another in a comparatively broad range of contexts, so conceivably there are motivations for social congregation other than those underlying reproduction, parental care or territoriality. Here, we show that reward mediated by social contact is a fundamental aspect of juvenile mouse sociality. Employing a novel social conditioned place preference (SCPP) procedure, we demonstrate that social proximity is rewarding for juvenile mice from three inbred strains (A/J, C57BL/6J and DBA/2J), while mice from a fourth strain (BALB/cJ) are much less responsive to social contact. Importantly, this strain-dependent difference was not related to phenotypic variability in exploratory behavior or contextual learning nor influenced by the genetic background associated with maternal care or social conditioning. Furthermore, the SCPP phenotype was expressed early in development (postnatal day 25) and did not require a specific sex composition within the conditioning group. Finally, SCPP responses resulted from an interaction between two specifiable processes: one component of the interaction facilitated approach toward environments that were associated with social salience, whereas a second component mediated avoidance of environmental cues that predicted social isolation. We have thus identified a genetically prescribed process that can attribute value onto conditions predicting a general form of social contact. To our knowledge, this is the first definitive evidence to show that genetic variation can influence a form of social valuation not directly related to a reproductive behavior.
Highlights
Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation
Strain-dependent variation Juvenile mice approached and explored environments associated with social contact to a greater degree than environments associated with social isolation (Fig. 2b; t 1⁄4 9.0, df 1⁄4 112, P < 0.0001; see Experiment 2 in Materials and methods)
This social conditioned place preference (SCPP) response was greatly reduced in juvenile mice from the BALB strain
Summary
Re-use of this article is permitted in accordance with the Creative Commons Deed, Attribution 2.5, which does not permit commercial exploitation. Reward is not necessary for social behavior to occur, reward processes have been shown in social contexts that include mating (Agmo & Gomez 1993; Drewett 1973), monogamous pair-bonding (Young & Wang 2004), aggression (Fish et al 2005), maternal–infant attachment (Insel 2003; Lee et al 1999) and rough-and-tumble play among juveniles (Calcagnetti & Schechter 1992; Ikemoto & Panksepp 1992). We have identified and characterized a genetically specified reward process that appears to facilitate social contact among juvenile mice
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