Social conditioned place preference in the captive ground squirrel (Ictidomys tridecemlineatus): Social reward as a natural phenotype.

Abstract

Social behaviors of wild animals are often considered within an ultimate framework of adaptive benefits versus survival risks. By contrast, studies of laboratory animals more typically focus on affective aspects of behavioral decisions, whether a rodent derives a rewarding experience from social encounter and how this experience might be initiated and maintained by neural circuits. Artificial selection and inbreeding have rendered laboratory animals more affiliative and less aggressive than their wild conspecifics, leaving open the possibility that social reward is an artifact of domestication. We compared social behaviors of wild and captive population of juvenile 13-lined ground squirrels (Ictidomys tridecemlineatus), the latter 2nd and 3rd generation descendents of wild individuals. At an age corresponding to emergence from the burrow, postnatal day 38, captive squirrels engaged in vigorous social approach and play; these juvenile behaviors declined significantly by postnatal day 56. Similarly, young wild squirrels expressed social proximity and play, affiliative interactions declined with summer’s progression and were replaced by agonistic chasing behaviors. Social conditioned place preference testing (conditioned postnatal days 40–50) indicated that adolescent squirrels derived a rewarding experience from social reunion. Our results support the contention that undomesticated rodents have the capacity for social reward and more generally suggest the possibility that positive affective experiences may support group cohesion and social cooperation in the wild.

Social Reward and Empathy as Proximal Contributions to Altruism: The Camaraderie Effect

“…However, in the social CPP test, captive juveniles that were second- and third-generation descendants of wild ground squirrels expressed a robust preference for environments paired with social access, indicating that social interactions can be rewarding for rodents with undomesticated genetic backgrounds (Lahvis et al 2015). This finding suggests that wild squirrels, known for their diminished sociality, can derive pleasure from a social interaction.…”

“…This finding suggests that wild squirrels, known for their diminished sociality, can derive pleasure from a social interaction. Additional comparisons of laboratory experiments with concurrent field experiments showed that while maturing wild juveniles gradually foraged at increasing distances from one another, a behavioral pattern that predicts dispersal, captive juveniles simultaneously expressed diminished social approach and increased play fighting (Lahvis et al 2015). Taken together, this comparison supports the idea that the adolescent thirteen-lined ground squirrel can experience social reward and that social motivation diminishes as maturing adolescents begin to disperse, an idea akin to the “ontogenetic switch” (Holekamp 1984).…”

“…In this regard, laboratory rodents may be similar to humans, who can have a basic need for social connections and find social separation or rejection psychologically painful (Eisenberger and Lieberman 2005). While domestication can engender prosocial behaviors that do not exist in the wild, experiments with captive ground squirrels show that undomesticated rodents can also derive pleasure from access to social interactions (Lahvis et al 2015), indicating that social reward is a natural motivation.…”

“…When a rat hears affiliative 50-kHz USVs, gene expression is activated in reward-related areas of the brain (Sadananda et al 2008) and dopamine is released in the nucleus accumbens (Willuhn et al 2014), a physiological correlate of a reward experience (Kelley and Berridge 2002; Smith and Berridge 2007). These affective experiences might help build strong social bonds that confer a variety of reproductive benefits (Lahvis et al 2015; Seyfarth and Cheney 2013). …”

The neurobiology of social play and its rewarding value in rats

“…Place conditioning has been used to demonstrate the pleasurable aspects of (playful) social interactions (Calcagnetti and Schechter, 1992; Crowder and Hutto, 1992; Douglas et al, 2004; Lahvis et al, 2015; Panksepp and Lahvis, 2007; Van den Berg et al, 1999b), access to pups (Mattson et al, 2001), sexual behaviour (Camacho et al, 2004; Jenkins and Becker, 2003; Kippin and van der Kooy, 2003), as well as aggressive social interactions (Martinez et al, 1995; Tzschentke, 2007). …”