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Social Reward As a Natural Phenotype

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Social Reward As a Natural Phenotype Journal of Comparative Psychology © 2015 American Psychological Association 2015, Vol. 129, No. 3, 291–303 0735-7036/15/$12.00 http://dx.doi.org/10.1037/a0039435 Social Conditioned Place Preference in the Captive Ground Squirrel (Ictidomys tridecemlineatus): Social Reward as a Natural Phenotype Garet P. Lahvis, Jules B. Panksepp, Clarinda R. Wilson and Bruce C. Kennedy University of Wisconsin–Madison Oregon Health and Science University Dana K. Merriman University of Wisconsin–Oshkosh 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 tridecemlin- eatus), the latter being 2nd- and 3rd-generation descendants of wild individuals. At an age corresponding to emergence from the burrow, postnatal day (PD) 38, captive squirrels engaged in vigorous social approach and play and these juvenile behaviors declined significantly by PD 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 (condi- tioned PDs 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, social cooperation, and altruism in the wild. Keywords: social reward, classical conditioning, play-fighting, altruism, camaraderie effect Mammals express an ontogeny of social behaviors, beginning mer progresses, play behaviors diminish (Betts, 1976; Nunes, with mother–infant interactions, continuing through playful inter- Muecke, Anthony, & Batterbee, 1999), with adolescents often actions with peers, and maturing into the more stereotypical, wandering beyond their natal range, an action that can lead to sex-dependent patterns characteristic of adults (Wolff & Sherman, emigration (Barash, 1974; Holekamp, 1984a, 1984b; McCarley, 2008). Though sharing these commonalities, the sociality of 1966; Michener & Michener, 1977; Rayor & Armitage, 1991). ground squirrel species varies in both duration and degree (Armit- Among the more social Columbian ground squirrels, S. columbia- age, 1981; Hare & Murie, 2008; Rayor & Armitage, 1991). Juve- nus, adult social interactions often appear affiliative, typically nile ground squirrels engage in social play soon after they emerge consisting of dyads and triads networked via social interactions from their natal burrows (Steiner, 1971; Yeaton, 1972). As sum- with extra-group individuals (Manno, 2008). Among less social species, including I. tridecemlineatus, arctic ground squirrels, S. parryii plesius, and Richardson’s ground squirrels, S. richardsonii, This document is copyrighted by the American Psychological Association or one of its allied publishers. social interactions are expressed rather as conflicts for mating This article is intended solely for the personal use of the individual userThis and is not to be disseminatedarticle broadly. was published Online First July 6, 2015. opportunities and territory (Lacey, Wieczorek, & Tucker, 1997; Garet P. Lahvis, Jules B. Panksepp, and Bruce C. Kennedy, Department Schwagmeyer & Woontner, 1986; Schwagmeyer & Parker, 1987; of Behavioral Neuroscience, Oregon Health and Science University; Clar- inda R. Wilson, Department of Surgery, University of Wisconsin–Madi- Luna & Baird, 2004). son; Dana K. Merriman, Department of Biology and Microbiology, Uni- Mammalian social behaviors are often considered within the versity of Wisconsin–Oshkosh. ultimate framework of adaptive benefits versus survival risks (Silk, Bruce C. Kennedy is now at the Department of Neuroscience, University 2007). For instance, juvenile play is thought to improve physical of Minnesota. and emotional responsiveness to unexpected events (Nunes et al., This work was supported by National Institutes of Health Research 1999; Spinka, Newberry, & Bekoff, 2001), familiarize juveniles Grants DA022543 and P30HD03. Garet P. Lahvis and Jules B. Panksepp with self-handicap and fair behavior (Bekoff, 2004), improve contributed equally to this work. Correspondence concerning this article should be addressed to Garet P. abilities to cope with social challenges (van den Berg et al., 1999), Lahvis, Department of Behavioral Neuroscience, Oregon Health and Sci- establish dominance relationships (Blumstein, Chung, & Smith, ence University, 3181 SW Sam Jackson Park Road, Mail Code L470, 2013), and help refine abilities to respond to subtle and ambiguous Portland, OR 97239-3011. E-mail: [email protected] social signals (Pellis, Pellis, & Reinhart, 2010). Such adaptive 291 292 LAHVIS ET AL. benefits are difficult to test (Burghardt, 2005; Pellis & Pellis, domestication and genetic inbreeding. This experimental gap leads 2006) but are suggested by evidence that social play promotes to an obvious question regarding the applicability and relevance of normal brain development (Gordon, Burke, Akil, Watson, & Pank- such testing scenarios to wild or captive rodents. sepp, 2003; Pellis & Pellis, 2007). In this paper, we present findings from a novel experimental Like juvenile play, dispersal also has adaptive benefits that opportunity that employs laboratory tests of rodent social interac- likely vary among squirrel species (Bowler & Benton, 2005; tion (Panksepp et al., 2007) and social reward (Panksepp & Lahvis, Lawson Handley & Perrin, 2007; Wolff, 1994). Benefits include 2007) to study captive 13-lined ground squirrels, Ictidomys tride- competitive mating advantages (Dobson, 1982), access to higher cemlineatus, second- and third-generation descendants of wild quality resources (Dobson, 1979), avoidance of inbreeding individuals (Merriman et al., 2012). Our choice of generation for (Wauters & Dhondt, 1993), and evasion from parasitism using captive-born ground squirrels is supported by studies show- (Hoogland, 1979). These benefits can offset dispersal’s enormous ing that wild Norway rats robustly express wild behaviors within survival risks (Byrom & Krebs, 1999). Proximate explanations for the first two to five generations of captivity in the absence of any variations in adolescent dispersal include differences in environ- direct selection for tameness (Stryjek & Pisula, 2008). Litters of mental harshness (Barash, 1974; Ritchie & Belovsky, 1990), adult 13-lined ground squirrel are born in late May to early June (Mc- aggression toward maturing adolescents (Steiner, 1972; Wolff, Carley, 1966; Merriman, Lahvis, Jooss, Gesicki, & Schill, 2012), 1993), and ontogenetic changes promoting excursion behavior emerging from their burrows at about 5 weeks of age, forage, (Holekamp, 1984a; 1984b). Proximate explanations might also engage in play, then disperse within a month of their emergence include psychological changes. Exploratory activity of laboratory (McCarley, 1966; Rayor & Armitage, 1991; Wistrand, 1974). rodents can be greater among adolescents than either younger Young females more commonly remain within the colony juveniles or adults (Macri, Adriani, Chiarotti, & Laviola, 2002). (Schwagmeyer, 1980), whereas males typically emigrate (Armit- Affiliative social behaviors also change with maturation (Panksepp age, 1981; McCarley, 1966). et al., 2007; Terranova, Laviola, & Alleva, 1993). Exploratory and We compared social interaction in captive, same- and mixed-sex social behaviors utilize neurocircuits (Laviola, Macri, Morley- dyads, with contemporaneous observations of wild squirrels at Fletcher, & Adriani, 2003; Liu & Wang, 2003; Resendez, Kuhn- times approximating emergence from the burrow and dispersal. muench, Krzywosinski, & Aragona, 2012) activated by natural and We found that captive and wild ground squirrels expressed anal- drug rewards (Spear, 2000; Kelley & Berridge, 2002; Dölen et al., ogous declines in affiliative behaviors with the progression of 2013). summer. Employing an adapted social CPP paradigm (Panksepp & We can infer an animal subject finds a stimulus rewarding if the Lahvis, 2007), we found that adolescent squirrels expressed a subject returns to an environment associated with that stimulus robust place preference for environments associated with social (Glickman & Schiff, 1967; Schneirla, 1959). Measures of condi- interactions, indicating social reward from reunion with their tioned place preference (CPP) allow us to formally assess this peers. Overall, squirrel social behaviors resemble patterns ex- possibility. In the conditioning phase, the subject is alternated pressed by highly domesticated and inbred rodents, strengthening between one environment paired with the presence of a stimulus the value of using psychological approaches for understanding the and a second environment associated with its absence. During the natural developmental transitions in rodent social affiliation.
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