The neurobiology of social play and its rewarding value in rats

Abstract

In the young of many mammalian species, including humans, a vigorous and highly rewarding social activity is abundantly expressed, known as social play behaviour. Social play is thought to be important for the development of social, cognitive and emotional processes and their neural underpinnings, and it is disrupted in pediatric psychiatric disorders. Here, we summarize recent progress in our understanding of the brain mechanisms of social play behaviour, with a focus on its rewarding properties. Opioid, endocannabinoid, dopamine and noradrenaline systems play a prominent role in the modulation of social play. Of these, dopamine is particularly important for the motivational properties of social play. The nucleus accumbens has been identified as a key site for opioid and dopamine modulation of social play. Endocannabinoid influences on social play rely on the basolateral amygdala, whereas noradrenaline modulates social play through the basolateral amygdala, habenula and prefrontal cortex. In sum, social play behaviour is the result of coordinated activity in a network of corticolimbic structures, and its monoamine, opioid and endocannabinoid innervation.

Reward-centricity and attenuated aversions: An adolescent phenotype emerging from studies in laboratory animals

“…Even the preference for a natural reward—sweet tastes—was found to be greater early in adolescence (11–15 years) than during late adolescence/emerging adulthood (19–25 years) (Desor and Beauchamp, 1987). A multitude of other studies have demonstrated enhanced sensitivity to rewarding stimuli in human adolescents for both decision-making/risk taking behaviors, as well as for cognitive control and learning behaviors, data that have been recently reviewed (see Andersen et al, 2002; and also in this issue: Luciana et al, 2016; Schulz and Sisk, 2016; Silveri et al, 2016; Spear, 2016; Vanderschuren et al, 2016; van Duijvenvoorde et al, 2016). …”

“…Results such as these serve as indirect evidence that enhanced endocannabinoid signaling during adolescence may contribute to the reward-centric phenotype characteristic of this age. Interestingly, these mutant Cnr1 mice also exhibited increases in peer-directed social behavior, potentially implicating the endocannabinoid system in the expression and rewarding aspects of social behavior during this developmental window as well (for further discussion see Vanderschuren et al, 2016.). …”

Interacting Cannabinoid and Opioid Receptors in the Nucleus Accumbens Core Control Adolescent Social Play

“…It can be used as an incentive for place conditioning, operant conditioning and maze learning in laboratory animals (for a review see Panksepp et al, 1987; Trezza et al, 2011a), and social play is modulated by neurotransmitters implicated in reward and motivation, such as endogenous opioids, endocannabinoids (eCBs), and dopamine (Trezza and Vanderschuren, 2008b; Trezza et al, 2010; Achterberg et al, 2016; Manduca et al, 2016; Vanderschuren et al, 2016). The nucleus accumbens (NAc) has been identified as an anatomical substrate for motivation and reward (Everitt and Robbins, 2005; Berridge and Kringelbach, 2015; Floresco, 2015).…”

Sex‐dependent effects of Cacna1c haploinsufficiency on juvenile social play behavior and pro‐social 50‐kHz ultrasonic communication in rats

“…41,42 This includes impairments in direct reciprocal interaction, lack of social approach, and failure of normal back-and-forth conversation. 46 Already from a very young age, rats begin interacting socially and engage in high levels of social play behavior [47][48][49] particularly during the middle of the juvenile stage, 50 including pinning, wrestling, and chasing. 45 As highly gregarious animals living in large groups characterized by prominent social hierarchies, rats display a rich and complex social behavior repertoire.…”

“…Contrary to social play behavior, concomitant emission of prosocial 50-kHz USV did not differ between genotypes. Pinning and the close physical contact it offers is arguably one of the most rewarding components of playful interactions, as indicated by conditioned place preference49 and surgical devocalization79,95 experiments. Because 50-kHz USV reflect positive affective states ("rat laughter") 61 associated with the rewarding nature of social play,63 this would suggest that playful encounters were equally rewarding for Cacna1c +/− females as they were for Cacna1c +/+ littermate controls.…”