Measuring motivation and performance of social play behavior in rats: Role of dopamine and noradrenaline

Abstract

Social play behavior is a vigorous form of social interaction, abundant in the young of many mammalian species, including humans. The experience of social play behavior during childhood and adolescence is critical for normal social and cognitive development. In rats, social play is characterized by distinct behaviors, (1) pouncing (invitation to play), when one animal attempts to touch the nape of the neck of another animal and (2) pinning (continuation play bout), upon contact of the nape, the recipient animal fully rotates around the longitudinal axis of its body, ending in a supine position with the other animals standing over it. Social play is highly rewarding, and as such, the expression of social play depends on its pleasurable and motivational properties [1-3]. Because dopamine and noradrenaline have been implicated in both social play and in reward processes, we here investigated the role of dopamine and noradrenaline in the pleasurable and motivational properties of social play behavior in rats. To assess social play motivation, we developed a setup in which rats responded for access to a playful partner under a progressive ratio schedule of reinforcement. To assess the pleasurable properties of social play, the acquisition of social play-induced conditioned place preference (CPP) was investigated. The psychostimulant drugs methylphenidate and cocaine both increased responding for social play (measured by the number of rewards obtained and the breakpoint reached), suppressed its expression (measured by the frequency of pinning and pouncing) but did not affect its pleasurable properties (measured by the time spent in the play associated compartment compared to the non-play compartment). The noradrenaline reuptake inhibitor atomoxetine decreased both social play motivation and expression, but spared social play-induced place conditioning. The dopamine reuptake inhibitor GBR12909 increased motivation for social play, did not affect its expression, but reduced its pleasurable properties. The effect of methylphenidate and cocaine on social play motivation was blocked by the dopamine receptor antagonist a-flupenthixol whereas play expression remained suppressed. Furthermore, the a-2 adrenoceptor antagonist RX821002 reversed the playsuppressing effect of methylphenidate, but left its effect on motivation for social play unaltered. The doses used of both the dopamine receptor antagonist alpha-flupenthixol and the alpha-2 adrenoceptor antagonist RX821002 did not affect operant responding or play behavior. These data demonstrate dissociable roles for dopamine and noradrenaline in social play behavior: dopamine is involved in the motivational and pleasurable properties of social play, whereas noradrenaline modulates the motivation for play and its expression. These data provide new insights into the intricate mechanisms by which catecholamines modulate social play behavior in rats. Elucidating the neural underpinnings of social behavior in the young may increase our understanding of normal, adaptive social development, and may shed light on the pathophysiology of childhood and adolescent psychiatric disorders characterized by aberrant social behavior such as autism spectrum disorder (ASD) or attention deficit/hyperactivity disorder (ADHD)