Contrasting Roles of Dopamine and Noradrenaline in the Motivational Properties of Social Play Behavior in Rats

Abstract

Social play behavior, abundant in the young of most mammalian species, is thought to be important for social and cognitive development. Social play is highly rewarding, and as such, the expression of social play depends on its pleasurable and motivational properties. Since the motivational properties of social play have only sporadically been investigated, we developed a setup in which rats responded for social play under a progressive ratio schedule of reinforcement. Dopaminergic neurotransmission plays a key role in incentive motivational processes, and both dopamine and noradrenaline have been implicated in the modulation of social play behavior. Therefore, we investigated the role of dopamine and noradrenaline in the motivation for social play. Treatment with the psychostimulant drugs methylphenidate and cocaine increased responding for social play, but suppressed its expression during reinforced play periods. The dopamine reuptake inhibitor GBR-12909 increased responding for social play, but did not affect its expression, whereas the noradrenaline reuptake inhibitor atomoxetine decreased responding for social play as well as its expression. The effects of methylphenidate and cocaine on responding for social play, but not their play-suppressant effects, were blocked by pretreatment with the dopamine receptor antagonist α-flupenthixol. In contrast, pretreatment with the α2-adrenoceptor antagonist RX821002 prevented the play-suppressant effect of methylphenidate, but left its effect on responding for social play unaltered. In sum, the present study introduces a novel method to study the incentive motivational properties of social play behavior in rats. Using this paradigm, we demonstrate dissociable roles for dopamine and noradrenaline in social play behavior: dopamine stimulates the motivation for social play, whereas noradrenaline negatively modulates the motivation for social play behavior and its expression.

Figure 1

Effect of social isolation duration on responding for social play behavior. After 24 h of social isolation, rats obtained more rewards (a) and reached a higher breakpoint (ie, the largest number of lever presses made for a single reward) (b) than after 2 h of social isolation. Frequency of pinning was higher after 24 h of isolation (c), whereas social exploration did not differ as a result of isolation (d). n=14; all rats were tested after both 2 and 24 h of social isolation. Data are presented as mean+SEM. **p<0.01, ***p<0.001.

Figure 2

Methylphenidate (mph; n=6) and cocaine (coc; n=5) enhanced operant responding, but inhibited the expression of social play. Treatment with methylphenidate (1–3 mg/kg, s.c.) and cocaine (5–10 mg/kg, s.c.) enhanced the number of rewards obtained (a, e) and the breakpoint (b, f). Both treatments reduced the frequency of pinning (c, g). Methylphenidate enhanced, while cocaine did not affect, the time spent on social exploratory behavior (d, h). Data are presented as mean+SEM. *p<0.05, **p<0.01, ***p<0.001, relative to saline (0 mg/kg mph/coc) treatment.

Figure 3

The effect of GBR-12909 (GBR; n=11) and atomoxetine (ato; n=8) on operant responding for social play behavior. Treatment with GBR-12909 (3–10 mg/kg, s.c.) enhanced responding for social play. GBR-12909 increased the number of rewards obtained (a) and the breakpoint (b). Administration of GBR-12909 did not affect the frequency of pinning (c), or the time spent on social exploration (d). Treatment with atomoxetine (1–3 mg/kg, i.p.) reduced operant responding and social play behavior. The number of rewards obtained was reduced (e) and the breakpoint was lower (f). In addition, the frequency of pinning (g) was reduced. The time spent on social exploration was unaffected (h). Data are presented as mean+SEM. *p<0.05, **p<0.01, ***p<0.001, relative to saline (0 mg/kg GBR/ato) treatment.

Figure 4

A double dissociation in the effect of methylphenidate on operant responding for social play behavior (n=8). Methylphenidate (MPH; 3 mg/kg, s.c.) increased the number of obtained rewards (a) and the breakpoint (b); this effect was prevented by pretreatment with α-flupenthixol (FLUP; 0.125 mg/kg, i.p.) but not RX821002 (RX; 0.2 mg/kg, i.p.). Methylphenidate reduced the frequency of pinning (c) and increased the time spent on social exploration (d); this effect was prevented by pretreatment with RX821002, but not α-flupenthixol. SAL, saline. Data are presented as mean+SEM. *p<0.05, **p<0.01, ***p<0.001.

Figure 5

Cocaine enhances responding for social play behavior via dopaminergic neurotransmission (n=7). Cocaine (COC; 10 mg/kg, s.c.) increased the number of obtained rewards (a) and the breakpoint (b). This effect was prevented by pretreatment with α-flupenthixol (FLUP; 0.125 mg/kg, i.p.). Cocaine reduced the frequency of pinning (c) but did not affect the time spent on social exploration (d). The effect of cocaine on pinning was not altered by pre/treatment with α-flupenthixol. SAL, saline. Data are presented as mean+SEM. *p<0.05, **p<0.01, ***p<0.001.