Dopamine mediates testosterone-induced social reward in male Syrian hamsters

Abstract

Adolescent maturation of responses to social stimuli is essential for adult-typical sociosexual behavior. Naturally occurring developmental changes in male Syrian hamster responses to a salient social cue, female hamster vaginal secretions (VS), provide a good model system for investigating neuroendocrine mechanisms of adolescent change in social reward. Sexually naïve adult, but not juvenile, males show a conditioned place preference (CPP) to VS, indicating that VS is not rewarding before puberty. In this series of experiments, the authors examined the roles of testosterone and dopamine receptor activation in mediating the adolescent gain in positive valence of VS. Experiment 1 showed that testosterone replacement is necessary for gonadectomized adult hamsters to form a CPP to VS. Experiment 2 showed that testosterone treatment is sufficient for juvenile hamsters to form a CPP to VS, and that the dopamine receptor antagonist haloperidol blocks formation of a CPP to VS in these animals. Experiments 3 and 4 demonstrated that the disruption of VS CPP with low doses of haloperidol is the result of a reduction in the attractive properties of VS and not attributable to aversive properties of haloperidol. Together, these studies demonstrate that the unconditioned rewarding properties of a social cue necessary for successful adult sociosexual interactions come about as the result of the pubertal increase in circulating testosterone in male hamsters. Furthermore, this social reward can be prevented by dopamine receptor antagonism, indicating that hypothalamic and/or mesocorticolimbic dopaminergic circuits are targets for hormonal activation of social reward.

Figure 1.

Conditioned place preference (CPP) to vaginal secretions (VS) in hormone-manipulated adult hamsters. Corrected changes in preference and difference scores are shown, mean ± SE. * Indicates difference from no change (zero), P < .05. Long-term gonadectomy with blank hormone capsules prevented the CPP for VS observed in the gonadectomized (GDX) + testosterone group.

Figure 2.

Conditioned place preference (CPP) to vaginal secretions (VS) in hormone- and dopamine-manipulated juvenile hamsters. Corrected changes in preference and difference scores are shown, mean ± SE. * Indicates difference from no change (zero), P < .05. Testosterone treatment in juvenile hamsters facilitated an adult-like CPP for VS, and dopamine antagonism prevented the CPP for VS at multiple doses.

Figure 3.

CPA to 0.45 mg/kg haloperidol in testosterone-manipulated juvenile hamsters. Corrected changes in preference and difference scores are shown; mean ± SE. * Indicates difference from no change (zero), P < .05. The 2 lower doses of dopamine antagonist did not result in a CPA.

Figure 4.

Movement (top) and fecal boli output (bottom) of hamsters in vehicle- and haloperidol-paired chambers, mean ± SE. * Indicates differences between chambers within an animal, P < .05. Haloperidol did not affect movement but did increase fecal boli output at the highest dose.

Figure 5.

Attraction score to vaginal secretions (VS) in haloperidol-treated hamsters, mean ± SE. # Indicates difference from vehicle. * Indicates difference from no preference (zero), P < .05. Haloperidol reduced attraction to VS at all doses but less so at the 0.15-mg/kg dose.