Mu opioid receptor stimulation in the nucleus accumbens increases vocal-social interactions in flocking European starlings, Sturnus vulgaris

Abstract

Social connections in gregarious species are vital for safety and survival. For these reasons, many bird species form large flocks outside the breeding season. It has been proposed that such large social groups may be maintained via reward induced by positive interactions with conspecifics and via the reduction of a negative affective state caused by social separation. Moreover, within a flock optimal social spacing between conspecifics is important, indicating that individuals may optimize spacing to be close but not too close to conspecifics. Mu opioid receptors (MORs) in the nucleus accumbens (NAc) are well known for their role in both reward and the reduction of negative affective states, suggesting that MOR stimulation in NAc may play a critical role in flock cohesion. To begin to test this hypothesis, social and non-social behaviors were examined in male and female European starlings (Sturnus vulgaris) in non-breeding flocks after intra-NAc infusion of saline and three doses of the selective MOR agonist D-Ala2, N-Me-Phe4, glycinol5-ENK (DAMGO). DAMGO in NAc dose-dependently increased singing behavior and facilitated social approaches while at the same time promoting displacements potentially used to maintain social spacing. These findings support the hypothesis that MORs in NAc promote social interactions important for group cohesion in non-sexual contexts and suggest the possibility that MOR in the NAc play a role in optimizing the pull of joining a flock with the push of potential agonistic encounters.

Significance Statement

Social interactions with conspecifics are vital for safety and survival. Group cohesion in gregarious species may be maintained by social reward and reduced negative affect, yet underlying mechanisms have not been well studied. Mu opioid receptors (MOR) in the nucleus accumbens (NAc) are strongly implicated in reward. Here, we demonstrate in flocks of European starlings that MOR stimulation in the NAc increases affiliative singing and approach behaviors as well as displacements. These results demonstrate a role for MOR in the NAc in both affiliative behaviors and behaviors used to maintain social spacing. Findings suggest that opioids in the NAc may play a role in optimizing the pull of joining a flock with the push of potential agonistic encounters.