Why Do Birds Flock? A Role for Opioids in the Reinforcement of Gregarious Social Interactions

Abstract

The formation of social groups provides safety and opportunities for individuals to develop and practice important social skills. However, joining a social group does not result in any form of obvious, immediate reinforcement (e.g., it does not result in immediate copulation or a food reward), and individuals often remain in social groups despite agonistic responses from conspecifics. Much is known about neural and endocrine mechanisms underlying the motivation to perform mate- or offspring-directed behaviors. In contrast, relatively little is known about mechanisms underlying affiliative behaviors outside of these primary reproductive contexts. Studies on flocking behavior in songbirds are beginning to fill this knowledge gap. Here we review behavioral evidence that supports the hypothesis that non-sexual affiliative, flocking behaviors are both (1) rewarded by positive social interactions with conspecifics, and (2) reinforced because affiliative contact reduces a negative affective state caused by social isolation. We provide evidence from studies in European starlings, Sturnus vulgaris, that mu opioid receptors in the medial preoptic nucleus (mPOA) play a central role in both reward and the reduction of a negative affective state induced by social interactions in flocks, and discuss potential roles for nonapeptide/opioid interactions and steroid hormones. Finally, we develop the case that non-sexual affiliative social behaviors may be modified by two complementary output pathways from mPOA, with a projection from mPOA to the periaqueductal gray integrating information during social interactions that reduces negative affect and a projection from mPOA to the ventral tegmental area integrating information leading to social approach and reward.

Keywords: affiliation; medial preoptic area; mu opioid receptors; periaqueductal gray; reinforcement; social cohesion; songbirds; ventral tegmental area.

FIGURE 1

Evidence that vocal-social interactions in starling flocks are associated with a positive affective state. (A) Mean time spent on the side of a CPP apparatus that had been paired previously with either low (open bar) or high (filled bar) rates of singing behavior in flocks of male starlings. ^∗p < 0.05. (B) Correlation between song and CPP in male starlings. Y-axis represents the proportion of all vocal behaviors that were songs produced by males during and just prior to being placed in one side of the CPP apparatus (song-paired side). The X-axis represents the proportion of time males spent on the previously song-paired side of the apparatus the following day (CPP, considered a reflection of song-associated reward). Each point represents data from a single male. Figures redrawn from Riters and Stevenson (2012).

FIGURE 2

Evidence that vocal-social interactions in starling flocks are associated with pain reduction. Correlation between song production and the latency for a male to withdraw its foot from a hot water bath. Each point represents one individual. Figure redrawn from Kelm-Nelson et al. (2012).

FIGURE 3

Measures of mu opioid receptor and met-enkephalin immunolabeling in mPOA correlate with vocal-social interactions in starling flocks. (A) An inverted-U shaped curve shows the measure of flock song on the x-axis and the mean area covered by mu opioid receptor immunolabeling on the y-axis. (B) A positive linear correlation between flock song on the y-axis and the area covered by met-enkephalin immunolabeling. Each point represents one individual. Figures redrawn from Riters et al. (2005) and Kelm-Nelson and Riters (2013).

FIGURE 4

The mPOA directly accesses both canonical reward (in blue) and pain (in red) pathways via projections to (1) the ventral tegmental area [VTA; which then projects to the nucleus accumbens (NAc)] and (2) the periaqueductal gray (PAG). We develop the case that the social pleasure and pain reduction that facilitate and maintain flocking behavior may be modified by these two complementary output pathways from mPOA, with PAG integrating information during social interactions that reduces negative affect and the VTA integrating information leading to social approach and reward. Two additional regions in which opioids are proposed to interact with nonapeptides, the bed nucleus of the stria terminalis (BSTm) and lateral septum (LS) are also shown. The LS, BSTm, POA, PAG, and VTA are all reciprocally connected (connections not shown).

FIGURE 5

Correlations support roles for neuromodulators in VTA in flocking behavior in starlings. Positive correlations between flock song on the y-axis and measures of (A) neurotensin and (B) tyrosine hydroxylase mRNA in VTA. (C) Positive correlation between CB1 cannabinoid receptor mRNA on the y-axis and song-associated CPP on the x-axis. Each point represents one individual. Figures redrawn from Merullo et al. (2016) and Hahn et al. (2017).

FIGURE 6

Correlations support roles for neuromodulators in PAG in flocking behavior in starlings. (A) An inverted-U shaped curve shows the measure of flock song on the x-axis and the mean area covered by mu opioid receptor immunolabeling in PAG on the y-axis. (B) A positive linear correlation between flock song on the x-axis and the dopamine metabolite DOPAC concentrations in PAG on the y-axis. Negative correlations between flock song-associated CPP on the x-axis and measures of (C) CB1 cannabinoid receptor and (D) the cannabinoid transporter FABP7 mRNA in PAG. Each point represents one individual. Figures redrawn from Heimovics et al. (2011); Kelm-Nelson and Riters (2013), and Hahn et al. (2017).

FIGURE 7

Steroid-dependent changes in opioids in mPOA may modify flocking behavior seasonally in starlings. Mean + sem mRNA expression measures in mPOA for (A) mu opioid receptors and (B) preproenkephalin in castrated (CX; open bars) and castrated males treated with testosterone (CX + T; filled bars). (C) Numbers of cells in mPOA immunolabeled for mu opioid receptor protein in males with naturally low testosterone that were not treated with testosterone (No T) and males that were treated with testosterone (T). The middle lines in the boxes are medians, the outer edges of the boxes are 1st and 3rd quartiles (i.e., the interquartile range). The whiskers represents data within 1.5 ^∗ the interquartile range (i.e., 1.5 ^∗ the width of the box). Figures redrawn from Spool et al. (2016, 2018b).