Birdsong and the Neural Regulation of Positive Emotion

Abstract

Birds are not commonly admired for emotional expression, and when they are, the focus is typically on negative states; yet vocal behavior is considered a direct reflection of an individual's emotional state. Given that over 4000 species of songbird produce learned, complex, context-specific vocalizations, we make the case that songbirds are conspicuously broadcasting distinct positive emotional states and that hearing songs can also induce positive states in other birds. Studies are reviewed that demonstrate that that the production of sexually motivated song reflects an emotional state of anticipatory reward-seeking (i.e., mate-seeking), while outside the mating context song in gregarious flocks reflects a state of intrinsic reward. Studies are also reviewed that demonstrate that hearing song induces states of positive anticipation and reward. This review brings together numerous studies that highlight a potentially important role for the songbird nucleus accumbens, a region nearly synonymous with reward in mammals, in positive emotional states that underlie singing behavior and responses to song. It is proposed that the nucleus accumbens is part of an evolutionarily conserved circuitry that contributes context-dependently to positive emotional states that motivate and reward singing behavior and responses to song. Neural mechanisms that underlie basic emotions appear to be conserved and similar across vertebrates. Thus, these findings in songbirds have the potential to provide insights into interventions that can restore positive social interactions disrupted by mental health disorders in humans.

Keywords: communication; emotion; motivation; nucleus accumbens (NAc); positive affect; reward; songbird; vocal behavior.

FIGURE 1

Conditioned place preference (CPP) tests demonstrate that sexually motivated and gregarious singing behavior reflect distinct emotional states. Mean proportion time spent in a location (i.e., song-associated CPP) that had been paired previously with either low (open bar) or high (filled bar) rates of singing behavior in male starlings singing in response to a female in spring (A) and singing in a flock in fall, *p = 0.006 (C). Figures A and C replotted to show correlations between song and CPP in male starlings in spring, ns (B) and fall, p = 0.000002 (D). Y-axis represents the proportion of all vocal behaviors that were songs produced by males during and just prior to being placed into a uniquely decorated place (i.e., a birdcage). The X-axis represents the proportion of time males later spent in that place 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

Conditioned place preference (CPP) tests demonstrate that hearing sexually motivated song induces a positive emotional state in sexually motivated females. Mean (+ sem) time spent (in the absence of song playback) on the side of the CPP apparatus previously paired with male starling courtship song (minus the baseline preference for that side during habitation) in female starlings that were not (open bar) or were (filled bar) sexually motivated as indicated by exploration of nesting sites. Each point represents data from a single female. Zero on the y axis indicates no preference. * = p < 0.0027. Figure redrawn from Riters et al. (2013).

FIGURE 3

Location of subdivisions of the songbird NAc. Illustrations showing locations of (A) the rostral pole of the nucleus accumbens (ACR) and (B) the nucleus accumbens core (ACC) and shell (ACS) in the left hemisphere of coronal sections. TSM = tractus septomesencephalicus.

FIGURE 4

Subdivisions of NAc contain dopamine- and opioid-related immunolabeling in male starlings. Photomicrographs of immunolabeling for tyrosine hydroxylase at low (A,C) and high (B,D) magnification and of met-enkephalin at low (E,G) and high (F,H) magnification. See Figure 3 for abbreviations. Figures modified with permission from Polzin et al. (2021).

FIGURE 5

Numbers of FOS labeled cells within each subdivision of NAc correlate positively with the production of gregarious but not sexually motivated song in male starlings. Correlations in panel (A,B) show the rostral pole of the nucleus accumbens (ACR), (C,D) the accumbens core (ACC), and (E,F) the accumbens shell (ACS). Each point represents an individual bird. Presence of regression line indicates statistical significance [(B): R² = 0.49, p = 0.022; (C): R² = 0.42, p = 0.041, (D): R² = 0.46, p = 0.046]. Figure redrawn with permission from Polzin et al. (2021).

FIGURE 6

Dopamine and opioid receptor mRNA ratios in NAc differ in males that produce low versus high rates of undirected song. (A,B) Mean relative mRNA ratios + sem for D1:D2 and MOR:KOR in males that produce low (open bars) or high (filled bars) rates of song as determined using a median split. The point at which ratios diverge from 1:1 is indicated by a horizontal line. * = p < 0.05. (C,D) Scatterplots illustrating relationships between dopamine and opioid receptor mRNA ratios in NAc and undirected song in males. Each point represents an individual male. Open dots indicate low and filled dots represent high singers in bar graphs. The regression line indicates a significant correlation (p < 0.05). Data from Alger et al. (2021). Reproduced with permission.

FIGURE 7

Stimulation of MOR in NAc increases gregarious song, approach, and displacements. Mean + sem (A) number of song bouts, (B) proportion of approach behaviors, and (C) proportion of displacements in male (squares) and female (circles) starlings in which the cannula tip missed the NAc (open bars; n = 8) or hit the NAc (filled bars; n = 6). Lines indicate significant effects (*p < 0.05). Misses were in numerous locations outside the NAc. Figure modified from Maksimoski et al. (2021).

FIGURE 8

Dopamine and opioid receptor mRNA ratios in NAc differ in females whose partners produced low versus high rates of undirected song. (A,B) Mean relative mRNA ratios + sem for D1:D2 and MOR:KOR in females paired with males that produced low (open bars) or high (filled bars) rates of song as determined using a median split. The point at which ratios diverge from 1:1 is indicated by a horizontal line. (C,D) Scatterplots illustrating relationships between dopamine and opioid receptor mRNA ratios in the female NAc and the number of undirected songs produced by her partner. Each point represents an individual female. Open dots indicate females with male partners that sang at low and filled dots represent partners that sang at high rates in bar graphs. The regression line indicates a significant correlation (p < 0.05). Data from Alger et al. (2021). Reproduced with permission.

FIGURE 9

A possible pathway by which the NAc may coordinate an individual’s emotional state with singing behavior. Sagittal illustration of a songbird brain. A circuit from the preoptic area (POM) to the ventral tegmental area (VTA) to the nucleus accumbens (NAc) and back to the POM is proposed to regulate affective states that can influence singing behavior and perception through its projections to song control nuclei. See text for additional details.