Birdsong and the Neural Regulation of Positive Emotion.

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.

Differences in dopamine and opioid receptor ratios in the nucleus accumbens relate to physical contact and undirected song in pair-bonded zebra finches.

Long-term social bonds are critical for survival and reproductive success in many species. Although courtship and pair-bond formation are relatively well studied, much less is known about the neural regulation of behaviors that occur after pair bonding that reinforce the bond and contribute to reproductive success. Dopamine and opioids in the nucleus accumbens (NAc) alter motivational state and reward by binding to receptor subtypes that engage distinct and opposing second messenger systems, and there is evidence that receptor ratios may influence social behavior. We used quantitative real-time PCR to explore relationships between messenger RNA ratios for dopamine D1 and D2 receptors (D1:D2) and mu and kappa opioid receptors (MOR:KOR) in NAc and behaviors implicated in reproductive investment and pair-bond maintenance in established male-female zebra finch pairs. In males, D1:D2 expression in NAc related negatively, whereas MOR:KOR related positively, to undirected song production. D1:D2 receptors also related positively to physical contact with a female. For females, D1:D2 expression was lower in females exposed to high compared to low rates of the partner's undirected song, and MOR:KOR expression in females related positively to undirected song exposure and allopreening. Analyses of single genes did not yield the same results. These findings suggest that the ratio of D1 to D2 and MOR to KOR receptor signaling in NAc causes differences in behavior or that behavior (or the partner's behavior) causes receptor ratio changes to modulate behaviors that maintain pair bonds and promote reproductive investment. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Complex patterns of dopamine-related gene expression in the ventral tegmental area of male zebra finches relate to dyadic interactions with long-term female partners.

Dopaminergic projections from the ventral tegmental area (VTA) to multiple efferent targets are implicated in pair bonding, yet the role of the VTA in the maintenance of long-term pair bonds is not well characterized. Complex interactions between numerous neuromodulators modify activity in the VTA, suggesting that individual differences in patterns of gene expression in this region may explain individual differences in long-term social interactions in bonded pairs. To test this hypothesis we used RNA-seq to measure expression of over 8000 annotated genes in male zebra finches in established male-female pairs. Weighted gene co-expression network analysis identified a gene module that contained numerous dopamine-related genes with TH found to be the most connected gene of the module. Genes in this module related to male agonistic behaviors as well as bonding-related behaviors produced by female partners. Unsupervised learning approaches identified two groups of males that differed with respect to expression of numerous genes. Enrichment analyses showed that many dopamine-related genes and modulators differed between these groups, including dopamine receptors, synthetic and degradative enzymes, the avian dopamine transporter and several GABA- and glutamate-related genes. Many of the bonding-related behaviors closely associated with VTA gene expression in the two male groups were produced by the male's partner, rather than the male himself. Collectively, results highlight numerous candidate genes in the VTA that can be explored in future studies and raise the possibility that the molecular/genetic organization of the VTA may be strongly shaped by a social partner and/or the strength of the pair bond.

A novel statistical method for behaviour sequence analysis and its application to birdsong.

Complex vocal signals, such as birdsong, contain acoustic elements that differ in both order and duration. These elements may convey socially relevant meaning, both independently and through their interactions, yet statistical methods that combine order and duration data to extract meaning have not, to our knowledge, been fully developed. Here we design novel semi-Markov methods, Bayesian estimation and classification trees to extract order and duration information from behavioural sequences and apply these methods to songs produced by male European starlings, Sturnus vulgaris, in two social contexts in which the function of song differs: a spring (breeding) and autumn (nonbreeding) context. Additionally, previous data indicate that damage to the medial preoptic nucleus (POM), a brain area known to regulate male sexually motivated behaviour, affects structural aspects of starling song such that males in a sexually relevant context (i.e. spring) sing shorter songs than appropriate for this context. We further test the utility of our statistical approach by comparing attributes of song structure in POM-lesioned males to song produced by control spring and autumn males. Spring and autumn songs were statistically separable based on the duration and order of phrase types. Males produced more structurally complex aspects of song in spring than in autumn. Spring song was also longer and more stereotyped than autumn song, both attributes used by females to select mates. Songs produced by POM-lesioned males in some cases fell between measures of spring and autumn songs but differed most from songs produced by autumn males. Overall, these statistical methods can effectively extract biologically meaningful information contained in many behavioural sequences given sufficient sample sizes and replication numbers.

Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings.

The medial preoptic nucleus (POM) is a brain region outside of the song control system of songbirds. It has been implicated in song production, sexual motivation, and the integration of both sensory and hormonal information with appropriate behavioral responses. The POM is well positioned neuroanatomically to interact with multiple regions involved in song, social behavior, and motivation. However, little is known about the brain regions with which the POM directly or indirectly communicates to influence song. To gain insight into the neuronal circuits normally activated in association with POM activity during male song, we compared activity within multiple brain regions using immunolabeling for protein products of immediate early genes (IEGs) zenk (aka egr-1) and c-fos (indirect markers of neuronal activity) in sham and POM-lesioned male European starlings (Sturnus vulgaris). As compared to sham lesions, POM lesions disrupted song and interest in a nest box, and females responded less to POM-lesioned males. POM lesions reduced numbers of IEG-labeled cells and disrupted correlations between numbers of IEG-labeled cells and song within several song control, limbic, hypothalamic and midbrain regions. These results are consistent with the possibility that the POM integrates activity among nuclei involved in song control, social behavior and motivational state that work in concert to promote sexually motivated communication.

Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris).

Little is known about how the brain regulates context-appropriate communication. European starlings produce song in various social contexts. During the breeding season, males with nest sites sing high levels of sexually motivated song in response to a female. Outside of this context, song rates are not affected by female presence. The medial preoptic nucleus (POM) regulates male sexual behavior, and studies in songbirds implicate the POM in sexually motivated song. Recent data suggest that the role of the POM might extend to song produced in other contexts as well. To examine this possibility, effects of bilateral electrolytic lesions of the POM on singing and other behaviors in adult male starlings within sexually relevant and nonsexual contexts were studied. Lesions to the POM exclusively reduced song and nest box-directed behaviors within highly sexually relevant contexts. Unexpectedly, POM lesions increased song in a nonsexual context, suggesting an inhibitory role for the POM in this context. These data suggest that the POM interacts with the song control system so that song occurs in an appropriate social context in response to appropriate stimuli.

Neuroanatomical evidence for indirect connections between the medial preoptic nucleus and the song control system: possible neural substrates for sexually motivated song.

In European starlings ( Sturnus vulgaris) as in other seasonally breeding songbirds, a major function of song during the breeding season is mate attraction, and song in this context is highly sexually motivated. Song learning, perception, and production are regulated by nuclei of the song control system, but there is no evidence that these nuclei participate in the motivation to sing. Evidence suggests that the medial preoptic nucleus (POM), a diencephalic nucleus outside of the song control system, might regulate the motivation to sing, at least in a sexual context. If the POM is involved in the regulation of sexually motivated song, then this structure must interact with the song control system. To examine possible neuroanatomical connections between the POM and song control nuclei a tract-tracing study was performed in male starlings using the antero- and retrograde tract tracer, biotinylated dextran amine (BDA). No direct connections were identified between the POM and song control nuclei; however, labeled fibers were found to terminate in a region bordering dorsal-medial portions of the robust nucleus of the archistriatum (RA). Additionally, several indirect routes via which the POM might communicate with the song control system were identified. Specifically, POM projected to dorsomedial nucleus intercollicularis (DM), mesencephalic central gray (GCt), area ventralis of Tsai (AVT), and locus ceruleus (LoC), structures projecting directly to nuclei involved in song production (DM --> vocal-patterning and respiratory nuclei; GCt, AVT, LoC --> RA and HVC, and the context in which song is sung (AVT --> area X). These results are consistent with the possibility that the POM regulates sexually motivated song through interactions with brain regions involved in vocal production.