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.
Little is known about how the brain regulates context appropriate communication. European starlings (Sturnus vulgaris) are seasonally-breeding songbirds that produce song in various social contexts. During the breeding season, males that acquire nest sites sing high levels of sexually-motivated song in response to a female. Outside of this context, however, song rates are not affected by female presence. The medial preoptic nucleus (POM) is a region outside of the song control system that regulates male sexual behavior, and several studies in songbirds implicate the POM in sexuallymotivated song. However, 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 non-sexual contexts in response to various social stimuli were examined. Lesions to the POM exclusively reduced song and nest box-directed behaviors within highly sexually relevant contexts. Unexpectedly, POM lesions increased song in a non-sexual 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.
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). 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.
The catecholamines dopamine and norepinephrine are implicated in affiliative behaviors, yet few studies have addressed the extent to which affiliative behaviors within distinct social settings rely upon similar or distinct catecholaminergic mechanisms. To explore the role of catecholamines in affiliative behavior within distinct long-term social contexts, we examined the density of the catecholamine synthetic enzyme tyrosine hydroxylase (TH) in brain regions within both the mesolimbic dopaminergic system and “social behavior network” in male and female zebra finches (Taeniopygia guttata) paired for 21 days with either a same- or opposite-sex conspecific. On days 16-21 after pairing, members of both same- and mixed-sex pairs produced similar rates of affiliative behaviors. Measures of affiliation related to TH labeling in the ventral tegmental area (VTA), nucleus accumbens (Ac), medial preoptic nucleus (POM), and ventromedial nucleus of the hypothalamus (VMH). Relationships between TH labeling density and specific measures of affiliative behavior differed in rostral compared to caudal subregions of Ac and VTA, suggesting distinct roles for these subregions in the regulation of affiliative behavior. Finally, TH labeling density in the VMH and rostral VTA were positively related to the amount of courtship received from the partner and TH labeling in Ac was denser in opposite-sex pairs compared to same-sex pairs, indicative of socially-induced brain plasticity. Overall, results highlight a complex region- and behavior-specific role for catecholamines in vertebrate affiliation.
Despite recent exciting research about pair bonding, little is known about how mammalian vocalizations change with the initiation and maintenance of pair bonding in monogamous species. Moreover, even less is known about the significance of pair bond resilience in the face of social challenges. In the strictly monogamous California mouse (Peromyscus californicus), we measured changes in ultrasonic vocalizations (USV) and other behaviors within male-female dyads over the course of pair bonding and characterized associations of USVs with affiliation and aggression. After 1 week of cohabitation, pairs exhibited decreased aggression and "bark" USVs, and increased "simple sweep" and "sustained vocalization" (SV) USV types. Accordingly, the number of barks was associated with aggression, whereas the number of simple sweeps and the number, call duration and bout size of SVs corresponded with affiliation. We then experimentally assessed the impact of an infidelity challenge (1 week cohabitation with an unfamiliar, opposite-sex, extra-pair individual) for both sexes on pair social behavior, acoustic behavior, and reproductive success. The infidelity challenge temporarily disrupted pair bond interactions during pair reunion, independent of which sex experienced the infidelity challenge, via both increases in aggression and barks, and a stunting of affiliation and SVs, compared to control pairs. Pair reproductive success, in the form of birth latency, litter size, pup survival and birth weight, did not differ between infidelity challenge pairs and controls. The quality of pair interactions, however, was associated with reproductive success: aggression during pair reunion across all pairs was associated with a lower likelihood of successfully producing a litter. Similarly, among infidelity challenge pairs, but not the controls, there was a positive association between pair affiliation and paternal care, and a negative association between pair aggression and paternal care. Overall, the infidelity challenge revealed a weak negative effect on reproductive success, but we speculate, based on our results, that greater resiliency of a pair bond can moderate negative effects of a social challenge.
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