Social cues modulate the performance of communicative behaviors in a range of species, including humans, and such changes can make the communication signal more salient. In songbirds, males use song to attract females, and song organization can differ depending on the audience to which a male sings. For example, male zebra finches (Taeniopygia guttata) change their songs in subtle ways when singing to a female (directed song) compared with when they sing in isolation (undirected song), and some of these changes depend on altered neural activity from a specialized forebrain-basal ganglia circuit, the anterior forebrain pathway (AFP). In particular, variable activity in the AFP during undirected song is thought to actively enable syllable variability, whereas the lower and less-variable AFP firing during directed singing is associated with more stereotyped song. Consequently, directed song has been suggested to reflect a “performance” state, and undirected song a form of vocal motor “exploration.” However, this hypothesis predicts that directed–undirected song differences, despite their subtlety, should matter to female zebra finches, which is a question that has not been investigated. We tested female preferences for this natural variation in song in a behavioral approach assay, and we found that both mated and socially naive females could discriminate between directed and undirected song—and strongly preferred directed song. These preferences, which appeared to reflect attention especially to aspects of song variability controlled by the AFP, were enhanced by experience, as they were strongest for mated females responding to their mate's directed songs. We then measured neural activity using expression of the immediate early gene product ZENK, and found that social context and song familiarity differentially modulated the number of ZENK-expressing cells in telencephalic auditory areas. Specifically, the number of ZENK-expressing cells in the caudomedial mesopallium (CMM) was most affected by whether a song was directed or undirected, whereas the caudomedial nidopallium (NCM) was most affected by whether a song was familiar or unfamiliar. Together these data demonstrate that females detect and prefer the features of directed song and suggest that high-level auditory areas including the CMM are involved in this social perception.

Summary Context-dependence is a key feature of cortical-basal ganglia circuit activity, and in songbirds, the cortical outflow of a basal ganglia circuit specialized for song, LMAN, shows striking increases in trial-by-trial variability and bursting when birds sing alone rather than to females. To reveal where this variability and its social regulation emerge, we recorded stepwise from cortico-striatal (HVC) neurons and their target spiny and pallidal neurons in Area X. We find that cortico-striatal and spiny neurons both show precise singing-related firing across both social settings. Pallidal neurons, in contrast, exhibit markedly increased trial-by-trial variation when birds sing alone, created by highly variable pauses in firing. This variability persists even when recurrent inputs from LMAN are ablated. These data indicate that variability and its context-sensitivity emerge within the basal ganglia network, suggest a network mechanism for this emergence, and highlight variability generation and regulation as basal ganglia functions.

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The performance of courtship signals provides information about the behavioural state and quality of the signaller, and females can use such information for social decision-making (e.g. mate choice). However, relatively little is known about the degree to which the perception of and preference for differences in motor performance are shaped by developmental experiences. Furthermore, the neural substrates that development could act upon to influence the processing of performance features remains largely unknown. In songbirds, females use song to identify males and select mates. Moreover, female songbirds are often sensitive to variation in male song performance. Consequently, we investigated how developmental exposure to adult male song affected behavioural and neural responses to song in a small, gregarious songbird, the zebra finch. Zebra finch males modulate their song performance when courting females, and previous work has shown that females prefer the high-performance, female-directed courtship song. However, unlike females allowed to hear and interact with an adult male during development, females reared without developmental song exposure did not demonstrate behavioural preferences for high-performance courtship songs. Additionally, auditory responses to courtship and non-courtship song were altered in adult females raised without developmental song exposure. These data highlight the critical role of developmental auditory experience in shaping the perception and processing of song performance.

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Selection of sexual partners is among the most critical decisions that individuals make and is therefore strongly shaped by evolution. In social species, where communication signals can convey substantial information about the identity, state, or quality of the signaler, accurate interpretation of communication signals for mate choice is crucial. Despite the importance of social information processing, to date, relatively little is known about the neurobiological mechanisms that contribute to sexual decision making and preferences. In this study, we used a combination of whole-brain functional magnetic resonance imaging (fMRI), immediate early gene expression, and behavior tests to identify the circuits that are important for the perception and evaluation of courtship songs in a female songbird, the zebra finch (Taeniopygia guttata). Female zebra finches are sensitive to subtle differences in male song performance and strongly prefer the longer, faster, and more stereotyped courtship songs to non-courtship renditions. Using BOLD fMRI and EGR1 expression assays, we uncovered a novel region involved in auditory perceptual decision making located in a sensory integrative region of the avian central nidopallium outside the traditionally studied auditory forebrain pathways. Changes in activity in this region in response to acoustically similar but categorically divergent stimuli showed stronger parallels to behavioral responses than an auditory sensory region. These data highlight a potential role for the caudocentral nidopallium (NCC) as a novel node in the avian circuitry underlying the evaluation of acoustic signals and their use in mate choice.

Social experiences can profoundly shape social behavior and the underlying neural circuits. Across species, the formation of enduring social relationships is associated with both neural and behavioral changes. However, it remains unclear how longer-term relationships between individuals influence brain and behavior. Here, we investigated how variation in social relationships relates to variation in female preferences for and neural responses to song in a pair-bonding songbird. We assessed variation in the interactions between individuals in male-female zebra finch pairs and found that female preferences for their mate's song were correlated with the degree of affiliation and amount of socially modulated singing, but not with the frequency of aggressive interactions. Moreover, variation in measures of pair quality and preference correlated with variation in the song-induced expression of EGR1, an immediate early gene related to neural activity and plasticity, in brain regions important for auditory processing and social behavior. For example, females with weaker preferences for their mate's song had greater EGR1 expression in the nucleus Taeniae, the avian homologue of the mammalian medial amygdala, in response to playback of their mate's courtship song. Our data indicate that the quality of social interactions within pairs relates to variation in song preferences and neural responses to ethologically relevant stimuli and lend insight into neural circuits sensitive to social information. © 2016 Wiley Periodicals, Inc. Develop Neurobiol 76: 1029-1040, 2016.

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