Social Context–Induced Song Variation Affects Female Behavior and Gene Expression

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Abstract
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. Vocal communication in many species, including humans, is affected by social cues. In the zebra finch, for example, males make subtle changes to the length, tempo, and variability of their courtship songs (directed songs) relative to songs performed in isolation (undirected songs). Using a behavioral approach assay, we found that female zebra finches strongly prefer the sound of directed over undirected song. Interestingly, female preferences were influenced by the variability of note pitch, showing stronger preferences for directed songs when they were less variable in pitch than the undirected songs. Pitch variability is controlled by a forebrain–basal ganglia circuit, which may represent a neural substrate on which selection acts to shape behavior. Preference for directed song was also increased when the singer was familiar to the listener, suggesting that song preferences are enhanced by experience. Based on the expression of an immediate early gene associated with memory formation and plasticity, we found that two high-level auditory areas were differentially responsive to the category of song females heard, with one area responding to whether songs were directed or undirected, and a second area to whether songs were familiar or unfamiliar. Together, these data demonstrate that females detect and prefer the male's changed performance during courtship singing and suggest that neurons in high-level auditory areas are involved in this social perception.