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

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.

A neural basis for password-based species recognition in an avian brood parasite

“…Studies of activity-dependent gene induction, such as expression of immediate-early genes (IEGs), demonstrate that the NCM and CMM exhibit specific neural responses to conspecific songs as opposed to heterospecific songs in both parental (Mello et al, 1992) and brood parasitic songbirds (Louder et al, 2016), attractive conspecific songs as opposed to less attractive songs (Leitner et al, 2005;Monbureau et al, 2015), recently experienced songs as opposed to novel songs (Sockman et al, 2002), songs that include the birds' local dialect as opposed to a foreign dialect (Maney et al, 2003), as well as non-learned calls versus silence (Gobes et al, 2009). The NCM and CMM also play distinct roles in song recognition, as some songbirds exhibit greater IEG induction in the CMM in response to preferred song, whereas IEG induction in the NCM reflects song familiarity (Woolley and Doupe, 2008). Thus, the NCM and CMM have emerged as key brain regions for social recognition of acoustic cues in many species of parental and parasitic oscine birds.…”

Discrete molecular states in the brain accompany changing responses to a vocal signal

“…Habituation is not simply the loss of all neural responses to the auditory stimulus, as neurons in the auditory forebrain still fire in response to the familiar song (albeit at a somewhat lower rate compared to when the song is first novel) (9-11). These changing neural responses may be related to shifts in how the singer is perceived in the context of territorial and colonial social life (3,12,13).Studies of song response habituation have focused on a single gene, ZENK. However, other genes are likely to be involved as well, as studies in other systems have indicated that experience can affect the expression of many genes in the brain (e.g., refs.…”

Early Language Learning and the Social Brain

“…The work of Allison Doupe and her colleagues has beautifully illustrated the role of social contexts on vocal learning in the zebra finch (Woolley and Doupe 2008;Kojima and Doupe 2011). Moreover, studies on the zebra finch have also shown that motor learning occurs earlier and is more sophisticated than previously thought (Raghav and Doupe 2013).…”