Male song quality modulates c-Fos expression in the auditory forebrain of the female canary

Abstract

In canaries, specific phrases of male song (sexy songs, SS) that are difficult to produce are especially attractive for females. Females exposed to SS produce more copulation displays and deposit more testosterone into their eggs than females exposed to non-sexy songs (NS). Increased expression of the immediate early genes c-Fos or zenk (a.k.a. egr-1) has been observed in the auditory forebrain of female songbirds hearing attractive songs. C-Fos immunoreactive (Fos-ir) cell numbers were quantified here in the brain of female canaries that had been collected 30 min after they had been exposed for 60 min to the playback of SS or NS or control white noise. Fos-ir cell numbers increased in the caudomedial mesopallium (CMM) and caudomedial nidopallium (NCM) of SS birds as compared to controls. Song playback (pooled SS and NS) also tended to increase average Fos-ir cell numbers in the mediobasal hypothalamus (MBH) but this effect did not reach full statistical significance. At the individual level, Fos expression in CMM was correlated with its expression in NCM and in MBH but also with the frequency of calls that females produced in response to the playbacks. These data thus indicate that male songs of different qualities induce a differential metabolic activation of NCM and CMM. The correlation between activation of auditory regions and of the MBH might reflect the link between auditory stimulation and changes in behavior and reproductive physiology.

Species-Specific Auditory Forebrain Responses to Non-Learned Vocalizations in Juvenile Blackbirds

“…For instance, both NCM and CMM are selective for conspecific songs over heterospecific songs in adults of both parental [Mello et al, 1992;Hauber et al, 2013] and in brood parasitic songbirds [Louder et al, 2016]. In songbirds, IEG induction in these auditory forebrain regions also responds selectively to attractive conspecific songs over less attractive songs [Leitner et al, 2005;Monbureau et al, 2015], recently experienced songs over novel songs [Sockman et al, 2002], and songs that include the birds' local dialect over a foreign dialect [Maney et al, 2003]. Thus, NCM and CMM are clearly critical regions that underlie social perception and recognition in songbirds and exhibit selective responses to biologically meaningful auditory stimuli [Louder et al, 2018].…”

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

“…The amount of expression of these genes in these two auditory regions is not simply related to whether the bird is exposed to conspecific song or some other sound, rather IEG induction also reflects biologically relevant characteristics of the song, such as: regional dialects (Maney et al, 2003), song quality (Leitner et al, 2005;Monbureau et al, 2015), recent experience with song (Sockman et al, 2002), associative and non-associative song learning (Gentner et al, 2004;Jarvis et al, 1995), and even whether the song is directed to a conspecific or undirected (Woolley and Doupe, 2008). These patterns of gene induction hold true across sexes Lynch et al, 2012;Mello et al, 2004;Monbureau et al, 2015;Woolley and Doupe, 2008) and various passerine species (Gentner et al, 2004;Louder et al, 2016;Maney et al, 2003;Mello et al, 1992;Schubloom and Woolley, 2016). Interestingly, our results not only reveal that the NCM also represents non-learned vocalizations in juvenile cowbirds but we also report that the NCM and CMM are responding differently to this vocalization in juvenile birds but not adults.…”

“…Just as the auditory cortex is vital to perceptual processing of auditory information in mammals (Kanwal and Rauschecker, 2007), the NCM and CMM are vital to social perception and recognition in songbirds, and exhibit selective responses to biologically meaningful auditory stimuli (Mello et al, 2004). 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).…”

Serotonin, estrus, and social context influence c-Fos immunoreactivity in the inferior colliculus.

“…Females may prefer particular types of male calls over others (e.g., Maney et al, 2003; Wilczynski & Lynch et al, 2011; Schubloom & Wooley, 2016; Brenowitz & Remage-Healey, 2016), and this preference behavior may track naturally varying reproductive status, or be influenced by the manipulation of ovarian hormones (Lynch et al, 2005; 2006; Ward et al, 2015). In parallel to this changing behavioral responsiveness, the auditory systems of females show preferential electrophysiological responses, or changes in immediate early gene expression, to male calls of particular structure, and these responses may also interact with variation in the hormonal milieu (Maney et al, 2006; Lynch & Wilczynski, 2008; Miranda & Wilczynski, 2009b; Svec & Wade, 2009; Chakraborty & Burmeister, 2015; Giret et al, 2015; Monbureau et al, 2015; Brenowitz & Remage-Healey, 2016). Peripheral or central changes in hormonal sensitivity may thus result in female auditory systems that are better matched to, more responsive to, or more discriminating of male signals (Forlano, et al, 2005; Sisneros, et al, 2004; Sisneros, 2009; Lynch & Wilczynski, 2008; Zeyl et al, 2013; Caras et al, 2015).…”