High responsiveness of auditory neurons to specific combination of acoustic features in female songbirds

Abstract

Zebra finch (Taeniopygia guttata) is a songbird species in which males sing their unique songs to attract females who then select their preferred male. Acoustic features in the songs of individual males are important features for female auditory perception. While the male of this species is a classic model of vocal production, it has been little known about auditory processing in female. In the higher auditory brain regions, the caudomedial mesopallium (CMM) and nidopallium (NCM) contribute to female's sound recognition, we, therefore, extracted acoustic features that induce neural activities with high detection power on both regions in female finches. A multiple linear regression analysis revealed that neurons were sensitive to mean frequency and Wiener entropy. In addition, we performed an experiment with modified artificial songs and harmonic songs to directly investigate neural responsiveness for deriving further evidence for the contribution of these two acoustic features. Finally, we illustrated a specific ratio combining these two acoustic features that showed highest sensitivity to neural responsiveness, and we found that properties of sensitivity are different between CMM and NCM. Our results indicate that the mixture of the two acoustic features with the specific ratio is important in the higher auditory regions of female songbirds, and these two regions have differences in encoding for sensitivity to these acoustic features.

Effects of Cortical FoxP1 Knockdowns on Learned Song Preference in Female Zebra Finches

“…CMM and HVC were tested specifically because both areas are involved in supporting memory, sensory feedback, and motor learning ( Bell et al, 2015 ; Roberts et al, 2017 ; Soyman and Vicario, 2017 ; Inda et al, 2020 , 2021 ), and typically show high FoxP1 expression in juvenile and adult zebra finches ( Fig. 2 a , g ; Teramitsu et al, 2004 ; Mendoza et al, 2015 ).…”

“…While HVC can be seen as a hub of auditory and motor input, relaying information and input from multiple sources in both the sensory and motor song circuit ( Roberts et al, 2012 ; Lynch et al, 2013 ), studies of immediate early gene (IEG) expression have implicated CMM in tutor song memory ( Bolhuis et al, 2000 ; Terpstra et al, 2006 ; Eda-Fujiwara et al, 2016 ) because neuronal activity increases more after familiar than unfamiliar stimulus presentation. CMM neuronal activity is also associated with auditory perception and discrimination based on extracellular recordings in female ( Inda et al, 2020 , 2021 ) and male zebra finches during passive playbacks ( Woolley et al, 2005 ), Go/Nogo tasks ( Bell et al, 2015 ), and functional fMRI ( Boumans et al, 2008 ). In this study, preferences for tutor song were equally strong in CMM knockdowns and untreated control females, suggesting no functional role of FoxP1 in song preference and its acquisition.…”

“…FoxP1 could be involved in this process because it is expressed in HVC and caudomedial mesopallium (CMM) of both sexes ( Teramitsu et al, 2004 ; Chen et al, 2013 ; Mendoza et al, 2015 ; this study) although it should be noted that HVC is significantly smaller in females when compared with males ( Nottebohm and Arnold, 1976 ; Nixdorf-Bergweiler, 1996 ). Both HVC and CMM are involved in song memory, auditory perception and auditory learning ( Bell et al, 2015 ; Roberts et al, 2017 ; Soyman and Vicario, 2017 ; Inda et al, 2020 , 2021 ). Other auditory areas which play important roles for song memory, preference and discrimination, such as NCM or NCL, show no elevated FoxP1 expression in comparison to the surrounding tissue in males, while this has not previously been formally evaluated in females ( Haesler et al, 2004 ; Teramitsu et al, 2004 ; Mendoza et al, 2015 ).…”