Seasonal regulation of singing-driven gene expression associated with song plasticity in the canary, an open-ended vocal learner

Shin Hayase,Kazuhiro Wada,Wan-Chun Liu,Chihiro Mori,Masahiko Kobayashi,Chengru Shao

doi:10.1186/s13041-021-00869-5

Shin Hayase, Kazuhiro Wada + Show 4 more

Open Access

https://doi.org/10.1186/s13041-021-00869-5

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Abstract

Songbirds are one of the few animal taxa that possess vocal learning abilities. Different species of songbirds exhibit species-specific learning programs during song acquisition. Songbirds with open-ended vocal learning capacity, such as the canary, modify their songs during adulthood. Nevertheless, the neural molecular mechanisms underlying open-ended vocal learning are not fully understood. We investigated the singing-driven expression of neural activity-dependent genes (Arc, Egr1, c-fos, Nr4a1, Sik1, Dusp6, and Gadd45β) in the canary to examine a potential relationship between the gene expression level and the degree of seasonal vocal plasticity at different ages. The expression of these genes was differently regulated throughout the critical period of vocal learning in the zebra finch, a closed-ended song learner. In the canary, the neural activity-dependent genes were induced by singing in the song nuclei throughout the year. However, in the vocal motor nucleus, the robust nucleus of the arcopallium (RA), all genes were regulated with a higher induction rate by singing in the fall than in the spring. The singing-driven expression of these genes showed a similar induction rate in the fall between the first year juvenile and the second year adult canaries, suggesting a seasonal, not age-dependent, regulation of the neural activity-dependent genes. By measuring seasonal vocal plasticity and singing-driven gene expression, we found that in RA, the induction intensity of the neural activity-dependent genes was correlated with the state of vocal plasticity. These results demonstrate a correlation between vocal plasticity and the singing-driven expression of neural activity-dependent genes in RA through song development, regardless of whether a songbird species possesses an open- or closed-ended vocal learning capacity.

Highlights

Learned behaviors have species-specific features that have originated owing to species differences in the structure and physiological function of neural circuits for generating associated behavior [1,2,3,4,5]
Seasonal difference in singing‐driven Arc expression We first examined the difference in the degree of vocal plasticity of canaries whose brain tissue was sampled after a 30-min singing session at the first fall, the second spring, and the second fall
We found that Area X and lateral magnocellular nucleus of the anterior nidopallium (LMAN) in canaries have relatively consistent induction of singing-driven immediate-early genes (IEGs) expression throughout the three seasons, similar to zebra finches during the critical period of song learning [41], suggesting a consistent degree of neural firing during singing in the AFP nuclei over the course of a year

Summary

Introduction

Learned behaviors have species-specific features that have originated owing to species differences in the structure and physiological function of neural circuits for generating associated behavior [1,2,3,4,5]. The song circuits in songbirds comprise discrete, well-defined forebrain regions known as song nuclei that have comparable characteristics in terms of topological and anatomical connectivities across species (Fig. 1a). AFP, which forms a pallial (cortical)–basal ganglia–thalamic loop, is a key site for generating vocal exploratory fluctuations for song learning [15,16,17,18]. It comprises the lateral magnocellular nucleus of the anterior nidopallium (LMAN), basal ganglia nucleus Area X, and the dorsal lateral nucleus of the medial thalamus (DLM).

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