Cholecystokinin induces crowing in chickens

Tsuyoshi Shimmura,Mai Tamura,Takamichi Yamanaka,Asuka Sasaki,Shinsaku Okamura,Takashi Yoshimura,Nobuhiro Nakao,Kunio Ihara,Shosei Ohashi

doi:10.1038/s41598-019-40746-9

Abstract

Animals that communicate using sound are found throughout the animal kingdom. Interestingly, in contrast to human vocal learning, most animals can produce species-specific patterns of vocalization without learning them from their parents. This phenomenon is called innate vocalization. The underlying molecular basis of both vocal learning in humans and innate vocalization in animals remains unknown. The crowing of a rooster is also innately controlled, and the upstream center is thought to be localized in the nucleus intercollicularis (ICo) of the midbrain. Here, we show that the cholecystokinin B receptor (CCKBR) is a regulatory gene involved in inducing crowing in roosters. Crowing is known to be a testosterone (T)-dependent behavior, and it follows that roosters crow but not hens. Similarly, T-administration induces chicks to crow. By using RNA-sequencing to compare gene expression in the ICo between the two comparison groups that either crow or do not crow, we found that CCKBR expression was upregulated in T-containing groups. The expression of CCKBR and its ligand, cholecystokinin (CCK), a neurotransmitter, was observed in the ICo. We also showed that crowing was induced by intracerebroventricular administration of an agonist specific for CCKBR. Our findings therefore suggest that the CCK system induces innate vocalization in roosters.

Highlights

There are many vertebrate and invertebrate animals that use sound for communication, and their patterns and functions are species-specific
Innate vocalization is a simpler behavior than human language and can serve as an excellent model to uncover the molecular basis of vocalization
One possible explanation for this is that changes in gene expression are smaller in the specific nucleus of the brain compared with peripheral tissues[19]

Summary

Introduction

There are many vertebrate and invertebrate animals that use sound for communication, and their patterns and functions are species-specific. In contrast to human vocal learning, most animals can produce species-specific patterns of vocalization without learning them from their parents[3], which is a phenomenon called innate vocalization. The underlying molecular basis of both vocal learning in humans and innate vocalization remains a mystery. Chicks do not crow, chick crowing can be induced by chronic T administration[9] As these reports have shown, T regulates innate vocalization, but the genes that are regulated by T in this process remain unknown. Electrical stimulation of vocalization in the intercollicular nucleus (ICo) region in a number of bird species is controversial due to the complex organization of this area and the current applied[11,12,13,14,15], the upstream center of vocalization has been proposed to be localized in the ICo of the midbrain[10] (Supplementary Fig. S1). We compared gene expression in the ICo using RNA-sequencing between the two comparison groups and showed that CCKBR, which encodes the cholecystokinin B receptor, is the gene that induces crowing

Methods

Results

Conclusion