The constitutive differential transcriptome of a brain circuit for vocal learning

Peter V Lovell,Morgan Wirthlin,Claudio V Mello,Samantha R Friedrich,Nicole A Huizinga

doi:10.1186/s12864-018-4578-0

Peter V Lovell, Morgan Wirthlin + Show 3 more

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https://doi.org/10.1186/s12864-018-4578-0

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Abstract

BackgroundThe ability to imitate the vocalizations of other organisms, a trait known as vocal learning, is shared by only a few organisms, including humans, where it subserves the acquisition of speech and language, and 3 groups of birds. In songbirds, vocal learning requires the coordinated activity of a set of specialized brain nuclei referred to as the song control system. Recent efforts have revealed some of the genes that are expressed in these vocal nuclei, however a thorough characterization of the transcriptional specializations of this system is still missing. We conducted a rigorous and comprehensive analysis of microarrays, and conducted a separate analysis of 380 genes by in situ hybridizations in order to identify molecular specializations of the major nuclei of the song system of zebra finches (Taeniopygia guttata), a songbird species.ResultsOur efforts identified more than 3300 genes that are differentially regulated in one or more vocal nuclei of adult male birds compared to the adjacent brain regions. Bioinformatics analyses provided insights into the possible involvement of these genes in molecular pathways such as cellular morphogenesis, intrinsic cellular excitability, neurotransmission and neuromodulation, axonal guidance and cela-to-cell interactions, and cell survival, which are known to strongly influence the functional properties of the song system. Moreover, an in-depth analysis of specific gene families with known involvement in regulating the development and physiological properties of neuronal circuits provides further insights into possible modulators of the song system.ConclusionOur study represents one of the most comprehensive molecular characterizations of a brain circuit that evolved to facilitate a learned behavior in a vertebrate. The data provide novel insights into possible molecular determinants of the functional properties of the song control circuitry. It also provides lists of compelling targets for pharmacological and genetic manipulations to elucidate the molecular regulation of song behavior and vocal learning.

Highlights

The ability to imitate the vocalizations of other organisms, a trait known as vocal learning, is shared by only a few organisms, including humans, where it subserves the acquisition of speech and language, and 3 groups of birds
Most thoroughly studied in the zebra finch (Taeniopygia guttata), a representative songbird species, the acquisition, memorization, and production of learned birdsong requires the coordinated activity of a set of specialized brain nuclei that are collectively referred to as the song control system [1, 2, 5,6,7]
The song control system is organized into two distinct but interconnected pathways, consisting of a direct vocalmotor pathway (DMP; whereas nXIIts markers were mostly Fig. 1; nuclei and projections in black), which is required for the production of song [8, 9], and an anterior forebrain pathway (AFP; Fig. 1; nuclei and projections in white), which is required for the acquisition of song [10,11,12], and adult vocal plasticity [13,14,15,16]

Summary

Introduction

The ability to imitate the vocalizations of other organisms, a trait known as vocal learning, is shared by only a few organisms, including humans, where it subserves the acquisition of speech and language, and 3 groups of birds. Vocal learning requires the coordinated activity of a set of specialized brain nuclei referred to as the song control system. Most thoroughly studied in the zebra finch (Taeniopygia guttata), a representative songbird species, the acquisition, memorization, and production of learned birdsong requires the coordinated activity of a set of specialized brain nuclei that are collectively referred to as the song control system [1, 2, 5,6,7]. The DMP is comprised of pre-motor pallial (cortical-like) nucleus HVC, which sends axonal projections to the robust nucleus of the arcopallium (RA), the vocal-motor output nucleus of the telencephalon

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