High throughput analysis reveals dissociable gene expression profiles in two independent neural systems involved in the regulation of social behavior

Tyler J Stevenson,Jenny Drnevich,Kirstin Replogle,David F Clayton,Gregory F Ball

doi:10.1186/1471-2202-13-126

Abstract

BackgroundProduction of contextually appropriate social behaviors involves integrated activity across many brain regions. Many songbird species produce complex vocalizations called ‘songs’ that serve to attract potential mates, defend territories, and/or maintain flock cohesion. There are a series of discrete interconnect brain regions that are essential for the successful production of song. The probability and intensity of singing behavior is influenced by the reproductive state. The objectives of this study were to examine the broad changes in gene expression in brain regions that control song production with a brain region that governs the reproductive state.ResultsWe show using microarray cDNA analysis that two discrete brain systems that are both involved in governing singing behavior show markedly different gene expression profiles. We found that cortical and basal ganglia-like brain regions that control the socio-motor production of song in birds exhibit a categorical switch in gene expression that was dependent on their reproductive state. This pattern is in stark contrast to the pattern of expression observed in a hypothalamic brain region that governs the neuroendocrine control of reproduction. Subsequent gene ontology analysis revealed marked variation in the functional categories of active genes dependent on reproductive state and anatomical localization. HVC, one cortical-like structure, displayed significant gene expression changes associated with microtubule and neurofilament cytoskeleton organization, MAP kinase activity, and steroid hormone receptor complex activity. The transitions observed in the preoptic area, a nucleus that governs the motivation to engage in singing, exhibited variation in functional categories that included thyroid hormone receptor activity, epigenetic and angiogenetic processes.ConclusionsThese findings highlight the importance of considering the temporal patterns of gene expression across several brain regions when engaging in social behaviors.

Highlights

Production of contextually appropriate social behaviors involves integrated activity across many brain regions
Using microarray cDNAs designed for use in songbirds [23] we investigated the patterns of gene expression from song control regions (HVC, RA and Area X) in relation to the nucleus that governs the seasonal change in reproductive state, the preoptic area (POA)
Breeding birds had significantly greater volumes compared to pre-breeding birds (SD56; p < 0.001). These findings indicate that the starlings were collected while in the intended physiological states and provide a reliable indicator that the song system brain regions and POA exhibited the predicted changes in neural plasticity

Summary

Introduction

Production of contextually appropriate social behaviors involves integrated activity across many brain regions. Discrete interconnected regions in the passerine brain control the vocal variability and stereotyped motor production required to produce an individual’s song [6,7](Figure 1A). Activity within these regions varies with the social environment to produce the contextually appropriate song [8,9]. A second afferent projection from HVC innervates the nucleus Area X This pathway is involved in processing auditory feedback needed to learn and maintain song, inducing vocal variability during song learning and adjusting song quality according to the social context [6,8,11,12]. These brain regions are part of a neural circuit regulating song behavior known as the song control system [5]

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