Abstract

BackgroundSpecialized neural pathways, the song system, are required for acquiring, producing, and perceiving learned avian vocalizations. Birds that do not learn to produce their vocalizations lack telencephalic song system components. It is not known whether the song system forebrain regions are exclusively evolved for song or whether they also process information not related to song that might reflect their ‘evolutionary history’.Methodology/Principal FindingsTo address this question we monitored the induction of two immediate-early genes (IEGs) c-Fos and ZENK in various regions of the song system in zebra finches (Taeniopygia guttata) in response to an aversive food learning paradigm; this involves the association of a food item with a noxious stimulus that affects the oropharyngeal-esophageal cavity and tongue, causing subsequent avoidance of that food item. The motor response results in beak and head movements but not vocalizations. IEGs have been extensively used to map neuro-molecular correlates of song motor production and auditory processing. As previously reported, neurons in two pallial vocal motor regions, HVC and RA, expressed IEGs after singing. Surprisingly, c-Fos was induced equivalently also after food aversion learning in the absence of singing. The density of c-Fos positive neurons was significantly higher than that of birds in control conditions. This was not the case in two other pallial song nuclei important for vocal plasticity, LMAN and Area X, although singing did induce IEGs in these structures, as reported previously.Conclusions/SignificanceOur results are consistent with the possibility that some of the song nuclei may participate in non-vocal learning and the populations of neurons involved in the two tasks show partial overlap. These findings underscore the previously advanced notion that the specialized forebrain pre-motor nuclei controlling song evolved from circuits involved in behaviors related to feeding.

Highlights

  • Spoken language, speech, is learned during early childhood via imitation

  • The song system of zebra finches was studied in numerous experiments in the context of vocal learning, song production and song processing, the present work examined for the first time a possible involvement of the song nuclei in a learning task which does not implicate song production or perception

  • immediate-early genes (IEGs) induction after a non-vocal one trial aversive food learning paradigm was compared to the well known IEG induction as a result of singing in song motor regions, or as a result of hearing song in auditory song regions

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Summary

Introduction

Speech, is learned during early childhood via imitation. Besides humans, a small number of vertebrate taxa, among them songbirds, are capable of vocal learning. How the brain regions required for learned speech in humans and learned song in songbirds evolved from species that lacked these traits is not known, it has been proposed that they duplicated from adjacent motor areas [4,15,16] or arose from auditory regions [17,18] It is not known whether the song nuclei are specialized exclusively for vocal behavior or whether they are implicated in other types of behavior as well. Birds that do not learn to produce their vocalizations lack telencephalic song system components It is not known whether the song system forebrain regions are exclusively evolved for song or whether they process information not related to song that might reflect their ‘evolutionary history’

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