Drinking songs: alcohol effects on learned song of zebra finches.

Andrey E Ryabinin,Devin C Owen,Christopher R Olson,Claudio V Mello,Stephanie Ann White

doi:10.1371/journal.pone.0115427

Andrey E Ryabinin, Devin C Owen + Show 3 more

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https://doi.org/10.1371/journal.pone.0115427

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Abstract

Speech impairment is one of the most intriguing and least understood effects of alcohol on cognitive function, largely due to the lack of data on alcohol effects on vocalizations in the context of an appropriate experimental model organism. Zebra finches, a representative songbird and a premier model for understanding the neurobiology of vocal production and learning, learn song in a manner analogous to how humans learn speech. Here we show that when allowed access, finches readily drink alcohol, increase their blood ethanol concentrations (BEC) significantly, and sing a song with altered acoustic structure. The most pronounced effects were decreased amplitude and increased entropy, the latter likely reflecting a disruption in the birds’ ability to maintain the spectral structure of song under alcohol. Furthermore, specific syllables, which have distinct acoustic structures, were differentially influenced by alcohol, likely reflecting a diversity in the neural mechanisms required for their production. Remarkably, these effects on vocalizations occurred without overt effects on general behavioral measures, and importantly, they occurred within a range of BEC that can be considered risky for humans. Our results suggest that the variable effects of alcohol on finch song reflect differential alcohol sensitivity of the brain circuitry elements that control different aspects of song production. They also point to finches as an informative model for understanding how alcohol affects the neuronal circuits that control the production of learned motor behaviors.

Highlights

Alcohol consumption has wide-ranging effects on behavioral and cognitive functions, including verbal and non-verbal retention [1], and can lead to structural brain changes [2, 3]
We found that the values decreased with blood ethanol concentrations (BEC) for amplitude (t524.53, p50.0001; Fig. 6A) and increased for entropy (t52.15, p50.04; Fig. 6B); the effects were most obvious in the lower range of BECs, up to,40 mg/dl
Using a model where syllables were nested within bird ID as random factors, and BEC was included as the main factor, we found that amplitude and syllable duration both decreased and that entropy increased with increased BEC

Summary

Introduction

Alcohol consumption has wide-ranging effects on behavioral and cognitive functions, including verbal and non-verbal retention [1], and can lead to structural brain changes [2, 3]. Vocal learning is a vital prerequisite for human language acquisition, but is rare among animals, described only in cetaceans, bats, and broadly among three avian lineages, namely songbirds, hummingbirds, and parrots [10, 11] Most of these mammalian species do not lend themselves to mechanistic studies of brain function in laboratory settings, and traditional model organisms like rodents and non-human primates lack vocal learning and associated brain circuits [12]. Male zebra finches are highly motivated to sing under a variety of conditions, and there are remarkable analogies in how zebra finch song and human speech are learned and produced [10, 13] Both groups require a prolonged development period with proper environmental cues and specialized brain circuitry for vocal acquisition. A set of sophisticated tools and algorithms are currently available for quantitative analyses of bioacoustics features of finch song [19]

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