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Adult birdsong is actively maintained by error correction.

ABSTRACT: Humans learn to speak by a process of vocal imitation that requires the availability of auditory feedback. Similarly, young birds rely on auditory feedback when learning to imitate the songs of adult birds, providing one of the few examples of nonhuman vocal learning. However, although humans continue to use auditory feedback to correct vocal errors in adulthood, the mechanisms underlying the stability of adult birdsong are unknown. We found that, similar to human speech, adult birdsong is maintained by error correction. We perturbed the pitch (fundamental frequency) of auditory feedback in adult Bengalese finches using custom-designed headphones. Birds compensated for the imposed auditory error by adjusting the pitch of song. When the perturbation was removed, pitch returned to baseline. Our results indicate that adult birds correct vocal errors by comparing auditory feedback to a sensory target and suggest that lifelong error correction is a general principle of learned vocal behavior.

SUBMITTER: Sober SJ

PROVIDER: S-EPMC2701972 | biostudies-literature | 2009 Jul

REPOSITORIES: biostudies-literature

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Adult birdsong is actively maintained by error correction.

Sober Samuel J SJ Brainard Michael S MS

Nature neuroscience 20090614 7

Humans learn to speak by a process of vocal imitation that requires the availability of auditory feedback. Similarly, young birds rely on auditory feedback when learning to imitate the songs of adult birds, providing one of the few examples of nonhuman vocal learning. However, although humans continue to use auditory feedback to correct vocal errors in adulthood, the mechanisms underlying the stability of adult birdsong are unknown. We found that, similar to human speech, adult birdsong is maint ...[more]

PMID: 19525945

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Project description:BackgroundRNA polymerase (pol) III transcribes a unique class of genes with intra-genic promoters and high transcriptional activity. The major contributors to the pol III transcriptome, tRNAs genes are found scattered on all chromosomes of yeast. A prototype tDNA of <150 bp length, is generally considered nucleosome-free while some pol III-transcribed genes have been shown to have nucleosome-positioning properties.ResultsUsing high resolution ChIP-chip and ChIP-seq methods, we found several unique features associated with nucleosome profiles on all tRNA genes of budding yeast, not seen on nucleosome-dense counterparts in fission yeast and resting human CD4+ T cells. The nucleosome-free region (NFR) on all but three yeast tDNAs is found bordered by an upstream (US) nucleosome strongly positioned at -140 bp position and a downstream (DS) nucleosome at variable positions with respect to the gene terminator. Perturbation in this nucleosomal arrangement interferes with the tRNA production. Three different chromatin remodelers generate and maintain the NFR by targeting different gene regions. Isw1 localizes to the gene body and makes it nucleosome-depleted, Isw2 maintains periodicity in the upstream nucleosomal array, while RSC targets the downstream nucleosome. Direct communication of pol III with RSC serves as a stress-sensory mechanism for these genes. In its absence, the downstream nucleosome moves towards the gene terminator. Levels of tRNAs from different families are found to vary considerably as different pol III levels are seen even on isogenes within a family. Pol III levels show negative correlation with the nucleosome occupancies on different genes.ConclusionsBudding yeast tRNA genes maintain an open chromatin structure, which is not due to sequence-directed nucleosome positioning or high transcription activity of genes. Unlike 5' NFR on pol II-transcribed genes, the tDNA NFR, which facilitates tDNA transcription, results from action of chromatin remodeler Isw1, aided by Isw2 and RSC. The RSC-regulated nucleosome dynamics at the 3' gene-end serves as a novel regulatory mechanism for pol III transcription in vivo, probably by controlling terminator-dependent facilitated recycling of pol III. Salient features of yeast tDNA chromatin structure reported in this study can explain the basis of the novel non-transcriptional roles ascribed to tDNAs.

Dataset Information

Adult birdsong is actively maintained by error correction.

Publications

Adult birdsong is actively maintained by error correction.

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