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Auditory feedback in learning and maintenance of vocal behaviour

Abstract

Songbirds are one of the best-studied examples of vocal learners. Learning of both human speech and birdsong depends on hearing. Once learned, adult song in many species remains unchanging, suggesting a reduced influence of sensory experience. Recent studies have revealed, however, that adult song is not always stable, extending our understanding of the mechanisms involved in song maintenance, and their similarity to those active during song learning. Here we review some of the processes that contribute to song learning and production, with an emphasis on the role of auditory feedback. We then consider some of the possible neural substrates involved in these processes, particularly basal ganglia circuitry. Although a thorough treatment of human speech is beyond the scope of this article, we point out similarities between speech and song learning, and ways in which studies of these disparate behaviours complement each other in developing an understanding of general principles that contribute to learning and maintenance of vocal behaviour.

Key Points

  • Behavioural observations indicate that similar processes contribute to the learning and maintenance of birdsong and speech. These observations suggest that during learning, both birds and humans form internal representations of species-specific vocalizations. They then use auditory feedback to match their developing vocal output to these internal sensory models. Once learned, vocalizations tend to remain stable. However, alterations of auditory feedback in adulthood lead to a deterioration of both birdsong and speech, indicating that they have not become ‘hard-wired’, that is, resistant to the influence of experience.

  • The mechanisms responsible for the influence of auditory feedback on the maintenance of vocalizations are unknown. It is possible that the observed deterioration in the absence of feedback is due to passive drift in vocal control structures. Alternatively, the lack of auditory feedback could cause the mechanisms that match the feedback to an internal model to generate an error signal that actively modifies the vocalizations.

  • Lesion studies in combination with manipulations of auditory feedback are consistent with the idea that the deterioration of adult song is indeed active. These experiments also raise the possibility that a basal ganglia circuit of songbirds, the anterior forebrain pathway, participates in the evaluation of song, and in the generation of an error signal when the bird does not receive feedback that matches its internal model. For example, the destruction of the lateral magnocellular nucleus of the anterior neostriatum (LMAN) — the output nucleus of the anterior forebrain pathway — prevents the song deterioration that normally results from the absence of feedback.

  • How the songbird brain evaluates song and matches it to the internal model is not known. Song-selective neurons — cells found throughout the songbird brain that fire more strongly to the bird's own song than to the songs of other birds of the same species — could be involved in this process.

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Figure 1: Timeline for zebra finch song learning.
Figure 2: Model of sensorimotor song learning.
Figure 3: Models of adult song stabilization.
Figure 4: Different models of the effects of deafening.
Figure 5: The song system and its forebrain auditory inputs.
Figure 6: Examples of changes to song for a deafened bird (a) and its brother (b), which further received bilateral lesions of the LMAN.

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Acknowledgements

We thank S. Lisberger for helpful comments on the manuscript. The work of the authors was supported by the National Institutes of Health, a Burroughs Wellcome Fund Fellowship of the Life Sciences Research Foundation, the John Merck Fund and the EJLB foundation.

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Allison Doupe's laboratory

ENCYLOPEDIA OF LIFE SCIENCES

Bird song: steroid hormones and plasticity

Glossary

PHONEME

A distinct unit of sound that distinguishes one word from another.

BASAL GANGLIA

A collection of brain structures that modulate cortical output.

WERNICKE'S AREA

Region of the parietal cortex involved in speech processing.

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Brainard, M., Doupe, A. Auditory feedback in learning and maintenance of vocal behaviour . Nat Rev Neurosci 1, 31–40 (2000). https://doi.org/10.1038/35036205

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