Neural processing of auditory feedback during vocal practice in a songbird

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Abstract

Songbirds are capable of vocal learning and communication1,2 and are ideally suited to the study of neural mechanisms of complex sensory and motor processing. Vocal communication in a noisy bird colony and vocal learning of a specific song template both require the ability to monitor auditory feedback3,4 to distinguish self-generated vocalizations from external sounds and to identify mismatches between the developing song and a memorized template acquired from a tutor5. However, neurons that respond to auditory feedback from vocal output have not been found in song-control areas despite intensive searching6,7,8. Here we investigate feedback processing outside the traditional song system, in single auditory forebrain neurons of juvenile zebra finches that were in a late developmental stage of song learning. Overall, we found similarity of spike responses during singing and during playback of the bird’s own song, with song responses commonly leading by a few milliseconds. However, brief time-locked acoustic perturbations of auditory feedback revealed complex sensitivity that could not be predicted from passive playback responses. Some neurons that responded to playback perturbations did not respond to song perturbations, which is reminiscent of sensory-motor mirror neurons8,9. By contrast, some neurons were highly feedback sensitive in that they responded vigorously to song perturbations, but not to unperturbed songs or perturbed playback. These findings suggest that a computational function of forebrain auditory areas may be to detect errors between actual feedback and mirrored feedback deriving from an internal model of the bird’s own song or that of its tutor. Such feedback-sensitive spikes could constitute the key signals that trigger adaptive motor responses to song disruptions10,11 or reinforce exploratory motor gestures for vocal learning12.

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Figure 1: Comparison of active responses with passive responses.
Figure 2: Example perturbation responses.
Figure 3: Summary of perturbation selectivity.

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Acknowledgements

This work was supported by a Swiss National Science Foundation Professorship Grant to R.H.R.H. We thank K. Martin, R. Mooney and R. Douglas for comments on the manuscript.

Author Contributions G.B.K. performed the experiments and analysed the data. Both authors wrote the manuscript.

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Correspondence to Richard H. R. Hahnloser.

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Keller, G., Hahnloser, R. Neural processing of auditory feedback during vocal practice in a songbird. Nature 457, 187–190 (2009) doi:10.1038/nature07467

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