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Precise auditory–vocal mirroring in neurons for learned vocal communication

Nature volume 451, pages 305–310 (2008)Cite this article

Abstract

Brain mechanisms for communication must establish a correspondence between sensory and motor codes used to represent the signal. One idea is that this correspondence is established at the level of single neurons that are active when the individual performs a particular gesture or observes a similar gesture performed by another individual. Although neurons that display a precise auditory–vocal correspondence could facilitate vocal communication, they have yet to be identified. Here we report that a certain class of neurons in the swamp sparrow forebrain displays a precise auditory–vocal correspondence. We show that these neurons respond in a temporally precise fashion to auditory presentation of certain note sequences in this songbird’s repertoire and to similar note sequences in other birds’ songs. These neurons display nearly identical patterns of activity when the bird sings the same sequence, and disrupting auditory feedback does not alter this singing-related activity, indicating it is motor in nature. Furthermore, these neurons innervate striatal structures important for song learning, raising the possibility that singing-related activity in these cells is compared to auditory feedback to guide vocal learning.

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Figure 1: In freely behaving swamp sparrows, HVC X neurons respond selectively to one song type in the bird’s repertoire.
Figure 2: Countersinging in response to song presentation reveals auditory and singing-related activity of HVC X neurons in the context of communication.
Figure 3: HVC X neurons exhibit a precise sensorimotor correspondence.
Figure 4: Action potentials in HVC X neurons during singing are a corollary discharge of song motor activity.
Figure 5: Swamp sparrow HVC X neurons respond to note sequences in the primary song type and to similar note sequences in other swamp sparrows’ songs.

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Acknowledgements

We thank M. Fee and A. Kozhevnikov for training and assistance in building the miniature microdrives used for these chronic recordings. D. Fitzpatrick, M. Ehlers, M. Platt, H. Greenside and J. Groh provided comments on the manuscript. This work was supported by grants from the NIDCD (R.M.) and the N.S.F. (S.N.). J.P. was supported by an NIH NRSA.

Author information

Authors and Affiliations

  1. Department of Neurobiology, Duke University Medical Center,

    J. F. Prather, S. Nowicki & R. Mooney

  2. Department of Biology, Duke University, Durham, North Carolina 27710, USA,

    S. Peters & S. Nowicki

Authors
  1. J. F. Prather
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  2. S. Peters
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  3. S. Nowicki
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  4. R. Mooney
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Corresponding author

Correspondence to R. Mooney.

Supplementary information

Supplementary Figures

This file contains Supplementary Figures S1-S4 with Legends. (PDF 2754 kb)

Audio 1

This file contains Supplementary Audio 1 with primary BOS type (Fig1). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 1. (WAV 218 kb)

Audio 2

This file contains Supplementary Audio 2 with other BOS type (Fig1). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 1. (WAV 209 kb)

Audio 3

This file contains Supplementary Audio 3 with random CON song (Fig1). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 1. (WAV 232 kb)

Audio 4

This file contains Supplementary Audio 4 matched countersinging (Fig 2A). This recording of the auditory stimulus followed by the bird’s vocal response is an example of countersinging, a natural territorial behavior that allowed to rapidly assess the auditory and singing-related activity of individual HVCX neurons in the context of communication. (WAV 689 kb)

Audio 5

This file contains Supplementary Audio 5 with unmatched countersinging (Fig 2B). This recording of the auditory stimulus followed by the bird’s vocal response is an example of countersinging, a natural territorial behavior that allowed to rapidly assess the auditory and singing-related activity of individual HVCX neurons in the context of communication. (WAV 534 kb)

Audio 6

This file contains Supplementary Audio 6 with unmatched countersinging (Fig 2C). This recording of the auditory stimulus followed by the bird’s vocal response is an example of countersinging, a natural territorial behavior that allowed to rapidly assess the auditory and singing-related activity of individual HVCX neurons in the context of communication. (WAV 602 kb)

Audio 7

This file contains Supplementary Audio 7 with primary BOS natural sequence (Fig 5A). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 5. (WAV 241 kb)

Audio 8

This file contains Supplementary Audio 8 with primary BOS reverse sequence (Fig 5A). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 5. (WAV 241 kb)

Audio 9

This file contains Supplementary Audio 9 with primary BOS type (Fig 5B left). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 5. (WAV 241 kb)

Audio 10

This file contains Supplementary Audio 10 with CON with salient sequence (Fig 5B left). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 5. (WAV 265 kb)

Audio 11

This file contains Supplementary Audio 11 with primary BOS type (Fig 5B right). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 5. (WAV 199 kb)

Audio 12

This file contains Supplementary Audio 12 with CON with salient sequence (Fig 5B right). This is the bird’s own song (BOS) and conspecific (CON) song type that evoked the auditory responses shown in Fig 5. (WAV 179 kb)

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Prather, J., Peters, S., Nowicki, S. et al. Precise auditory–vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008). https://doi.org/10.1038/nature06492

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