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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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References

  1. Fee, M. S. & Leonardo, A. Miniature motorized microdrive and commutator system for chronic neural recording in small animals. J. Neurosci. Methods 112, 83–94 (2001)

    Article  CAS  Google Scholar 

  2. Marler, P. & Tamura, M. Culturally transmitted patterns of vocal behavior in sparrows. Science 146, 1483–1486 (1964)

    Article  ADS  CAS  Google Scholar 

  3. Konishi, M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22, 770–783 (1965)

    CAS  PubMed  Google Scholar 

  4. Marler, P. & Peters, S. Sparrows learn adult song and more from memory. Science 213, 780–782 (1981)

    Article  ADS  CAS  Google Scholar 

  5. Marler, P. & Pickert, R. Species-universal microstructure in the learned song of the swamp sparrow (Melospiza georgiana). Anim. Behav. 32, 673–689 (1984)

    Article  Google Scholar 

  6. Nottebohm, F., Stokes, T. M. & Leonard, C. M. Central control of song in the canary, Serinus canarius . J. Comp. Neurol. 165, 457–486 (1976)

    Article  CAS  Google Scholar 

  7. Gentner, T. Q., Hulse, S. H., Bentley, G. E. & Ball, G. F. Individual vocal recognition and the effect of partial lesions to HVc on discrimination, learning, and categorization of conspecific song in adult songbirds. J. Neurobiol. 42, 117–133 (2000)

    Article  CAS  Google Scholar 

  8. Hahnloser, R. H., Kozhevnikov, A. A. & Fee, M. S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (2002)

    Article  ADS  CAS  Google Scholar 

  9. Margoliash, D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J. Neurosci. 3, 1039–1057 (1983)

    Article  CAS  Google Scholar 

  10. Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000)

    Article  CAS  Google Scholar 

  11. Yu, A. C. & Margoliash, D. Temporal hierarchical control of singing in birds. Science 273, 1871–1875 (1996)

    Article  ADS  CAS  Google Scholar 

  12. Mooney, R., Hoese, W. & Nowicki, S. Auditory representation of the vocal repertoire in a songbird with multiple song types. Proc. Natl Acad. Sci. USA 98, 12778–12783 (2001)

    Article  ADS  CAS  Google Scholar 

  13. Wild, J. M., Williams, M. N., Howie, G. J. & Mooney, R. Calcium-binding proteins define interneurons in HVC of the zebra finch (Taeniopygia guttata). J. Comp. Neurol. 483, 76–90 (2005)

    Article  CAS  Google Scholar 

  14. Farries, M. A. & Perkel, D. J. A telencephalic nucleus essential for song learning contains neurons with physiological characteristics of both striatum and globus pallidus. J. Neurosci. 22, 3776–3787 (2002)

    Article  CAS  Google Scholar 

  15. Scharff, C. & Nottebohm, F. A comparative study of the behavioral deficits following lesions of various parts of the zebra finch song system: implications for vocal learning. J. Neurosci. 11, 2896–2913 (1991)

    Article  CAS  Google Scholar 

  16. Scharff, C., Nottebohm, F. & Cynx, J. Conspecific and heterospecific song discrimination in male zebra finches with lesions in the anterior forebrain pathway. J. Neurobiol. 36, 81–90 (1998)

    Article  CAS  Google Scholar 

  17. McCasland, J. S. & Konishi, M. Interaction between auditory and motor activities in an avian song control nucleus. Proc. Natl Acad. Sci. USA 78, 7815–7819 (1981)

    Article  ADS  CAS  Google Scholar 

  18. Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812–816 (2000)

    Article  ADS  CAS  Google Scholar 

  19. Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning I. Efference copy and the learning of song syllables. J. Neurophysiol. 84, 1204–1223 (2000)

    Article  CAS  Google Scholar 

  20. Okanoya, K. & Yamaguchi, A. Adult bengalese finches (Lonchura striata var domestica) require real-time auditory feedback to produce normal song syntax. J. Neurobiol. 33, 343–356 (1997)

    Article  CAS  Google Scholar 

  21. Woolley, S. M. & Rubel, E. W. Bengalese finches Lonchura striata domestica depend upon auditory feedback for the maintenance of adult song. J. Neurosci. 17, 6380–6390 (1997)

    Article  CAS  Google Scholar 

  22. Lewicki, M. S. Intracellular characterization of song-specific neurons in the zebra finch auditory forebrain. J. Neurosci. 16, 5855–5863 (1996)

    CAS  PubMed  Google Scholar 

  23. Liberman, A. M., Cooper, F. S., Shankweiler, D. P. & Studdert-Kennedy, M. Perception of the speech code. Psychol. Rev. 74, 431–461 (1967)

    Article  CAS  Google Scholar 

  24. Gallese, V., Fadiga, L., Fogassi, L. & Rizzolatti, G. Action recognition in the premotor cortex. Brain 119, 593–609 (1996)

    Article  Google Scholar 

  25. Rizzolatti, G. & Craighero, L. The mirror-neuron system. Annu. Rev. Neurosci. 27, 169–192 (2004)

    Article  CAS  Google Scholar 

  26. Ferrari, P. F., Gallese, V., Rizzolatti, G. & Fogassi, L. Mirror neurons responding to the observation of ingestive and communicative mouth actions in the monkey ventral premotor cortex. Eur. J. Neurosci. 17, 1703–1714 (2003)

    Article  Google Scholar 

  27. Iacoboni, M. et al. Grasping the intentions of others with one's own mirror neuron system. PLoS Biol. 3, e79 (2005)

    Article  Google Scholar 

  28. Rizzolatti, G., Fogassi, L. & Gallese, V. Neurophysiological mechanisms underlying the understanding and imitation of action. Nature Rev. Neurosci. 2, 661–670 (2001)

    Article  CAS  Google Scholar 

  29. Iacoboni, M. et al. Cortical mechanisms of human imitation. Science 286, 2526–2528 (1999)

    Article  CAS  Google Scholar 

  30. Rizzolatti, G. & Arbib, M. A. Language within our grasp. Trends Neurosci. 21, 188–194 (1998)

    Article  CAS  Google Scholar 

  31. Arbib, M. A. From monkey-like action recognition to human language: an evolutionary framework for neurolinguistics. Behav. Brain Sci. 28, 105–124. 125–167 (2005)

    Article  Google Scholar 

  32. Mooney, R. & Prather, J. F. The HVC microcircuit: the synaptic basis for interactions between song motor and vocal plasticity pathways. J. Neurosci. 25, 1952–1964 (2005)

    Article  CAS  Google Scholar 

  33. Rosen, M. J. & Mooney, R. Inhibitory and excitatory mechanisms underlying auditory responses to learned vocalizations in the songbird nucleus HVC. Neuron 39, 177–194 (2003)

    Article  CAS  Google Scholar 

  34. Poulet, J. F. & Hedwig, B. The cellular basis of a corollary discharge. Science 311, 518–522 (2006)

    Article  ADS  CAS  Google Scholar 

  35. Bell, C. C. An efference copy which is modified by reafferent input. Science 214, 450–453 (1981)

    Article  ADS  CAS  Google Scholar 

  36. Kozhevnikov, A. A. & Fee, M. S. Singing-related activity of identified HVC neurons in the zebra finch. J. Neurophysiol. 97, 4271–4283 (2007)

    Article  Google Scholar 

  37. Perkel, D. J., Farries, M. A., Luo, M. & Ding, L. Electrophysiological analysis of a songbird basal ganglia circuit essential for vocal plasticity. Brain Res. Bull. 57, 529–532 (2002)

    Article  Google Scholar 

  38. Vargha-Khadem, F., Gadian, D. G., Copp, A. & Mishkin, M. FOXP2 and the neuroanatomy of speech and language. Nature Rev. Neurosci. 6, 131–138 (2005)

    Article  CAS  Google Scholar 

  39. Lai, C. S., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F. & Monaco, A. P. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519–523 (2001)

    Article  ADS  CAS  Google Scholar 

  40. Quiroga, R. Q., Nadasdy, Z. & Ben-Shaul, Y. Unsupervised spike detection and sorting with wavelets and superparamagnetic clustering. Neural Comput. 16, 1661–1687 (2004)

    Article  Google Scholar 

  41. Hyman, J. Countersinging as a signal of aggression in a territorial songbird. Anim. Behav. 65, 1179–1185 (2003)

    Article  Google Scholar 

  42. Griffiths, R., Double, M., Orr, K. & Dawson, R. A. DNA test to sex most birds. Mol. Ecol. 7, 1071–1075 (1998)

    Article  CAS  Google Scholar 

  43. Marler, P., Peters, S., Ball, G. F., Dufty, A. M. & Wingfield, J. C. The role of sex steroids in the acquisition and production of birdsong. Nature 336, 770–772 (1988)

    Article  ADS  CAS  Google Scholar 

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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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