Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Elemental gesture dynamics are encoded by song premotor cortical neurons

Nature volume 495, pages 59–64 (2013)Cite this article

Subjects

Abstract

Quantitative biomechanical models can identify control parameters that are used during movements, and movement parameters that are encoded by premotor neurons. We fit a mathematical dynamical systems model including subsyringeal pressure, syringeal biomechanics and upper-vocal-tract filtering to the songs of zebra finches. This reduces the dimensionality of singing dynamics, described as trajectories (motor ‘gestures’) in a space of syringeal pressure and tension. Here we assess model performance by characterizing the auditory response ‘replay’ of song premotor HVC neurons to the presentation of song variants in sleeping birds, and by examining HVC activity in singing birds. HVC projection neurons were excited and interneurons were suppressed within a few milliseconds of the extreme time points of the gesture trajectories. Thus, the HVC precisely encodes vocal motor output through activity at the times of extreme points of movement trajectories. We propose that the sequential activity of HVC neurons is used as a ‘forward’ model, representing the sequence of gestures in song to make predictions on expected behaviour and evaluate feedback.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Schematized view of a dynamical systems model describing syringeal labial dynamics and tracheal vocal-tract filtering.
Figure 2: A low-dimensional model for reconstructing gestures.
Figure 3: Testing the low-dimensional model.
Figure 4: Timing of gestures relative to bursting of projection neurons.
Figure 5: Suppressed interneuron activity is associated with GTE.
Figure 6: During singing, HVC projection neurons fired in the vicinity of GTE.

Similar content being viewed by others

References

  1. Hatsopoulos, N. G., Xu, Q. & Amit, Y. Encoding of movement fragments in the motor cortex. J. Neurosci. 27, 5105–5114 (2007)

    Article  CAS  Google Scholar 

  2. Nishikawa, K. et al. Neuromechanics: an integrative approach for understanding motor control. Integr. Comp. Biol. 47, 16–54 (2007)

    Article  Google Scholar 

  3. Perl, Y. S., Arneodo, E. M., Amador, A., Goller, F. & Mindlin, G. B. Reconstruction of physiological instructions from Zebra finch song. Phys. Rev. E 84, 051909 (2011)

    Article  ADS  Google Scholar 

  4. 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 

  5. Hahnloser, R. H. R., 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 

  6. Prather, J. F., Peters, S., Nowicki, S. & Mooney, R. Precise auditory-vocal mirroring in neurons for learned vocal communication. Nature 451, 305–310 (2008)

    Article  ADS  CAS  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  8. 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 

  9. Margoliash, D. Preference for autogenous song by auditory neurons in a song system nucleus of the white-crowned sparrow. J. Neurosci. 6, 1643–1661 (1986)

    Article  CAS  Google Scholar 

  10. Shank, S. S. & Margoliash, D. Sleep and sensorimotor integration during early vocal learning in a songbird. Nature 458, 73–77 (2009)

    Article  ADS  CAS  Google Scholar 

  11. Amador, A., Goller, F. & Mindlin, G. B. Frequency modulation during song in a suboscine does not require vocal muscles. J. Neurophysiol. 99, 2383–2389 (2008)

    Article  Google Scholar 

  12. Elemans, C. P. H., Laje, R., Mindlin, G. B. & Goller, F. Smooth operator: avoidance of subharmonic bifurcations through mechanical mechanisms simplifies song motor control in adult zebra finches. J. Neurosci. 30, 13246–13253 (2010)

    Article  CAS  Google Scholar 

  13. Fee, M. S., Shraiman, B., Pesaran, B. & Mitra, P. P. The role of nonlinear dynamics of the syrinx in the vocalizations of a songbird. Nature 395, 67–71 (1998)

    Article  ADS  CAS  Google Scholar 

  14. Mindlin, G. B. & Laje, R. The Physics of Birdsong. (Springer Verlag, 2005)

    Google Scholar 

  15. Laje, R., Gardner, T. J. & Mindlin, G. B. Neuromuscular control of vocalizations in birdsong: A model. Phys. Rev. E 65, 05192 (2002)

    Article  Google Scholar 

  16. Sitt, J. D., Amador, A., Goller, F. & Mindlin, G. B. Dynamical origin of spectrally rich vocalizations in birdsong. Phys. Rev. E 78, 011905 (2008)

    Article  ADS  CAS  Google Scholar 

  17. Amador, A. & Mindlin, G. B. Beyond harmonic sounds in a simple model for birdsong production. Chaos 18, 043123 (2008)

    Article  ADS  Google Scholar 

  18. Riede, T., Suthers, R. A., Fletcher, N. H. & Blevins, W. E. Songbirds tune their vocal tract to the fundamental frequency of their song. Proc. Natl Acad. Sci. USA 103, 5543–5548 (2006)

    Article  ADS  CAS  Google Scholar 

  19. Hartley, R. S. & Suthers, R. A. Air-flow and pressure during canary song: direct evidence for mini-breaths. J. Comp. Physiol. A 165, 15–26 (1989)

    Article  Google Scholar 

  20. Suthers, R. A., Goller, F. & Wild, J. M. Somatosensory feedback modulates the respiratory motor program of crystallized birdsong. Proc. Natl Acad. Sci. USA 99, 5680–5685 (2002)

    Article  ADS  CAS  Google Scholar 

  21. Wild, J. M. Functional neuroanatomy of the sensorimotor control of singing. Ann. NY Acad. Sci. 1016, 438–462 (2004)

    Article  ADS  Google Scholar 

  22. Suthers, R. A., Goller, F. & Pytte, C. The neuromuscular control of birdsong. Phil. Trans. R. Soc. B 354, 927–939 (1999)

    Article  CAS  Google Scholar 

  23. Fee, M. S., Kozhevnikov, A. A. & Hahnloser, R. H. Neural mechanisms of vocal sequence generation in the songbird. Ann. NY Acad. Sci. 1016, 153–170 (2004)

    Article  ADS  Google Scholar 

  24. 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 

  25. Fiete, I. R., Hahnloser, R. H. R., Fee, M. S. & Seung, H. S. Temporal sparseness of the premotor drive is important for rapid learning in a neural network model of birdsong. J. Neurophysiol. 92, 2274–2282 (2004)

    Article  Google Scholar 

  26. Vu, E. T., Mazurek, M. E. & Kuo, Y. C. Identification of a forebrain motor programming network for the learned song of zebra finches. J. Neurosci. 14, 6924–6934 (1994)

    Article  CAS  Google Scholar 

  27. Williams, H. & Vicario, D. S. Temporal patterning of song production: Participation of nucleus uvaeformis of the thalamus. J. Neurobiol. 24, 903–912 (1993)

    Article  CAS  Google Scholar 

  28. Margoliash, D. & Fortune, E. S. Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J. Neurosci. 12, 4309–4326 (1992)

    Article  CAS  Google Scholar 

  29. Nick, T. A. & Konishi, M. Neural auditory selectivity develops in parallel with song. J. Neurobiol. 62, 469–481 (2005)

    Article  Google Scholar 

  30. Prather, J. F., Nowicki, S., Anderson, R. C., Peters, S. & Mooney, R. Neural correlates of categorical perception in learned vocal communication. Nature Neurosci. 12, 221–228 (2009)

    Article  CAS  Google Scholar 

  31. Brainard, M. S. & Doupe, A. J. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404, 762–766 (2000)

    Article  ADS  CAS  Google Scholar 

  32. Ölveczky, B. P., Andalman, A. S. & Fee, M. S. Vocal experimentation in the juvenile songbird requires a basal ganglia circuit. PLoS Biol. 3, e153 (2005)

    Article  Google Scholar 

  33. 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 

  34. Ashmore, R. C., Wild, J. M. & Schmidt, M. F. Brainstem and forebrain contributions to the generation of learned motor behaviors for song. J. Neurosci. 25, 8543–8554 (2005)

    Article  CAS  Google Scholar 

  35. Wolpert, D. M., Ghahramani, Z. & Jordan, M. I. An internal model for sensorimotor integration. Science 269, 1880–1882 (1995)

    Article  ADS  CAS  Google Scholar 

  36. Roberts, T. F., Klein, M. E., Kubke, M. F., Wild, J. M. & Mooney, R. Telencephalic neurons monosynaptically link brainstem and forebrain premotor networks necessary for song. J. Neurosci. 28, 3479–3489 (2008)

    Article  CAS  Google Scholar 

  37. Coleman, M. J., Roy, A., Wild, J. M. & Mooney, R. Thalamic gating of auditory responses in telencephalic song control nuclei. J. Neurosci. 27, 10024–10036 (2007)

    Article  CAS  Google Scholar 

  38. Bauer, E. E. et al. A synaptic basis for auditory-vocal integration in the songbird. J. Neurosci. 28, 1509–1522 (2008)

    Article  CAS  Google Scholar 

  39. Mulliken, G. H., Musallam, S. & Andersen, R. A. Forward estimation of movement state in posterior parietal cortex. Proc. Natl Acad. Sci. USA 105, 8170–8177 (2008)

    Article  ADS  CAS  Google Scholar 

  40. Leyton, S. S. & Sherrington, C. S. Observations on the excitable cortex of the chimpanzee, orangutan and gorilla. Q. J. Exp. Physiol. 11, 135–222 (1917)

    Article  Google Scholar 

  41. Sutter, M. L. & Margoliash, D. Global synchronous response to autogenous song in zebra finch HVC. J. Neurophysiol. 72, 2105–2123 (1994)

    Article  CAS  Google Scholar 

  42. Press, W. H., Teukolsky, S. A., Vetterling, W. T. & Flannery, B. P. Numerical Recipes: The Art of Scientific Computing 3rd edn (Cambridge Univ. Press, 2007)

    MATH  Google Scholar 

  43. Guckenheimer, J. & Holmes, P. Nonlinear Oscillations, Dynamical Systems, and Bifurcations of Vector Fields. (Springer Verlag, 1997)

    MATH  Google Scholar 

  44. Fletcher, N. H., Riede, T. & Suthers, R. A. Model for vocalization by a bird with distensible vocal cavity and open beak. J. Acoust. Soc. Am. 119, 1005–1011 (2006)

    Article  ADS  Google Scholar 

  45. Daley, M. & Goller, F. Tracheal length changes during zebra finch song and their possible role in upper vocal tract filtering. J. Neurobiol. 59, 319–330 (2004)

    Article  Google Scholar 

Download references

Acknowledgements

We are grateful to R. H. R. Hahnloser for help with the microdrives and techniques used to record from singing birds. We thank H. D. I. Abarbanel, T. Q. Gentner, H. C. Nusbaum and S. E. Palmer for valuable comments on the manuscript. This work was supported by a Human Frontiers Science Program cross-disciplinary fellowship award to A.A., NIDCD006876, ANCyT, CONICET and UBA awards to G.B.M. and Y.S.P., and NIDCD and NSF/CRCNS awards to D.M.

Author information

Author notes

  1. Ana Amador

    Present address: Present address: Department of Physics, FCEN, University of Buenos Aires, Intendente Guiraldes 2160, Pabellon 1, Buenos Aires 1428, Argentina.,

Authors and Affiliations

  1. Department of Organismal Biology and Anatomy, University of Chicago, 1027 East 57th Street, Chicago, Ilinois 60637, USA,

    Ana Amador & Daniel Margoliash

  2. Department of Physics, FCEN, University of Buenos Aires, Intendente Guiraldes 2160, Pabellon 1, Buenos Aires 1428, Argentina,

    Yonatan Sanz Perl & Gabriel B. Mindlin

Authors
  1. Ana Amador
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yonatan Sanz Perl
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gabriel B. Mindlin
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Daniel Margoliash
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Author Contributions A.A., G.B.M. and Y.S.P. developed the syringeal model, G.B.M. and Y.S.P. modelled the songs, A.A. conducted surgeries, sound recordings and collected the electrophysiological data, A.A., G.B.M. and D.M. conceived and designed the experiments, and prepared the manuscript. All four authors participated in data analysis.

Corresponding author

Correspondence to Daniel Margoliash.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary Information

This file contains Supplementary Text, additional references and Supplementary Figures 1-8. (PDF 2660 kb)

PowerPoint slides

Rights and permissions

Reprints and permissions

About this article

Cite this article

Amador, A., Perl, Y., Mindlin, G. et al. Elemental gesture dynamics are encoded by song premotor cortical neurons. Nature 495, 59–64 (2013). https://doi.org/10.1038/nature11967

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature11967

This article is cited by

Comments

By submitting a comment you agree to abide by our Terms and Community Guidelines. If you find something abusive or that does not comply with our terms or guidelines please flag it as inappropriate.

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing