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.

  • Letter
  • Published:

Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song

Nature volume 433, pages 638–643 (2005)Cite this article

Abstract

Cortical–basal ganglia circuits have a critical role in motor control and motor learning1. In songbirds, the anterior forebrain pathway (AFP) is a basal ganglia–forebrain circuit required for song learning and adult vocal plasticity but not for production of learned song2,3,4,5. Here, we investigate functional contributions of this circuit to the control of song, a complex, learned motor skill. We test the hypothesis that neural activity in the AFP of adult birds can direct moment-by-moment changes in the primary motor areas responsible for generating song. We show that song-triggered microstimulation in the output nucleus of the AFP induces acute and specific changes in learned parameters of song6,7. Moreover, under both natural and experimental conditions, variability in the pattern of AFP activity is associated with variability in song structure. Finally, lesions of the output nucleus of the AFP prevent naturally occurring modulation of song variability. These findings demonstrate a previously unappreciated capacity of the AFP to direct real-time changes in song. More generally, they suggest that frontal cortical and basal ganglia areas may contribute to motor learning by biasing motor output towards desired targets or by introducing stochastic variability required for reinforcement learning.

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: Song-triggered microstimulation in LMAN elicits acute changes in learned parameters of syllable structure.
Figure 2: Specificity of stimulation.
Figure 3: Context-dependent changes in variability.
Figure 4: Contributions of the AFP to real-time song modulation.

Similar content being viewed by others

References

  1. Graybiel, A. M., Aosaki, T., Flaherty, A. W. & Kimura, M. The basal ganglia and adaptive motor control. Science 265, 1826–1831 (1994)

    Article  ADS  CAS  Google Scholar 

  2. Bottjer, S. W., Miesner, E. A. & Arnold, A. P. Forebrain lesions disrupt development but not maintenance of song in passerine birds. Science 224, 901–903 (1984)

    Article  ADS  CAS  Google Scholar 

  3. 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 

  4. 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 

  5. Williams, H. & Mehta, N. Changes in adult zebra finch song require a forebrain nucleus that is not necessary for song production. J. Neurobiol. 39, 14–28 (1999)

    Article  CAS  Google Scholar 

  6. Tchernichovski, O., Mitra, P. P., Lints, T. & Nottebohm, F. Dynamics of the vocal imitation process: how a zebra finch learns its song. Science 291, 2564–2569 (2001)

    Article  ADS  CAS  Google Scholar 

  7. Williams, H., Cynx, J. & Nottebohm, F. Timbre control in zebra finch (Taeniopygia guttata) song syllables. J. Comp. Psychol. 103, 366–380 (1989)

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  9. Perkel, D. J. in Behavioral Neurobiology of Birdsong (eds Zeigler, H. P. & Marler, P.) 736–748 (New York Academy of Sciences, New York, 2004)

    Google Scholar 

  10. Troyer, T. W. & Doupe, A. J. An associational model of birdsong sensorimotor learning. II. Temporal hierarchies and the learning of song sequence. J. Neurophys. 84, 1224–1239 (2000)

    Article  CAS  Google Scholar 

  11. Doya, K. & Sejnowski, T. J. in The New Cognitive Neurosciences (ed. Gazzaniga, M. S.) 469–482 (MIT Press, Cambridge, Massachusetts, 2000)

    Google Scholar 

  12. Hessler, N. A. & Doupe, A. J. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci. 2, 209–211 (1999)

    Article  CAS  Google Scholar 

  13. Hessler, N. A. & Doupe, A. J. Singing-related neural activity in a dorsal forebrain–basal ganglia circuit of adult zebra finches. J. Neurosci. 19, 10461–10481 (1999)

    Article  CAS  Google Scholar 

  14. 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 

  15. Vicario, D. S. & Simpson, H. B. Electrical stimulation in forebrain nuclei elicits learned vocal patterns in songbirds. J. Neurophys. 73, 2602–2607 (1995)

    Article  CAS  Google Scholar 

  16. Brumm, H. & Todt, D. Male–male vocal interactions and the adjustment of song amplitude in a territorial bird. Anim. Behav. 67, 281–286 (2004)

    Article  Google Scholar 

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

    Article  ADS  CAS  Google Scholar 

  18. Johnson, F., Sablan, M. M. & Bottjer, S. W. Topographic organization of a forebrain pathway involved with vocal learning in zebra finches. J. Comp. Neurol. 358, 260–278 (1995)

    Article  CAS  Google Scholar 

  19. 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 

  20. Jarvis, E. D., Scharff, C., Grossman, M. R., Ramos, J. A. & Nottebohm, F. For whom the bird sings: context-dependent gene expression. Neuron 21, 775–788 (1998)

    Article  CAS  Google Scholar 

  21. Hikosaka, O., Nakamura, K., Sakai, K. & Nakahara, H. Central mechanisms of motor skill learning. Curr. Opin. Neurobiol. 12, 217–222 (2002)

    Article  CAS  Google Scholar 

  22. Miller, E. K. The prefrontal cortex and cognitive control. Nature Rev. Neurosci. 1, 59–65 (2000)

    Article  CAS  Google Scholar 

  23. Troyer, T. W. & Bottjer, S. W. Birdsong: models and mechanisms. Curr. Opin. Neurobiol. 11, 721–726 (2001)

    Article  CAS  Google Scholar 

  24. Mooney, R. & Konishi, M. Two distinct inputs to an avian song nucleus activate different glutamate receptor subtypes on individual neurons. Proc. Natl Acad. Sci. USA 88, 4075–4079 (1991)

    Article  ADS  CAS  Google Scholar 

  25. Kittelberger, J. M. & Mooney, R. Lesions of an avian forebrain nucleus that disrupt song development alter synaptic connectivity and transmission in the vocal premotor pathway. J. Neurosci. 19, 9385–9398 (1999)

    Article  CAS  Google Scholar 

  26. Stark, L. L. & Perkel, D. J. Two-stage input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch. J. Neurosci. 19, 9107–9116 (1999)

    Article  CAS  Google Scholar 

  27. Komatsu, H. & Wurtz, R. H. Modulation of pursuit eye movements by stimulation of cortical areas MT and MST. J. Neurophys. 62, 31–47 (1989)

    Article  CAS  Google Scholar 

  28. Tanaka, M. & Lisberger, S. G. Regulation of the gain of visually guided smooth-pursuit eye movements by frontal cortex. Nature 409, 191–194 (2001)

    Article  ADS  CAS  Google Scholar 

  29. Canales, J. J. & Graybiel, A. M. A measure of striatal function predicts motor stereotypy. Nature Neurosci. 3, 377–383 (2000)

    Article  CAS  Google Scholar 

  30. Matsumoto, N., Hanakawa, T., Maki, S., Graybiel, A. M. & Kimura, M. Nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J. Neurophys. 82, 978–997 (1999)

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank N. Hessler for a portion of the data in Fig. 3e. We thank A. Basbaum, S. Lisberger, J. Sakata and B. Wright for helpful comments on this manuscript and A. Arteseros and K. McManaway for technical assistance. This work was supported by an HHMI Predoctoral Fellowship (M.H.K.), the MacArthur Foundation, the Steven and Michele Kirsch Foundation, NARSAD and NIH (A.J.D.), and the HHMI Biomedical Research Support Program grant, the McKnight Foundation, the Klingenstein Fund, a Searle Scholars Award and NIH (M.S.B.).

Author information

Authors and Affiliations

  1. Keck Center for Integrative Neuroscience, Departments of Physiology and Psychiatry, University of California, San Francisco, California, 94143-0444, USA

    Mimi H. Kao, Allison J. Doupe & Michael S. Brainard

Authors
  1. Mimi H. Kao
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Allison J. Doupe
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Michael S. Brainard
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mimi H. Kao.

Ethics declarations

Competing interests

The authors declare that they have no competing financial interests.

Supplementary information

Supplementary Figure 1

This figure provides additional information for how the latency between the application of a stimulus and the onset of a change in syllable structure was measured. Latency measurements could be complicated because the effects of stimulation at a given site could be specific to a subset of syllables. (GIF 46 kb)

Supplementary Figure 2

This figure shows a correlation between the magnitude of changes in LMAN variability and the magnitude of changes in song variability. (GIF 36 kb)

Supplementary Table 1

Summary of the effects of stimulation in LMAN for each syllable tested in 5 birds. (DOC 72 kb)

Supplementary Table 2

Summary of the effects of LMAN stimulation for each bird by site. Stimulation evoked significant changes in syllable structure in 18/20 sites in LMAN of 5 birds. (DOC 34 kb)

Supplementary Table 3

Summary of the effects of differential activation of LMAN neurons at a particular site. (DOC 51 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Kao, M., Doupe, A. & Brainard, M. Contributions of an avian basal ganglia–forebrain circuit to real-time modulation of song. Nature 433, 638–643 (2005). https://doi.org/10.1038/nature03127

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nature03127

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