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Philosophical Transactions of the Royal Society B: Biological Sciences logoLink to Philosophical Transactions of the Royal Society B: Biological Sciences
. 1999 May 29;354(1385):927–939. doi: 10.1098/rstb.1999.0444

The neuromuscular control of birdsong.

R A Suthers 1, F Goller 1, C Pytte 1
PMCID: PMC1692586  PMID: 10382225

Abstract

Birdsong requires complex learned motor skills involving the coordination of respiratory, vocal organ and craniomandibular muscle groups. Recent studies have added to our understanding of how these vocal subsystems function and interact during song production. The respiratory rhythm determines the temporal pattern of song. Sound is produced during expiration and each syllable is typically followed by a small inspiration, except at the highest syllable repetition rates when a pattern of pulsatile expiration is used. Both expiration and inspiration are active processes. The oscine vocal organ, the syrinx, contains two separate sound sources at the cranial end of each bronchus, each with independent motor control. Dorsal syringeal muscles regulate the timing of phonation by adducting the sound-generating labia into the air stream. Ventral syringeal muscles have an important role in determining the fundamental frequency of the sound. Different species use the two sides of their vocal organ in different ways to achieve the particular acoustic properties of their song. Reversible paralysis of the vocal organ during song learning in young birds reveals that motor practice is particularly important in late plastic song around the time of song crystallization in order for normal adult song to develop. Even in adult crystallized song, expiratory muscles use sensory feedback to make compensatory adjustments to perturbations of respiratory pressure. The stereotyped beak movements that accompany song appear to have a role in suppressing harmonics, particularly at low frequencies.

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Selected References

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  1. Allan S. E., Suthers R. A. Lateralization and motor stereotypy of song production in the brown-headed cowbird. J Neurobiol. 1994 Sep;25(9):1154–1166. doi: 10.1002/neu.480250910. [DOI] [PubMed] [Google Scholar]
  2. Bottjer S. W., Arnold A. P. Afferent neurons in the hypoglossal nerve of the zebra finch (Poephila guttata): localization with horseradish peroxidase. J Comp Neurol. 1982 Sep 10;210(2):190–197. doi: 10.1002/cne.902100209. [DOI] [PubMed] [Google Scholar]
  3. Bottjer S. W., Arnold A. P. The role of feedback from the vocal organ. I. Maintenance of stereotypical vocalizations by adult zebra finches. J Neurosci. 1984 Sep;4(9):2387–2396. doi: 10.1523/JNEUROSCI.04-09-02387.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Brittan-Powell E. F., Dooling R. J., Larsen O. N., Heaton J. T. Mechanisms of vocal production in budgerigars (Melopsittacus undulatus). J Acoust Soc Am. 1997 Jan;101(1):578–589. doi: 10.1121/1.418121. [DOI] [PubMed] [Google Scholar]
  5. Calder W. A. Respiration during song in the canary (Serinus canaria). Comp Biochem Physiol. 1970 Jan 15;32(2):251–258. doi: 10.1016/0010-406x(70)90938-2. [DOI] [PubMed] [Google Scholar]
  6. DeVoogd T. J. Endocrine modulation of the development and adult function of the avian song system. Psychoneuroendocrinology. 1991;16(1-3):41–66. doi: 10.1016/0306-4530(91)90070-a. [DOI] [PubMed] [Google Scholar]
  7. DeVoogd T. J., Nottebohm F. Sex differences in dendritic morphology of a song control nucleus in the canary: a quantitative Golgi study. J Comp Neurol. 1981 Feb 20;196(2):309–316. doi: 10.1002/cne.901960209. [DOI] [PubMed] [Google Scholar]
  8. DeWet P. D., Fedde M. R., Kitchell R. L. Innervation of the respiratory muscles of Gallus domesticus. J Morphol. 1967 Sep;123(1):17–34. doi: 10.1002/jmor.1051230103. [DOI] [PubMed] [Google Scholar]
  9. Devoogd T. J., Nixdorf B., Nottebohm F. Synaptogenesis and changes in synaptic morphology related to acquisition of a new behavior. Brain Res. 1985 Mar 11;329(1-2):304–308. doi: 10.1016/0006-8993(85)90539-6. [DOI] [PubMed] [Google Scholar]
  10. Goller F., Larsen O. N. A new mechanism of sound generation in songbirds. Proc Natl Acad Sci U S A. 1997 Dec 23;94(26):14787–14791. doi: 10.1073/pnas.94.26.14787. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Goller F., Suthers R. A. Role of syringeal muscles in controlling the phonology of bird song. J Neurophysiol. 1996 Jul;76(1):287–300. doi: 10.1152/jn.1996.76.1.287. [DOI] [PubMed] [Google Scholar]
  12. Goller F., Suthers R. A. Role of syringeal muscles in gating airflow and sound production in singing brown thrashers. J Neurophysiol. 1996 Feb;75(2):867–876. doi: 10.1152/jn.1996.75.2.867. [DOI] [PubMed] [Google Scholar]
  13. Hartley R. S. Expiratory muscle activity during song production in the canary. Respir Physiol. 1990 Aug;81(2):177–187. doi: 10.1016/0034-5687(90)90044-y. [DOI] [PubMed] [Google Scholar]
  14. Konishi M. Birdsong: from behavior to neuron. Annu Rev Neurosci. 1985;8:125–170. doi: 10.1146/annurev.ne.08.030185.001013. [DOI] [PubMed] [Google Scholar]
  15. Konishi M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z Tierpsychol. 1965 Dec;22(7):770–783. [PubMed] [Google Scholar]
  16. Luine V., Nottebohm F., Harding C., McEwen B. S. Androgen affects cholinergic enzymes in syringeal motor neurons and muscle. Brain Res. 1980 Jun 16;192(1):89–107. doi: 10.1016/0006-8993(80)91011-2. [DOI] [PubMed] [Google Scholar]
  17. Margoliash D. Functional organization of forebrain pathways for song production and perception. J Neurobiol. 1997 Nov;33(5):671–693. doi: 10.1002/(sici)1097-4695(19971105)33:5<671::aid-neu12>3.0.co;2-c. [DOI] [PubMed] [Google Scholar]
  18. Morrison R. G., Nottebohm F. Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches. J Neurobiol. 1993 Aug;24(8):1045–1064. doi: 10.1002/neu.480240805. [DOI] [PubMed] [Google Scholar]
  19. Nordeen K. W., Nordeen E. J. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches. Behav Neural Biol. 1992 Jan;57(1):58–66. doi: 10.1016/0163-1047(92)90757-u. [DOI] [PubMed] [Google Scholar]
  20. Nottebohm F., Arnold A. P. Sexual dimorphism in vocal control areas of the songbird brain. Science. 1976 Oct 8;194(4261):211–213. doi: 10.1126/science.959852. [DOI] [PubMed] [Google Scholar]
  21. Nottebohm F., Kasparian S., Pandazis C. Brain space for a learned task. Brain Res. 1981 May 25;213(1):99–109. doi: 10.1016/0006-8993(81)91250-6. [DOI] [PubMed] [Google Scholar]
  22. Nowicki S. Vocal tract resonances in oscine bird sound production: evidence from birdsongs in a helium atmosphere. Nature. 1987 Jan 1;325(6099):53–55. doi: 10.1038/325053a0. [DOI] [PubMed] [Google Scholar]
  23. Suthers R. A., Goller F., Hartley R. S. Motor dynamics of song production by mimic thrushes. J Neurobiol. 1994 Aug;25(8):917–936. doi: 10.1002/neu.480250803. [DOI] [PubMed] [Google Scholar]
  24. Suthers R. A., Goller F., Hartley R. S. Motor stereotypy and diversity in songs of mimic thrushes. J Neurobiol. 1996 Jun;30(2):231–245. doi: 10.1002/(SICI)1097-4695(199606)30:2<231::AID-NEU5>3.0.CO;2-6. [DOI] [PubMed] [Google Scholar]
  25. Suthers R. A. Peripheral control and lateralization of birdsong. J Neurobiol. 1997 Nov;33(5):632–652. [PubMed] [Google Scholar]
  26. Vicario D. S. A new brain stem pathway for vocal control in the zebra finch song system. Neuroreport. 1993 Jul;4(7):983–986. doi: 10.1097/00001756-199307000-00037. [DOI] [PubMed] [Google Scholar]
  27. Vicario D. S., Nottebohm F. Organization of the zebra finch song control system: I. Representation of syringeal muscles in the hypoglossal nucleus. J Comp Neurol. 1988 May 15;271(3):346–354. doi: 10.1002/cne.902710305. [DOI] [PubMed] [Google Scholar]
  28. Vicario D. S. Organization of the zebra finch song control system: II. Functional organization of outputs from nucleus Robustus archistriatalis. J Comp Neurol. 1991 Jul 22;309(4):486–494. doi: 10.1002/cne.903090405. [DOI] [PubMed] [Google Scholar]
  29. 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. 1994 Nov;14(11 Pt 2):6924–6934. doi: 10.1523/JNEUROSCI.14-11-06924.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Westneat M. W., Long J. H., Jr, Hoese W., Nowicki S. Kinematics of birdsong: functional correlation of cranial movements and acoustic features in sparrows. J Exp Biol. 1993 Sep;182:147–171. doi: 10.1242/jeb.182.1.147. [DOI] [PubMed] [Google Scholar]
  31. Wild J. M. Descending projections of the songbird nucleus robustus archistriatalis. J Comp Neurol. 1993 Dec 8;338(2):225–241. doi: 10.1002/cne.903380207. [DOI] [PubMed] [Google Scholar]
  32. Wild J. M., Goller F., Suthers R. A. Inspiratory muscle activity during bird song. J Neurobiol. 1998 Sep 5;36(3):441–453. doi: 10.1002/(sici)1097-4695(19980905)36:3<441::aid-neu11>3.0.co;2-e. [DOI] [PubMed] [Google Scholar]
  33. Wild J. M. Neural pathways for the control of birdsong production. J Neurobiol. 1997 Nov;33(5):653–670. doi: 10.1002/(sici)1097-4695(19971105)33:5<653::aid-neu11>3.0.co;2-a. [DOI] [PubMed] [Google Scholar]
  34. Wild J. M. The auditory-vocal-respiratory axis in birds. Brain Behav Evol. 1994;44(4-5):192–209. doi: 10.1159/000113577. [DOI] [PubMed] [Google Scholar]
  35. Yu A. C., Margoliash D. Temporal hierarchical control of singing in birds. Science. 1996 Sep 27;273(5283):1871–1875. doi: 10.1126/science.273.5283.1871. [DOI] [PubMed] [Google Scholar]

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