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.

Auditory feedback in learning and maintenance of vocal behaviour

Abstract

Songbirds are one of the best-studied examples of vocal learners. Learning of both human speech and birdsong depends on hearing. Once learned, adult song in many species remains unchanging, suggesting a reduced influence of sensory experience. Recent studies have revealed, however, that adult song is not always stable, extending our understanding of the mechanisms involved in song maintenance, and their similarity to those active during song learning. Here we review some of the processes that contribute to song learning and production, with an emphasis on the role of auditory feedback. We then consider some of the possible neural substrates involved in these processes, particularly basal ganglia circuitry. Although a thorough treatment of human speech is beyond the scope of this article, we point out similarities between speech and song learning, and ways in which studies of these disparate behaviours complement each other in developing an understanding of general principles that contribute to learning and maintenance of vocal behaviour.

Key Points

  • Behavioural observations indicate that similar processes contribute to the learning and maintenance of birdsong and speech. These observations suggest that during learning, both birds and humans form internal representations of species-specific vocalizations. They then use auditory feedback to match their developing vocal output to these internal sensory models. Once learned, vocalizations tend to remain stable. However, alterations of auditory feedback in adulthood lead to a deterioration of both birdsong and speech, indicating that they have not become ‘hard-wired’, that is, resistant to the influence of experience.

  • The mechanisms responsible for the influence of auditory feedback on the maintenance of vocalizations are unknown. It is possible that the observed deterioration in the absence of feedback is due to passive drift in vocal control structures. Alternatively, the lack of auditory feedback could cause the mechanisms that match the feedback to an internal model to generate an error signal that actively modifies the vocalizations.

  • Lesion studies in combination with manipulations of auditory feedback are consistent with the idea that the deterioration of adult song is indeed active. These experiments also raise the possibility that a basal ganglia circuit of songbirds, the anterior forebrain pathway, participates in the evaluation of song, and in the generation of an error signal when the bird does not receive feedback that matches its internal model. For example, the destruction of the lateral magnocellular nucleus of the anterior neostriatum (LMAN) — the output nucleus of the anterior forebrain pathway — prevents the song deterioration that normally results from the absence of feedback.

  • How the songbird brain evaluates song and matches it to the internal model is not known. Song-selective neurons — cells found throughout the songbird brain that fire more strongly to the bird's own song than to the songs of other birds of the same species — could be involved in this process.

Access options

Rent or Buy article

Get time limited or full article access on ReadCube.

from$8.99

All prices are NET prices.

Figure 1: Timeline for zebra finch song learning.
Figure 2: Model of sensorimotor song learning.
Figure 3: Models of adult song stabilization.
Figure 4: Different models of the effects of deafening.
Figure 5: The song system and its forebrain auditory inputs.
Figure 6: Examples of changes to song for a deafened bird (a) and its brother (b), which further received bilateral lesions of the LMAN.

References

  1. 1

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

    CAS  Article  PubMed  Google Scholar 

  2. 2

    Thorpe, W. H. The learning of song patterns by birds with especial reference to the song of the chaffinch, Fringilla coelebs. Ibis 100 , 535–570 (1958).

    Article  Google Scholar 

  3. 3

    Immelmann, K. in Bird Vocalizations (ed. Hinde, R. A.) 61–74 (Cambridge Univ. Press, London, 1969).

    Google Scholar 

  4. 4

    Marler, P. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 71, 1–25 (1970).This important work describes many aspects of vocal learning in white-crowned sparrows, including imitation of tutor song, critical periods for sensory learning, the structure of songs of birds raised in isolation, the stability of adult song and the innate selectivity for the species own song. The discussion highlights the numerous parallels between bird song and speech learning, and stresses the importance of studying natural behaviours for understanding what the nervous system evolved to do.

    Article  Google Scholar 

  5. 5

    Konishi, M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22, 770– 783 (1965).This seminal work showed that deafening after tutoring but before song motor learning has profound effects on the vocalizations of white-crowned sparrows, whereas deafening of adult sparrows has little effect on their song. This showed that hearing was crucial not only for memorizing the tutor song, but for learning to produce a copy of it, and led to the concept of a stored template, formed during exposure to tutor, and later used to guide motor learning.

    CAS  PubMed  PubMed Central  Google Scholar 

  6. 6

    Price, P. H. Developmental determinants of structure in zebra finch song. J. Comp. Physiol. Psychol. 93, 268–277 (1979).

    Article  Google Scholar 

  7. 7

    Konishi, M. Birdsong: From behavior to neuron. Annu. Rev. Neurosci. 8, 125–170 (1985).

    CAS  PubMed  Article  Google Scholar 

  8. 8

    Fromkin, V., Krashen, S., Curtis, S., Rigler, D. & Rigler, M. The development of language in Genie: A case of language acquisition beyond the ‘critical period’. Brain Lang. 1, 81–107 ( 1974).

    Article  Google Scholar 

  9. 9

    Waldstein, R. S. Effects of postlingual deafness on speech production: Implications for the role of auditory feedback. J. Acoust. Soc. Am. 88, 2099–2144 (1990).

    CAS  PubMed  Article  Google Scholar 

  10. 10

    Cowie, R. & Douglas–Cowie, E. Postlingually Acquired Deafness: Speech Deterioration and the Wider Consequences (Mouton de Gruyter, Berlin, 1992).

    Book  Google Scholar 

  11. 11

    Snow, C. & Hoefnagel–Hohle, M. The critical period for language acquisition: Evidence from second language learning. Child Dev. 49, 1114–1128 (1978).

    Article  Google Scholar 

  12. 12

    Bradlow, A. R., Pisoni, D. B., Akahane-Yamada, R. & Tohkura, Y. Training Japanese listeners to identify English /r/ and /l/: IV. Some effects of perceptual learning on speech production. J. Acoust. Soc. Am. 101, 2299–2310 ( 1997).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. 13

    Werker, J. F. & Tees, R. C. The organization and reorganization of human speech perception. Annu. Rev. Neurosci. 15 , 377–402 (1992).

    CAS  PubMed  Article  Google Scholar 

  14. 14

    Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  15. 15

    Nordeen, K. W. & Nordeen, E. J. Auditory feedback is necessary for the maintenance of stereotyped song in adult zebra finches . Behav. Neural Biol. 57, 58– 66 (1992).

    CAS  PubMed  Article  Google Scholar 

  16. 16

    Lombardino, A. J. & Nottebohm, F. Age at deafening affects the stability of learned song in adult male zebra finches. J. Neurosci. 20, 5054–5064 (2000).

    CAS  PubMed  Article  Google Scholar 

  17. 17

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  18. 18

    Wang, N., Aviram, R. & Kirn, J. R. Deafening alters neuron turnover within the telencephalic motor pathway for song control in adult zebra finches. J. Neurosci. 19, 10554–10561 ( 1999).Deafening in adult zebra finches reduces the rate of neuronal replacement in the HVc. The authors point out that it remains unclear whether these changes are dependent on the loss of auditory feedback per se or on indirect consequences of deafening. Nevertheless, the results illustrate that deafening can induce profound changes in the regulation of the neural substrates for song production.

    CAS  PubMed  Article  Google Scholar 

  19. 19

    Nottebohm, F. Auditory experience and song learning in the chaffinch Fringilla coelebs . Ibis 111, 386–387 (1968).

    Article  Google Scholar 

  20. 20

    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).

    CAS  PubMed  Article  Google Scholar 

  21. 21

    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).

    CAS  PubMed  Article  Google Scholar 

  22. 22

    Nottebohm, F., Stokes, T. M. & Leonard, C. M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165, 457– 486 (1976).A combination of lesion, anatomical and behavioural analyses provide the first description of the nuclei essential for vocal control of song, including HVc, RA, Area X and nXII. The authors noted how useful the identification of a discrete system would be for the study of vocal learning, and delineated many of the questions that still occupy the field, including the localization of auditory and motor song memories, the interhemispheric coordination of vocalization and the evolutionary relationship of these vocal areas to structures in other birds and in mammals, including humans.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  23. 23

    Nottebohm, F. & Nottebohm, M. E. Relationship between song repertoire and age in the canary, Serinus canarius. Z. Tierpsychol. 46, 298–305 ( 1978).

    Article  Google Scholar 

  24. 24

    Mountjoy, D. J. & Lemon, R. E. Extended song learning in wild European starlings. Animal Behav. 49, 357–366 (1995).

    Article  Google Scholar 

  25. 25

    Bohner, J., Chaiken, M. L., Ball, G. F. & Marler, P. Song acquisition in photosensitive and photorefractory male European starlings . Horm. Behav. 24, 582– 594 (1990).

    CAS  PubMed  Article  Google Scholar 

  26. 26

    Goldman, S. A. & Nottebohm, F. Neuronal projection, migration and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl Acad. Sci. USA 80, 2390–2394 (1983).

    CAS  PubMed  Article  Google Scholar 

  27. 27

    Alvarez-Buylla, A. & Kirn, J. R. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol. 33, 585–601 (1997).

    CAS  PubMed  Article  Google Scholar 

  28. 28

    Scott, L. L., Nordeen, E. J. & Nordeen, K. W. The relationship between rates of HVc neuron addition and vocal plasticity in adult songbirds. J. Neurobiol. 43, 79–88 (2000).

    CAS  PubMed  Article  Google Scholar 

  29. 29

    Nordeen, K. W. & Nordeen, E. J. Projection neurons within a vocal motor pathway are born during song learning in zebra finches. Nature 334, 149– 151 (1988).

    CAS  PubMed  Article  Google Scholar 

  30. 30

    Arnold, A. P. The effects of castration and androgen replacement on song, courtship, and aggression in zebra finches (Poephila guttata). J. Exp. Zool. 191, 309–326 ( 1975).

    CAS  PubMed  Article  Google Scholar 

  31. 31

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

    CAS  PubMed  Article  Google Scholar 

  32. 32

    DeVoogd, T. & Nottebohm, F. Gonadal hormones induce dendritic growth in the adult avian brain. Science 214, 202–204 (1981).

    CAS  PubMed  Article  Google Scholar 

  33. 33

    Bottjer, S. W. & Johnson, F. Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol. 33, 602–618 (1997).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  34. 34

    Rasika, S., Nottebohm, F. & Alvarez-Buylla, A. Testosterone increases the recruitment and/or survival of new high vocal center neurons in adult female canaries. Proc. Natl Acad. Sci. USA 91, 7854–7858 (1994).

    CAS  PubMed  Article  Google Scholar 

  35. 35

    Burek, M. J., Nordeen, K. W. & Nordeen, E. J. Neuron loss and addition in developing zebra finch song nuclei are independent of auditory experience during song learning. J. Neurobiol. 22, 215–223 (1991).

    CAS  PubMed  Article  Google Scholar 

  36. 36

    Livingston, F. S., White, S. A. & Mooney, R. Slow NMDA-EPSCs at synapses critical for song development are not required for song learning in zebra finches. Nature Neurosci. 3, 482–488 ( 2000).

    CAS  PubMed  Article  Google Scholar 

  37. 37

    Li, X.-C., Jarvis, E. D., Alvarez-Borda, B., Lim, D. A. & Nottebohm, F. A relationship between behavior, neurotrophin expression, and new neuron survival. Proc. Natl Acad. Sci. USA 97, 8584–8589 ( 2000).

    CAS  PubMed  Article  Google Scholar 

  38. 38

    Leonardo, A. & Konishi, M. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399, 466–470 (1999).

    CAS  PubMed  Article  Google Scholar 

  39. 39

    Lee, B. S. Effects of delayed speech feedback. J. Acoust. Soc. Am. 22, 824–826 (1950).

    Article  Google Scholar 

  40. 40

    Howell, P. & Archer, A. Susceptibility to the effects of delayed auditory feedback. Percept. Psychophysiol. 36, 296–302 (1984).

    CAS  Article  Google Scholar 

  41. 41

    Houde, J. F. & Jordan, M. I. Sensorimotor adaptation in speech production. Science 279, 1213– 1216 (1998).

    CAS  PubMed  Article  Google Scholar 

  42. 42

    Kelley, D. B. & Nottebohm, F. Projections of a telencephalic auditory nucleus — Field L — in the canary. J. Comp. Neurol. 183, 455–470 ( 1979).

    CAS  PubMed  Article  Google Scholar 

  43. 43

    Fortune, E. S. & Margoliash, D. Parallel pathways and convergence onto HVc and adjacent neostriatum of adult zebra finches ( Taeniopygia guttata). J. Comp. Neurol. 360, 413–441 (1995).

    CAS  PubMed  Article  Google Scholar 

  44. 44

    Vates, G. E., Broome, B. M., Mello, C. V. & Nottebohm, F. Auditory pathways of caudal telencephalon and their relation to the song system of adult male zebra finches (Taeniopygia guttata). J. Comp. Neurol. 366, 613–642 ( 1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  45. 45

    Wild, J. M. Neural pathways for the control of birdsong production. J. Neurobiol. 33, 653–670 ( 1997).

    CAS  PubMed  Article  Google Scholar 

  46. 46

    Nottebohm, F., Kelley, D. B. & Paton, J. A. Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207, 344 –357 (1982).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. 47

    McCasland, J. S. Neuronal control of bird song production. J. Neurosci. 7, 23–39 (1987).

    CAS  PubMed  Article  Google Scholar 

  48. 48

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

    CAS  PubMed  Article  Google Scholar 

  49. 49

    Janata, P. & Margoliash, D. Gradual emergence of song selectivity in sensorimotor structures of the male zebra finch song system. J. Neurosci. 19, 5108–5118 (1999).

    CAS  PubMed  Article  Google Scholar 

  50. 50

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  51. 51

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  52. 52

    Luo, M. & Perkel, D. J. Long-range GABAergic projection in a circuit essential for vocal learning. J. Comp. Neurol. 403, 68–84 (1999).

    CAS  PubMed  Article  Google Scholar 

  53. 53

    Reiner, A., Medina, L. & Veenman, C. L. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res. Brain Res. Rev. 28, 235–285 (1998).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  54. 54

    Okuhata, S. & Saito, N. Synaptic connections of thalamo-cerebral vocal control nuclei of the canary. Brain Res. Bull. 18, 35–44 (1987).

    CAS  PubMed  Article  Google Scholar 

  55. 55

    Bottjer, S. W., Halsema, K. A., Brown, S. A. & Miesner, E. A. Axonal connections of a forebrain nucleus involved with vocal learning in zebra finches. J. Comp. Neurol. 279, 312 –326 (1989).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  56. 56

    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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  57. 57

    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). This paper showed that lesions of Area X and LMAN in young birds affect song learning, but that the resulting song differs in each case. LMAN-lesioned birds show abnormal but prematurely crystallized song, whereas birds with Area X lesions show abnormal song that does not crystallize. This raised the possibility that LMAN lesions removed signals critical for plasticity as well as information necessary for guiding song. In contrast, Area X lesions may remove only the song-related information, leaving song plasticity intact but unguided. Regardless of mechanism, this result is a reminder that the complex processing in this basal ganglia circuit deserves further investigation.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  58. 58

    Sohrabji, F., Nordeen, E. J. & Nordeen, K. W. Selective impairment of song learning following lesions of a forebrain nucleus in the juvenile zebra finch. Behav. Neural Biol. 53, 51–63 ( 1990).

    CAS  PubMed  Article  Google Scholar 

  59. 59

    Nordeen, K. W. & Nordeen, E. J. Long-term maintenance of song in adult zebra finches is not affected by lesions of a forebrain region involved in song learning. Behav. Neural Biol. 59, 79–82 (1993).

    CAS  PubMed  Article  Google Scholar 

  60. 60

    Basham, M. E., Nordeen, E. J. & Nordeen, K. W. Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch. Neurobiol. Learning Mem. 66, 295–304 ( 1996).Reversible inactivation of the AFP specifically during tutoring sessions, but not during song rehearsal, disrupted song learning. Pharmacological treatment of the AFP did not affect birds' performance on a song discrimination task, ruling out gross effects of the treatment on hearing or attention, although it remains possible that song memorization is more susceptible than discrimination to such effects. Nonetheless, this intriguing result provides perhaps the most direct evidence that the AFP is involved in memorization of the tutor song.

    CAS  Article  Google Scholar 

  61. 61

    Doupe, A. J. Song- and order-selective neurons in the songbird anterior forebrain and their emergence during vocal development. J. Neurosci. 17 , 1147–1167 (1997).

    CAS  PubMed  Article  Google Scholar 

  62. 62

    Solis, M. M. & Doupe, A. J. Anterior forebrain neurons develop selectivity by an intermediate stage of birdsong learning. J. Neurosci. 17, 6447–6462 ( 1997).A key question is whether song selectivity reflects the tutor song or the bird's experience of its own voice. This work tackled the issue for AFP neurons by studying birds induced to sing songs very different from their tutor by manipulation of the peripheral vocal musculature. This revealed that song-selective neurons are shaped by experience of the bird's own vocalizations, but that many of them also respond to the tutor song. Therefore both bird's own song and tutor song experience seem to shape the properties of individual AFP neurons.

    CAS  PubMed  Article  Google Scholar 

  63. 63

    Solis, M. M. & Doupe, A. J. Contributions of tutor and bird's own song experience to neural selectivity in the songbird anterior forebrain . J. Neurosci. 19, 4559– 4584 (1999).

    CAS  PubMed  Article  Google Scholar 

  64. 64

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

    CAS  PubMed  Article  Google Scholar 

  65. 65

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

    CAS  PubMed  Article  Google Scholar 

  66. 66

    Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000). This work showed that both sets of HVc projection neurons (to RA and to Area X) as well as the HVc interneurons show song-selective responses in anaesthetized animals. There are subtle but potentially important differences between their properties, which begin to shed light on synaptic interactions within the nucleus as well as on how information being sent to the motor pathway and the AFP might differ.

    CAS  PubMed  Article  Google Scholar 

  67. 67

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

    CAS  PubMed  Article  Google Scholar 

  68. 68

    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).

    CAS  PubMed  Article  Google Scholar 

  69. 69

    Burt, J. M., Lent, K. L., Beecher, M. D. & Brenowitz, E. A. Lesions of the anterior forebrain song control pathway in female canaries affect song perception in an operant task. J. Neurobiol. 42, 1–13 (2000).

    CAS  PubMed  Article  Google Scholar 

  70. 70

    Morrison, R. G. & Nottebohm, F. Role of a telencephalic nucleus in the delayed song learning of socially isolated zebra finches. J. Neurobiol. 24, 1045–1064 (1993).

    CAS  PubMed  Article  Google Scholar 

  71. 71

    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).

    CAS  PubMed  Article  Google Scholar 

  72. 72

    Herrmann, K. & Arnold, A. P. The development of afferent projections to the robust archistriatal nucleus in male zebra finches: A quantitative electron microscopic study. J. Neurosci. 11, 2063–2074 (1991).

    CAS  PubMed  Article  Google Scholar 

  73. 73

    Mooney, R. Synaptic basis for developmental plasticity in a birdsong nucleus. J. Neurosci. 12, 2464–2477 (1992).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  74. 74

    Kubota, M. & Saito, N. NMDA receptors participate differentially in two different synaptic inputs in neurons of the zebra finch robust nucleus of the archistriatum in vitro. Neurosci. Lett. 125, 107–109 (1991).

    CAS  PubMed  Article  Google Scholar 

  75. 75

    Johnson, F., Hohmann, S. E., DiStefano, P. S. & Bottjer, S. W. Neurotrophins suppress apoptosis induced by deafferentation of an avian motor-cortical region. J. Neurosci. 17, 2101– 2111 (1997).

    CAS  PubMed  Article  Google Scholar 

  76. 76

    Akutagawa, E. & Konishi, M. Two separate areas of the brain differentially guide the development of a song control nucleus in the zebra finch. Proc. Natl Acad. Sci. USA 91, 12413 –12417 (1994).

    CAS  PubMed  Article  Google Scholar 

  77. 77

    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).

    CAS  PubMed  Article  Google Scholar 

  78. 78

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

    CAS  PubMed  Article  Google Scholar 

  79. 79

    Houk, J. C., Davis, J. L. & Beiser, D. G. in Models of Information Processing in the Basal Ganglia 1–382 (MIT Press, Cambridge, Massachusetts, 1994).

    Book  Google Scholar 

  80. 80

    Smith, M. A., Brandt, J. & Shadmehr, R. Motor disorder in Huntington's disease begins as a dysfunction in error feedback control. Nature 403, 544 –549 (2000).Examined motor control in carriers of the gene for Huntington's disease. Before the clinical onset of disease, gene carriers show deficits in correction of arm movements in response to internally or externally generated errors. The results are consistent with a possible role of the basal ganglia in error feedback control.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  81. 81

    Nakamura, K., Sakai, K. & Hikosaka, O. Effects of local inactivation of monkey medial frontal cortex in learning of sequential procedures. J. Neurophysiol. 82, 1063–1068 (1999).

    CAS  PubMed  Article  Google Scholar 

  82. 82

    Volman, S. F. Development of neural selectivity for birdsong during vocal learning. J. Neurosci. 13, 4737–4747 (1993).

    CAS  PubMed  Article  Google Scholar 

  83. 83

    Mello, C. V., Vicario, D. S. & Clayton, D. F. Song presentation induces gene expression in the songbird forebrain. Proc. Natl Acad. Sci. USA 89, 6818–6822 (1992).

    CAS  PubMed  Article  Google Scholar 

  84. 84

    Chew, S. J., Vicario, D. S. & Nottebohm, F. A large-capacity memory system that recoginzes the calls and songs of individual birds. Proc. Natl Acad. Sci. USA 93, 1950–1955 (1996).

    CAS  PubMed  Article  Google Scholar 

  85. 85

    Stripling, R., Volman, S. F. & Clayton, D. F. Response modulation in the zebra finch neostriatum: relationship to nuclear gene regulation. J. Neurosci. 17, 3883–3893 (1997).

    CAS  PubMed  Article  Google Scholar 

  86. 86

    Jin, H. & Clayton, D. F. Localized changes in immediate-early gene regulation during sensory and motor learning in zebra finches. Neuron 19, 1049–1059 ( 1997).

    CAS  PubMed  Article  Google Scholar 

  87. 87

    Mello, C. V. & Ribeiro, S. ZENK protein regulation by song in the brain of songbirds. J. Comp. Neurol. 393, 426–438 (1998).

    CAS  PubMed  Article  Google Scholar 

  88. 88

    Bolhuis, J. J., Zijlstra, G. G., den Boer-Visser, A. M. & Van Der Zee, E. A. Localized neuronal activation in the zebra finch brain is related to the strength of song learning. Proc. Natl Acad. Sci. USA 97, 2282–2285 (2000).

    CAS  PubMed  Article  Google Scholar 

  89. 89

    Dave, A. S., Yu, A. C. & Margoliash, D. Behavioral state modulation of auditory activity in a vocal motor system. Science 282, 2250– 2254 (1998).Neurons of RA showed far weaker auditory responses in awake than in anaesthetized zebra finches. However, sleep uncovered vigorous auditory responses of RA neurons, and injections of noradrenaline into HVc of anaesthetized birds could mimic the suppression of RA responses normally observed during wakefulness. So auditory feedback may be subject to neuromodulatory control.

    CAS  PubMed  Article  Google Scholar 

  90. 90

    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).

    CAS  PubMed  Article  Google Scholar 

  91. 91

    Schmidt, M. F. & Konishi, M. Gating of auditory responses in the vocal control system of awake songbirds. Nature Neurosci. 1, 513–518 ( 1998).Showed that many HVc neurons with song-selective responses under anaesthesia show no responses to the same songs in the awake, unrestrained bird. This suppression of auditory responses in awake birds does not occur in the field L complex, which is one of the sources of auditory input to HVc. Such ‘gating’ of auditory input to a vocal control nucleus may reflect the regulation of sensory feedback signals generated by an animal's own motor behaviour.

    CAS  PubMed  Article  Google Scholar 

  92. 92

    Pearson, K. G. Common principles of motor control in vertebrates and invertebrates. Annu. Rev. Neurosci. 16, 265–297 (1993).

    CAS  PubMed  Article  Google Scholar 

  93. 93

    Jordan, M. I. in The Cognitive Neurosciences (ed. Gazzaniga, M.) 567– 610 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  94. 94

    Hirano, S. et al. Cortical processing mechanism for vocalization with auditory verbal feedback. Neuroreport 8, 2379– 2382 (1997).

    CAS  PubMed  Article  Google Scholar 

  95. 95

    McGuire, P. K., Silbersweig, D. A. & Frith, C. D. Functional neuroanatomy of verbal self-monitoring . Brain 119, 907–917 (1996).

    PubMed  PubMed Central  Article  Google Scholar 

  96. 96

    Troyer, T. & 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).

    CAS  PubMed  Article  Google Scholar 

  97. 97

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

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  98. 98

    Pepperberg, I. M. The Alex Studies: Cognitive and Communicative Abilities of Grey Parrots. (Harvard Univ. Press, Cambridge, Massachusetts, 1999).

    Google Scholar 

  99. 99

    Baptista, L. F. & Petrinovich, L. Song development in the white-crowned sparrow: Social factors and sex differences. Animal Behav. 34, 1359–1371 (1986).

    Article  Google Scholar 

  100. 100

    Eales, L. A. The influences of visual and vocal interaction on song learning in zebra finches . Animal Behav. 37, 507– 508 (1989).

    Article  Google Scholar 

  101. 101

    Marler, P. & Peters, S. Developmental overproduction and selective attrition: new processes in the epigenesis of birdsong. Dev. Psychobiol. 15, 369–378 (1982).

    CAS  PubMed  Article  Google Scholar 

  102. 102

    West, M. J. & King, A. P. Female visual displays affect the development of male song in the cowbird. Nature 334 , 244–246 (1988).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  103. 103

    Nelson, D. A. & Marler, P. Selection-based learning in bird song development. Proc. Natl Acad. Sci. USA 91, 10498–10501 (1994).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  104. 104

    Sossinka, R. & Bohner, J. Song types in the zebra finch Poephila guttata castanotis. Z. Tierpsychol. 53 , 123–132 (1980).

    Article  Google Scholar 

  105. 105

    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).

    CAS  PubMed  Article  Google Scholar 

  106. 106

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

    CAS  PubMed  Article  Google Scholar 

Download references

Acknowledgements

We thank S. Lisberger for helpful comments on the manuscript. The work of the authors was supported by the National Institutes of Health, a Burroughs Wellcome Fund Fellowship of the Life Sciences Research Foundation, the John Merck Fund and the EJLB foundation.

Author information

Affiliations

Authors

Supplementary information

Related links

Related links

FURTHER INFORMATION

Allison Doupe's laboratory

ENCYLOPEDIA OF LIFE SCIENCES

Bird song: steroid hormones and plasticity

Glossary

PHONEME

A distinct unit of sound that distinguishes one word from another.

BASAL GANGLIA

A collection of brain structures that modulate cortical output.

WERNICKE'S AREA

Region of the parietal cortex involved in speech processing.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Brainard, M., Doupe, A. Auditory feedback in learning and maintenance of vocal behaviour . Nat Rev Neurosci 1, 31–40 (2000). https://doi.org/10.1038/35036205

Download citation

Further reading

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