Bird fanciers have known for centuries that songbirds learn their songs. This learning has striking parallels to speech acquisition: like humans, birds must hear the sounds of adults during a sensitive period, and must hear their own voice while learning to vocalize. With the discovery and investigation of discrete brain structures required for singing, songbirds are now providing insights into neural mechanisms of learning. Aided by a wealth of behavioural observations and species diversity, studies in songbirds are addressing such basic issues in neuroscience as perceptual and sensorimotor learning, developmental regulation of plasticity, and the control and function of adult neurogenesis.
Subscribe to Journal
Get full journal access for 1 year
only $3.90 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Rent or Buy article
Get time limited or full article access on ReadCube.
All prices are NET prices.
Thorpe, W. H. Bird-Song (Cambridge Univ. Press, Cambridge, 1961).
Marler, P. A comparative approach to vocal learning: song development in white-crowned sparrows. J. Comp. Physiol. Psychol. 71, 1–25 (1970).
Konishi, M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22, 770–783 (1965).
Konishi, M. Birdsong: from behavior to neuron. Annu. Rev. Neurosci. 8, 125–170 (1985).
Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999).
Cowie, R. & Douglas-Cowie, E. Postlingually Acquired Deafness: Speech Deterioration and the Wider Consequences (Mouton de Gruyter, Berlin, 1992).
Wild, J. M. Neural pathways for the control of birdsong production. J. Neurobiol. 33, 653–670 (1997).
Suthers, R. A., Goller, F. & Pytte, C. The neuromuscular control of birdsong. Phil. Trans. R. Soc. Lond. B 354, 927–939 (1999).
Nottebohm, F., Stokes, T. M. & Leonard, C. M. Central control of song in the canary, Serinus canarius. J. Comp. Neurol. 165, 457–486 (1976).
McCasland, J. S. Neuronal control of bird song production. J. Neurosci. 7, 23–39 (1987).
Chi, Z. & Margoliash, D. Temporal precision and temporal drift in brain and behavior of zebra finch song. Neuron 32, 899–910 (2001).
Yu, A. C. & Margoliash, D. Temporal hierarchical control of singing in birds. Science 273, 1871–1875 (1996).
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).
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).
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).
Margoliash, D. Acoustic parameters underlying the responses of song-specific neurons in the white-crowned sparrow. J. Neurosci. 3, 1039–1057 (1983).
Margoliash, D. & Fortune, E. S. Temporal and harmonic combination-sensitive neurons in the zebra finch's HVc. J. Neurosci. 12, 4309–4326 (1992).
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).
Bottjer, S. W. & Johnson, F. Circuits, hormones, and learning: vocal behavior in songbirds. J. Neurobiol. 33, 602–618 (1997).
Luo, M., Ding, L. & Perkel, D. J. An avian basal ganglia pathway essential for vocal learning forms a closed topographic loop. J. Neurosci. 21, 6836–6845 (2001).
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).
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).
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).
Dooling, R. & Searcy, M. Early perceptual selectivity in the swamp sparrow. Dev. Psychobiol. 13, 499–506 (1980).
Nelson, D. A. & Marler, P. Innate recognition of song in white-crowned sparrows: a role in selective vocal learning? Anim. Behav. 46, 806–808 (1993).
Marler, P. & Peters, S. The role of song phonology and syntax in vocal learning preferences in the song sparrow, Melospiza melodia. Ethology 77, 125–149 (1988).
Hultsch, H. & Todt, D. Song acquisition and acquisition constraints in the nightingale, Luscinia megarhynchos. Naturwissenschaften 76, 83–85 (1989).
Tchernichovski, O., Lints, T., Mitra, P. P. & Nottebohm, F. Vocal imitation in zebra finches is inversely related to model abundance. Proc. Natl Acad. Sci. USA 96, 12901–12904 (1999).
Slater, P. J. B., Eales, L. A. & Clayton, N. S. Song learning in zebra finches (Taeniopygia guttata): progress and prospects. Adv. Study Behav. 18, 1–34 (1988).
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).
Baptista, L. F. & Petrinovich, L. Song development in the white-crowned sparrow: social factors and sex differences. Anim. Behav. 34, 1359–1371 (1986).
Nordby, J. C., Campbell, S. E., Burt, J. M. & Beecher, M. D. Social influences during song development in the song sparrow: a laboratory experiment simulating field conditions. Anim. Behav. 59, 1187–1197 (2000).
Whaling, C. S., Soha, J. A., Nelson, D. A., Lasley, B. & Marler, P. Photoperiod and tutor access affect the process of vocal learning. Anim. Behav. 56, 1075–1082 (1998).
Volman, S. F. Development of neural selectivity for birdsong during vocal learning. J. Neurosci. 13, 4737–4747 (1993).
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).
Schmidt, M. F. & Konishi, M. Gating of auditory responses in the vocal control system of awake songbirds. Nature Neurosci. 1, 513–518 (1998).
Dave, A. S., Yu, A. C. & Margoliash, D. Behavioral state modulation of auditory activity in a vocal motor system. Science 282, 2250–2254 (1998).
Pearson, K. G. Common principles of motor control in vertebrates and invertebrates. Annu. Rev. Neurosci. 16, 265–297 (1993).
Mello, C. V. & Clayton, D. F. Song-induced ZENK gene expression in auditory pathways of songbird brain and its relation to the song control system. J. Neurosci. 14, 6652–6666 (1994).
Stripling, R., Kruse, A. A. & Clayton, D. F. Development of song responses in the zebra finch caudomedial neostriatum: role of genomic and electrophysiological activities. J. Neurobiol. 48, 163–180 (2001).
Theunissen, F. E., Sen, K. & Doupe, A. J. Spectral-temporal receptive fields of nonlinear auditory neurons obtained using natural sounds. J. Neurosci. 20, 2315–2331 (2000).
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).
Marler, P. & Doupe, A. J. Singing in the brain. Proc. Natl Acad. Sci. USA 97, 2965–2967 (2000).
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. Learn. Mem. 66, 295–304 (1996).
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).
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).
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).
Nordeen, K. W. & Nordeen, E. J. Anatomical and synaptic substrates for avian song learning. J. Neurobiol. 33, 532–548 (1997).
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).
Iyengar, S., Viswanathan, S. S. & Bottjer, S. W. Development of topography within song control circuitry of zebra finches during the sensitive period for song learning. J. Neurosci. 19, 6037–6057 (1999).
Wallhausser-Franke, E., Nixdorf-Bergweiler, B. E. & DeVoogd, T. J. Song isolation is associated with maintaining high spine frequencies on zebra finch LMAN neurons. Neurobiol. Learn. Mem. 64, 25–35 (1995).
Iyengar, S. & Bottjer, S. Development of individual axon arbors in a thalamocortical circuit necessary for song learning in zebra finches. J. Neurosci. 22, 901–911 (2002).
Aamodt, S. M., Kozlowski, M. R., Nordeen, E. J. & Nordeen, K. W. Distribution and developmental change in [3H]MK-801 binding within zebra finch song nuclei. J. Neurobiol. 23, 997–1005 (1992).
Boettiger, C. A. & Doupe, A. J. Developmentally restricted synaptic plasticity in a songbird nucleus required for song learning. Neuron 31, 809–818 (2001).
Price, P. H. Developmental determinants of structure in zebra finch song. J. Comp. Physiol. Psychol. 93, 268–277 (1979).
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).
Brainard, M. S. & Doupe, A. J. Interruption of a basal ganglia-forebrain circuit prevents plasticity of learned vocalizations. Nature 404, 762–766 (2000).
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).
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).
Jarvis, E. D. & Nottebohm, F. Motor-driven gene expression. Proc. Natl Acad. Sci. USA 94, 4097–4102 (1997).
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).
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).
Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812–816 (2000).
Nelson, D. A. & Marler, P. Selection-based learning in bird song development. Proc. Natl Acad. Sci USA 91, 10498–10501 (1994).
West, M. J. & King, A. P. Female visual displays affect the development of male song in the cowbird. Nature 334, 244–246 (1988).
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).
Hessler, N. A. & Doupe, A. J. Social context modulates singing-related neural activity in the songbird forebrain. Nature Neurosci. 2, 209–211 (1999).
Pytte, C. L. & Suthers, R. A. Sensitive period for sensorimotor integration during vocal motor learning. J. Neurobiol. 42, 172–189 (2000).
Williams, H. & McKibben, J. R. Changes in stereotyped central motor patterns controlling vocalization are induced by peripheral nerve injury. Behav. Neural Biol. 57, 67–78 (1992).
Hough, G. & Volman, S. Short-term and long-term effects of vocal distortion on song maintenance in zebra finches. J. Neurosci. 22, 1177–1186 (2002).
Brainard, M. S. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behavior. Nature Rev. Neurosci. 1, 31–40 (2000).
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).
Leonardo, A. & Konishi, M. Decrystallization of adult birdsong by perturbation of auditory feedback. Nature 399, 466–470 (1999).
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).
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).
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).
Brainard, M. S. & Doupe, A. J. Post-learning consolidation of the motor program for birdsong: stabilizing effects of age and anterior forebrain lesions. J. Neurosci. 21, 2501–2517 (2001).
Stickgold, R., Hobson, J. A., Fosse, R. & Fosse, M. Sleep, learning, and dreams: off-line memory reprocessing. Science 294, 1052–1057 (2001).
Nottebohm, F., Nottebohm, M. E., Crane, L. & Wingfield, J. C. Seasonal change in gonadal hormone levels of adult male canaries and their relation to song. Behav. Neural Biol. 47, 197–211 (1987).
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).
Arnold, A. P., Bottjer, S. W., Brenowitz, E. A., Nordeen, E. J. & Nordeen, K. W. Sexual dimorphisms in the neural vocal control system in song birds: ontogeny and phylogeny. Brain Behav. Evol. 28, 22–31 (1986).
Holloway, C. C. & Clayton, D. F. Estrogen synthesis in the male brain triggers development of the avian song control pathway in vitro. Nature Neurosci. 4, 170–175 (2001).
Korsia, S. & Bottjer, S. W. Chronic testosterone treatment impairs vocal learning in male zebra finches during a restricted period of development. J. Neurosci. 11, 2362–2371 (1991).
Whaling, C. S., Nelson, D. A. & Marler, P. Testosterone-induced shortening of the storage phase of song development in birds interferes with vocal learning. Dev. Psychobiol. 28, 367–376 (1995).
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).
Bottjer, S. W. & Hewer, S. J. Castration and antisteroid treatment impair vocal learning in male zebra finches. J. Neurobiol. 23, 337–353 (1992).
Ball, G. F. in The Design of Animal Communication (eds Hauser, M.D. & Konishi, M.) 215–253 (MIT Press, Cambridge, MA, 1999).
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).
Altman, J. & Das, G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319–336 (1965).
Goldman, S. A. & Nottebohm, F. Neuronal production, migration, and differentiation in a vocal control nucleus in the adult female canary brain. Proc. Natl Acad. Sci. USA 80, 2390–2394 (1983).
Kirn, J. R., Alvarez-Buylla, A. & Nottebohm, F. Production and survival of projection neurons in a forebrain vocal center of adult male canaries. J. Neurosci. 11, 1756–1762 (1991).
Alvarez-Buylla, A. & Kirn, J. R. Birth, migration, incorporation, and death of vocal control neurons in adult songbirds. J. Neurobiol. 33, 585–601 (1997).
Gould, E. & Gross, C. G. Neurogenesis in adult mammals: some progress and problems. J. Neurosci. 22, 619–623 (2002).
Scharff, C., Kirn, J. R., Grossman, M., Macklis, J. D. & Nottebohm, F. Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25, 481–492 (2000).
Rasika, S., Alvarez-Buylla, A. & Nottebohm, F. BDNF mediates the effects of testosterone on the survival of new neurons in an adult brain. Neuron 22, 53–62 (1999).
Brown, S. D., Johnson, F. & Bottjer, S. W. Neurogenesis in adult canary telencephalon is independent of gonadal hormone levels. J. Neurosci. 13, 2024–2032 (1993).
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).
Tramontin, A. D. & Brenowitz, E. A. A field study of seasonal neuronal incorporation into the song control system of a songbird that lacks adult song learning. J. Neurobiol. 40, 316–326 (1999).
Lewicki, M. & Konishi, M. Mechanisms underlying the sensitivity of songbird forebrain neurons to temporal order. Proc. Natl Acad. Sci. USA 92, 5582–5586 (1995).
Mooney, R. Different subthreshold mechanisms underlie song selectivity in identified HVc neurons of the zebra finch. J. Neurosci. 20, 5420–5436 (2000).
We are grateful to M. Kao for thoughtful comments on the manuscript and help with figures. Work in the authors' laboratories is supported by the NIH, the Sandler Family Supporting Foundation, NARSAD and the Grable Foundation, and the Kirsch Foundation.
About this article
Chronic exposure to urban noise during the vocal learning period does not lead to increased song frequencies in zebra finches
Behavioral Ecology and Sociobiology (2021)
Journal of Neurophysiology (2020)
Neural properties of fundamental function encoding of sound selectivity in the female avian auditory cortex
European Journal of Neuroscience (2020)
Frontiers in Neural Circuits (2020)