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Twitter evolution: converging mechanisms in birdsong and human speech

Key Points

  • Unlike non-human primates, songbirds learn to vocalize very much like human infants learn to speak. In both cases, young individuals form auditory memories of the vocalizations of adults during a sensitive period, and they acquire their own vocalizations through a transitional phase that is called 'subsong' in birds and 'babbling' in infants.

  • In songbirds, a network of interconnected brain nuclei, known as the song system, is involved in the perception, learning and production of song. Parts of the song system are analogous — and possibly homologous — to human basal ganglia as well as regions in the frontal cortex that are involved in speech.

  • In songbirds, regions outside the song system, in the caudal pallium, are involved in auditory memory; activation of one of these regions, the caudiomedial nidopallium (NCM), is related to the strength of tutor song memory. These pallial regions are analogous — and possibly homologous — to a region in the human temporal lobe known as the auditory association cortex that is involved in speech processing.

  • In both humans and songbirds, the vocal 'motor regions' are also involved in auditory perception. For learning and maintenance of speech and birdsong, continual interaction between auditory and motor regions to match what is heard and what is produced is necessary.

  • Some species of songbirds including Bengalese finches (Lonchura striata domestica) have types of note-to-note transition rules that could be expressed as 'finite-state syntax', which is a simpler form of human syntax.

  • FOXP2 is the first gene specifically implicated in speech and language, and its sequences are more than 90% conserved between birds and mammals. FOXP2 is regulated developmentally and seasonally and by singing activity in songbirds, and experimentally downregulated FOXP2 levels impair song learning.

  • Further multidisciplinary research is needed to study the molecular, neural and cognitive mechanisms of birdsong, and its similarities with human speech. Such analyses may ultimately have heuristic value for the study of speech acquisition and production in humans and its underlying mechanisms.

Abstract

Vocal imitation in human infants and in some orders of birds relies on auditory-guided motor learning during a sensitive period of development. It proceeds from 'babbling' (in humans) and 'subsong' (in birds) through distinct phases towards the full-fledged communication system. Language development and birdsong learning have parallels at the behavioural, neural and genetic levels. Different orders of birds have evolved networks of brain regions for song learning and production that have a surprisingly similar gross anatomy, with analogies to human cortical regions and basal ganglia. Comparisons between different songbird species and humans point towards both general and species-specific principles of vocal learning and have identified common neural and molecular substrates, including the forkhead box P2 (FOXP2) gene.

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Figure 1: The songbird brain and the human brain.
Figure 2: Neural dissociation between birdsong recognition and production.

References

  1. Darwin, C. The Descent of Man and Selection in Relation to Sex. (Murray, London, 1882).

    Book  Google Scholar 

  2. Bolhuis, J. J. & Wynne, C. D. L. Can evolution explain how minds work? Nature 458, 832–833 (2009).

    CAS  PubMed  Article  Google Scholar 

  3. Hauser, M. D., Chomsky, N. & Fitch, W. T. The faculty of language: what is it, who has it, and how did it evolve? Science, 298, 1569–1579 (2002). A thought-provoking opinion article on the possible evolution of language, with suggested criteria for language, including recursion.

    CAS  PubMed  Article  Google Scholar 

  4. Fitch, W. T. The evolution of speech: a comparative review. Trends Cogn. Sci. 4, 258–267 (2000).

    CAS  PubMed  Article  Google Scholar 

  5. Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999). The first detailed review of the many behavioural and neural parallels between birdsong and human speech.

    CAS  PubMed  Article  Google Scholar 

  6. Brainard, M. S. & Doupe, A. J. What songbirds teach us about learning. Nature 417, 351–358 (2002).

    CAS  PubMed  Article  Google Scholar 

  7. Bolhuis, J. J. & Gahr, M. Neural mechanisms of birdsong memory. Nature Rev. Neurosci. 7, 347–357 (2006).

    CAS  Article  Google Scholar 

  8. Yip, M. The search for phonology in other species. Trends Cogn. Sci. 10, 442–446 (2006).

    PubMed  Article  Google Scholar 

  9. Balter, M. Animal communication helps reveal the roots of language. Science 328, 969–971 (2010).

    CAS  PubMed  Article  Google Scholar 

  10. Wilbrecht, L. & Nottebohm, F. Vocal learning in birds and humans. Ment. Retard. Dev. Disabil. Res. Rev. 9, 135–148 (2003).

    PubMed  Article  Google Scholar 

  11. Scharff, C. & Haesler, S. An evolutionary perspective on FoxP2: strictly for the birds? Curr. Opin. Neurobiol. 15, 694–703 (2005).

    CAS  PubMed  Article  Google Scholar 

  12. Okanoya, K. Song syntax in Bengalese finches: proximate and ultimate analyses. Adv. Study Behav. 34, 297–346 (2004).

    Article  Google Scholar 

  13. Okanoya, K. Language evolution and an emergent property. Curr. Opin. Neurobiol. 17, 271–276 (2007).

    CAS  PubMed  Article  Google Scholar 

  14. Reiner, A. et al. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377–414 (2004). A landmark paper presenting a complete overhaul of the nomenclature of the avian brain, indicating possible homologies with the brain of mammals, including humans.

    PubMed  PubMed Central  Article  Google Scholar 

  15. Jarvis, E. D. et al. Avian brains and a new understanding of vertebrate brain evolution. Nature Rev. Neurosci. 6, 151–159 (2005). An important review of the consequences of the new nomenclature of the avian brain for the evolution of brain and behaviour, and our view of the 'birdbrain'.

    CAS  Article  Google Scholar 

  16. Mooney, R. Neural mechanisms for learned birdsong. Learn. Mem. 16, 655–669 (2009). An excellent contemporary review that synthesises recent findings to present a state-of-the-art view of the neural mechanisms of song learning.

    PubMed  Article  Google Scholar 

  17. Doupe, A. J., Perkel, D. J., Reiner, A. & Stern, E. A. Birdbrains could teach basal ganglia research a new song. Trends Neurosci. 28, 353–363 (2005).

    CAS  PubMed  Article  Google Scholar 

  18. Lai, C. S. L., Fisher, S. E., Hurst, J. A., Vargha-Khadem, F. & Monaco, A. P. A forkhead-domain gene is mutated in a severe speech and language disorder. Nature 413, 519–523 (2001). The first demonstration of a link between a specific gene, FOXP2 , and a human speech disorder called developmental verbal dyspraxia.

    CAS  PubMed  Article  Google Scholar 

  19. Fisher S. E. & Scharff, C. FOXP2 as a molecular window into speech and language. Trends Genet. 25, 166–177 (2009).

    CAS  PubMed  Article  Google Scholar 

  20. Haesler, S. et al. Incomplete and inaccurate vocal imitation after knockdown of FoxP2 in songbird basal ganglia nucleus Area X. PLoS Biol. 5, e321 (2007). The first in vivo gene-function analysis in songbirds, demonstrating that lentivirally-mediated knock down of the FOXP2 gene impairs the complete and accurate imitation of tutor song during song learning.

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  21. Fernald, R. D. Casting a genetic light on the evolution of eyes. Science 313, 1914–1918 (2006).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  23. Marler, P. in The Epigenesis of Mind: Essays on Biology and Cognition (eds Carey, S. & Gelman, R.) 37–66 (Lawrence Erlbaum Associates, Hillsdale, New Jersey, 1991).

    Google Scholar 

  24. Marler, P. & Peters, S. S. in The Comparative Psychology of Audition: Perceiving Complex Sounds (eds Hulse, S. & Dooling, R.) 243–273 (Lawrence Erlbaum, Hillsdale, New Jersey, 1989).

    Google Scholar 

  25. Pinker, S. The Language Instinct: How the Mind Creates Language (W. Morrow and Co., New York, 1994).

    Book  Google Scholar 

  26. Goller, F & Cooper B. G. In Neuroscience of Birdsong (eds Zeigler, H. P. & Marler, P.) 99–114 (Cambridge Univ. Press, New York, 2008).

    Google Scholar 

  27. 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 

  28. Catchpole, C. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations 2nd edn (Cambridge Univ. Press, Cambridge, 2008).

    Book  Google Scholar 

  29. Feher, O., Wang, H., Saar, S., Mitra, P. P. & Tchernichovski, O. De novo establishment of wild-type song culture in the zebra finch. Nature 459, 564–568 (2009). A demonstration that species-specific songs can emerge through a few generations of individual learning in the absence of correct external models.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  30. Hurford, J. R. The Evolution of the critical period for language acquisition. Cognition 40, 159–201 (1991).

    CAS  PubMed  Article  Google Scholar 

  31. Kipper, S. & Kiefer, S. Age-related changes in birds' singing styles: on fresh tunes and fading voices? Adv. Study Behav. 41, 77–118 (2010).

    Article  Google Scholar 

  32. Funabiki, Y. & Funabiki, K. Factors limiting song acquisition in adult zebra finches. Dev. Neurobiol. 69, 752–759 (2009).

    PubMed  Article  Google Scholar 

  33. Marler, P. Three models of song learning: evidence from behaviour. J. Neurobiol. 33, 501–516 (1997).

    CAS  PubMed  Article  Google Scholar 

  34. Hultsch, H. & Todt, D. in Nature's Music — The Science of Birdsong (eds Marler, P. & Slabbekoorn, H.) 80–107 (Academic Press, Amsterdam & Boston, 2004).

    Book  Google Scholar 

  35. Roper, A. & Zann, R. The onset of song learning and song tutor selection in fledgling zebra finches. Ethology 112, 458–470 (2006).

    Article  Google Scholar 

  36. Liu, W. C. & Nottebohm, F. A learning program that ensures prompt and versatile vocal imitation. Proc. Natl Acad. Sci. USA 104, 20398–20403 (2007).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  37. 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).

    CAS  PubMed  Article  Google Scholar 

  38. Aronov, D., Andalman, A. S. & Fee, M. S. A specialized forebrain circuit for vocal babbling in the juvenile songbird. Science 320, 630–634 (2008).

    CAS  PubMed  Article  Google Scholar 

  39. Deacon, T. W. Evolutionary perspectives on language and brain plasticity. J. Commun. Disord. 33, 273–291 (2000).

    CAS  PubMed  Article  Google Scholar 

  40. Hage, R. S. Neural networks involved in the generation of vocalization. Handb. Behav. Neurosci. 19, 339–349 (2009).

    Article  Google Scholar 

  41. Goldstein, M. H., King, A. P. & West, M. J. Social interaction shapes babbling: testing parallels between birdsong and speech. Proc. Natl Acad. Sci. USA 100, 8030–8035 (2003).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  42. Kuhl, P. K. & Rivera-Gaxiola, M. Neural substrates of early language acquisition. Annu. Rev. Neurosci. 31, 511–534 (2008).

    CAS  PubMed  Article  Google Scholar 

  43. Smith, V. A., King, A. P. & West, M. J. A role of her own: female cowbirds, Molothrus ater, influence the development and outcome of song learning. Anim. Behav. 60, 599–609 (2000).

    CAS  PubMed  Article  Google Scholar 

  44. Levelt, W. L. M. in The Neurocognition of Language. (eds Brown, C. M. & Hagoort, P.) 83–122 (Oxford Univ. Press, Oxford, 1999).

    Google Scholar 

  45. Fitch, W. T., Hauser, M. D. & Chomsky, N. The evolution of the language faculty: clarifications and implications. Cognition 97, 179–210 (2005).

    PubMed  Article  Google Scholar 

  46. Pinker, S. & Jackendoff, R. The faculty of language: what's special about it? Cognition 95, 201–236 (2005).

    PubMed  Article  Google Scholar 

  47. Staal, F. Rules Without Meaning. Ritual, Mantras and the Human Sciences (Peter Lang, New York, 1989).

    Google Scholar 

  48. Kumar, S. & Hedges, S. B. A molecular timescale for vertebrate evolution. Nature 392, 917–920 (1998).

    CAS  PubMed  Article  Google Scholar 

  49. Brainard, M. S. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behaviour. Nature Rev. Neurosci. 1, 31–40 (2000). An important review of the evidence pertaining to the role of auditory feedback in birdsong learning and production.

    CAS  Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  51. Bolhuis, J. J., Zijlstra, G. G. O., 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  PubMed Central  Google Scholar 

  52. Bolhuis, J. J., Hetebrij, E., Den Boer-Visser, A. M., De Groot, J. H. & Zijlstra, G. G. O. Localized immediate early gene expression related to the strength of song learning in socially reared zebra finches, Eur. J. Neurosci. 13, 2165–2170 (2001).

    CAS  PubMed  Article  Google Scholar 

  53. Terpstra, N. J., Bolhuis, J. J. & den Boer-Visser, A. M. An analysis of the neural representation of bird song memory. J. Neurosci. 24, 4971–4977 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  54. Phan, M. L., Pytte, C. L. & Vicario, D. S. Early auditory experience generates long-lasting memories that may subserve vocal learning in songbirds. Proc. Natl Acad. Sci. USA 103, 1088–1093 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  55. Demonet, J. F., Thierry, G. & Cardebat, D. Renewal of the neurophysiology of language: functional neuroimaging. Physiol. Rev. 85, 49–95 (2005).

    PubMed  Article  Google Scholar 

  56. Viceic, D. et al. Human auditory belt areas specialized in sound recognition: a functional magnetic resonance imaging study. Neuroreport 17, 1659–1662 (2006).

    PubMed  Article  Google Scholar 

  57. Karten, H. J. Evolutionary developmental biology meets the brain: the origins of mammalian cortex. Proc. Natl Acad. Sci. USA 94, 2800–2804 (1997).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  58. Reiner, A., Yamamoto, K. & Karten, H. J. Organization and evolution of the avian forebrain. Anat. Rec. A Discov. Mol. Cell. Evol. Biol. 287, 1080–1102 (2005).

    PubMed  Article  Google Scholar 

  59. Jarvis, E. D. Learned birdsong and the neurobiology of human language. Ann. NY Acad. Sci., 1016, 749–777 (2004).

    Article  Google Scholar 

  60. Okanoya, K. & Merker, B. in Emergence of Communication and Language (eds Lyon, C., Nehaniv, C. L. & Cangelosi, A.) 421–434 (Springer Verlag, London, 2007).

    Book  Google Scholar 

  61. Dehaene-Lambertz, G. et al. Functional organization of perisylvian activation during presentation of sentences in preverbal infants. Proc. Natl Acad. Sci. USA 103, 14240–14245 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  62. Gobes, S. M. H. & Bolhuis, J. J. Bird song memory: a neural dissociation between song recognition and production. Curr. Biol. 17, 789–793 (2007).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  64. Nick, T. A. & Konishi, M. Neural song preference during vocal learning in the zebra finch depends on age and state. J. Neurobiol. 62, 231–242 (2005).

    PubMed  Article  Google Scholar 

  65. Gentner, T. Q., Hulse, S. H., Bentley, G. E. & Ball, G. 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).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  Google Scholar 

  67. Gobes, S.M.H., Zandbergen, M.A. & Bolhuis, J.J. Memory in the making: Localized brain activation related to song learning in young songbirds. Proc. Roy. Soc. Lond., B. 277, 3343–3351 (2010).

    Article  Google Scholar 

  68. Nottebohm, F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214, 1368–1370 (1981).

    CAS  PubMed  Article  Google Scholar 

  69. Solis, M. M., Brainard, M. S., Hessler, N. A. & Doupe, A. J. Song selectivity and sensorimotor signals in vocal learning and production. Proc. Natl Acad. Sci. USA, 97, 11836–11842 (2000).

    CAS  Article  Google Scholar 

  70. Margoliash, D. & Konishi, M. Auditory representation of autogenous song in the song system of white-crowned sparrows. Proc. Natl Acad. Sci. USA 82, 5997–6000 (1985).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  71. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  72. 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 

  73. Gobes, S. M. H., Bolhuis, J. J., Terpstra, N. J., den Boer-Visser, A. M. & Zandbergen, M. A. Immediate early gene expression in the zebra finch song system in response to familiar and novel song. Soc. Neurosci. Abstr. 33, 646.13 (2007).

    Google Scholar 

  74. Imada, T. et al. Infant speech perception activates Broca's area: a developmental magnetoencephalography study. Neuroreport 17, 957–962 (2006).

    PubMed  Article  Google Scholar 

  75. 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  Article  Google Scholar 

  76. Möttönen, R. & Watkins K. E. Motor representations of articulators contribute to categorical perception of speech sounds. J. Neurosci. 29, 9819–9825 (2009).

    PubMed  Article  CAS  PubMed Central  Google Scholar 

  77. Bauer, E. E., Coleman, M. J., Roberts, T. F., Roy, A., Prather, J. F. & Mooney, R. A synaptic basis for auditory-vocal integration in the songbird. J. Neurosci. 28, 1509–1522 (2008).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  78. Coleman, M. J. & Mooney, R. Synaptic transformations underlying highly selective auditory representations of learned birdsong. J. Neurosci. 24, 7251–7265 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  79. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  80. 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 

  81. Williams, H. & Nottebohm, F. Auditory response in avian vocal motor neurons: a motor theory for song perception in birds. Science 229, 279–282 (1985).

    CAS  PubMed  Article  Google Scholar 

  82. Fadiga, L. Speech listening specifically modulates the excitability of tongue muscles: a TMS study. Eur. J. Neurosci. 15, 399–402 (2002).

    PubMed  Article  Google Scholar 

  83. 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).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  84. 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  Article  Google Scholar 

  85. 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 

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

    CAS  PubMed  Article  Google Scholar 

  87. Dave, A. S. & Margoliash, D. Song replay during sleep and computational rules for sensorimotor vocal learning. Science 290, 812–816 (2000). This study demonstrates 'replay' of singing-induced neuronal activity during sleep in zebra finches.

    CAS  PubMed  Article  Google Scholar 

  88. 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  PubMed Central  Google Scholar 

  89. Katz, L. C. & Gurney, M. E. Auditory responses in the zebra finch's motor system for song. Brain Res. 221, 192–197 (1981).

    CAS  PubMed  Article  Google Scholar 

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

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  91. Doupe, A. J. & Konishi, M. Song-selective auditory circuits in the vocal control system of the zebra finch. Proc. Natl Acad. Sci. USA 88, 11339–11343 (1991).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  92. Leonardo, A. Experimental test of the birdsong error-correction model. Proc. Natl Acad. Sci. USA 101, 16935–16940 (2004). The author used a combination of behavioural and electrophysiological techniques to show that the AFP does not provide the feedback error itself. After this study, efforts were directed towards detecting instructive signals in the AFP.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  93. Gale, S. D. & Perkel, D. J. A basal ganglia pathway drives selective auditory responses in songbird dopaminergic neurons via disinhibition. J. Neurosci. 30, 1027–1037 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  94. Keller, G. B. & Hahnloser, R. H. R. Neural processing of auditory feedback during vocal practice in a songbird. Nature 457, 187–190 (2009). This study showed that there are neurons in auditory regions of the songbird brain that are sensitive to changes in auditory feedback during song learning.

    CAS  PubMed  Article  Google Scholar 

  95. 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 

  96. Sober, S. J. & Brainard, M. S. Adult birdsong is actively maintained by error correction. Nature Neurosci. 12, 927–931 (2009).

    CAS  PubMed  Article  Google Scholar 

  97. Doya, K. & Sejnowski, T. J. A novel reinforcement model of birdsong vocalization learning. Adv. Neural Inf. Process. Syst. 7, 101–108 (1995).

    Google Scholar 

  98. Tumer, E. C. & Brainard, M. S. Performance variability enables adaptive plasticity of 'crystallized' adult birdsong. Nature 450, 1240–1244 (2007).

    CAS  PubMed  Article  Google Scholar 

  99. Andalman, A. S. & Fee, M. S. A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors. Proc. Natl Acad. Sci. USA 106, 12518–12523 (2009). Using pharmacological manipulation, this study demonstrated that the song system nucleus LMAN provides instructive signals that can be used to correct song if it does not match the template.

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  100. Christoffels, I. K., Formisano, E. & Schiller, N. O. Neural correlates of verbal feedback processing: an fMRI study employing overt speech. Hum. Brain Mapp. 28, 868–879 (2007).

    PubMed  Article  PubMed Central  Google Scholar 

  101. Magno, E., Foxe, J. J., Molholm, S., Robertson, I. H. & Garavan, H. The anterior cingulate and error avoidance. J. Neurosci. 26, 4769–4773 (2006).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  102. Chater, N., Reali, F. & Christiansen M. H. Restrictions on biological adaptation in language evolution. Proc. Natl Acad. Sci. USA 106, 1015–1020 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  103. Vernes, S. C. & Fisher, S. E. Unravelling neurogenetic networks implicated in developmental language disorders. Biochem. Soc. Trans. 37, 1263–1269 (2009).

    CAS  PubMed  Article  Google Scholar 

  104. Vernes, S. C. et al. A functional genetic link between distinct developmental language disorders. N. Engl. J. Med. 359, 2337–2345 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  105. Vargha-Khadem, F., Gadian, D. G., Copp, A. & Mishkin, M. FOXP2 and the neuroanatomy of speech and language. Nature Rev. Neurosci. 6, 131–138 (2005).

    CAS  Article  Google Scholar 

  106. White, S. A., Fisher, S. E., Geschwind, D. H., Scharff, C. & Holy, T. E. Singing mice, songbirds, and more: models for FOXP2 function and dysfunction in human speech and language. J. Neurosci. 26, 10376–10379 (2006).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  107. Hannenhalli, S. & Kaestner, K. H. The evolution of Fox genes and their role in development and disease. Nature Rev. Genet. 10, 233–240 (2009).

    CAS  PubMed  Article  Google Scholar 

  108. Rochefort, C., He, X., Scotto-Lomassese, S. & Scharff, C. Recruitment of FoxP2-expressing neurons to area X varies during song development. Dev. Neurobiol. 67, 809–817 (2007).

    CAS  PubMed  Article  Google Scholar 

  109. Kotz, S. A. & Schwartze, M. Cortical speech processing unplugged: a timely subcortico-cortical framework. Trends Cogn. Sci. 14, 392–399 (2010).

    PubMed  Article  Google Scholar 

  110. Person, A. L., Gale, S. D., Farries, M. A. & Perkel, D. J. Organization of the songbird basal ganglia, including area X. J. Comp. Neurol. 508, 840–866 (2008).

    PubMed  Article  Google Scholar 

  111. Teramitsu, I. & White, S. A. FoxP2 regulation during undirected singing in adult songbirds. J. Neurosci. 26, 7390–7394 (2006). The first report that FoxP2 expression is modulated in adult zebra finches by singing, demonstrating a regulatory role of FoxP2 in adult brain circuitry.

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  112. Teramitsu, I., Poopatanapong, A., Torrisi, S. & White, S. A. Striatal FoxP2 is actively regulated during songbird sensorimotor learning. PLoS ONE 5, e8548 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  113. Haesler, S. et al. FoxP2 expression in avian vocal learners and non-learners. J. Neurosci. 24, 3164–3175 (2004).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  114. Iyengar, S., Viswanathan, S. S. & Bottjer, S. Development of topography within song control circuitry of zebra finches during the sensitive period of song learning. J. Neurosci. 19, 6037–6057 (1999).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  115. Horng, S. et al. Differential gene expression in the developing lateral geniculate nucleus and medial geniculate nucleus reveals novel roles for Zic4 and Foxp2 in visual and auditory pathway development. J. Neurosci. 29 13672–13683 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  116. Marquardt, T. P., Jacks, A. & Davis, B. L. Token-to-token variability in developmental apraxia of speech: three longitudinal case studies. Clin. Linguist. Phon. 18, 127–144 (2004).

    PubMed  Article  Google Scholar 

  117. Gaub, S., Groszer, M. Fisher, S. E. & Ehret, G. The structure of innate vocalizations in Foxp2 deficient mouse pups. Genes Brain Behav. 9, 390–401 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  118. Farries, M. A. Ding, L. & Perkel, D. J. Evidence for ''direct'' and ''indirect'' pathways through the song system basal ganglia. J. Comp. Neurol. 484, 93–104 (2005).

    PubMed  Article  Google Scholar 

  119. Prather, J.F, Peters, S., Nowicki, S. & Mooney, R. Precise auditory-vocal mirroring in neurons for learned vocal comunication. Nature 451, 305–310 (2008). The first demonstration of auditory–vocal mirror neurons in birds with detailed neuroanatomical and electrophysiological analyses.

    CAS  PubMed  Article  Google Scholar 

  120. Schulz, S. B., Haesler, S., Scharff, C. & Rochefort, C. Knockdown of FoxP2 alters spine density in Area X of the zebra finch. Genes Brain Behav. 6 Jul 2010 (doi:10.1111/j.1601-183X.2010.00607.x).

    CAS  Article  Google Scholar 

  121. Groszer, M. et al. Impaired synaptic plasticity and motor learning in mice with a point mutation implicated in human speech deficits. Curr. Biol. 18, 354–362 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  122. Winograd, C., Clayton, D. & Ceman, S. Expression of fragile X mental retardation protein within the vocal control system of developing and adult male zebra finches. Neuroscience 157, 132–142 (2008).

    CAS  PubMed  Article  Google Scholar 

  123. White, S. A. Genes and vocal learning. Brain Lang. 12 Nov 2009 (doi: 10.1016/j.bandl.2009.10.002).

    PubMed  Article  Google Scholar 

  124. Wada, K. et al. A molecular neuroethological approach for identifying and characterizing a cascade of behaviorally regulated genes. Proc. Natl Acad. Sci. USA, 103, 15212–15217 (2006).

    CAS  Article  Google Scholar 

  125. Kalscheuer, V. M. et al. A balanced chromosomal translocation disrupting ARHGEF9 is associated with epilepsy, anxiety, aggression, and mental retardation. Hum. Mutat. 30, 61–68 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  126. Lovell P. V., Clayton D. F., Replogle K. L. & Mello C. V. Birdsong “transcriptomics”: neurochemical specializations of the oscine song system. PLoS ONE 3, e3440 (2008).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  127. Warren, W. C. et al. The genome of a songbird. Nature 464, 757–762 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  128. Kang C. et al. Mutations in the lysosomal enzyme-targeting pathway and persistent stuttering. N. Engl. J. Med. 362, 677–685 (2010).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  129. Beckers, G. J. L. & Gahr, M. Neural processing of short-term recurrence in songbird vocal communication. PLoS ONE 5, e11129 (2010).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  130. Agate R. J., Scott B. B., Haripal B., Lois C. & Nottebohm F. Transgenic songbirds offer an opportunity to develop a genetic model for vocal learning. Proc. Natl Acad. Sci. USA 106, 17963–17967 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  131. Gentner, T., Fenn., K., Margoliash, D. & Nusbaum, H. Recursive syntactic pattern learning by songbirds. Nature 440, 1204–1207 (2005). An intriguing study into the ability of starlings to recognize recursive patterns in conspecific vocalizations. See also references 132 and 133.

    Article  CAS  Google Scholar 

  132. Corballis, M. C. Recursion, language, and starlings. Cogn. Sci. 31, 697–704 (2007).

    PubMed  Article  Google Scholar 

  133. van Heijningen, C. A. A., de Visser, J., Zuidema, W. & ten Cate, C. Simple rules can explain discrimination of putative recursive syntactic structures by a songbird species. Proc. Natl Acad. Sci. USA 106, 20538–20543 (2009).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  134. Tomasello, M. Constructing A Language: A Usage-Based Theory of Language Acquisition. (Harvard Univ. Press, Cambridge, Massachusetts, 2003).

    Google Scholar 

  135. Kao M. H. & Brainard, M.S. Lesions of an avian basal ganglia circuit prevent context-dependent changes to song variability. J. Neurophysiol. 96, 1441–1455 (2006).

    PubMed  Article  Google Scholar 

  136. Kao M. H., Wright B. D. & Doupe A. J. Neurons in a forebrain nucleus required for vocal plasticity rapidly switch between precise firing and variable bursting depending on social context. J. Neurosci. 28, 13232–13247 (2008).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  137. Hahnloser, R. H. R., Kozhevnikov, A. & Fee, M. S. An ultra-sparse code underlies the generation of neural sequences in a songbird. Nature 419, 65–70 (2002).

    CAS  Article  PubMed  Google Scholar 

  138. Gibb, L., Gentner, T. Q. & Abarbanel, H. D. I. Inhibition and recurrent excitation in a computational model of sparse bursting in song nucleus HVC. J. Neurophysiol. 102, 1748–1762 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  139. Lewicki, M. S. & Arthur, B. J. Hierarchical organization of auditory temporal context sensitivity. J. Neurosci. 16, 6987–6998 (1996).

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  140. Nishikawa, J., Okada, M. & Okanoya, K. Population coding of song element sequence in the Bengalese finch HVC. Eur. J. Neurosci. 27, 3273–3283 (2008).

    PubMed  Article  Google Scholar 

  141. Stahl, P. D. & Wainszelbaum, M. J. Human-specific genes may offer a unique window into human cell signaling Sci. Signal. 2, pe59 (2009).

    PubMed  PubMed Central  Article  Google Scholar 

  142. Enard W. et al. Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418, 869–872 (2002).

    CAS  Article  PubMed  Google Scholar 

  143. Konopka, G. et al. Human-specific transcriptional regulation of CNS development genes by FOXP2. Nature 462, 213–217 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  144. Spiteri E. et al. Identification of the transcriptional targets of FOXP2, a gene linked to speech and language, in developing human brain. Am. J. Hum. Genet. 81, 1144–1157 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  145. Vernes, S. C. et al. High-throughput analysis of promoter occupancy reveals direct neural targets of FOXP2, a gene mutated in speech and language disorders. Am. J. Hum. Genet. 81, 1232–1250 (2007).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgements

We are grateful to R. C. Berwick and to three anonymous referees for their constructive comments on an earlier version of the manuscript.

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Correspondence to Johan J. Bolhuis, Kazuo Okanoya or Constance Scharff.

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Supplementary information

Supplementary information S1 (box)

Birdsong learning: variations on a theme (PDF 216 kb)

Supplementary information S2 (box)

A specialised neural circuit involved in avian 'babbling' (PDF 206 kb)

Supplementary information S3 (box)

Syntax and semantics in bird vocalisations (PDF 218 kb)

Supplementary information S4 (box)

Neural mechanisms of human syntax (PDF 213 kb)

Supplementary information S5 (box)

Syntactic organisation and recursion in birds and humans (PDF 218 kb)

Supplementary information S6 (box)

Mirror neurons in song and speech (PDF 218 kb)

Supplementary information S7 (box)

The role of sleep in song and speech (PDF 218 kb)

Related links

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FURTHER INFORMATION

Johan J. Bolhuis' homepage

Kazuo Okanoya's homepage

Constance Scharff's homepage

NCBI Zebra Finch Genome Resources website

Glossary

FOXP2

A transcription factor of the large forkhead box (Fox) family, originally discovered in Drosophila. FOX genes have important roles in the development of many tissues and diseases.

Seasonal breeder

An animal (for example, a songbird species) that breeds only during a specific period of the year.

Opportunistic breeder

An animal (for example, a songbird species) that can breed year-round.

Action-based learning

Also known as selective learning. A song learning style that selects the final sound repertoire after an initial overproduction of song elements, based on auditory or visual feedback from conspecifics.

Instruction-based learning

Also known as sensorimotor learning. A song learning style principally exemplified by the zebra finch, in which vocal 'babbling' is gradually modified through auditory guided sensorimotor learning. Both 'instruction-based' and 'action-based' learning can occur in the same species to various degrees.

Syntax

In a narrow sense, syntax refers to a set of rules that governs the arrangements of words to produce a sentence. In a broader sense, syntax refers to a set of rules to hierarchically and sequentially arrange elements to produce a string.

Song system

A network of forebrain nuclei that is involved in the perception, acquisition and production of song.

Working memory

A form of memory in which information is stored for a limited period during which it can be used; in humans the classic example is remembering a telephone number that is then dialled and immediately forgotten.

Homologous

Homologous traits (or brain regions) are thought to have evolved from a common ancestor.

Analogous

Analogous traits (or brain regions) have a similar function, but are thought to have evolved independently in distantly related species.

Template

A term used to denote the central representation of birdsong. It is thought that songbirds are born with a crude template that has species-specific characteristics. Auditory experience, first with the song of an adult conspecific male and later with the individual's own vocal output, then moulds the template into a more precise representation of the tutor song.

Semantics

In a narrow sense, semantics refers to the study of meaning in language. In a broader sense, semantics refers to information content of a signal.

Amniotes

The collective name for mammals, reptiles and birds that are characterized by four limbs, a spinal column and embryos that develop within a fluid-filled cavity that is enclosed by membranes ('amnion').

Transgenesis

The introduction of an exogenous gene — a transgene — into an organism which results in expression of the new gene and its transmission into the next generation.

Non-vocal learner

A bird species that does not learn its vocalizations.

Recursion

A term used by linguists to refer to the embedding of a structure into the same type of structure — for example, embedding a sentence into another sentence.

Phonological

In a narrow sense, referring to the set of physical and psychological features of a unit of speech. In a broader sense, referring to the acoustic characteristics of a unit of sound.

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Bolhuis, J., Okanoya, K. & Scharff, C. Twitter evolution: converging mechanisms in birdsong and human speech. Nat Rev Neurosci 11, 747–759 (2010). https://doi.org/10.1038/nrn2931

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