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.

Neural mechanisms of birdsong memory

Key Points

  • Song learning in songbirds has strong similarities with speech acquisition in human infants. Songbirds need to learn their songs from an adult conspecific. This occurs in two phases: a memorization phase, early in life, during which the young bird forms a neural representation (a 'template') of the song of a tutor; and a sensorimotor phase, during which the bird's own vocal output is matched to the stored template.

  • A network of interconnected brain nuclei, known as the 'song system', is involved in the perception, learning and production of song. Within the song system, the caudal pathway is important for song production. The rostral pathway is involved in song perception and in vocal sensorimotor learning. Initial claims that there are correlations between functional (for example, seasonal or sex) song differences and differences in song system morphology have not been supported by recent findings.

  • Two regions outside the song system show neuronal activation (measured as increased expression of immediate early genes) when zebra finches are exposed to song. In one of these regions, the caudomedial nidopallium (NCM), neuronal activation on exposure to the tutor song is significantly correlated with the strength of song learning. An electrophysiological study showed that a familiarity index, based on neuronal habituation rates in the NCM, was significantly greater in tutored males than in untutored males, and significantly positively correlated with the strength of song learning.

  • Zebra finch females do not sing, but nevertheless can learn the characteristics of their father's song and form a preference for it over novel songs. When female zebra finches that were reared with their fathers were re-exposed to their fathers' song, they showed significantly greater neuronal activation in the caudomedial mesopallium (CMM), but not in the NCM or hippocampus, compared with when they were exposed to novel song.

  • Neuronal activation in the NCM and CMM is not an artefact of isolation rearing, and is not related to attentional mechanisms.

  • The NCM and the CMM might be parallel stores that contain the neural substrate for tutor (or father's) song memory, or the 'template'. The NCM might be more directly functionally linked to the premotor nuclei in the song system. The CMM overlaps with the intermediate and medial mesopallium (IMM) that contains the neural substrate for imprinting memory in domestic chicks. The NCM and CMM may be homologous with subdivisions of the mammalian auditory association cortex, which in humans are associated with auditory learning in relation to speech acquisition.

  • Further multidisciplinary research is needed to determine whether the NCM and CMM contain the neural substrates of song memory, or whether this information is stored elsewhere in the brain. The neuroanatomical connectivity and functional relationship between these two brain regions and the song system needs to be investigated, in order for us to better understand the overall process of bird song learning. Such analyses may, ultimately, have heuristic value for the study of speech aquisition in humans.

Abstract

The process through which young male songbirds learn the characteristics of the songs of an adult male of their own species has strong similarities with speech acquisition in human infants. Both involve two phases: a period of auditory memorization followed by a period during which the individual develops its own vocalizations. The avian 'song system', a network of brain nuclei, is the probable neural substrate for the second phase of sensorimotor learning. By contrast, the neural representation of song memory acquired in the first phase is localized outside the song system, in different regions of the avian equivalent of the human auditory association cortex.

This is a preview of subscription content

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1: Birdsong develops through different stages.
Figure 2: The brains of songbirds and non-songbirds differ.
Figure 3: The songbird brain.
Figure 4: Brain activation in response to song.
Figure 5: Seasonal changes in physiology and vocal repertoire of wild canaries on Madeira.

References

  1. Avian Brain Nomenclature Consortium. Avian brains and a new understanding of vertebrate brain evolution. Nature Rev. Neurosci. 6, 151–159 (2005). An important review on the implications of the new nomenclature of the avian brain for our understanding of the evolution of brain and behaviour, and our view of the 'birdbrain'.

  2. Clayton, N. S. & Dickinson, A. Episodic-like memory during cache recovery by scrub jays. Nature 395, 272–274 (1998).

    Article  CAS  PubMed  Google Scholar 

  3. Emery, N. J. & Clayton, N. S. Effects of experience and social context on prospective caching strategies by scrub jays. Nature 414, 443–446 (2001).

    Article  CAS  PubMed  Google Scholar 

  4. Vignal, C., Mathevon, N. & Mottin, S. Audience drives male songbird response to partner's voice. Nature 430, 448–451 (2004).

    Article  CAS  PubMed  Google Scholar 

  5. Emery, N. J. & Clayton, N. S. The mentality of crows: convergent evolution of intelligence in corvids and apes. Science 306, 1903–1907 (2004).

    Article  CAS  PubMed  Google Scholar 

  6. Horn, G. Pathways of the past: the imprint of memory. Nature Rev. Neurosci. 5, 108–120 (2004). A detailed review of research into the neural mechanisms of memory in filial impinting in chicks, demonstrating localization of the memory trace in a restricted brain region, the IMM, which overlaps with the CMM, as discussed in our review.

    Article  CAS  Google Scholar 

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

    Book  Google Scholar 

  8. Doupe, A. J. & Kuhl, P. K. Birdsong and human speech: common themes and mechanisms. Annu. Rev. Neurosci. 22, 567–631 (1999). A detailed review of the many parallels between birdsong learning and the acquisition of speech in humans.

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  10. 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).

    Article  CAS  PubMed  Google Scholar 

  11. Funabiki, Y. & Konishi, M. Long memory in song learning by zebra finches. J. Neurosci. 23, 6928–6935 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Nottebohm, F. in The Design of Animal Communication (eds Hauser, M. D. & Konishi, M.) 63–110 (MIT Press, Cambridge, Massachusetts, 2000). An excellent review by one of the leaders in the field that highlights our lack of knowledge of the neural substrate of tutor song memory.

    Google Scholar 

  13. Bolhuis, J. J. & Macphail, E. M. A critique of the neuroecology of learning and memory. Trends Cogn. Sci. 5, 426–433 (2001).

    Article  PubMed  Google Scholar 

  14. Macphail, E. M. & Bolhuis, J. J. The evolution of intelligence: adaptive specialisations versus general process. Biol. Rev. 76, 341–364 (2001).

    Article  CAS  PubMed  Google Scholar 

  15. Bolhuis, J. J. Function and mechanism in neuroecology: looking for clues. Anim. Biol. 55, 457–490 (2005).

    Article  Google Scholar 

  16. Sherry, D. F. Neuroecology. Annu. Rev. Psychol. 57, 167–197 (2006).

    Article  PubMed  Google Scholar 

  17. Gahr, M. Hormones make songs sexually attractive: hormone-dependent neural changes in the vocal control system of songbirds. Zoology 100, 260–272 (1997).

    Google Scholar 

  18. Nottebohm, F. & Arnold, A. P. Sexual dimorphism in vocal control areas of the songbird brain. Science 194, 212–213 (1976).

    Article  Google Scholar 

  19. MacDougall-Shackleton, S. A. & Ball, G. F. Comparative studies of sex differences in the song-control system of songbirds. Trends Neurosci. 22, 432–436 (1999).

    Article  CAS  PubMed  Google Scholar 

  20. Nottebohm, F. A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214, 1368–1370 (1981). The first demonstration that seasonal changes occur in the volume of nuclei in the song system of songbirds.

    Article  CAS  PubMed  Google Scholar 

  21. Tramontin, A. D. & Brenowitz, E. Seasonal plasticity in the adult brain. Trends Neurosci. 23, 251–258 (2000).

    Article  CAS  PubMed  Google Scholar 

  22. Nottebohm, F., Kasparian, S. & Pandazis, C. Brain space for a learned task. Brain Res. 213, 99–109 (1981).

    Article  CAS  PubMed  Google Scholar 

  23. DeVoogd, T. J., Krebs, J. R. Healy, S. D. & Purvis, A. Relations between song repertoire size and the volume of brain nuclei related to song: comparative evolutionary analyses amongst oscine birds. Proc. R. Soc. Lond. B 254, 75–82 (1993).

    Article  CAS  Google Scholar 

  24. Ward, B. C., Nordeen, E. J. & Nordeen, K. W. Individual variation in neuron number predicts differences in the propensity for avian vocal imitation. Proc. Natl Acad. Sci. USA 95, 1277–1282 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Airey, D. C., Buchanan, K. L., Szekely, T., Catchpole, C. K. & DeVoogd, T. J. Song, sexual selection, and song control nucleus (HVc) in the brains of European sedge warblers. J. Neurobiol. 44, 1–6 (2000).

    Article  CAS  PubMed  Google Scholar 

  26. Kirn, J. R., Clower, R. P., Kroodsma, D. E. & DeVoogd, T. J. Song-related brain regions in the red winged blackbird are affected by sex and season but not repertoire size. J. Neurobiol. 20, 139–163 (1989).

    Article  CAS  PubMed  Google Scholar 

  27. Bernard, D. J., Eens, M. & Ball, G. F. Age and behavior-related variation in the volume of song control nuclei in male European starlings. J. Neurobiol. 30, 329–339 (1996).

    Article  CAS  PubMed  Google Scholar 

  28. MacDougall-Shackleton, S. A., Hulse, S. H. & Ball, G. F. Neural correlates of singing behavior in male zebra finches (Taeniopygia guttata). J. Neurobiol. 36, 421–430 (1998).

    Article  CAS  PubMed  Google Scholar 

  29. Gahr, M., Sonnenschein, E. & Wickler, W. Sex difference in the size of the neural song control regions in a dueting songbird with similar song repertoire size of males and females. J. Neurosci. 18, 1124–1131 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Leitner, S., Voigt, C., Garcia-Segura, L.-M., Van't Hof, T. & Gahr, M. Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Horm. Behav. 40, 160–168 (2001).

    Article  CAS  PubMed  Google Scholar 

  31. Leitner, S. & Catchpole, C. K. Syllable repertoire and the size of the song control system in captive canaries (Serinus canaria). J. Neurobiol. 60, 21–27 (2004).

    Article  PubMed  Google Scholar 

  32. Gahr, M. Delineation of a brain nucleus: comparisons of cytochemical, hodological, and cytoarchitectural views of the song control nucleus HVc of the adult canary. J. Comp. Neurol. 294, 30–36 (1990).

    Article  CAS  PubMed  Google Scholar 

  33. Gahr, M. How should brain nuclei be delineated? Consequences for developmental mechanisms and for correlations of area size, neuron numbers and functions of brain nuclei. Trends Neurosci. 20, 58–62 (1997).

    Article  CAS  PubMed  Google Scholar 

  34. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Volman, S. F. Development of neural selectivity for birdsong during vocal learning. J. Neurosci. 13, 4737–4747 (1993). An important electrophysiological study showing that in the memorization phase in juvenile white-crowned sparrows, neurons in the song system nucleus HVC do not preferentially respond to the tutor song, whereas they develop preferential responsiveness to the BOS once the bird starts singing itself.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. 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).

    Article  PubMed  Google Scholar 

  39. Aamodt, S. M., Nordeen, E. J. & Nordeen, K. W. Early isolation from conspecific song does not affect the normal developmental decline of NMDA receptor binding in an avian song nucleus. J. Neurobiol. 27, 76–84 (1995).

    Article  CAS  PubMed  Google Scholar 

  40. Heinrich, J. E., Singh, T. D., Nordeen, K. W. & Nordeen, E. J. NR2B downregulation in a forebrain region required for avian vocal learning is not sufficient to close the sensitive period for song learning. Neurobiol. Learn. Mem. 79, 99–108 (2003).

    Article  CAS  PubMed  Google Scholar 

  41. 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).

    Article  CAS  PubMed  Google Scholar 

  42. Nordeen, K. W. & Nordeen, E. J. Synaptic and molecular mechanisms regulating plasticity during early learning. Ann. NY Acad. Sci. 1016, 416–437 (2004).

    Article  CAS  PubMed  Google Scholar 

  43. Aamodt, S. M., Nordeen, E. J. & Nordeen, K. W. Blockade of NMDA receptors during song model exposure impairs song development in juvenile zebra finches. Neurobiol. Learn. Mem. 65, 91–98 (1996).

    Article  CAS  PubMed  Google Scholar 

  44. Basham, M. E. Nordeen, E. J. & Nordeen, K. W. Blockade of NMDA receptors in the anterior forebrain impairs sensory acquisition in the zebra finch (Poephila guttata). Neurobiol. Learn. Mem. 66, 295–304 (1996).

    Article  CAS  PubMed  Google Scholar 

  45. Morris, R. G. M., Anderson, E., Lynch, G. S. & Baudry, M. Selective impairment of learning and blockade of long-term potentiation by an N-methyl-D-aspartate receptor antagonist, AP5. Nature 319, 774–776 (1986).

    Article  CAS  PubMed  Google Scholar 

  46. Jeffery, K. J. LTP and spatial learning — where to next? Hippocampus 7, 95–110 (1997).

    Article  CAS  PubMed  Google Scholar 

  47. Bolhuis, J. J. & Reid, I. C. Effects of intraventricular infusion of the N-methyl-D-aspartate (NMDA) receptor antagonist AP5 on spatial memory of rats in a radial arm maze. Behav. Brain Res. 47, 151–157 (1992).

    Article  CAS  PubMed  Google Scholar 

  48. Bannerman, D. M., Good, M. A., Butcher, S. P., Ramsay, M. & Morris, R. G. M. Distinct components of spatial learning revealed by prior training and NMDA receptor blockade. Nature 378, 182–186 (1995).

    Article  CAS  PubMed  Google Scholar 

  49. Saucier, D. & Cain, D. P. Spatial learning without NMDA receptor-dependent long-term potentiation. Nature 378, 186–189 (1995).

    Article  CAS  PubMed  Google Scholar 

  50. Otnæss, M. K., Brun, V. H., Moser, M.-B. & Moser, E. I. Pretraining prevents spatial learning impairment after saturation of hippocampal long-term potentiation. J. Neurosci. 19, RC49, 1–5 (1999).

    Article  Google Scholar 

  51. Marler, P. & Doupe, A. Singing in the brain. Proc. Natl Acad. Sci. USA 97, 2965–2967 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Nottebohm, F., Stokes, T. & Leonard, C. M. Central control of song in the canary. J. Comp. Neurol. 165, 457–486 (1976). The first detailed study showing the involvement of nuclei in the 'song system' in birdsong.

    Article  CAS  PubMed  Google Scholar 

  53. DeVoogd, T. J. in Causal Mechanisms of Behavioural Development (eds Hogan, J. A. & Bolhuis, J. J.) 49–81 (Cambridge Univ. Press, Cambridge, 1994).

    Book  Google Scholar 

  54. Brenowitz, E. A. & Beecher, M. D. Song learning in birds: diversity and plasticity, opportunities and challenges. Trends Neurosci. 28, 127–132 (2005).

    Article  CAS  PubMed  Google Scholar 

  55. Nordeen, K. W., Marler, P. & Nordeen, E. J. Addition of song-related neurons in swamp sparrows coincides with memorization, not production, of learned songs. J. Neurobiol. 20, 651–661 (1989).

    Article  CAS  PubMed  Google Scholar 

  56. Jarvis, E. D. & Nottebohm, F. Motor-driven gene expression. Proc. Natl Acad. Sci. USA 94, 4097–4102 (1997). Shows a clear dissociation between song production (which involved increased neuronal activation in nuclei in the 'song system') and song perception (which involved increased neuronal activation in the NCM and CMM, but not the song system).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. 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). The first study to apply the IEG technique to birdsong, showing that exposure of male zebra finches or canaries to conspecific song led to increased IEG expression in brain regions outside the conventional 'song system'.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. 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).

    Article  CAS  PubMed  Google Scholar 

  60. Brainard, M. S. & Doupe, A. J. Auditory feedback in learning and maintenance of vocal behaviour. Nature Rev. Neurosci. 1, 31–40 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  62. Konishi, M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22, 770–783 (1965). This classic study separated experimentally the memorization and sensorimotor phases of birdsong acquisition and introduced the 'template' concept.

    CAS  PubMed  Google Scholar 

  63. Bottjer, S. W. & Arnold, A. P. Developmental plasticity in neural circuits for a learned behavior. Annu. Rev. Neurosci. 20, 459–481 (1997).

    Article  CAS  PubMed  Google Scholar 

  64. Sagar, S. M., Sharp, F. R. & Curran, T. Expression of c-fos protein in brain: metabolic mapping at the cellular level. Science 240, 1328–1331 (1988).

    Article  CAS  PubMed  Google Scholar 

  65. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Bolhuis, J. J. in Causal Mechanisms of Behavioural Development (eds Hogan, J. A. & Bolhuis, J. J.) 16–46 (Cambridge Univ. Press, Cambridge, 1994).

    Book  Google Scholar 

  67. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Mello, C. V., Nottebohm, F. & Clayton, D. F. Repeated exposure to one song leads to a rapid and persistent decline in an immediate early gene's response to that song in zebra finch telencephalon. J. Neurosci. 15, 6919–6925 (1995).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. 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). Electrophysiological demonstration of differential neuronal habituation to familiar and novel songs, correlated with the strength of song learning, that is consistent with earlier findings using expression of IEGs.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Eda-Fujiwara, H., Satoh, R., Bolhuis, J. J. & Kimura, T. Neuronal activation in female budgerigars is localized and related to male song complexity. Eur. J. Neurosci. 17, 149–154 (2003).

    Article  PubMed  Google Scholar 

  72. Sockman, K. W., Gentner, T. Q. & Ball, G. F. Recent experience modulates forebrain gene-expression in response to mate-choice cues in European starlings. Proc. R. Soc. Lond. B 269, 2479–2485 (2002).

    Article  Google Scholar 

  73. Bolhuis, J. J. & Eda-Fujiwara, H. Bird brains and songs: neural mechanisms of birdsong perception and memory. Anim. Biol. 53, 129–145 (2003).

    Article  Google Scholar 

  74. Miller, D. B. Long-term recognition of father's song by female zebra finches. Nature 280, 389–391 (1979).

    Article  Google Scholar 

  75. Riebel, K. Early exposure leads to repeatable preferences for male song in female zebra finches. Proc. R. Soc. Lond. B 267, 2553–2558 (2000).

    Article  CAS  Google Scholar 

  76. Riebel, K., Smallegange, I. M., Terpstra, N. J. & Bolhuis, J. J. Sexual equality in zebra finch song preference: evidence for a dissociation between song recognition and production learning. Proc. R. Soc. Lond. B 269, 729–733 (2002).

    Article  Google Scholar 

  77. Riebel, K. Developmental influences on auditory perception in female zebra finches — is there a sensitive phase for song preference learning? Anim. Biol. 53, 73–87 (2003).

    Article  Google Scholar 

  78. Brenowitz, E. A. Altered perception of species-specific song by female birds after lesions of a forebrain nucleus. Science 251, 303–304 (1991).

    Article  CAS  PubMed  Google Scholar 

  79. Del Negro, C., Gahr, M., Leboucher, G. & Kreutzer, M. The selectivity of sexual responses to song displays: effects of partial chemical lesion of the HVC in female canaries. Behav. Brain Res. 96, 151–159 (1998).

    Article  CAS  PubMed  Google Scholar 

  80. Halle, F., Gahr, M., Pieneman, A. W. & Kreutzer, M. Recovery of song preferences after excitotoxic HVC lesion in female canaries. J. Neurobiol. 52, 1–13 (2002).

    Article  CAS  PubMed  Google Scholar 

  81. Del Negro, C., Kreutzer, M. & Gahr, M. Sexually stimulating signals of canary (Serinus canaria) songs: evidence for a female-specific auditory representation in the HVc nucleus during the breeding season. Behav. Neurosci. 114, 526–542 (2000).

    Article  CAS  PubMed  Google Scholar 

  82. Leitner, S. & Catchpole, C. K. Female canaries that respond and discriminate more between male songs of different quality have a larger song control nucleus (HVC) in the brain. J. Neurobiol. 52, 294–301 (2002).

    Article  PubMed  Google Scholar 

  83. Hamilton, K. S., King, A. P., Sengelaub, D. R. & West, M. J. A brain of her own: a neural correlate of song assessment in a female songbird. Neurobiol. Learn. Mem. 68, 325–332 (1997).

    Article  CAS  PubMed  Google Scholar 

  84. MacDougall-Shackleton, S. A., Hulse, S. H. & Ball, G. F. Neural bases of song preferences in female zebra finches (Taeniopygia guttata). Neuroreport 9, 3047–3052 (1998).

    Article  CAS  PubMed  Google Scholar 

  85. Duffy, D. L., Bentley, G. E. & Ball, G. F. Does sex or photoperiodic condition influence ZENK induction in response to song in European starlings? Brain Res. 844, 78–82 (1999).

    Article  CAS  PubMed  Google Scholar 

  86. Gentner, T. Q., Hulse, S. H., Duffy, D. & Ball, G. F. Response biases in auditory forebrain regions of female songbirds following exposure to sexually relevant variation in male song. J. Neurobiol. 46, 48–58 (2001).

    Article  CAS  PubMed  Google Scholar 

  87. Ribeiro, S., Cecchi, G. A., Magnasco, M. O. & Mello, C. V. Toward a song code: evidence for a syllabic representation in the canary brain. Neuron 21, 359–371 (1998).

    Article  CAS  PubMed  Google Scholar 

  88. Bailey, D. J., Rosebush, J. C. & Wade, J. The hippocampus and caudomedial neostriatum show selective responsiveness to conspecific song in the female zebra finch. J. Neurobiol. 52, 43–51 (2002).

    Article  PubMed  Google Scholar 

  89. Terpstra, N. J., Bolhuis, J. J., Riebel, K., van der Burg, J. M. M. & den Boer-Visser, A. M. Localised brain activation specific to auditory memory in a female songbird. J. Comp. Neurol. 494, 784–781 (2006).

    Article  PubMed  Google Scholar 

  90. Maney, D. L., MacDougall-Shackleton, E. A., MacDougall-Shackleton, S. A., Ball, G. F. & Hahn, T. P. Immediate early gene response to hearing song correlates with receptive behavior and depends on dialect in a female songbird. J. Comp. Physiol. A 189, 667–674 (2002).

    Article  Google Scholar 

  91. Leitner, S., Voigt, C., Metzdorf, R. & Catchpole, C. K. Immediate early gene (ZENK, Arc) expression in the auditory forebrain of female canaries varies in response to male song quality. J. Neurobiol. 64, 275–284 (2005).

    Article  CAS  PubMed  Google Scholar 

  92. Gentner, T. Q. & Margoliash, D. Neuronal populations and single cells representing learned auditory objects. Nature 424, 669–674 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Gentner, T. Q., Hulse, S. H. & Ball, G. F. Functional differences in forebrain auditory regions during learned vocal recognition in songbirds. J. Comp. Physiol. A 190, 1001–1010 (2004).

    Article  Google Scholar 

  94. Jarvis, E. D. et al. Behaviourally driven gene expression reveals song nuclei in hummingbird brain. Nature 406, 628–632 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Reiner, A. et al. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377–414 (2004). A detailed proposal for a new nomenclature of the avian brain that makes it clear that there are important homologies between the brains of birds and mammals that were obscured by the old terminology.

    Article  PubMed  PubMed Central  Google Scholar 

  96. Terpstra, N. J., Bolhuis, J. J., den Boer-Visser, A. M. & ten Cate, C. Neuronal activation related to auditory perception in the brain of a non-songbird, the ring dove. J. Comp. Neurol. 488, 342–351 (2005).

    Article  PubMed  Google Scholar 

  97. Horn, G. Memory, Imprinting, and the Brain (Clarendon, Oxford, 1985). A detailed review of pioneering research into the neural mechanisms of learning and memory in filial imprinting in chicks, put into a wider perspective of brain mechanisms of memory.

    Book  Google Scholar 

  98. Horn, G. Visual imprinting and the neural mechanisms of recognition memory. Trends Neurosci. 21, 300–305 (1998).

    Article  CAS  PubMed  Google Scholar 

  99. Patterson, T. A. & Rose, S. P. R. Memory in the chick: multiple cues, distinct brain locations. Behav. Neurosci. 106, 465–470 (1992).

    Article  CAS  PubMed  Google Scholar 

  100. Bolhuis, J. J., Johnson, M. H., Horn, G. & Bateson, P. Long-lasting effects of IMHV lesions on social preferences in domestic fowl. Behav. Neurosci. 103, 438–441 (1989).

    Article  Google Scholar 

  101. Wise, R. J. Language systems in normal and aphasic human subjects: functional imaging studies and inferences from animal studies. Br. Med. Bull. 65, 95–119 (2003).

    Article  PubMed  Google Scholar 

  102. Kaas, J. H. & Hackett, T. A. 'What' and 'where' processing in auditory cortex. Nature Neurosci. 2, 1045–1047 (1999).

    Article  CAS  PubMed  Google Scholar 

  103. Kaas, J. H. & Hackett, T. A. Subdivisions of auditory cortex and processing streams in primates. Proc. Natl Acad. Sci. USA 97, 11793–11799 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Romanski, L. M. et al. Dual streams of auditory afferents target multiple domains in the primate prefrontal cortex. Nature Neurosci. 2, 1131–1136 (1999).

    Article  CAS  PubMed  Google Scholar 

  105. Wan, H. et al. Fos imaging reveals differential neuronal activation of areas of rat temporal cortex by novel and familiar sounds. Eur. J. Neurosci. 14, 118–124 (2001).

    Article  CAS  PubMed  Google Scholar 

  106. Poremba, A. et al. Species-specific calls evoke asymmetric activity in the monkey's temporal poles. Nature 427, 448–451 (2004).

    Article  CAS  PubMed  Google Scholar 

  107. Colombo, M., D'Amato, M. R., Rodman, H. R. & Gross, C. R. Auditory association cortex lesions impair auditory short-term memory in monkeys. Science 247, 336–338 (1990).

    Article  CAS  PubMed  Google Scholar 

  108. Colombo, M., Rodman, H. R. & Gross, C. R. The effects of superior temporal cortex lesions on the processing and retention of auditory information in monkeys (Cebus apella). J. Neurosci. 16, 4501–4517 (1996).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Fritz, J., Mishkin, M. & Saunders, R. C. In search of an auditory engram. Proc. Natl Acad. Sci. USA 102, 9359–9364 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Kuhl, P. K. A new view of language acquisition. Proc. Natl Acad. Sci. USA 97, 11850–11857 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Price, C., Thierry, G. & Griffiths, T. Speech-specific auditory processing: where is it? Trends Cogn. Sci. 9, 271–276 (2005).

    Article  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  113. Dehaene-Lambertz, G., Dehaene, S. & Hertz-Pannier, L. Functional neuroimaging of speech perception in infants. Science 298, 2013–2015 (2002).

    Article  CAS  PubMed  Google Scholar 

  114. Scoville, W. B. & Milner, B. Loss of recent memory after bilateral hippocampal lesions. J. Neurol. Neurosurg. Psychiatry 20, 11–21 (1957).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Brown, M. W. in Brain, Perception, Memory: Advances in Cognitive Neuroscience (ed. Bolhuis, J. J.) 185–208 (Oxford Univ. Press, Oxford, 2000).

    Book  Google Scholar 

  116. Buckley, M. J. & Gaffan, D. in Brain, Perception, Memory: Advances in Cognitive Neuroscience (ed. Bolhuis, J. J.) 279–298 (Oxford Univ. Press, Oxford, 2000).

    Book  Google Scholar 

  117. Sherry, D. F. & Vaccarino, A. L. Hippocampus and memory for food caches in black-capped chickadees. Behav. Neurosci. 103, 308–318 (1989).

    Article  Google Scholar 

  118. Bolhuis, J. J., Stewart, C. A. & Forrest, E. M. Retrograde amnesia and memory reactivation in rats with ibotenate lesions to the hippocampus or subiculum. Q. J. Exp. Psychol. 47B, 129–150 (1994).

    Google Scholar 

  119. Murray, E. A. What have ablation studies told us about the neural substrates of stimulus memory? Semin. Neurosci. 8, 13–22 (1996).

    Article  Google Scholar 

  120. Corkin, S. et al. H. M.'s medial temporal lobe lesion: findings from magnetic resonance imaging. J. Neurosci. 17, 3964–3979 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Malkova, L. & Mishkin, M. One-trial memory for object-place associations after separate lesions of hippocampus and posterior parahippocampal region in the monkey. J. Neurosci. 23, 1956–1965 (2003).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  122. Knudsen, E. I., Zheng, W. & DeBello, W. M. Traces of learning in the auditory localization pathway. Proc. Natl Acad. Sci. USA 97, 11815–11820 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  123. Bailey, D. J. & Wade, J. Differential expression of the immediate early genes FOS and ZENK following auditory stimulation in the juvenile male and female zebra finch. Mol. Brain Res. 116, 147–154 (2003).

    Article  CAS  PubMed  Google Scholar 

  124. Bailey, D. J. & Wade, J. FOS and ZENK responses in 45-day-old zebra finches vary with auditory stimulus and brain region, but not sex. Behav. Brain Res. 162, 108–115 (2005).

    Article  CAS  PubMed  Google Scholar 

  125. Van Meir, V. et al. Spatiotemporal properties of the BOLD response in the songbirds' auditory circuit during a variety of listening tasks. Neuroimage 25, 1242–1255 (2005).

    Article  PubMed  Google Scholar 

  126. Boumans, T. et al. Functional magnetic resonance imaging of the zebra finch auditory forebrain during exposure to original and altered versions of the bird's own song. Soc. Neurosci. Abstr. 1002.16 (2005).

  127. Schregardus, D. S. et al. A lightweight telemetry system for recording neuronal activity in freely behaving small animals. J. Neurosci. Meth. (in the press, doi: 10.1016/j.jneumeth.2005.12.028).

  128. Frankland, P. W., Bontempi, B., Talton, L. E., Kaczmarek, L. & Silva, A. J. The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304, 881–883 (2004).

    Article  CAS  PubMed  Google Scholar 

  129. Lee, J. L. C., Everitt, B. J. & Thomas, K. L. Independent cellular processes for hippocampal memory consolidation and reconsolidation. Science 304, 839–843 (2004).

    Article  CAS  PubMed  Google Scholar 

  130. Gobes, S. M. H., Bolhuis, J. J., Roosemalen, K., Pots, J. M. & Zandbergen, M. A. Effects of neurotoxic lesions to the caudomedial nidopallium on song production and tutor song preference in male zebra finches. Soc. Neurosci. Abstr. 31,1002.15 (2005).

  131. Mooney, R. Synaptic mechanisms for auditory–vocal integration and the correction of vocal errors. Ann. NY Acad. Sci. 1016, 476–494 (2004).

    Article  PubMed  Google Scholar 

  132. Catchpole, C. K. & Slater, P. J. B. Bird Song: Biological Themes and Variations (Cambridge Univ. Press, Cambridge, 1995).

    Google Scholar 

  133. Marler, P. in Simpler Networks and Behavior (ed. Fentress, J.) 314–329 (Sinauer, Sunderland, Massachusetts, 1976).

    Google Scholar 

  134. 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 

  135. Clayton, D. F. in Brain, Perception, Memory: Advances in Cognitive Neuroscience (ed. Bolhuis, J. J.) 113–125 (Oxford Univ. Press, Oxford, 2000).

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  137. 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).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  140. Brenowitz, E. A., Nalls, B., Wingfield, J. & Kroodsma, D. Seasonal changes in avian song nuclei without seasonal changes in song repertoire. J. Neurosci. 11, 1367–1374 (1991). A clear demonstration that seasonal changes in the volume of song system nuclei are not related to song learning.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Gahr, M., Leitner, S., Fusani, L. & Rybak, F. in Progress in Brain Research Vol. 138 (eds Hofman, M. A. et al.) 233–254 (Elsevier Science, Amsterdam, 2002).

    Google Scholar 

  142. Gahr, M. Neural song control system of hummingbirds: comparison to swifts, vocal learning (songbirds) and nonlearning (suboscines) passerines, and vocal learning (budgerigars) and nonlearning (dove, owl, gull, quail, chicken) nonpasserines. J. Comp. Neurol. 426, 182–192 (2000).

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

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

Author information

Authors and Affiliations

Authors

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Related links

Related links

FURTHER INFORMATION

Bolhuis's homepage

Max Planck Institute for Ornithology

Avianbrain.org

Glossary

Song system

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

Neuroecology

The study of the neural mechanisms of behaviour and cognition, using functional or evolutionary considerations. In a neuroecological analysis of memory, functional differences are related to neuromorphological differences.

Subsong

The first songs produced by young songbirds. These songs are relatively simple and may not resemble the song of the tutor. Subsong may still change and will eventually become crystallized song, which in many songbird species is the definitive song for that particular individual.

Immediate early genes

(IEGs). Genes that can respond rapidly (within minutes) to stimulation of a cell such as a neuron. The protein products of such genes return to the cell nucleus where they affect the transcription of other, 'late response' genes. Expression of these genes (such as c-fos or ZENK) or their protein products (Fos and Zenk, respectively) signifies that the cell is activated. Therefore, IEG expression is used as a marker for neuronal activation. The genes can be stained by means of an in situ hybridization procedure, whereas the protein products can be made visible through immunocytochemistry.

Template

A metaphor for the central representation of song. Conventionally, it has been suggested that songbirds are born with a crude template that has species-specific characteristics. Auditory experience with the song of an adult conspecific male will then mould the template into a more precise representation of the tutor song.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Bolhuis, J., Gahr, M. Neural mechanisms of birdsong memory. Nat Rev Neurosci 7, 347–357 (2006). https://doi.org/10.1038/nrn1904

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1038/nrn1904

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