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Slow NMDA-EPSCs at synapses critical for song development are not required for song learning in zebra finches

Nature Neuroscience volume 3, pages 482–488 (2000)Cite this article

Abstract

Birdsong, like human speech, is learned via auditory experience during a developmentally restricted sensitive period. Within projection neurons of two avian forebrain nuclei, NMDA receptor-mediated EPSCs (NMDA-EPSCs) become fast during song development, a transition posited to limit learning. To discover whether slow NMDA-EPSCs at these synapses are required for learning, we delayed song learning beyond its normal endpoint, post-hatch day (PHD) 65, by raising zebra finches in isolation from song tutors. At PHD45, before learning, isolation delayed NMDA-EPSC maturation, but only transiently. By PHD65, NMDA-EPSCs in isolates were fast and adult-like, yet isolates presented with tutors readily learned song. Thus song learning did not require slow NMDA-EPSCs at synapses critical for song development.

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Figure 1: Time line of song development and schematic of song system.
Figure 2: Isolation from tutor song extends the period of sensory acquisition into the time when NMDA-EPSCs are fast and adult-like.
Figure 3: NMDA-EPSC development in LMAN is delayed at PHD45 in isolates.
Figure 4: Early deafening delays late NMDA-EPSC maturation in RA.
Figure 5: Serum testosterone levels are depressed in isolates and deafened birds at PHD45.

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Notes

  1. Note: audio files of example songs from Fig. 2a can be found on the Nature Neuroscience web site ( http://www.nature.com/neuro/web_specials/).

References

  1. Carmignoto, G. & Vicini, S. Activity-dependent decrease in NMDA receptor responses during development of the visual cortex. Science 258, 1007–1011 ( 1992).

    Article  CAS  Google Scholar 

  2. Hestrin, S. Developmental regulation of NMDA receptor-mediated synaptic currents at a central synapse. Nature 357, 686– 689 (1992).

    Article  CAS  Google Scholar 

  3. Crair, M. R. & Malenka, R. C. A critical period for long-term potentiation at thalamocortical synapses. Nature 375 , 325–328 (1995).

    Article  CAS  Google Scholar 

  4. Shi, J., Aamodt, S. M. & Constantine-Paton, M. Temporal correlations between functional and molecular changes in NMDA receptors and GABA neurotransmission in the superior colliculus. J. Neurosci. 17, 6264 –6276 (1997).

    Article  CAS  Google Scholar 

  5. Livingston, F. S. & Mooney, R. Development of intrinsic and synaptic properties in a forebrain nucleus essential to avian song learning. J. Neurosci. 17, 8997– 9009 (1997).

    Article  CAS  Google Scholar 

  6. White, S. A., Livingston, F. S. & Mooney, R. D. Androgens modulate NMDA receptor-mediated EPSCs in the zebra finch song system. J. Neurophysiol. 82, 2221–2234 (1999).

    Article  CAS  Google Scholar 

  7. Tang, Y. et al. Genetic enhancement of learning and memory in mice. Nature 401, 63–69 ( 1999).

    Article  CAS  Google Scholar 

  8. 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).

    Article  CAS  Google Scholar 

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

    Google Scholar 

  10. Eales, L. A. Song learning in zebra finches: some effects of song model availability on what is learnt and when. Anim. Behav. 33, 1293–1300 (1985).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  13. Jones, A. E., ten Cate, C. & Slater, P. J. B. Early experience and plasticity of song in adult male zebra finches (Taeniopygia guttata). J. Comp. Psychol. 110, 354–369 (1996).

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  16. 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  Google Scholar 

  17. 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).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  21. Basham, M. E., Nordeen, E. J. & Nordeen, K. M. 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  Google Scholar 

  22. Konishi, M. The role of auditory feedback in the control of vocalization in the white-crowned sparrow. Z. Tierpsychol. 22, 770– 783 (1965).

    Article  CAS  Google Scholar 

  23. Price, P. H. Developmental determinants of structure in zebra finch song. J. Comp. Physiol. Psychol. 93, 260–277 (1979).

    Article  Google Scholar 

  24. Arnold, A. P. The effects of castration on song development in zebra finches (Poephila guttata). J. Exp. Zool. 191, 261– 278 (1975).

    Article  CAS  Google Scholar 

  25. Bottjer, S. W. & Hewer, S. J. Castration and antisteroid treatment impair vocal learning in male zebra finches. J. Neurobiol. 23, 337–353 (1992).

    Article  CAS  Google Scholar 

  26. Prove, E. in Hormones and Behavior in Higher Vertebrates (eds. Balthazart, J., Prove, E. & Gilles, R.) 368–374 (Springer, Berlin, 1983).

    Book  Google Scholar 

  27. Wingfield, J. C. & Moore, M. C. in Psychobiology of Reproduction: An Evolutionary Approach (ed. Crews, D.) 149– 175 (Prentice Hall, Englewood Cliffs, New Jersey, 1987 ).

    Google Scholar 

  28. 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).

    Article  CAS  Google Scholar 

  29. 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).

    Article  CAS  Google Scholar 

  30. Hubel, D. H., Wiesel, T. N. & LeVay, S. Plasticity of ocular dominance columns in monkey striate cortex. Phil. Trans. R. Soc. Lond. B Biol. Sci. 278 , 377–409 (1977).

    Article  CAS  Google Scholar 

  31. Quinlan, E. M., Philpot, B. D., Huganir, R. L. & Bear, M. F. Rapid, experience-dependent expression of synaptic NMDA receptors in visual cortex in vivo. Nat. Neurosci. 2, 352–357 (1999).

    Article  CAS  Google Scholar 

  32. Flint, A. C., Maisch, U. S., Weishaupt, J. H., Kriegstein, A. R. & Monyer, H. NR2A subunit expression shortens NMDA receptor synaptic currents in developing neocortex. J. Neurosci. 17, 2469–2476 (1997).

    Article  CAS  Google Scholar 

  33. Roberts, E. B. & Ramoa, A. S. Enhanced NR2A subunit expression and decreased NMDA receptor decay time at the onset of ocular dominance plasticity in the ferret. J. Neurophysiol. 81, 2587–2591 (1999).

    Article  CAS  Google Scholar 

  34. 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).

    Article  CAS  Google Scholar 

  35. Stark, L. L. & Perkel, D. J. Two-stage, input-specific synaptic maturation in a nucleus essential for vocal production in the zebra finch . J. Neurosci. 19, 9107– 9116 (1999)

    Article  CAS  Google Scholar 

  36. 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).

    Article  CAS  Google Scholar 

  37. Mayer, M. L., Westbrook, G. L. & Guthrie, P. B. Voltage-dependent block by Mg2+ of NMDA responses in spinal cord neurones. Nature 309, 261–263 (1984).

    Article  CAS  Google Scholar 

  38. Nowak, L., Bregestovski, P., Ascher, P., Herbet, A. & Prochiantz, A. Magnesium gates glutamate-activated channels in mouse central neurones. Nature 307, 462–465 (1984).

    Article  CAS  Google Scholar 

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Acknowledgements

We thank Dona Chikaraishi, Mike Ehlers, Felix Schweizer and all members of the Mooney lab for providing discussion of the manuscript. In particular, J. Matthew Kittelberger assisted with song analysis and Stacey S. James designed and constructed vinyl covers for isolation cages. In addition, Eugene A. Zimmerman gave assistance with the hormone measurements, and Mark Schmidt taught us the deafening technique. This research was supported by NRSA F31 MH11872 to F.S.L., H.H. Whitney fellowship to S.A.W. and by NIH R01 DC02524, McKnight, Klingenstein and Sloan Foundation awards to R.M.

Author information

Author notes

  1. Frederick S. Livingston and Stephanie A. White: The first two authors contributed equally to this work.

Authors and Affiliations

  1. Department of Neurobiology, Duke University Medical Center, Box 3209, Durham, 27710, North Carolina , USA

    Frederick S. Livingston, Stephanie A. White & Richard Mooney

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  1. Frederick S. Livingston
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  2. Stephanie A. White
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Correspondence to Richard Mooney.

Supplementary information

Requires quicktime plug-in, download quicktime now

Spectrograms for one isolate, one control and one tutor. Click on a spectrogram to listen to the song.

i-postut

Song i-postut (WAV 138 KB)

tutor

Song tutor (WAV 138 KB)

i-pretut

Song i-pretut (WAV 137 KB)

c-postut

Song c-postut (WAV 137 KB)

c-pretut

Song c-pretut (WAV 136 KB)

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Livingston, F., White, S. & Mooney, R. Slow NMDA-EPSCs at synapses critical for song development are not required for song learning in zebra finches. Nat Neurosci 3, 482–488 (2000). https://doi.org/10.1038/74857

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