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Instructed learning in the auditory localization pathway of the barn owl

Abstract

A bird sings and you turn to look at it — a process so automatic it seems simple. But is it? Our ability to localize the source of a sound relies on complex neural computations that translate auditory localization cues into representations of space. In barn owls, the visual system is important in teaching the auditory system how to translate cues. This example of instructed plasticity is highly quantifiable and demonstrates mechanisms and principles of learning that may be used widely throughout the central nervous system.

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Figure 1: The relationship between auditory cue values and locations in space for a barn owl.
Figure 2: Plasticity of auditory orienting behaviour of a juvenile owl, resulting from prism experience.
Figure 3: Midbrain and forebrain pathways that mediate auditory orienting responses.
Figure 4: Plasticity of auditory tuning in the optic tectum of a juvenile barn owl resulting from prism experience.
Figure 5: Plasticity of the anatomical projection from the ICC to the ICX, resulting from prism experience.
Figure 6: Changes in neuronal connectivity that accompany the acquisition of a new map of ITD in the ICX.
Figure 7: The effect of prism experience on information flow in the midbrain auditory localization pathway.
Figure 8: Effect of age and prior experience on ITD map plasticity, as induced by prism experience.

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References

  1. Field, J., Muir, D., Pilon, R., Sinclair, M. & Dodwell, P. Infants' orientation to lateral sounds from birth to three months. Child Dev. 51, 295–298 (1980).

    Article  CAS  PubMed  Google Scholar 

  2. Ashmead, D. H., Clifton, R. K. & Reese, E. P. Development of auditory localization in dogs: single source and precedence effect sounds. Dev. Psychobiol. 19, 91–103 (1986).

    Article  CAS  PubMed  Google Scholar 

  3. Hofman, P. M., Van Riswick, J. G. A. & Van Opstal, A. J. Relearning sound localization with new ears. Nature Neurosci. 1, 417–421 (1998).

    Article  CAS  PubMed  Google Scholar 

  4. King, A. J., Schnupp, J. W. & Doubell, T. P. The shape of ears to come: dynamic coding of auditory space. Trends Cogn. Sci. 5, 261–270 (2001).

    Article  PubMed  Google Scholar 

  5. Knudsen, E. I. Mechanisms of experience-dependent plasticity in the auditory localization pathway of the barn owl. J. Comp. Physiol. 185, 305–321 (1999).

    Article  CAS  Google Scholar 

  6. King, A. J. A map of auditory space in the mammalian brain: neural computation and development. Exp. Physiol. 78, 559–590 (1993).

    Article  CAS  PubMed  Google Scholar 

  7. Shinn-Cunningham, B. Adapting to remapped auditory localization cues: a decision-theory model. Percept. Psychophys. 62, 33–47 (2000).

    Article  CAS  PubMed  Google Scholar 

  8. Knudsen, E. I., Blasdel, G. G. & Konishi, M. Sound localization by the barn owl measured with the search coil technique. J. Comp. Physiol. 133, 1–11 (1979).

    Article  Google Scholar 

  9. Middlebrooks, J. C. & Green, D. M. Sound localization by human listeners. Annu. Rev. Psychol. 42, 135–159 (1991).

    Article  CAS  PubMed  Google Scholar 

  10. Konishi, M., Takahashi, T. T., Wagner, H., Sullivan, W. E. & Carr, C. E. in Auditory Function (eds Edelman, G. M., Gall, W. E. & Cowan, W. M.) 721–745 (Wiley, New York, 1988).

    Google Scholar 

  11. Blauert, J. Spatial Hearing: The Psychophysics of Human Sound Localization (MIT Press, Cambridge, MA, 1997).

    Google Scholar 

  12. Carr, C. E. & Boudreau, R. E. Development of the time coding pathways in the auditory brainstem of the barn owl. J. Comp. Neurol. 373, 467–483 (1996).

    Article  CAS  PubMed  Google Scholar 

  13. Knudsen, E. I., Esterly, S. D. & Knudsen, P. F. Monaural occlusion alters sound localization during a sensitive period in the barn owl. J. Neurosci. 4, 1001–1011 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Knudsen, E. I., Knudsen, P. F. & Esterly, S. D. A critical period for the recovery of sound localization accuracy following monaural occlusion in the barn owl. J. Neurosci. 4, 1012–1020 (1984).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Brainard, M. S. & Knudsen, E. I. Sensitive periods for visual calibration of the auditory space map in the barn owl optic tectum. J. Neurosci. 18, 3929–3942 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lackner, J. R. in Intersensory Perception and Sensory Integration (eds Walk, R. D. & Pisk, H. L.) 143–173 (Plenum, New York, 1981).

    Book  Google Scholar 

  17. Knudsen, E. I. & Knudsen, P. F. Visuomotor adaptation to displacing prisms by adult and baby barn owls. J. Neurosci. 9, 3297–3305 (1989).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Baizer, J. S., Kralj-hans, I. & Glickstein, M. Cerebellar lesions and prism adaptation in macaque monkeys. J. Neurophysiol. 81, 1960–1965 (1999).

    Article  CAS  PubMed  Google Scholar 

  19. Irvine, D. R. F. in The Mammalian Auditory Pathway: Neurophysiology (eds Popper, A. N. & Fay, R. R.) 153–231 (Springer, New York, 1992).

    Book  Google Scholar 

  20. Cohen, Y. E. & Knudsen, E. I. Maps versus clusters: different representations of auditory space in the midbrain and forebrain. Trends Neurosci. 22, 128–135 (1999).

    Article  CAS  PubMed  Google Scholar 

  21. Clarey, J. C., Barone, P. & Imig, T. J. in The Mammalian Auditory Pathway: Neurophysiology (eds Popper, A. N. & Fay, R. R.) 232–334 (Springer, New York, 1992).

    Book  Google Scholar 

  22. Cohen, Y. E. & Knudsen, E. I. Representation of binaural spatial cues in Field L of the barn owl forebrain. J. Neurophysiol. 79, 879–890 (1998).

    Article  CAS  PubMed  Google Scholar 

  23. Brainard, M. D., Knudsen, E. I. & Esterly, S. D. Neural derivation of sound source location: resolution of spatial ambiguity in binaural cues. J. Acoust. Soc. Am. 91, 1015–1027 (1992).

    Article  ADS  CAS  PubMed  Google Scholar 

  24. Wagner, H., Takahashi, T. & Konishi, M. Representation of interaural time difference in the central nucleus of the barn owl's inferior colliculus. J. Neurosci. 7, 3105–3116 (1987).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Stein, B. E. & Meredith, M. A. The Merging of the Senses (MIT Press, Cambridge, MA, 1993).

    Google Scholar 

  26. Wagner, H. Sound-localization deficits induced by lesions in the barn owl's auditory space map. J. Neurosci. 13, 371–386 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Knudsen, E. I., Knudsen, P. F. & Masino, T. Parallel pathways mediating both sound localization and gaze control in the forebrain and midbrain of the barn owl. J. Neurosci. 13, 2837–2852 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Schreiner, C. E. Order and disorder in auditory cortical maps. Curr. Opin. Neurobiol. 5, 489–496 (1995).

    Article  CAS  PubMed  Google Scholar 

  29. Recanzone, G. H. Spatial processing in the auditory cortex of the macaque monkey. Proc. Natl Acad. Sci. USA 97, 11829–11835 (2000).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  30. Rauschecker, J. P. & Tian, B. Mechanisms and streams for processing of “what” and “where” in auditory cortex. Proc. Natl Acad. Sci. USA 97, 11800–11806 (2000).

    Article  ADS  CAS  PubMed  PubMed Central  Google Scholar 

  31. Heffner, H. & Heffner, R. S. Effect of bilateral auditory cortex lesions on sound localization in Japanese macaques. J. Neurophysiol. 64, 915–931 (1990).

    Article  CAS  PubMed  Google Scholar 

  32. Knudsen, E. I. & Knudsen, P. F. Disruption of auditory spatial working memory by inactivation of the forebrain archistriatum in barn owls. Nature 383, 428–431 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  33. Miller, G. L. & Knudsen, E. I. Early visual experience shapes the representation of auditory space in the forebrain gaze fields of the barn owl. J. Neurosci. 19, 2326–2336 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Miller, G. L. & Knudsen, E. I. Early auditory experience induces frequency-specific, adaptive plasticity in the forebrain gaze fields of the barn owl. J. Neurophysiol. 85, 2184–2194 (2001).

    Article  CAS  PubMed  Google Scholar 

  35. Knudsen, E. I. Auditory and visual maps of space in the optic tectum of the owl. J. Neurosci. 2, 1177–1194 (1982).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Brainard, M. S. & Knudsen, E. I. Experience-dependent plasticity in the inferior colliculus: a site for visual calibration of the neural representation of auditory space in the barn owl. J. Neurosci. 13, 4589–4608 (1993).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Mogdans, J. & Knudsen, E. I. Early monaural occlusion alters the neural map of interaural level difference in the inferior colliculus of the barn owl. Brain Res. 619, 29–38 (1993).

    Article  CAS  PubMed  Google Scholar 

  38. Feldman, D. E. & Knudsen, E. I. Pharmacological specialization of learned auditory responses in the inferior colliculus of the barn owl. J. Neurosci. 18, 3073–3087 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Feldman, D. E. & Knudsen, E. I. An anatomical basis for visual calibration of the auditory space map in the barn owl's midbrain. J. Neurosci. 17, 6820–6837 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. DeBello, W. M., Feldman, D. E. & Knudsen, E. I. Adaptive axonal remodeling in the midbrain auditory space map. J. Neurosci. 21, 3161–3174 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Feldman, D. E. & Knudsen, E. I. NMDA and non-NMDA glutamate receptors in auditory transmission in the barn owl inferior colliculus. J. Neurosci. 14, 5939–5958 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Feldman, D. E. & Knudsen, E. I. Experience-dependent plasticity and the maturation of glutamergic synapses. Neuron 20, 1067–1071 (1998).

    Article  CAS  PubMed  Google Scholar 

  43. Cotman, C. W., Monaghan, D. T. & Ganong, A. H. Excitatory amino acid neurotransmission: NMDA receptors and Hebb-type synaptic plasticity. Annu. Rev. Neurosci. 11, 61–80 (1988).

    Article  CAS  PubMed  Google Scholar 

  44. Fujita, I. & Konishi, M. The role of GABAergic inhibition in processing of interaural time difference in the owl's auditory system. J. Neurosci. 11, 722–729 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Zheng, W. & Knudsen, E. I. GABAergic inhibition antagonizes adaptive adjustment of the owl's auditory space map during the initial phase of plasticity. J. Neurosci. 21, 4356–4365 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Zheng, G. L. & Knudsen, E. I. Functional selection of adaptive auditory space map by GABA-mediated inhibition. Science 284, 962–965 (1999).

    Article  ADS  CAS  PubMed  Google Scholar 

  47. Kaas, J. H. Plasticity of sensory and motor maps in adult mammals. Annu. Rev. Neurosci. 14, 137–167 (1991).

    Article  CAS  PubMed  Google Scholar 

  48. Gilbert, C. D., Sigman, M. & Crist, R. E. The neural basis of perceptual learning. Neuron 31, 681–697 (2001).

    Article  CAS  PubMed  Google Scholar 

  49. Knudsen, E. I. Supervised learning in the brain. J. Neurosci. 14, 3985–3997 (1994).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Knudsen, E. I. & Mogdans, J. Vision-independent adjustment of unit tuning to sound localization cues in response to monaural occlusion in developing owl tectum. J. Neurosci. 12, 3485–3493 (1992).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Rucci, M., Tononi, G. & Edelman, G. M. Registration of neural maps through value-dependent learning: modeling the alignment of auditory and visual maps in the barn owl's optic tectum. J. Neurosci. 17, 334–352 (1997).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Hyde, P. S. & Knudsen, E. I. A topographic instructive signal guides the adjustment of the auditory space map in the optic tectum. J. Neurosci. 21, 8586–8593 (2001).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Hyde, P. S. & Knudsen, E. I. Topographic projection from the optic tectum to the auditory space map in the inferior colliculus of the barn owl. J. Comp. Neurol. 421, 146–160 (2000).

    Article  CAS  PubMed  Google Scholar 

  54. Luksch, H., Gauger, B. & Wagner, H. A candidate pathway for a visual instructional signal to the barn owl's auditory system. J. Neurosci. 20, RC70 (2000).

  55. Hyde, P. S. & Knudsen, E. I. The optic tectum controls visually guided adaptive plasticity in the owl's auditory space map. Nature 415, 73–76 (2002).

    Article  ADS  CAS  PubMed  Google Scholar 

  56. King, A. J., Schnupp, J. W. & Thompson, I. D. Signals from the superficial layers of the superior colliculus enable the development of the auditory space map in the deeper layers. J. Neurosci. 18, 9394–9408 (1998).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Knudsen, E. I. Experience alters spatial tuning of auditory units in the optic tectum during a sensitive period in the barn owl. J. Neurosci. 5, 3094–3109 (1985).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Gold, J. I. & Knudsen, E.I. A site of auditory experience-dependent plasticity in the neural representation of auditory space in the barn owl's inferior colliculus. J. Neurosci. 20, 3469–3486 (2000).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Batista, A. P., Buneo, C. A., Snyder, L. H. & Anderson, R. A. Reach plans in eye-centered coordinates. Science 285, 257–260 (1999).

    Article  CAS  PubMed  Google Scholar 

  60. Cohen, Y. E. & Andersen, R. A. Reaches to sounds encoded in an eye-centered reference frame. Neuron 27, 647–652 (2000).

    Article  CAS  PubMed  Google Scholar 

  61. Troyer, T. W. & 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).

    Article  CAS  PubMed  Google Scholar 

  62. Klier, E. M., Wang, H. & Crawford, J. D. The superior colliculus encodes gaze commands in retinal coordinates. Nature Neurosci. 4, 627–632 (2001).

    Article  CAS  PubMed  Google Scholar 

  63. Katz, L. C. & Shatz, C. J. Synaptic activity and the construction of cortical circuits. Science 274, 1133–1138 (1996).

    Article  ADS  CAS  PubMed  Google Scholar 

  64. Tinbergen, N. The Study of Instinct (Oxford Univ. Press, New York, 1976).

    Google Scholar 

  65. Knudsen, E. I., Esterly, S. D. & du Lac, S. Stretched and upside-down maps of auditory space in the optic tectum of blind-reared owls: acoustic basis and behavioral correlates. J. Neurosci. 11, 1727–1747 (1991).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Withington-Wray, D. J., Binns, K. E. & Keating, M. J. A four-day period of bimodality auditory and visual experience is sufficient to permit normal emergence of the map of auditory space in the guinea pig superior colliculus. Neurosci. Lett. 116, 280–286 (1990).

    Article  CAS  PubMed  Google Scholar 

  67. Knudsen, E. I. Capacity for plasticity in the adult owl auditory system expanded by juvenile experience. Science 279, 1531–1533 (1998).

    Article  ADS  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  69. Hess, E. H. Imprinting: Early Experience and the Developmental Psychobiology of Attachment (Van Nostrand Reinhold, New York, 1973).

  70. Scott, J. P. Critical periods in behavioral development. Science 138, 949–958 (1962).

    Article  ADS  CAS  PubMed  Google Scholar 

  71. Newport, E. L., Bavelier, D. & Neville, H. J. in Language, Brain and Cognitive Development: Essays in Honor of Jacques Mehler (ed. Doupoux, E.) 481–502 (MIT Press, Cambridge, MA, 2001).

    Google Scholar 

  72. Knudsen, E. I. & Knudsen, P. F. Sensitive and critical periods for visual calibration of sound localization by barn owls. J. Neurosci. 63, 131–149 (1990).

    Google Scholar 

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Acknowledgements

I thank P. Knudsen for technical support and B. Linkenhoker and Y. Gutfreund for helpful comments on the manuscript. This work was support by grants from the National Institutes of Health, the March of Dimes and the McKnight Foundation.

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Correspondence to Eric I. Knudsen.

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Knudsen, E. Instructed learning in the auditory localization pathway of the barn owl. Nature 417, 322–328 (2002). https://doi.org/10.1038/417322a

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