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Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex

Abstract

Auditory localization relies on the detection and interpretation of acoustic cues that change in value as the head and external ears grow. Here we show that the maturation of these structures is an important determinant for the development of spatial selectivity in the ferret auditory cortex. Spatial response fields (SRFs) of high-frequency cortical neurons recorded at postnatal days (P) 33–39 were broader, and transmitted less information about stimulus direction, than in older ferrets. They also exhibited slightly broader frequency tuning than neurons recorded in adult animals. However, when infant neurons were stimulated through virtual ears of adults, SRFs sharpened significantly and the amount of transmitted information increased. This improvement was predicted by a model that generates SRF shape from the localization cue values and the neurons' binaural spectrotemporal response properties. The maturation of spatial response characteristics in auditory cortex therefore seems to be limited by peripheral rather than by central factors.

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Figure 1: Representative examples of near-threshold SRFs in ferret A1 at various developmental ages.
Figure 2: Sound-level dependence of SRF tuning parameters at different ages.
Figure 3: Summary of directional preferences of all recordings in infant (left) and adult (right) animals.
Figure 4: Infant spatial cues are less directional than in adult ferrets.
Figure 5: Pair-wise comparison of infant (P33–39) SRFs recorded with the animal's own acoustic cues (own ears) and with those from an adult ferret (adult ears) for five representative single units.
Figure 6: Listening through adult ears reduces the size of and increases the amount of information transmitted by infant near-threshold SRFs.
Figure 7: Switching between infant and adult acoustic cue values changes the size of the predicted SRFs of A1 units.
Figure 8: Temporal and spectral response properties of A1 neurons in infants and adults.

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References

  1. Jacobs, D.S. & Blakemore, C. Factors limiting the postnatal development of visual acuity in the monkey. Vis. Res. 28, 947–958 (1988).

    Article  CAS  Google Scholar 

  2. Kiorpes, L. & Movshon, J.A. Behavioural analysis of visual development. in Development of Sensory Systems in Mammals. (ed. Coleman, J.R.) 125–154 (John Wiley & Sons, New York, 1990).

    Google Scholar 

  3. Tavazoie, S.F. & Reid, R.C. Diverse receptive fields in the lateral geniculate nucleus during thalamocortical development. Nat. Neurosci. 3, 608–616 (2000).

    Article  CAS  Google Scholar 

  4. Sanes, D.H. & Walsh, E.J. The development of central auditory processing. in Development of the Auditory System. (eds. Rubel, E.R., Popper, A.N. & Fay, R.R.) 271–314 (Springer, New York, 1998).

    Chapter  Google Scholar 

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

    Article  Google Scholar 

  6. Carlile, S. The auditory periphery of the ferret: postnatal development of acoustic properties. Hear. Res. 51, 265–277 (1991).

    Article  CAS  Google Scholar 

  7. Clifton, R.K., Gwiazda, J., Bauer, J.A., Clarkson, M.G. & Held, R.M. Growth in head size during infancy: implcations for sound localization. Dev. Psychol. 24, 477–483 (1988).

    Article  Google Scholar 

  8. Moore, D.R. & Irvine, D.R.F. A developmental study of the sound pressure transformation by the head of the cat. Acta Otolaryngol. Stockh. 87, 434–440 (1979).

    Article  CAS  Google Scholar 

  9. Schnupp, J.W.H., Booth, J. & King, A.J. Modeling individual differences in ferret external ear transfer functions. J. Acoust. Soc. Am. 113, 2021–2030 (2003).

    Article  Google Scholar 

  10. King, A.J. & Carlile, S. Neural coding for auditory space. in The Cognitive Neurosciences (ed. Gazzaniga, M.S.) 279–293 (MIT Press, Cambridge, Massachusetts, 1995).

    Google Scholar 

  11. Brugge, J.F., Javel, E. & Kitzes, L.M. Signs of functional maturation of peripheral auditory system in discharge patterns of neurons in anteroventral cochlear nucleus of kitten. J. Neurophysiol. 41, 1557–1559 (1978).

    Article  CAS  Google Scholar 

  12. Sanes, D.H. & Rubel, E.W. The ontogeny of inhibition and excitation in the gerbil lateral superior olive. J. Neurosci. 8, 682–700 (1988).

    Article  CAS  Google Scholar 

  13. Woolf, N.K. & Ryan, A.F. Ontogeny of neural discharge patterns in the ventral cochlear nucleus of the mongolian gerbil. Brain Res. 349, 131–147 (1985).

    Article  CAS  Google Scholar 

  14. Brugge, J.F., Kitzes, L.M. & Javel, E. Postnatal development of frequency and intensity sensitivity of neurons in the anteroventral cochlear nucleus of kittens. Hear. Res. 5, 217–229 (1981).

    Article  CAS  Google Scholar 

  15. Moore, D.R. & Irvine, D.R.F. Development of responses to acoustic interaural intensity differences in the cat inferior colliculus. Exp. Brain Res. 41, 301–309 (1981).

    CAS  PubMed  Google Scholar 

  16. Fitzakerley, J.L., McGee, J.A. & Walsh, E.J. Paradoxical relationship between frequency selectivity and threshold sensitivity during auditory-nerve fiber development. J. Acoust. Soc. Am. 103, 3464–3477 (1998).

    Article  CAS  Google Scholar 

  17. Moore, D.R. & Irvine, D.R.F. The development of some peripheral and central auditory responses in the neonatal cat. Brain Res. 163, 49–59 (1979).

    Article  CAS  Google Scholar 

  18. Zhang, L.I., Bao, S. & Merzenich, M.M. Persistent and specific influences of early acoustic environments on primary auditory cortex. Nat. Neurosci. 4, 1123–1130 (2001).

    Article  CAS  Google Scholar 

  19. Cant, N.B. Structural development of mammalian auditory pathways. in Development of the Auditory System (eds. Rubel, E.W., Popper, A.N. & Fay, R.R.) 315–414 (Springer, New York, 1998).

    Chapter  Google Scholar 

  20. Kapfer C., Seidl A.H., Schweizer H. & Grothe B. Experience-dependent refinement of inhibitory inputs to auditory coincidence–detector neurons. Nat. Neurosci. 5, 247–253 (2002).

    Article  CAS  Google Scholar 

  21. Kotak, V.C. & Sanes, D.H. Long-lasting inhibitory synaptic depression is age- and calcium- dependent. J. Neurosci. 20, 5820–5826 (2000).

    Article  CAS  Google Scholar 

  22. Rietzel, H.J. & Friauf, E. Neuron types in the rat lateral superior olive and developmental changes in the complexity of their dendritic arbors. J. Comp. Neurol. 390, 20–40 (1998).

    Article  CAS  Google Scholar 

  23. Sanes, D.H. & Friauf, E. Development and influence of inhibition in the lateral superior olivary nucleus. Hear. Res. 147, 46–58 (2000).

    Article  CAS  Google Scholar 

  24. Brugge, J.F. et al. Simulation of free-field sound sources and its application to studies of cortical mechanisms of sound localization in the cat. Hear. Res. 73, 67–84 (1994).

    Article  CAS  Google Scholar 

  25. Clarke, S., Bellmann, A., Meuli, R.A., Assal, G. & Steck, A.J. Auditory agnosia and auditory spatial deficits following left hemispheric lesions: evidence for distinct processing pathways. Neuropsychologia 38, 797–807 (2000).

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  27. Jenkins, W.M. & Merzenich, M.M. Role of cat primary auditory cortex for sound-localization behavior. J. Neurophysiol. 52, 819–847 (1984).

    Article  CAS  Google Scholar 

  28. Kavanagh, G.L. & Kelly, J.B. Contribution of auditory cortex to sound localization by the ferret (Mustela putorius). J. Neurophysiol. 57, 1746–1766 (1987).

    Article  CAS  Google Scholar 

  29. Wightman, F.L. & Kistler, D.J. Headphone simulation of free–field listening. II: psychophysical validation. J. Acoust. Soc. Am. 85, 868–878 (1989).

    Article  CAS  Google Scholar 

  30. Moore, D.R. & Hine, J.E. Rapid development of the auditory brainstem response threshold in individual ferrets. Brain Res. Dev. Brain Res. 66, 229–235 (1992).

    Article  CAS  Google Scholar 

  31. Brugge, J.F., Reale, R.A. & Hind, J.E. The structure of spatial receptive fields of neurons in primary auditory cortex of the cat. J. Neurosci. 16, 4420–4437 (1996).

    Article  CAS  Google Scholar 

  32. Middlebrooks, J.C. & Pettigrew, J.D. Functional classes of neurons in primary auditory cortex of the cat distinguished by sensitivity to sound location. J. Neurosci. 1, 107–120 (1981).

    Article  CAS  Google Scholar 

  33. Mrsic-Flogel, T.D., King, A.J., Jenison, R.L. & Schnupp, J.W.H. Listening through different ears alters spatial response fields in ferret primary auditory cortex. J. Neurophysiol. 86, 1043–1046 (2001).

    Article  CAS  Google Scholar 

  34. Furukawa, S. & Middlebrooks, J.C. Cortical representation of auditory space: information–bearing features of spike patterns. J. Neurophysiol. 87, 1749–1762 (2002).

    Article  Google Scholar 

  35. Kelly, J.B., Judge, P.W. & Phillips, D.P. Representation of the cochlea in primary auditory cortex of the ferret (Mustela putorius). Hear. Res. 24, 111–115 (1986).

    Article  CAS  Google Scholar 

  36. Schnupp, J.W.H., Mrsic–Flogel, T.D. & King, A.J. Linear processing of spatial cues in primary auditory cortex. Nature 414, 200–204 (2001).

    Article  CAS  Google Scholar 

  37. Rübsamen, R. & Lippe, W.R. The development of cochlear function. in Development of the Auditory System (eds. Rubel, E.R., Popper, A.N. & Fay, R.R.) 193–270 (Springer, New York, 1998).

    Chapter  Google Scholar 

  38. Gao, W.J., Newman, D.E., Wormington, A.B. & Pallas, S.L. Development of inhibitory circuitry in visual and auditory cortex of postnatal ferrets: immunocytochemical localization of GABAergic neurons. J. Comp. Neurol. 409, 261–273 (1999).

    Article  CAS  Google Scholar 

  39. Brown, P.E., Grinnel, A.D. & Harrison, J.B. The development of hearing in the pallid bat, Antrozous pallidus. J. Comp. Physiol. 126, 169–182 (1978).

    Article  Google Scholar 

  40. Sanes, D.H. The development of synaptic function and integration in the central auditory system. J. Neurosci. 13, 2627–2637 (1993).

    Article  CAS  Google Scholar 

  41. Blatchley, B.J. & Brugge, J.F. Sensitivity to binaural intensity and phase difference cues in kitten inferior colliculus. J. Neurophysiol. 64, 582–597 (1990).

    Article  CAS  Google Scholar 

  42. Brugge, J.F., Reale, R.A. & Wilson, G.F. Sensitivity of auditory cortical neurons of kittens to monaural and binaural high frequency sound. Hear. Res. 34, 127–140 (1988).

    Article  CAS  Google Scholar 

  43. Werner, L.A. & Gray, L. Behavioral studies of hearing development. in Development of the Auditory System (eds. Rubel, E.R., Fay, R.R. & Popper, A.N.) 12–79 (Springer, New York, 1998).

    Chapter  Google Scholar 

  44. Brugge, J.F., Orman, S.S., Coleman, J.R., Chan, J.C.K. & Phillips, D.P. Binaural interactions in cortical area AI of cats reared with unilateral atresia of the external ear canal. Hear. Res. 20, 275–287 (1985).

    Article  CAS  Google Scholar 

  45. Gold, J.I. & Knudsen, E.I. Hearing impairment induces frequency–specific adjustments in auditory spatial tuning in the optic tectum of young owls. J. Neurophysiol. 82, 2197–2209 (1999).

    Article  CAS  Google Scholar 

  46. King, A.J., Parsons, C.H. & Moore, D.R. Plasticity in the neural coding of auditory space in the mammalian brain. Proc. Natl. Acad. Sci. USA 97, 11821–11828 (2000).

    Article  CAS  Google Scholar 

  47. Rauschecker, J.P. Auditory cortical plasticity: a comparison with other sensory systems. Trends Neurosci. 22, 74–80 (1999).

    Article  CAS  Google Scholar 

  48. Middlebrooks, J.C. & Green, D.M. Directional dependence of interaural envelope delays. J. Acoust. Soc. Am. 87, 2149–2162 (1990).

    Article  CAS  Google Scholar 

  49. deCharms, R.C., Blake, D.T. & Merzenich, M.M. Optimizing sound features for cortical neurons. Science 280, 1439–1443 (1998).

    Article  CAS  Google Scholar 

  50. Golomb, D., Hertz, J., Panzeri, S., Treves, A. & Richmond, B. How well can we estimate the information carried in neuronal responses from limited samples? Neural Comput. 9, 649–665 (1997).

    Article  CAS  Google Scholar 

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Acknowledgements

We are grateful to I. Thompson for critique of an earlier draft, and to I. Nelken for advice on information theory. Our research was sponsored by the Wellcome Trust (Senior Research Fellowship to A.J.K., Research Studentship to T.D.M.F.) and Defeating Deafness (Dunhill Medical Research Trust Research Fellowship to J.W.H.S.).

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Correspondence to Andrew J King.

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Mrsic-Flogel, T., Schnupp, J. & King, A. Acoustic factors govern developmental sharpening of spatial tuning in the auditory cortex. Nat Neurosci 6, 981–988 (2003). https://doi.org/10.1038/nn1108

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