Severe and extensive neonatal hearing loss in cats results in auditory cortex plasticity that differentiates into two regions

European Journal of Neuroscience

Volumn 31, Issue 11, 2010, Pages 1999-2013

  Rajan, R ^a   Irvine, D R F ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Auditory cortex; Cochlea; Deafness; Development; Hearing loss; Plasticity

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUDITORY CORTEX; EXPERIMENTAL CAT; HEARING LOSS; NERVE CELL PLASTICITY; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; ANATOMY AND HISTOLOGY; ANIMAL; AUDITORY THRESHOLD; BRAIN MAPPING; CAT; CHEMICALLY INDUCED; COCHLEA; HEARING; HEARING IMPAIRMENT; NEWBORN; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TOXICITY;

AMINOGLYCOSIDE;

AMINOGLYCOSIDES; ANIMALS; ANIMALS, NEWBORN; AUDITORY CORTEX; AUDITORY THRESHOLD; BRAIN MAPPING; CATS; COCHLEA; HEARING; HEARING LOSS; NEURONAL PLASTICITY;

EID: 77953184920     PISSN: 0953816X     EISSN: 14609568     Source Type: Journal    
DOI: 10.1111/j.1460-9568.2010.07214.x     Document Type: Article

References (71)

1. Angelucci, A., Levitt, J.B., Walton, E.J.S., Hupe, J.-M., Bullier, J. Lund, J.S. (2002) Circuits for local and global signal integration in primary visual cortex. J. Neurosci., 22, 8633 8646.
2. Benali, A., Weiler, E., Benali, Y., Dinse, H.R. Eysel, U.T. (2008) Excitation and inhibition jointly regulate cortical reorganization in adult rats. J. Neurosci., 28, 12284 12293.
3. Bringuier, V., Chavane, F., Glaeser, L. Fregnac, Y. (1999) Horizontal propagation of visual activity in the synaptic integration field of area 17 neurons. Science, 283, 695 699.
4. Buonomano, D.V. Merzenich, M.M. (1998) Cortical plasticity: from synapses to maps. Ann. Rev. Neurosci., 21, 149 186.
5. Calford, M.B. (2002) Dynamic representational plasticity in sensory cortex. Neuroscience, 111, 709 738.
6. Calford, M.B., Wright, L.L., Metha, A.B. Taglianetti, V. (2003) Topographic plasticity in primary visual cortex is mediated by local corticocortical connections. J. Neurosci., 23, 6434 6442.
7. Clarke, S., de Ribaupierre, F., Rouiller, E.M. de Ribaupierre, Y. (1993) Several neuronal and axonal types form long intrinsic connections in the cat primary auditory cortical field (AI). Anat. Embryol., 188, 117 138.
8. Coco, A., Epp, S.B., Fallon, J.B., Xu, J., Millard, R.E. Shepherd, R.K. (2007) Does cochlear implantation and electrical stimulation affect residual hair cells and spiral ganglion neurons? Hear. Res., 225, 60 70.
9. Dan, Y. Poo, M.-M. (2006) Spike timing-dependent plasticity: from synapse to perception. Physiol. Rev., 86, 1033 1048.
10. Darian-Smith, C. Gilbert, C.D. (1994) Axonal sprouting accompanies functional reorganization in adult cat striate cortex. Nature, 368, 737 740.
11. Darian-Smith, C. Gilbert, C.D. (1995) Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J. Neurosci., 15, 1631 1647.
12. Das, A. Gilbert, C.D. (1995) Long-range horizontal connections and their role in cortical reorganization revealed by optical recording of cat primary visual cortex. Nature, 375, 780 784.
13. Dietrich, V., Nieschalk, M., Stoll, W., Rajan, R. Pantev, C. (2001) Cortical reorganization in patients with high frequency cochlear hearing loss. Hear. Res., 158, 1 7.
14. Eggermont, J.J. Komiya, H. (2000) Moderate noise trauma in juvenile cats results in profound cortical topographic map changes in adulthood. Hear. Res., 142, 89 101.
15. Eggermont, J.J. Roberts, L.E. (2004) The neuroscience of tinnitus. Trends Neurosci., 27, 676 682.
16. Eysel, U.T., Gonzalez-Aguilar, F. Mayer, U. (1981) Time-dependent decrease in the extent of visual deafferentation in the lateral geniculate nucleus of adult cats with small retinal lesions. Exp. Brain Res., 41, 256 263.
17. Fallon, J.B., Shepherd, R.K., Brown, M. Irvine, D.R.F. (2009) Effects of neonatal partial deafness and chronic intracochlear electrical stimulation on auditory and electrical response characteristics in primary auditory cortex. Hear. Res., 257, 93 105.
18. Flor, H., Nikolajsen, L. Staehelin Jensen, T. (2006) Phantom limb pain: a case of maladaptive CNS plasticity? Nat. Rev. Neurosci., 7, 873 881.
19. Fox, K. Zahs, K. (1994) Critical period control in sensory cortex. Curr. Opin. Neurobiol., 4, 112 119.
20. Gao, W.-J. Pallas, S.L. (1999) Cross-modal reorganization of horizontal connectivity in auditory cortex without altering thalamocortical projections. J. Neurosci., 19, 7940 7950.
21. Giannikopoulos, D.V. Eysel, U.T. (2006) Dynamics and specificity of cortical map reorganization after retinal lesions. Proc. Natl Acad. Sci. USA, 103, 10805 10810.
22. Gilbert, C.D. (1992) Horizontal integration and cortical dynamics. Neuron, 9, 1 13.
23. Gilbert, C.D. Wiesel, T.N. (1992) Receptive field dynamics in adult primary visual cortex. Nature, 356, 150 152.
24. Harrison, R.V., Nagasawa, A., Smith, D.W., Stanton, S. Mount, R.J. (1991) Reorganization of auditory cortex after neonatal high frequency cochlear hearing loss. Hear. Res., 54, 11 19.
25. Harrison, R.V., Smith, D.W., Nagasawa, A., Stanton, S. Mount, R.J. (1992) Developmental plasticity of auditory cortex in cochlear hearing loss: physiological and psychophysical findings. In Cazals, Y., Horner, K. Demany, L. (Eds Auditory Physiology and Perception. Pergamon
26. Harrison, R.V., Stanton, S.G., Ibrahim, D., Nagasawa, A. Mount, R.J. (1993) Neonatal cochlear hearing loss results in developmental abnormalities of the central auditory pathways. Acta Otolarygol., 113, 296 302. (Pubitemid 23123979)
27. Heil, P., Rajan, R. Irvine, D.R.F. (1992) Sensitivity of neurons in cat primary auditory cortex to tones and frequency-modulated stimuli. II. Organization of response properties along the "isofrequency" dimension. Hear. Res., 63, 135 156.
28. Huang, C.L. Winer, J.A. (2000) Auditory thalamocortical projections in the cat: laminar and areal patterns of input. J. Comp. Neurol., 427, 302 331.
29. Imaizumi, K., Priebe, N.J., Crum, P.A.C., Bedenbaugh, P.H., Cheung, S.W. Schreiner, C.E. (2004) Modular functional organization of cat anterior auditory field. J. Neurophysiol., 92, 444 457.
30. Irvine, D.R.F. Wright, B.A. (2005) Plasticity in spectral processing. In Malmierca, M. Irvine, D.R.F. (Eds Auditory Spectral Processing. Elsevier Academic
31. Irvine, D.R.F., Rajan, R. Smith, S. (2003) Effects of restricted cochlear lesions in adult cats on the frequency organization of the inferior colliculus. J. Comp. Neurol., 467, 354 374.
32. Kaas, J.H. Florence, S.L. (2001) Reorganization of sensory and motor systems in adult mammals after injury. In Kaas, J.H. (Ed. The Mutable Brain. Harwood Academic Publishers
33. Kaas, J.H., Merzenich, M.M. Killackey, H.P. (1983) The reorganization of somatosensory cortex following peripheral nerve damage in adult and developing mammals. Ann. Rev. Neurosci., 6, 325 356.
34. Kakigi, A., Hirakawa, H., Harel, N., Mount, R.J. Harrison, R.V. (2000) Tonotopic mapping in auditory cortex of the adult chinchilla with amikacin-induced cochlear lesions. Audiology, 39, 153 160.
35. Kaltenbach, J.A., Czaja, J.M. Kaplan, C.R. (1992) Changes in the tonotopic map of the dorsal cochlear nucleus following induction of cochlear lesions by exposure to intense sound. Hear. Res., 59, 213 223.
36. Kamke, M.R., Brown, M. Irvine, D.R.F. (2003) Plasticity in the tonotopic organization of the medial geniculate body in adult cats following restricted unilateral cochlear lesions. J. Comp. Neurol., 459, 355 367.
37. Kamke, M.R., Brown, M. Irvine, D.R.F. (2005) Basal forebrain cholinergic input is not essential for lesion-induced plasticity in mature auditory cortex. Neuron, 48, 675 686.
38. Kaur, S., Lazar, R. Metherate, R. (2004) Intracortical pathways determine breadth of subthreshold frequency receptive fields in primary auditory cortex. J. Neurophysiol., 91, 2551 2567.
39. Keck, T., Mrsic-Flogel, T.D., Vaz Afonso, M., Eysel, U.T., Bonhoeffer, T. Hubener, M. (2008) Massive restructuring of neuronal circuits during functional reorganization of adult visual cortex. Nat. Neurosci., 11, 1162 1167.
40. Kisvárday, Z.F., Tóth, E., Rausch, M. Eysel, U.T. (1997) Orientation-specific relationship between populations of excitatory and inhibitory lateral connections in the visual cortex of the cat. Cereb. Cortex, 7, 605 618.
41. Kotak, V.C., Takesian, A.E. Sanes, D.H. (2008) Hearing loss prevents the maturation of GABAergic transmission in the auditory cortex. Cereb. Cortex, 18, 2098 2108.
42. Lee, C.C., Imaizumi, K., Schreiner, C.E. Winer, J.A. (2004a) Concurrent tonotopic processing streams in auditory cortex. Cereb. Cortex, 14, 441 451.
43. Lee, C.C., Schreiner, C.E., Imaizumi, K. Winer, J.A. (2004b) Tonotopic and heterotopic projection systems in physiologically defined auditory cortex. Neuroscience, 128, 871 887.
44. Matsubara, J.A. Phillips, D.P. (1988) Intracortical connections and their physiological correlates in the primary auditory cortex (AI) of the cat. J. Comp. Neurol., 268, 38 48.
45. McDermott, H.J., Lech, M., Kornblum, M.S. Irvine, D.R.F. (1998) Loudness perception and frequency discrimination in subjects with steeply sloping hearing loss: possible correlates of neural plasticity. J. Acoust. Soc. Am., 104, 2314 2325.
46. Metherate, R., Kaur, S., Kawai, H., Lazar, R., Liang, K. Rose, H.J. (2005) Spectral integration in auditory cortex: mechanisms and modulation. Hear. Res., 206, 146 158.
47. Moore, B.C.J. (2004) Dead regions in the cochlea: conceptual foundations, diagnosis, and clinical applications. Ear Hear., 25, 98 116.
48. Noreña, A.J. Eggermont, J.J. (2005) Enriched Acoustic environment after noise trauma reduces hearing loss and prevents cortical map reorganization. J. Neurosci., 25, 699 705.
49. O'Leary, D.D.M., Ruff, N.L. Dyck, R.H. (1994) Development, critical period plasticity, and adult reorganizations of mammalian somatosensory systems. Curr. Opin. Neurobiol., 4, 535 544.
50. Palagina, G., Eysel, U.T. Jancke, D. (2009) Strengthening of lateral activation in adult rat visual cortex after retinal lesions captured with voltage-sensitive dye imaging in vivo. Proc. Natl Acad. Sci. USA, 106, 8743 8747.
51. Rajan, R. (1998) Receptor organ damage causes loss of cortical surround inhibition without topographic map plasticity. Nat. Neurosci., 1, 138 143.
52. Rajan, R. (2001) Plasticity of excitation and inhibition in the receptive field of primary auditory cortical neurons after limited receptor organ damage. Cereb. Cortex, 11, 171 182.
53. Rajan, R. Irvine, D.R.F. (1998a) Absence of plasticity of the frequency map in dorsal cochlear nucleus of adult cats after unilateral partial cochlear lesions. J. Comp. Neurol., 399, 35 46.
54. Rajan, R. Irvine, D.R.F. (1998b) Neuronal responses across cortical field A1 in plasticity induced by peripheral auditory organ damage. Audiol. Neurootol., 3, 123 144.
55. 1 audiogram data for the barbiturate-anaesthetised domestic cat. Hear. Res., 53, 153 158.
56. Rajan, R., Irvine, D.R.F., Wise, L.Z. Heil, P. (1993) Effect of unilateral partial cochlear lesions in adult cats on the representation of lesioned and unlesioned cochleas in primary auditory cortex. J. Comp. Neurol., 338, 17 49.
57. Rausell, E. Jones, E.G. (1995) Extent of intracortical arborization of thalamocortical axons as a determinant of representational plasticity in monkey somatic sensory cortex. J. Neurosci., 15, 4270 4288.
58. Read, H.L., Winer, J.A. Schreiner, C.E. (2001) Modular organization of intrinsic connections associated with spectral tuning in cat auditory cortex. Proc. Natl Acad. Sci. USA, 98, 8042 8047.
59. Reale, R.A., Brugge, J.F. Feng, J.Z. (1983) Geometry and orientation of neuronal processes in cat primary auditory cortex (AI) related to characteristic-frequency maps. Proc. Natl Acad. Sci. USA, 80, 5449 5453.
60. Richardson, R.J., Blundon, J.A., Bayazitov, I.T. Zakharenko, S.S. (2009) Connectivity patterns revealed by mapping of active inputs on dendrites of thalamorecipient neurons in the auditory cortex. J. Neurosci., 29, 6406 6417.
61. Robertson, D. Irvine, D.R.F. (1989) Plasticity of frequency organization in auditory cortex of guinea pigs with partial unilateral deafness. J. Comp. Neurol., 282, 456 471.
62. Shepherd, R.K. Martin, R.L. (1995) Onset of ototoxicity in the cat is related to onset of auditory function. Hear. Res., 92, 131 142.
63. Snyder, R.L. Sinex, D.G. (2002) Immediate changes in tuning of inferior colliculus neurons following acute lesions of cat spiral ganglion. J. Neurophysiol., 87, 434 452.
64. Suga, N. Ma, X. (2003) Multiparametric corticofugal modulation and plasticity in the auditory system. Nat. Rev. Neurosci., 4, 783 794.
65. Sutter, M.L. Schreiner, C.E. (1995) Topography of intensity tuning in cat primary auditory cortex: single-neuron versus multiple-neuron recordings. J. Neurophysiol., 73, 190 204.
66. Tailby, C., Wright, L.L., Metha, A.B. Calford, M.B. (2005) Activity-dependent maintenance and growth of dendrites in adult cortex. Proc. Natl Acad. Sci. USA, 102, 4631 4636.
67. Thai-Van, H., Micheyl, C., Noreña, A., Veuillet, E., Gabriel, D. Collet, L. (2007) Enhanced frequency discrimination in hearing-impaired individuals: a review of perceptual correlates of central neural plasticity induced by cochlear damage. Hear. Res., 233, 14 22.
68. Turner, C.W., Reiss, L.A.J. Gantz, B.J. (2008) Combined acoustic and electric hearing: preserving residual acoustic hearing. Hear. Res., 242, 164 171.
69. Valentine, P.A. Eggermont, J.J. (2003) Intracortical microstimulation induced changes in spectral and temporal response properties in cat auditory cortex. Hear. Res., 183, 109 125.
70. Velenovsky, D.S., Cetas, J.S., Price, R.O., Sinex, D.G. McMullen, N.T. (2003) Functional subregions in primary auditory cortex defined by thalamocortical terminal arbors: an electrophysiological and anterograde labeling study. J. Neurosci., 23, 308 316.
71. Wallace, M.N., Kitzes, L.M. Jones, E.G. (1991) Intrinsic inter- and intralaminar connections and their relationship to the tonotopic map in cat primary auditory cortex. Exp. Brain Res., 86, 527 544.