Somatosensory and visual crossmodal plasticity in the anterior auditory field of early-deaf cats

Hearing Research

Volumn 280, Issue 1-2, 2011, Pages 38-47

  Meredith, M Alex ^a   Lomber, Stephen G ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUDITORY CORTEX; AUDITORY DISCRIMINATION; AUDITORY LATERALIZATION; AUDITORY RESPONSE; AUDITORY STIMULATION; AUDITORY THRESHOLD; AUTONOMIC INNERVATION; CAT; CONTROLLED STUDY; EVOKED SOMATOSENSORY RESPONSE; EVOKED VISUAL RESPONSE; HEARING IMPAIRMENT; NERVE CELL PLASTICITY; NONHUMAN; OTOTOXICITY; PRIORITY JOURNAL; RECEPTIVE FIELD; SOMATOSENSORY SYSTEM; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ADAPTATION, PHYSIOLOGICAL; AGING; ANIMALS; AUDITORY CORTEX; CATS; DEAFNESS; ELECTROPHYSIOLOGICAL PHENOMENA; MODELS, ANIMAL; NEURONAL PLASTICITY; PHOTIC STIMULATION; SENSORY RECEPTOR CELLS; SOMATOSENSORY CORTEX; VISUAL CORTEX;

EID: 80053051799     PISSN: 03785955     EISSN: 18785891     Source Type: Journal    
DOI: 10.1016/j.heares.2011.02.004     Document Type: Article

References (79)

1. Aitkin L.M., Kenyon C.E., Philpott P. The representation of the auditory and somatosensory systems in the external nucleus of the cat inferior colliculus. J. Comp. Neurol. 1981, 196:25-40.
2. Allman B.L., Keniston L.P., Meredith M.A. Adult-deafness induces somatosensory conversion of ferret auditory cortex. Proc. Natl. Acad. Sci. USA 2009, 106:5925-5930.
3. Allman B.L., Keniston L.P., Meredith M.A. Not just for bimodal neurons anymore: the contribution of unimodal neurons to cortical multisensory processing. Brain Topogr. 2009, 21:157-167.
4. Auer E.T., Bernstein L.E., Sunkarat W., Singh M. Vibrotactile activation of the auditory cortices in deaf versus hearing adults. Neuroreport 2007, 18:645-648.
5. Bavelier D., Neville H.J. Cross-modal plasticity: where and how?. Nat. Rev. Neurosci. 2002, 3:443-452.
6. Bavelier D., Tomann A., Hutton C., Mitchell T., Corina D., Liu G., Neville H. Visual attention to the periphery is enhanced in congenitally deaf individuals. J. Neurosci. 2000, 20(RC93):1-6.
7. Budinger E., Heil P., Hess A., Scheich H. Multisensory processing via early cortical stages: connections of the primary auditory cortical field with other sensory systems. Neuroscience 2006, 28:1064-1083.
8. Burton H., Kopf E.M. Ipsilateral cortical connections from the second and fourth somatosensory areas of the cat. J. Comp. Neurol. 1984, 225:527-553.
9. Carrasco A., Lomber S.G. Differential modulatory influences between primary auditory cortex and the anterior auditory field. J. Neurosci. 2009, 29:8350-8362.
10. Chang E.F., Merzenich M.M. Environmental noise retards auditory cortical development. Science 2003, 300:498-502.
11. Clemo H.R., Allman B.L., Donlan M.A., Meredith M.A. Sensory and multisensory representations within the cat rostral suprasylvian cortices. J. Comp. Neurol. 2007, 503:110-127.
12. Cynader M., Mitchell D.E. Prolonged sensitivity to monocular deprivation in dark-reared cats. J. Neurophysiol. 1980, 43:1026-1040.
13. Cynader M., Timney B., Mitchell D.E. Period of susceptibility of kitten visual cortex to the effects of monocular deprivation extends beyond six months of age. Brain Res. 1980, 191:545-550.
14. Dinse H.R., Reuter G., Cords S.M., Godde B., Hilger T., Lenarz T. Optical imaging of cat auditory cortical organization after electrical stimulation of a multichannel cochlear implant: differential effects of acute and chronic stimulation. Am. J. Otol. 1997, 18:S17-S18.
15. Dinse H.R., Godde B., Reuter G., Cords S.M., Hilger T. Auditory cortical plasticity under operation: reorganization of auditory cortex induced by electric cochlear stimulation reveals adaptation to altered sensory input statistics. Speech Commun. 2003, 41:201-219.
16. Fallon J.B., Irvine D.R., Shepherd R.K. Cochlear implant use following neonatal deafness influences the cochleotopic organization of primary auditory cortex in cats. J. Comp. Neurol. 2009, 512:101-114.
17. Finney E.M., Fine I., Dobkins K.R. Visual stimuli activate auditory cortex in the deaf. Nat. Neurosci. 2001, 4:1171-1173.
18. Foxe J.J., Morocz I.A., Murray M.M., Higgins B.A., Javitt D.C., Schroeder C.E. Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res.Cogn. Brain Res. 2000, 10:77-83.
19. Frost D.O., Metin C. Induction of functional retinal projections to the somatosensory system. Nature 1985, 317:162-164.
20. He H.Y., Hodos W., Quinlan E.M. Visual deprivation reactivates rapid ocular dominance plasticity in adult visual cortex. J. Neurosci. 2006, 26:2951-2955.
21. He H.Y., Ray B., Dennis K., Quinlan E.M. Experience-dependent recovery of vision following chronic deprivation amblyopia. Nat. Neurosci. 2007, 10:1134-1136.
22. Hickok G., Poeppel D., Clark K., Buxton R.B., Rowley H.A., Roberts T.P. Sensory mapping in a congenitally deaf subject: MEG and fMRI studies of cross-modal non-plasticity. Hum. Brain Mapp. 1997, 5:437-444.
23. Hubel D.H., Wiesel T.N. Receptive fields and functional architecture in two non-striate visual areas (18 and 19) of the cat. J. Neurophysiol. 1965, 28:229-289.
24. Hunt D.L., Yamoah E.N., Krubitzer L. Multisensory plasticity in congenitally deaf mice: how are cotical areas functionally specified?. Neuroscience 2006, 139:1507-1524.
25. Imaizumi K., Priebe N.J., Crum P.A., Bedenbaugh P.H., Cheung S.W., Schreiner C.E. Modular functional organization of cat anterior auditory field. J. Neurophysiol. 2004, 92:444-457.
26. Imig T.J., Reale R.A. Patterns of cortico-cortical connections related to tonotopic maps in cat auditory cortex. J. Comp. Neurol. 1980, 192:293-332.
27. Kaas J.H., Nelson R.J., Sur M., Lin C.-S., Merzenich M.M. Multiple representations of the body within the primary somatosensory cortex of primates. Science 1979, 204:521-523.
28. Kanold P.O., Young E.D. Proprioceptive information from the pinna provides somatosensory input to cat dorsal cochlear nucleus. J. Neurosci. 2001, 21:7848-7858.
29. Kayser C., Petkov C.I., Logothetis N.K. Visual modulation of neurons in auditory cortex. Cereb. Cortex 2008, 18:1560-1574.
30. King A.J., Parsons C.H. Improved auditory spatial acuity in visually deprived ferrets. Eur. J. Neurosci. 1999, 11:3945-3956.
31. Kitzes L.M., Semple M.N. Single-unit responses in the inferior colliculus: effects of neonatal unilateral cochlear ablation. J. Neurophysiol. 1985, 53:1483-1500.
32. Knight P.L. Representation of the cochlea within the anterior auditory field (AAF) of the cat. Brain Res. 1977, 130:447-467.
33. Korte M., Rauschecker J.P. Auditory spatial tuning of cortical neurons is sharpened in cats with early blindness. J. Neurophysiol. 1993, 70:1717-1721.
34. Kral A. Unimodal and cross-modal plasticity in the 'deaf' auditory cortex. Int. J. Audiol. 2007, 46:479-493.
35. Kral A., Eggermont J.J. What's to lose and what's to learn: development under auditory derivation, cochlear implants and limits of cortical plasticity. Brain Res. Rev 2007, 56:259-269.
36. Kral A., Hartmann R., Tillein J., Heid S., Klinke R. Congenital auditory deprivation reduces synaptic activity within the auditory cortex in a layer specific manner. Cereb. Cortex 2000, 10:714-726.
37. Kral A., Schroder J.H., Klinke R., Engel A.K. Absence of cross-modal reorganization in the primary auditory cortex of congenitally deaf cats. Exp. Brain Res. 2003, 153:605-613.
38. Kral A., Tillein J., Heid J., Hartmann R., Klinke R. Postnatal cortical development in congenital auditory deprivation. Cereb. Cortex 2005, 15:552-562.
39. Lee C.C., Imaizumi K., Schreiner C.E., Winer J.A. Concurrent tonotopic processing streams in auditory cortex. Cereb. Cortex 2004, 14:441-451.
40. Lee C.C., Winer J.A. Principles governing auditory cortex connections. Cereb. Cortex 2005, 15:1804-1814.
41. Levanen S., Hamdof D. Feeling vibrations: enhanced tactile sensitivity in congenitally deaf humans. Neurosci. Lett. 2001, 301:75-77.
42. Lomber S.G., Meredith M.A., Kral A. Crossmodal Plasticity specific auditory cortices underlies compensatory visual functions Deaf. Nat. Neurosci. 2010, 13:1421-1427.
43. Mellott J.G., Van der Gucht E., Lee C.C., Carrasco A., Winer J.A., Lomber S.G. Areas of cat auditory cortex as defined by neurofilament proteins expressing SMI-32. Hear. Res. 2010, 267:119-136.
44. Merabet L.B., Pascual-Leone A. Neural reorganization following sensory loss: the opportunity of change. Nat. Rev. Neurosci. 2010, 11:44-52.
45. Meredith, M.A., Kryklywy, J., McMillan, A.J., Malhotra, S., Lum-Tai, R., Lomber, S.G. Crossmodal reorganization in the early-deaf switches sensory, but not behavioral roles of auditory cortex. Proc. Natl. Acad. Sci. USA, in press.
46. Meredith M.A., Lomber S.G. Crossmodal reorganization of the anterior auditory field (AAF) in postnatally deafened cats. Soc. Neurosci. Abstr. 2009, 39. 260.13.
47. Merzenich M.M., Knight P.L., Roth G.L. Representation of cochlea within primary auditory cortex in the cat. J. Neurophysiol. 1975, 38:231-249.
48. Middlebrooks J.C., Dykes R.W., Merzenich M.M. Binaural response-specific bands in primary auditory cortex (A1) of the cat: topographic organization orthogonal to isofrequency contours. Brain Res. 1980, 181:31-48.
49. Moore D.R. Auditory brainstem of the ferret: long survival following cochlear removal progressively changes projections from the cochlea nucleus to the inferior colliculus. J. Comp. Neurol. 1994, 339:301-310.
50. Moore D.R., Russell F.A., Cathcart N.C. Lateral superior olive projections to the inferior colliculus in normal and unilaterally deafened ferrets. J. Comp. Neurol. 1994, 357:204-216.
51. Mower G.D. The effect of dark rearing on the time course of the critical period in cat visual cortex. Brain Res. Dev. Brain Res. 1991, 58:151-158.
52. Mower G.D., Caplan C.J., Christen W.G., Duffy F.H. Dark rearing prolongs physiological but not anatomical plasticity of the cat visual cortex. J. Comp. Neurol. 1985, 235:448-466.
53. Mower G.D., Christen W.G., Caplan C.J. Very brief visual experience eliminates plasticity in the cat visual cortex. Science 1983, 221:178-180.
54. Olson C.R., Graybiel A.M. Ectosylvian visual area of the cat: location, retinotopic organization and connections. J. Comp. Neurol. 1987, 261:277-294.
55. Orban G.A., Kennedy H., Maes H. Functional changes across the 17-18 border in the cat. Exp. Brain Res. 1980, 39:177-186.
56. Phillips D.P., Irvine D.R. Properties of single neurons in the anterior auditory field (AAF) of cat cerebral cortex. Brain Res. 1982, 248:237-244.
57. Piche M., Chalbot N., Bronchti G., Miceli D., Lepore F., Guillemot J.P. Auditory responses in the visual cortex of neonatally enucleated rats. Neuroscience 2007, 144:1144-1156.
58. Raggio M.W., Schreiner C.E. Neuronal responses in cat primary auditory cortex to electrical cochlear stimulation. III. Activation patterns in short- and long-term deafness. J. Neurophysiol. 1999, 82:3506-3526.
59. Rauschecker J.P. Compensatory plasticity and sensory substitution in the cerebral cortex. Trends Neurosci. 1995, 18:36-43.
60. Rauschecker J.P., Kniepert U. Auditory localization behaviour in visually deprived cats. Eur. J. Neurosci. 1994, 6:149-160.
61. Rauschecker J.P., Korte M. Auditory compensation for early blindness in cat cerebral cortex. J. Neurosci. 1993, 13:4538-4548.
62. Reale R.A., Imig T.J. Tonotopic organization in auditory cortex of the cat. J. Comp. Neurol. 1980, 192:265-291.
63. Roe A.W., Pallas S.L., Kwon Y.H., Sur M. Visual projections routed to the auditory pathway in ferrets: receptive fields of visual neurons in primary auditory cortex. J. Neurosci. 1992, 12:3651-3664.
64. Rouiller E.M., Simm G.M., Villa A.E., de Ribaupierre Y., de Ribaupierre F. Auditory corticocortical interconnections in the cat: evidence for parallel and hierarchical arrangement of the auditory cortical areas. Exp. Brain Res. 1991, 86:483-505.
65. Sanchez-Vives M.V., Nowak L.G., Descalzo V.F., Garcia-Velasco J.V., Gallego R., Berbel P. Crossmodal audio-visual interactions in the primary visual cortex of the visually deprived cat: a physiological and anatomical study. Prog. Brain Res. 2006, 155:287-311.
66. A receptors in the auditory cortex. Cereb. Cortex 2008, 18:2855-2867.
67. Scannell J.W., Sengpiel F., Tovee M., Benson P.J., Blakemore C., Young M.P. Visual motion processing in the anterior ectosylvian sulcus of the cat. J. Neurophysiol. 1996, 76:895-907.
68. Shepherd R.K., Hardie N.A. Deafness-induced changes in the auditory pathway: implications for cochlear implants. Audiol. Neurootol. 2001, 6:305-318.
69. Shipley C., Buchwald J.S., Norman R., Guthrie D. Brain stem auditory evoked response development in the kitten. Brain Res. 1980, 182:313-326.
70. Shore S.E., Vass Z., Wys N.L., Altschuler R.A. Trigeminal ganglion innervates the auditory brainstem. J. Comp. Neurol. 2000, 419:271-285.
71. Shore S.E., Koehler S., Oldakowski M., Hughes L.F., Syed S. Dorsal cochlear nucleus responses to somatosensory stimulation are enhanced after noise-induced hearing loss. Eur. J. Neurosci. 2008, 27:155-168.
72. Stein B.E., Meredith M.A., Wallace M.T. The visually responsive neuron and beyond: multisensory integration in cat and monkey. Progress in Brain Research 1993, vol. 95:79-90. Elsevier. T.P. Hicks, S. Molochnikoff, T. Ono (Eds.).
73. Sur M., Garraghty P.E., Roe A.W. Experimentally induced visual projections into auditory thalamus and cortex. Science 1988, 242:1437-1441.
74. Tillien J., Hubka P., Syed E., Hartmann R., Engel A.K., Kral A. Cortical representation of interaural time difference in congenital deafness. Cereb. Cortex 2010, 20:492-506.
75. Timney B., Mitchell D.E., Cynader M. Behavioral evidence for prolonged sensitivity to effects of monocular deprivation in dark-reared cats. J. Neurophysiol. 1980, 43:1041-1054.
76. Tusa R.J., Rosenquist A.C., Palmer L.A. Retinotopic organization of areas 18 and 19 in the cat. J. Comp. Neurol. 1979, 185:657-678.
77. Wandell B.A., Smirnakis S.M. Plasticity and stability of visual field maps in adult primary visual cortex. Nat. Rev. Neurosci. 2009, 10:873-884.
78. Xu H., Kotak V.C., Sanes D.H. Conductive hearing loss disrupts synaptic and spike adaptation in the developing auditory cortex. J. Neurosci. 2007, 27:9417-9426.
79. Xu S.A., Shepherd R.K., Chen Y., Clark G.M. Profound hearing loss in the cat following the single co-administration of kanamycin and ethacrynic acid. Hear. Res. 1993, 70:205-215.