Bilateral input protects the cortex from unilaterally-driven reorganization in children who are deaf

Brain

Volumn 136, Issue 5, 2013, Pages 1609-1625

  Gordon, Karen A ^a,b   Wong, Daniel D E ^a,c   Papsin, Blake C ^a,b  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

auditory brain; beamformer; cochlear implantation; EEG dipole source localization; hearing loss

Indexed keywords

ARTICLE; AUDITORY CORTEX; AUDITORY LATERALIZATION; AUDITORY STIMULATION; BRAIN CORTEX; BRAIN PROTECTION; CHILD; CLINICAL ARTICLE; COCHLEA PROSTHESIS; CONTROLLED STUDY; ELECTRODE; ELECTROENCEPHALOGRAPHY; HEARING IMPAIRMENT; HEMISPHERE; HUMAN; PRIORITY JOURNAL; SPEECH PERCEPTION;

EID: 84877305570     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awt052     Document Type: Article

References (74)

1. Bavelier D, Neville HJ. Cross-modal plasticity: where and how? Nat Rev Neurosci 2002; 3: 443-52.
2. Beijen JW, Mylanus EA, Leeuw AR, Snik AF. Should a hearing aid in the contralateral ear be recommended for children with a unilateral cochlear implant? Ann Otol Rhinol Laryngol 2008; 117: 397-403.
3. Bess FH, Tharpe AM, Gibler AM. Auditory performance of children with unilateral sensorineural hearing loss. Ear Hear 1986; 7: 20-6.
4. Burton H, Firszt JB, Holden T, Agato A, Uchanski RM. Activation lateralization in human core, belt, and parabelt auditory fields with unilateral deafness compared to normal hearing. Brain Res 2012; 1454: 33-47.
5. Chadha NK, Papsin BC, Jiwani S, Gordon KA. Speech detection in noise and spatial unmasking in children with simultaneous versus sequential bilateral cochlear implants. Otol Neurotol 2011; 32: 1057-64.
6. Crane BT, Gottschalk B, Kraut M, Aygun N, Niparko JK. Magnetic resonance imaging at 1.5 T after cochlear implantation. Otol Neurotol 2010; 31: 1215-20.
7. Firszt JB, Ulmer JL, Gaggl W. Differential representation of speech sounds in the human cerebral hemispheres. Anat Rec A Discov Mol Cell Evol Biol 2006; 288: 345-57.
8. Fujiki N, Naito Y, Nagamine T, Shiomi Y, Hirano S, Honjo I, et al. Influence of unilateral deafness on auditory evoked magnetic field. Neuroreport 1998; 9: 3129-33.
9. Gordon KA, Papsin BC. Benefits of short interimplant delays in children receiving bilateral cochlear implants. Otol Neurotol 2009; 30: 319-31.
10. Gordon KA, Papsin BC, Harrison RV. Activity-dependent developmental plasticity of the auditory brain stem in children who use cochlear implants. Ear Hear 2003; 24: 485-500.
11. Gordon KA, Papsin BC, Harrison RV. Effects of cochlear implant use on the electrically evoked middle latency response in children. Hear Res 2005; 204: 78-89.
12. Gordon KA, Papsin BC, Harrison RV. An evoked potential study of the developmental time course of the auditory nerve and brainstem in children using cochlear implants. Audiol Neurootol 2006; 11: 7-23.
13. Gordon KA, Valero J, Papsin BC. Auditory brainstem activity in children with 9-30 months of bilateral cochlear implant use. Hear Res 2007a; 233: 97-107.
14. Gordon KA, Valero J, Papsin BC. Binaural processing in children using bilateral cochlear implants. Neuroreport 2007b; 18: 613-7.
15. Gordon KA, Papsin BC, Harrison RV. Auditory brainstem activity and development evoked by apical versus basal cochlear implant electrode stimulation in children. Clin Neurophysiol 2007c; 118: 1671-84.
16. Gordon KA, Valero J, van Hoesel R, Papsin BC. Abnormal timing delays in auditory brainstem responses evoked by bilateral cochlear implant use in children. Otol Neurotol 2008; 29: 193-8.
17. Gordon KA, Salloum C, Toor GS, van Hoesel R, Papsin BC. Binaural interactions develop in the auditory brainstem of children who are deaf: effects of place and level of bilateral electrical stimulation. J Neurosci 2012; 32: 4212-23.
18. Grothe B, Pecka M, McAlpine D. Mechanisms of sound localization in mammals. Physiol Rev 2010; 90: 983-1012.
19. Hanss J, Veuillet E, Adjout K, Besle J, Collet L, Thai-Van H. The effect of long-term unilateral deafness on the activation pattern in the auditory cortices of French-native speakers: influence of deafness side. BMC Neurosci 2009; 10: 23.
20. Hebb D. The organization of behavior: a neuropsychological theory. New York: Wiley (reprinted by Lawrence Erlbaum Associates, 2002); 1949.
21. Hine J, Debener S. Late auditory evoked potentials asymmetry revisited. Clin Neurophysiol 2007; 118: 1274-85.
22. Hine J, Thornton R, Davis A, Debener S. Does long-term unilateral deafness change auditory evoked potential asymmetries? Clin Neurophysiol 2008; 119: 576-86.
23. Johnson BW, Hautus MJ. Processing of binaural spatial information in human auditory cortex: neuromagnetic responses to interaural timing and level differences. Neuropsychologia 2010; 48: 2610-9.
24. Khosla D, Ponton CW, Eggermont JJ, Kwong B, Don M, Vasama JP. Differential ear effects of profound unilateral deafness on the adult human central auditory system. J Assoc Res Otolaryngol 2003; 4: 235-49.
25. Kitzes LM, Kageyama GH, Semple MN, Kil J. Development of ectopic projections from the ventral cochlear nucleus to the superior olivary Kral A. Single-sided deafness leads to unilateral aural preference within an early sensitive period. Brain 2013; doi: 10.1093/brain/aws305. [Epub ahead of print].
26. Kral A, O'Donoghe GM. Profound deafness in childhood. N Engl J Med 2010; 363: 1438-50.
27. Kral A, Hartmann R, Tillein J, Heid S, Klinke R. Hearing after congenital deafness: central auditory plasticity and sensory deprivation. Cereb Cortex 2002; 12: 797-807.
28. Krumbholz K, Hewson-Stoate N, Schonwiesner M. Cortical response to auditory motion suggests an asymmetry in the reliance on inter-hemispheric connections between the left and right auditory cortices. J Neurophysiol 2007; 97: 1649-55.
29. Langers DR, van Dijk P, Backes WH. Lateralization, connectivity and plasticity in the human central auditory system. Neuroimage 2005; 28: 490-9.
30. Lazard DS, Collette JL, Perrot X. Speech processing: from peripheral to hemispheric asymmetry of the auditory system. Laryngoscope 2012; 122: 167-73.
31. Lazard DS, Giraud AL, Truy E, Lee HJ. Evolution of non-speech sound memory in postlingual deafness: implications for cochlear implant rehabilitation. Neuropsychologia 2011; 49: 2475-82.
32. Lee DS, Lee JS, Oh SH, Kim SK, Kim JW, Chung JK, et al. Deafness: crossmodal plasticity and cochlear implants. Nature 2001; 409: 149-50.
33. Leijon A. Quantization error in clinical pure-tone audiometry. Scand Audiol 1992; 21: 103-8.
34. Li LP, Shiao AS, Chen LF, Niddam DM, Chang SY, Lien CF, et al. Healthy-side dominance of middle-and long-latency neuromagnetic fields in idiopathic sudden sensorineural hearing loss. Eur J Neurosci 2006; 24: 937-46.
35. Litovsky RY, Johnstone PM, Godar S, Agrawal S, Parkinson A, Peters R, et al. Bilateral cochlear implants in children: localization acuity measured with minimum audible angle. Ear Hear 2006; 27: 43-59.
36. Lomber SG, Meredith MA, Kral A. Cross-modal plasticity in specific auditory cortices underlies visual compensations in the deaf. Nat Neurosci 2010; 13: 1421-7.
37. Majdani O, Rau TS, Gotz F, Zimmerling M, Lenarz M, Lenarz T, et al. Artifacts caused by cochlear implants with non-removable magnets in 3T MRI: phantom and cadaveric studies. Eur Arch Otorhinolaryngol 2009; 266: 1885-90.
38. Malhotra S, Lomber SG. Sound localization during homotopic and heterotopic bilateral cooling deactivation of primary and nonprimary auditory cortical areas in the cat. J Neurophysiol 2007; 97: 26-43.
39. Malhotra S, Stecker GC, Middlebrooks JC, Lomber SG. Sound localization deficits during reversible deactivation of primary auditory cortex and/or the dorsal zone. J Neurophysiol 2008; 99: 1628-42.
40. Moore DR. Anatomy and physiology of binaural hearing. Audiology 1991; 30: 125-34.
41. Moore DR. Auditory brainstem of the ferret: long survival following cochlear removal progressively changes projections from the cochlear nucleus to the inferior colliculus. J Comp Neurol 1994; 339: 301-10.
42. Moore DR, Kowalchuk NE. Auditory brainstem of the ferret: effects of unilateral cochlear lesions on cochlear nucleus volume and projections to the inferior colliculus. J Comp Neurol 1988; 272: 503-15.
43. Moore JK. Maturation of human auditory cortex: implications for speech perception. Ann Otol Rhinol Laryngol Suppl 2002; 189: 7-10.
44. Moore JK, Guan YL. Cytoarchitectural and axonal maturation in human auditory cortex. J Assoc Res Otolaryngol 2001; 2: 297-311.
45. Nordeen KW, Killackey HP, Kitzes LM. Ascending projections to the inferior colliculus following unilateral cochlear ablation in the neonatal gerbil, Meriones unguiculatus. J Comp Neurol 1983; 214: 144-53.
46. Palomaki K, Alku P, Makinen V, May P, Tiitinen H. Sound localization in the human brain: neuromagnetic observations. Neuroreport 2000; 11: 1535-8.
47. Palomaki KJ, Tiitinen H, Makinen V, May PJ, Alku P. Spatial processing in human auditory cortex: the effects of 3D, ITD, and ILD stimulation techniques. Brain Res Cogn Brain Res 2005; 24: 364-79.
48. Papsin BC, Gordon KA. Cochlear implants for children with severe-to-profound hearing loss. N Engl J Med 2007; 357: 2380-7.
49. Ponton C, Eggermont JJ, Khosla D, Kwong B, Don M. Maturation of human central auditory system activity: separating auditory evoked potentials by dipole source modeling. Clin Neurophysiol 2002; 113: 407-20.
50. Ponton CW, Vasama JP, Tremblay K, Khosla D, Kwong B, Don M. Plasticity in the adult human central auditory system: evidence from late-onset profound unilateral deafness. Hear Res 2001; 154: 32-44.
51. Popescu MV, Polley DB. Monaural deprivation disrupts development of binaural selectivity in auditory midbrain and cortex. Neuron 2010; 65: 718-31.
52. Riedel H, Kollmeier B. Auditory brain stem responses evoked by lateralized clicks: is lateralization extracted in the human brain stem? Hear Res 2002; 163: 12-26.
53. Roth BJ, Balish M, Gorbach A, Sato S. How well does a three-sphere model predict positions of dipoles in a realistically shaped head? Electroencephalogr Clin Neurophysiol 1993; 87: 175-84.
54. Salloum CA, Valero J, Wong DD, Papsin BC, van Hoesel R, Gordon KA. Lateralization of interimplant timing and level differences in children who use bilateral cochlear implants. Ear Hear 2010; 31: 441-56.
55. Sandmann P, Eichele T, Buechler M, Debener S, Jancke L, Dillier N, et al. Evaluation of evoked potentials to dyadic tones after cochlear implantation. Brain 2009; 132 (Pt 7): 1967-79.
56. Sandmann P, Dillier N, Eichele T, Meyer M, Kegel A, Pascual-Marqui RD, et al. Visual activation of auditory cortex reflects maladaptive plasticity in cochlear implant users. Brain 2012; 135 (Pt 2): 555-68.
57. Schonwiesner M, Krumbholz K, Rubsamen R, Fink GR, von Cramon DY. Hemispheric asymmetry for auditory processing in the human auditory brain stem, thalamus, and cortex. Cereb Cortex 2007; 17: 492-9.
58. Sharma A, Dorman MF, Spahr AJ. Rapid development of cortical auditory evoked potentials after early cochlear implantation. Neuroreport 2002; 13: 1365-8.
59. Smith ZM, Delgutte B. Using evoked potentials to match interaural electrode pairs with bilateral cochlear implants. J Assoc Res Otolaryngol 2007; 8: 134-51.
60. Snyder RL, Rebscher SJ, Cao KL, Leake PA, Kelly K. Chronic intracochlear electrical stimulation in the neonatally deafened cat. I: expansion of central representation. Hear Res 1990; 50: 7-33.
61. Sparreboom M, Beynon AJ, Snik AF, Mylanus EA. Electrically evoked auditory brainstem responses in children with sequential bilateral cochlear implants. Otol Neurotol 2010; 31: 1055-61.
62. Takesian AE, Kotak VC, Sanes DH. Developmental hearing loss disrupts synaptic inhibition: implications for auditory processing. Future Neurol 2009; 4: 331-49.
63. Thompson SK, von Kriegstein K, Deane-Pratt A, Marquardt T, Deichmann R, Griffiths TD, et al. Representation of interaural time delay in the human auditory midbrain. Nat Neurosci 2006; 9: 1096-8.
64. Tibbetts K, Ead B, Umansky A, Coalson R, Schlaggar BL, Firszt JB, et al. Interregional brain interactions in children with unilateral hearing loss. Otolaryngol Head Neck Surg 2011; 144: 602-11.
65. Van Deun L, van Wieringen A, Scherf F, Deggouj N, Desloovere C, Offeciers FE, et al. Earlier intervention leads to better sound localization in children with bilateral cochlear implants. Audiol Neurootol 2010; 15: 7-17.
66. Van Deun L, van Wieringen A, Francart T, Scherf F, Dhooge IJ, Deggouj N, et al. Bilateral cochlear implants in children: binaural unmasking. Audiol Neurootol 2009; 14: 240-7.
67. Vasama JP, Makela JP. Auditory cortical responses in humans with profound unilateral sensorineural hearing loss from early childhood. Hear Res 1997; 104: 183-90.
68. Vrba J, Robinson SE. Signal processing in magnetoencephalography. Methods 2001; 25: 249-71.
69. Wendel K, Vä isä nen J, Seemann G, Hyttinen J, Malmivuo J. The influence of age and skull conductivity on surface and subdermal bipolar EEG leads. Comput. Intell Neurosci 2010; 2010: 397272.
70. Wilke M, Holland SK, Altaye M, Gaser C. Template-O-Matic: a toolbox for creating customized pediatric templates. Neuroimage 2008; 41: 903-13.
71. Wolfe J, Baker S, Caraway T, Kasulis H, Mears A, Smith J, et al. 1-year postactivation results for sequentially implanted bilateral cochlear implant users. Otol Neurotol 2007; 28: 589-96.
72. Wong DD, Gordon KA. Beamformer suppression of cochlear implant artifacts in an electroencephalography dataset. IEEE Trans Biomed Eng 2009; 56: 2851-7.
73. Zatorre RJ, Penhune VB. Spatial localization after excision of human auditory cortex. J Neurosci 2001; 21: 6321-8.
74. Zatorre RJ, Belin P. Spectral and temporal processing in human auditory cortex. Cereb Cortex 2001; 11: 946-53.