Functionally specific oscillatory activity correlates between visual and auditory cortex in the blind

Brain

Volumn 135, Issue 3, 2012, Pages 922-934

  Schepers, Inga M ^a   Hipp, Joerg F ^a,b   Schneider, Till R ^a   Röder, Brigitte ^c   Engel, Andreas K ^a  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c UNIVERSITY OF HAMBURG   (Germany)

Author keywords

congenital blindness; cross modal plasticity; gamma oscillations; magnetoencephalography; visual cortex

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; CLINICAL ARTICLE; COGNITION; CONGENITAL BLINDNESS; CONTROLLED STUDY; EVENT RELATED POTENTIAL; FEMALE; HUMAN; MAGNETOENCEPHALOGRAPHY; MALE; OSCILLATION; PRIORITY JOURNAL; SEMANTICS; TASK PERFORMANCE; VISUAL CORTEX; VISUAL STIMULATION;

EID: 84857583049     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/aws014     Document Type: Article

References (82)

1. Alary F, Duquette M, Goldstein R, Elaine Chapman C, Voss P, La Buissonniere-Ariza V, et al. Tactile acuity in the blind: a closer look reveals superiority over the sighted in some but not all cutaneous tasks. Neuropsychologia 2009;47:2037-43.
2. Amedi A, Floel A, Knecht S, Zohary E, Cohen LG. Transcranial magnetic stimulation of the occipital pole interferes with verbal processing in blind subjects. Nat Neurosci 2004;7:1266-70.
3. Amedi A, Raz N, Pianka P, Malach R, Zohary E. Early 'visual' cortex activation correlates with superior verbal memory performance in the blind. Nat Neurosci 2003;6:758-66.
4. Asanuma C, Stanfield BB. Induction of somatic sensory inputs to the lateral geniculate nucleus in congenitally blind mice and in phenotypically normal mice. Neuroscience 1990;39:533-45.
5. Bavelier D, Neville HJ. Cross-modal plasticity: where and how? Nat Rev Neurosci 2002;3:443-52.
6. Bedny M, Pascual-Leone A, Dodell-Feder D, Fedorenko E, Saxe R. Language processing in the occipital cortex of congenitally blind adults. Proc Natl Acad Sci U S A 2011;108:4429-34.
7. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc B Methodol 1995;57:289-300.
8. Bhattacharjee A, Ye AJ, Lisak JA, Vargas MG, Goldreich D. Vibrotactile masking experiments reveal accelerated somatosensory processing in congenitally blind Braille readers. J Neurosci 2010;30:14288-98.
9. Bruns A, Eckhorn R, Jokeit H, Ebner A. Amplitude envelope correlation detects coupling among incoherent brain signals. Neuroreport 2000;11:1509-14.
10. Büchel C, Price C, Frackowiak RS, Friston K. Different activation patterns in the visual cortex of late and congenitally blind subjects. Brain 1998;121:409-19.
11. Burton H, Sinclair RJ, McLaren DG. Cortical activity to vibrotactile stimulation: an functional MRI study in blind and sighted individuals. Hum Brain Mapp 2004;23:210-28.
12. Cardin JA, Carlen M, Meletis K, Knoblich U, Zhang F, Deisseroth K, et al. Driving fast-spiking cells induces gamma rhythm and controls sensory responses. Nature 2009;459:663-67.
13. Carl C, Acik A, König P, Engel AK, Hipp JF. The saccadic spike artifact in MEG. Neuroimage 2012;59:1657-67.
14. Cohen LG, Celnik P, Pascual-Leone A, Corwell B, Falz L, Dambrosia J, et al. Functional relevance of cross-modal plasticity in blind humans. Nature 1997;389:180-3.
15. Collignon O, Vandewalle G, Voss P, Albouy G, Charbonneau G, Lassonde M, et al. Functional specialization for auditory-spatial processing in the occipital cortex of congenitally blind humans. Proc Natl Acad Sci USA 2011;108:4435-40.
16. Collignon O, Voss P, Lassonde M, Lepore F. Cross-modal plasticity for the spatial processing of sounds in visually deprived subjects. Exp Brain Res 2009;192:343-58.
17. Collins DL, Neelin P, Peters TM, Evans AC. Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. J Comput Assist Tomogr 1994;18:192-205.
18. Crone NE, Boatman D, Gordon B, Hao L. Induced electrocorticographic gamma activity during auditory perception. Clin Neurophysiol 2001;112:565-82.
19. Doehrmann O, Weigelt S, Altmann CF, Kaiser J, Naumer MJ. Audiovisual functional magnetic resonance imaging adaptation reveals multisensory integration effects in object-related sensory cortices. J Neurosci 2010;30:3370-9.
20. Donner TH, Siegel M. A framework for local cortical oscillation patterns. Trends Cogn Sci 2011;15:191-9.
21. Edwards E, Soltani M, Deouell LY, Berger MS, Knight RT. High gamma activity in response to deviant auditory stimuli recorded directly from human cortex. J Neurophysiol 2005;94:4269-80.
22. Elbert T, Sterr A, Rockstroh B, Pantev C, Muller MM, Taub E. Expansion of the tonotopic area in the auditory cortex of the blind. J Neurosci 2002;22:9941-4.
23. Engel AK, Fries P, Singer W. Dynamic predictions: oscillations and synchrony in top-down processing. Nat Rev Neurosci 2001;2:704-16.
24. Genovese CR, Lazar NA, Nichols T. Thresholding of statistical maps in functional neuroimaging using the false discovery rate. Neuroimage 2002;15:870-8.
25. Gougoux F, Belin P, Voss P, Lepore F, Lassonde M, Zatorre RJ. Voice perception in blind persons: a functional magnetic resonance imaging study. Neuropsychologia 2009;47:2967-74.
26. Gougoux F, Lepore F, Lassonde M, Voss P, Zatorre RJ, Belin P. Neuropsychology: pitch discrimination in the early blind. Nature 2004;430:309.
27. Gougoux F, Zatorre RJ, Lassonde M, Voss P, Lepore F. A functional neuroimaging study of sound localization: visual cortex activity predicts performance in early-blind individuals. PLoS Biol 2005;3:324-33.
28. Gross J, Kujala J, Hamalainen M, Timmermann L, Schnitzler A, Salmelin R. Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Natl Acad Sci USA 2001;98:694-9.
29. Hasenstaub A, Shu Y, Haider B, Kraushaar U, Duque A, McCormick DA. Inhibitory postsynaptic potentials carry synchronized frequency information in active cortical networks. Neuron 2005;47:423-35.
30. Hein G, Doehrmann O, Muller NG, Kaiser J, Muckli L, Naumer MJ. Object familiarity and semantic congruency modulate responses in cortical audiovisual integration areas. J Neurosci 2007;27:7881-7.
31. Hipp JF, Engel AK, Siegel M. Oscillatory Synchronization in large-scale cortical networks predicts perception. Neuron 2011;69:387-96.
32. Holmes CJ, Hoge R, Collins L, Woods R, Toga AW, Evans AC. Enhancement of MR images using registration for signal averaging. J Comput Assist Tomogr 1998;22:324-33.
33. Hoogenboom N, Schoffelen JM, Oostenveld R, Parkes LM, Fries P. Localizing human visual gamma-band activity in frequency, time and space. Neuroimage 2006;29:764-73.
34. Hyvärinen J, Carlson S, Hyvärinen L. Early visual deprivation alters modality of neuronal responses in area 19 of monkey cortex. Neuroscience Letters 1981;26:239-43.
35. Izraeli R, Koay G, Lamish M, Heicklen-Klein AJ, Heffner HE, Heffner RS, et al. Cross-modal neuroplasticity in neonatally enucleated hamsters: structure, electrophysiology and behaviour. Eur J Neurosci 2002;15:693-712.
36. Jiang J, Zhu W, Shi F, Liu Y, Li J, Qin W, et al. Thick visual cortex in the early blind. J Neurosci 2009;29:2205-11.
37. Kahn DM, Krubitzer L. Massive cross-modal cortical plasticity and the emergence of a new cortical area in developmentally blind mammals. Proc Natl Acad Sci USA 2002;99:11429-34.
38. Karlen SJ, Kahn DM, Krubitzer L. Early blindness results in abnormal corticocortical and thalamocortical connections. Neuroscience 2006;142:843-58.
39. Klinge C, Eippert F, Röder B, Büchel C. Corticocortical connections mediate primary visual cortex responses to auditory stimulation in the blind. J Neurosci 2010;30:12798-12805.
40. Korte M, Rauschecker JP. Auditory spatial tuning of cortical neurons is sharpened in cats with early blindness. J Neurophysiol 1993;70:1717-21.
41. Lepore N, Voss P, Lepore F, Chou YY, Fortin M, Gougoux F, et al. Brain structure changes visualized in early-and late-onset blind subjects. Neuroimage 2010;49:134-40.
42. Lessard N, Pare M, Lepore F, Lassonde M. Early-blind human subjects localize sound sources better than sighted subjects. Nature 1998;395:278-80.
43. Liu Y, Yu C, Liang M, Li J, Tian L, Zhou Y, et al. Whole brain functional connectivity in the early blind. Brain 2007;130:2085-96.
44. Merabet LB, Pascual-Leone A. Neural reorganization following sensory loss: the opportunity of change. Nat Rev Neurosci 2010;11:44-52.
45. Mitra PP, Pesaran B. Analysis of dynamic brain imaging data. Biophys J 1999;76:691-708.
46. Näätänen R, Picton T. The N1 wave of the human electric and magnetic response to sound: a review and an analysis of the component structure. Psychophysiology 1987;24:375-425.
47. Nolte G. The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys Med Biol 2003;48:3637-52.
48. Noppeney U, Friston KJ, Ashburner J, Frackowiak R, Price CJ. Early visual deprivation induces structural plasticity in gray and white matter. Curr Biol 2005;15:488-90.
49. Noppeney U, Friston KJ, Price CJ. Effects of visual deprivation on the organization of the semantic system. Brain 2003;126:1620-7.
50. Noppeney U, Josephs O, Hocking J, Price CJ, Friston KJ. The effect of prior visual information on recognition of speech and sounds. Cereb Cortex 2008;18:598-609.
51. Noppeney U, Ostwald D, Werner S. Perceptual decisions formed by accumulation of audiovisual evidence in prefrontal cortex. J Neurosci 2010;30:7434-46.
52. Norman JF, Bartholomew AN. Blindness enhances tactile acuity and haptic 3-D shape discrimination. Atten Percept Psychophys 2011;73:2323-31.
53. Oostenveld R, Fries P, Maris E, Schoffelen JM. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011;2011:1-9.
54. Park HJ, Lee JD, Kim EY, Park B, Oh MK, Lee S, et al. Morphological alterations in the congenital blind based on the analysis of cortical thickness and surface area. Neuroimage 2009;47:98-106.
55. Pavani F, Röder B. Crossmodal plasticity as a consequence of sensory loss: insights from blindness and deafness. In: Stein BE, editor. The new handbook of multisensory processes. MIT Press, 2012.
56. Pollok B, Schnitzler I, Stoerig P, Mierdorf T, Schnitzler A. Image-to-sound conversion: experience-induced plasticity in auditory cortex of blindfolded adults. Exp Brain Res 2005;167:287-91.
57. Rauschecker JP. Compensatory plasticity and sensory substitution in the cerebral cortex. Trends Neurosci 1995;18:36-43.
58. Raz N, Amedi A, Zohary E. V1 activation in congenitally blind humans is associated with episodic retrieval. Cereb Cortex 2005;15:1459-68.
59. Renier LA, Anurova I, De Volder AG, Carlson S, Vanmeter J, Rauschecker JP. Preserved functional specialization for spatial processing in the middle occipital gyrus of the early blind. Neuron 2010;68:138-48.
60. Röder B, Demuth L, Streb J, Rösler F. Semantic and morpho-syntactic priming in auditory word recognition in congenitally blind adults. Lang Cogn Processes 2003;18:1-20.
61. Röder B, Rösler F, Hennighausen E, Nacker F. Event-related potentials during auditory and somatosensory discrimination in sighted and blind human subjects. Brain Res Cogn Brain Res 1996;4:77-93.
62. Röder B, Stock O, Bien S, Neville H, Rösler F. Speech processing activates visual cortex in congenitally blind humans. Eur J Neurosci 2002;16:930-6.
63. Röder B, Teder-Salejarvi W, Sterr A, Rösler F, Hillyard SA, Neville HJ. Improved auditory spatial tuning in blind humans. Nature 1999;400:162-6.
64. Rösler F, Röder B, Heil M, Hennighausen E. Topographic differences of slow event-related brain potentials in blind and sighted adult human subjects during haptic mental rotation. Brain Res Cogn Brain Res 1993;1:145-59.
65. Saalmann YB, Kastner S. Cognitive and perceptual functions of the visual thalamus. Neuron 2011;71:209-23.
66. Sadato N, Pascual-Leone A, Grafman J, Deiber MP, Ibanez V, Hallett M. Neural networks for Braille reading by the blind. Brain 1998;121(Pt 7):1213-29.
67. Sadato N, Pascual-Leone A, Grafman J, Ibanez V, Deiber MP, Dold G, et al. Activation of the primary visual cortex by Braille reading in blind subjects. Nature 1996;380:526-8.
68. Schneider TR, Lorenz S, Senkowski D, Engel AK. Gamma-band activity as a signature for cross-modal priming of auditory object recognition by active haptic exploration. J Neurosci 2011;31:2502-10.
69. Schoffelen JM, Gross J. Source connectivity analysis with MEG and EEG. Hum Brain Mapp 2009;30:1857-65.
70. Sherman SM. The thalamus is more than just a relay. Curr Opin Neurobiol 2007;17:417-22.
71. Shimony JS, Burton H, Epstein AA, McLaren DG, Sun SW, Snyder AZ. Diffusion tensor imaging reveals white matter reorganization in early blind humans. Cereb Cortex 2006;16:1653-61.
72. Singer W, Gray CM. Visual feature integration and the temporal correlation hypothesis. Annu Rev Neurosci 1995;18:555-86.
73. Talairach J, Tournoux P. Co-planar stereotaxic atlas of the human brain: 3-Dimensional proportional system-An approach to cerebral imaging. New York, NY: Thieme Medical Publishers; 1988.
74. Thomson DJ. Spectrum estimation and harmonic analysis. Proc IEEE 1982;70:1055-96.
75. Van Boven RW, Hamilton RH, Kauffman T, Keenan JP, Pascual-Leone A. Tactile spatial resolution in blind braille readers. Neurology 2000;54:2230-6.
76. Van Veen BD, van Drongelen W, Yuchtman M, Suzuki A. Localization of brain electrical activity via linearly constrained minimum variance spatial filtering. IEEE Trans Biomed Eng 1997;44:867-80.
77. Veraart C, De Volder AG, Wanet-Defalque MC, Bol A, Michel C, Goffinet AM. Glucose utilization in human visual cortex is abnormally elevated in blindness of early onset but decreased in blindness of late onset. Brain Res 1990;510:115-21.
78. Voss P, Lassonde M, Gougoux F, Fortin M, Guillemot JP, Lepore F. Earlyand late-onset blind individuals show supra-normal auditory abilities in far-space. Curr Biol 2004;14:1734-8.
79. Wan CY, Wood AG, Reutens DC, Wilson SJ. Congenital blindness leads to enhanced vibrotactile perception. Neuropsychologia 2010a;48:631-5.
80. Wan CY, Wood AG, Reutens DC, Wilson SJ. Early but not late-blindness leads to enhanced auditory perception. Neuropsychologia 2010b;48:344-8.
81. Weeks R, Horwitz B, Aziz-Sultan A, Tian B, Wessinger CM, Cohen LG, et al. A positron emission tomographic study of auditory localization in the congenitally blind. J Neurosci 2000;20:2664-72.
82. Yaka R, Yinon U, Wollberg Z. Auditory activation of cortical visual areas in cats after early visual deprivation. Eur J Neurosci 1999;11:1301-12.