Effects of parietal TMS on visual and auditory processing at the primary cortical level-a concurrent TMS-fMRI study

Cerebral Cortex

Volumn 23, Issue 4, 2013, Pages 873-884

  Leitão, Joana ^a,b   Thielscher, Axel ^a,b   Werner, Sebastian ^a,b   Pohmann, Rolf ^a,b   Noppeney, Uta ^a,b,c  

^a Cognitive Neuroimaging Group ^*  (Germany)

^b MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^c UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

crossmodal deactivations; interleaved concurrent TMS fMRI; multisensory integration; multisensory interactions; right intraparietal sulcus

Indexed keywords

ADULT; ARTICLE; AUDITORY CORTEX; AUDITORY STIMULATION; BOLD SIGNAL; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HUMAN; INTRAPARIETAL SULCUS; MALE; PRIORITY JOURNAL; TRANSCRANIAL MAGNETIC STIMULATION; VISUAL CORTEX; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ADULT; BRAIN MAPPING; EVOKED POTENTIALS; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS; OXYGEN; PARIETAL LOBE; PHOTIC STIMULATION; PSYCHOPHYSICS; TRANSCRANIAL MAGNETIC STIMULATION; YOUNG ADULT;

EID: 84874578279     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhs078     Document Type: Article

References (84)

1. Abbruzzese G, Trompetto C, Schieppati M. 1996. The excitability of the human motor cortex increases during execution and mental imagination of sequential but not repetitive finger movements. Exp Brain Res. 111:465-472
2. Ackermann H, Scholz E, Koehler W, Dichgans J. 1991. Influence of posture and voluntary background contraction upon compound muscle action potentials from anterior tibial and soleus muscle following transcranial magnetic stimulation. Electroencephalogr Clin Neurophysiol. 81:71-80.
3. Antal A, Nitsche MA, Kincses TZ, Lampe C, Paulus W. 2004. No correlation between moving phosphene and motor thresholds: a transcranial magnetic stimulation study. Neuroreport. 15:297-302.
4. Arai N, Okabe S, Furubayashi T, Terao Y, Yuasa K, Ugawa Y. 2005. Comparison between short train, monophasic and biphasic repetitive transcranial magnetic stimulation (rTMS) of the human motor cortex. Clin Neurophysiol. 116:605-613.
5. Baudewig J, Siebner HR, Bestmann S, Tergau F, Tings T, PaulusW, Frahm J. 2001. Functional MRI of cortical activations induced by transcranial magnetic stimulation (TMS). Neuroreport. 12:3543-3548.
6. Beauchamp MS, Argall BD, Bodurka J, Duyn JH, Martin A. 2004. Unraveling multisensory integration: patchy organization within human STS multisensory cortex. Nat Neurosci. 7:1190-1192.
7. Beer AL, Plank T, Greenlee MW. 2011. Diffusion tensor imaging shows white matter tracts between human auditory and visual cortex. Exp Brain Res. 213:299-308.
8. Bestmann S, Baudewig J, Frahm J. 2003. On the synchronization of transcranial magnetic stimulation and functional echo-planar imaging. J Magn Reson Imaging. 17:309-316.
9. Bestmann S, Swayne O, Blankenburg F, Ruff CC, Haggard P, Weiskopf N, Josephs O, Driver J, Rothwell JC, Ward NS. 2008. Dorsal premotor cortex exerts state-dependent causal influences on activity in contralateral primary motor and dorsal premotor cortex. Cereb Cortex. 18:1281-1291.
10. Blankenburg F, Ruff CC, Bestmann S, Bjoertomt O, Eshel N, Josephs O, Weiskopf N, Driver J. 2008. Interhemispheric effect of parietal TMS on somatosensory response confirmed directly with concurrent TMS-fMRI. J Neurosci. 28:13202-13208.
11. Blankenburg F, Ruff CC, Bestmann S, Bjoertomt O, Josephs O, Deichmann R, Driver J. 2010. Studying the role of human parietal cortex in visuospatial attention with concurrent TMS-fMRI. Cereb Cortex. 20:2702-2711.
12. Boroojerdi B, Meister IG, Foltys H, Sparing R, Cohen LG, Topper R. 2002. Visual and motor cortex excitability: a transcranial magnetic stimulation study. Clin Neurophysiol. 113:1501-1504.
13. Boussaoud D, Ungerleider LG, Desimone R. 1990. Pathways for motion analysis: cortical connections of the medial superior temporal and fundus of the superior temporal visual areas in the macaque. J Comp Neurol. 296:462-495.
14. Brainard DH. 1997. The Psychophysics Toolbox. Spat Vis. 10:433-436.
15. Bremmer F, Schlack A, Shah NJ, Zafiris O, Kubischik M, Hoffmann K, Zilles K, Fink GR. 2001. Polymodal motion processing in posterior parietal and premotor cortex: a human fMRI study strongly implies equivalencies between humans and monkeys. Neuron. 29:287-296.
16. Bushara KO, Weeks RA, Ishii K, Catalan MJ, Tian B, Rauschecker JP, Hallett M. 1999. Modality-specific frontal and parietal areas for auditory and visual spatial localization in humans. Nat Neurosci. 2:759-766.
17. Calvert GA. 2001. Crossmodal processing in the human brain: insights from functional neuroimaging studies. Cereb Cortex. 11:1110-1123.
18. Cappe C, Morel A, Barone P, Rouiller EM. 2009. The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay. Cereb Cortex. 19:2025-2037.
19. Cappe C, Thut G, Romei V, Murray MM. 2010. Auditory-visual multisensory interactions in humans: timing, topography, directionality, and sources. J Neurosci. 30:12572-12580.
20. Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL. 2000. Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci. 3:292-297.
21. de la Mothe LA, Blumell S, Kajikawa Y, Hackett TA. 2006. Thalamic connections of the auditory cortex in marmoset monkeys: core and medial belt regions. J Comp Neurol. 496:72-96.
22. Deblieck C, Thompson B, Iacoboni M, Wu AD. 2008. Correlation between motor and phosphene thresholds: a transcranial magnetic stimulation study. Hum Brain Mapp. 29:662-670.
23. Driver J, Noesselt T. 2008. Multisensory interplay reveals crossmodal influences on 'sensory-specific' brain regions, neural responses, and judgments. Neuron. 57:11-23.
24. Eickhoff SB, Stephan KE, Mohlberg H, Grefkes C, Fink GR, Amunts K, Zilles K. 2005. A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data. Neuroimage. 25:1325-1335.
25. Falchier A, Clavagnier S, Barone P, Kennedy H. 2002. Anatomical evidence of multimodal integration in primate striate cortex. J Neurosci. 22:5749-5759.
26. Foxe JJ, Morocz IA, Murray MM, Higgins BA, Javitt DC, Schroeder CE. 2000. Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res Cogn Brain Res. 10:77-83.
27. Friston K, Holmes A, Worsley KJ, Poline JB, Frith C, Frackowiak R. 1995. Statistical parametric mapping: a general linear approach. Hum Brain Mapp. 2:22.
28. Friston KJ, Buchel C. 2000. Attentional modulation of effective connectivity from V2 to V5/MT in humans. Proc Natl Acad Sci U S A. 97:7591-7596.
29. Friston KJ, Holmes AP, Price CJ, Buchel C, Worsley KJ. 1999. Multisubject fMRI studies and conjunction analyses. Neuroimage. 10:385-396.
30. Ghazanfar AA, Schroeder CE. 2006. Is neocortex essentially multisensory? Trends Cogn Sci. 10:278-285.
31. Hackett TA, De La Mothe LA, Ulbert I, Karmos G, Smiley J, Schroeder CE. 2007. Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane. J Comp Neurol. 502:924-952.
32. Hackett TA, Stepniewska I, Kaas JH. 1998. Thalamocortical connections of the parabelt auditory cortex in macaque monkeys. J Comp Neurol. 400:271-286.
33. Hanakawa T, Mima T, Matsumoto R, Abe M, Inouchi M, Urayama S, Anami K, Honda M, Fukuyama H. 2009. Stimulus-response profile during single-pulse transcranial magnetic stimulation to the primary motor cortex. Cereb Cortex. 19:2605-2615.
34. Haxby JV, Horwitz B, Ungerleider LG, Maisog JM, Pietrini P, Grady CL. 1994. The functional organization of human extrastriate cortex: a PET-rCBF study of selective attention to faces and locations. J Neurosci. 14:6336-6353.
35. Hyvarinen J. 1982. Posterior parietal lobe of the primate brain. Physiol Rev. 62:1060-1129.
36. Izumi S, Findley TW, Ikai T, Andrews J, Daum M, Chino N. 1995. Facilitatory effect of thinking about movement on motor-evoked potentials to transcranial magnetic stimulation of the brain. Am J Phys Med Rehabil. 74:207-213.
37. Johnson JA, Zatorre RJ. 2005. Attention to simultaneous unrelated auditory and visual events: behavioral and neural correlates. Cereb Cortex. 15:1609-1620.
38. Johnson JA, Zatorre RJ. 2006. Neural substrates for dividing and focusing attention between simultaneous auditory and visual events. Neuroimage. 31:1673-1681.
39. Kawashima R, O'Sullivan BT, Roland PE. 1995. Positron-emission tomography studies of cross-modality inhibition in selective attentional tasks: closing the ''mind's eye''. Proc Natl Acad Sci U S A. 92:5969-5972.
40. Kayser C, Logothetis NK. 2007. Do early sensory cortices integrate cross-modal information? Brain Struct Funct. 212:121-132.
41. Kleiner M, Baarmand MM, Pelli D. 2007. What's new in Psychtoolbox-3? Perception. 36(ECVP Abstract Supplement):14.
42. Laurienti PJ, Burdette JH, Wallace MT, Yen YF, Field AS, Stein BE. 2002. Deactivation of sensory-specific cortex by cross-modal stimuli. J Cogn Neurosci. 14:420-429.
43. Leon-Sarmiento FE, Bara-Jimenez W, Wassermann EM. 2005. Visual deprivation effects on human motor cortex excitability. Neurosci Lett. 389:17-20.
44. Lewis JW, Beauchamp MS, DeYoe EA. 2000. A comparison of visual and auditory motion processing in human cerebral cortex. Cereb Cortex. 10:873-888.
45. Lewis JW, Van Essen DC. 2000a. Corticocortical connections of visual, sensorimotor, and multimodal processing areas in the parietal lobe of the macaque monkey. J Comp Neurol. 428:112-137.
46. Lewis JW, Van Essen DC. 2000b. Mapping of architectonic subdivisions in the macaque monkey, with emphasis on parieto-occipital cortex. J Comp Neurol. 428:79-111.
47. Macaluso E, Driver J. 2005. Multisensory spatial interactions: a window onto functional integration in the human brain. Trends Neurosci. 28:264-271.
48. Macaluso E, Driver J, Frith CD. 2003. Multimodal spatial representations engaged in human parietal cortex during both saccadic and manual spatial orienting. Curr Biol. 13:990-999.
49. Macaluso E, Eimer M, Frith CD, Driver J. 2003. Preparatory states in crossmodal spatial attention: spatial specificity and possible control mechanisms. Exp Brain Res. 149:62-74.
50. Macaluso E, Frith CD, Driver J. 2000. Modulation of human visual cortex by crossmodal spatial attention. Science. 289:1206-1208.
51. Martinez-Trujillo JC, Treue S. 2004. Feature-based attention increases the selectivity of population responses in primate visual cortex. Curr Biol. 14:744-751.
52. Maunsell JH, van Essen DC. 1983. The connections of the middle temporal visual area (MT) and their relationship to a cortical hierarchy in the macaque monkey. J Neurosci. 3:2563-2586.
53. McAdams CJ, Maunsell JH. 1999. Effects of attention on the reliability of individual neurons in monkey visual cortex. Neuron. 23:765-773.
54. Moisa M, Pohmann R, Ewald L, Thielscher A. 2009. New coil positioning method for interleaved transcranial magnetic stimulation (TMS)/ functional MRI (fMRI) and its validation in a motor cortex study. J Magn Reson Imaging. 29:189-197.
55. Moisa M, Pohmann R, Uludag K, Thielscher A. 2010. Interleaved TMS/CASL: comparison of different rTMS protocols. Neuroimage. 49:612-620.
56. Molholm S, Ritter W, Murray MM, Javitt DC, Schroeder CE, Foxe JJ. 2002. Multisensory auditory-visual interactions during early sensory processing in humans: a high-density electrical mapping study. Brain Res Cogn Brain Res. 14:115-128.
57. Murray MM, Molholm S, Michel CM, Heslenfeld DJ, Ritter W, Javitt DC, Schroeder CE, Foxe JJ. 2005. Grabbing your ear: rapid auditorysomatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. Cereb Cortex. 15:963-974.
58. Musacchia G, Schroeder CE. 2009. Neuronal mechanisms, response dynamics and perceptual functions of multisensory interactions in auditory cortex. Hear Res. 258:72-79.
59. O'Craven KM, Rosen BR, Kwong KK, Treisman A, Savoy RL. 1997. Voluntary attention modulates fMRI activity in human MT-MST. Neuron. 18:591-598.
60. Oliver R, Bjoertomt O, Driver J, Greenwood R, Rothwell J. 2009. Novel 'hunting' method using transcranial magnetic stimulation over parietal cortex disrupts visuospatial sensitivity in relation to motor thresholds. Neuropsychologia. 47:3152-3161.
61. Paus T, Jech R, Thompson CJ, Comeau R, Peters T, Evans AC. 1998. Dose-dependent reduction of cerebral blood flow during rapid-rate transcranial magnetic stimulation of the human sensorimotor cortex. J Neurophysiol. 79:1102-1107.
62. Pessoa L, Rossi A, Japee S, Desimone R, Ungerleider LG. 2009. Attentional control during the transient updating of cue information. Brain Res. 1247:149-158.
63. Raij T, Ahveninen J, Lin FH, Witzel T, Jaaskelainen IP, Letham B, Israeli E, Sahyoun C, Vasios C, Stufflebeam S, et al. 2010. Onset timing of cross-sensory activations and multisensory interactions in auditory and visual sensory cortices. Eur J Neurosci. 31:1772-1782.
64. Rockland KS, Ojima H. 2003. Multisensory convergence in calcarine visual areas in macaque monkey. Int J Psychophysiol. 50:19-26.
65. Romei V, Murray MM, Merabet LB, Thut G. 2007. Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: implications for multisensory interactions. J Neurosci. 27:11465-11472.
66. Ruff CC, Bestmann S, Blankenburg F, Bjoertomt O, Josephs O, Weiskopf N, Deichmann R, Driver J. 2008. Distinct causal influences of parietal versus frontal areas on human visual cortex: evidence from concurrent TMS-fMRI. Cereb Cortex. 18:817-827.
67. Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Freeman E, Haynes JD, Rees G, Josephs O, Deichmann R, Driver J. 2006. Concurrent TMS-fMRI and psychophysics reveal frontal influences on human retinotopic visual cortex. Curr Biol. 16:1479-1488.
68. Ruff CC, Blankenburg F, Bjoertomt O, Bestmann S, Weiskopf N, Driver J. 2009. Hemispheric differences in frontal and parietal influences on human occipital cortex: direct confirmation with concurrent TMSfMRI. J Cogn Neurosci. 21:1146-1161.
69. Rushworth MF, Paus T, Sipila PK. 2001. Attention systems and the organization of the human parietal cortex. J Neurosci. 21:5262-5271.
70. Sack AT, Kohler A, Bestmann S, Linden DE, Dechent P, Goebel R, Baudewig J. 2007. Imaging the brain activity changes underlying impaired visuospatial judgments: simultaneous FMRI, TMS, and behavioral studies. Cereb Cortex. 17:2841-2852.
71. Sadaghiani S, Maier JX, Noppeney U. 2009. Natural, metaphoric, and linguistic auditory direction signals have distinct influences on visual motion processing. J Neurosci. 29:6490-6499.
72. Salinas E, Sejnowski TJ. 2001. Gain modulation in the central nervous system: where behavior, neurophysiology, and computation meet. Neuroscientist. 7:430-440.
73. Santangelo V, Olivetti Belardinelli M, Spence C, Macaluso E. 2009. Interactions between voluntary and stimulus-driven spatial attention mechanisms across sensory modalities. J Cogn Neurosci. 21:2384-2397.
74. Schonfeldt-Lecuona C, Thielscher A, Freudenmann RW, Kron M, Spitzer M, Herwig U. 2005. Accuracy of stereotaxic positioning of transcranial magnetic stimulation. Brain Topogr. 17:253-259.
75. Schroeder CE, Foxe J. 2005. Multisensory contributions to low-level, 'unisensory' processing. Curr Opin Neurobiol. 15:454-458.
76. Schroeder CE, Smiley J, Fu KG, McGinnis T, O'Connell MN, Hackett TA. 2003. Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing. Int J Psychophysiol. 50:5-17.
77. Shomstein S, Yantis S. 2004. Control of attention shifts between vision and audition in human cortex. J Neurosci. 24:10702-10706.
78. Speer AM, Willis MW, Herscovitch P, Daube-Witherspoon M, Shelton JR, Benson BE, Post RM, Wassermann EM. 2003. Intensity-dependent regional cerebral blood flow during 1-Hz repetitive transcranial magnetic stimulation (rTMS) in healthy volunteers studied with H215O positron emission tomography: II. Effects of prefrontal cortex rTMS. Biol Psychiatry. 54:826-832.
79. Stewart LM, Walsh V, Rothwell JC. 2001. Motor and phosphene thresholds: a transcranial magnetic stimulation correlation study. Neuropsychologia. 39:415-419.
80. Werner S, Noppeney U. 2010a. Distinct functional contributions of primary sensory and association areas to audiovisual integration in object categorization. J Neurosci. 30:2662-2675.
81. Werner S, Noppeney U. 2010b. Superadditive responses in superior temporal sulcus predict audiovisual benefits in object categorization. Cereb Cortex. 20:1829-1842.
82. Werner S, Noppeney U. 2011. The contributions of transient and sustained response codes to audiovisual integration. Cereb Cortex. 21:920-931.
83. Womelsdorf T, Anton-Erxleben K, Treue S. 2008. Receptive field shift and shrinkage in macaque middle temporal area through attentional gain modulation. J Neurosci. 28:8934-8944.
84. Yantis S, Schwarzbach J, Serences JT, Carlson RL, Steinmetz MA, Pekar JJ, Courtney SM. 2002. Transient neural activity in human parietal cortex during spatial attention shifts. Nat Neurosci. 5:995-1002.