The behavioral relevance of multisensory neural response interactions

Frontiers in Neuroscience

Volumn 4, Issue MAY, 2010, Pages

  Sperdin, Holger F ^a,b   Cappe, Céline ^a   Murray, Micah M ^a,c,d  

^a LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

^b UNIVERSITY OF LAUSANNE   (Switzerland)

^c Electroencephalography Brain Mapping Core   (Switzerland)

^d VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Behavior; Brain imaging; Crossmodal; Multisensory; Neurophysiology

Indexed keywords

EID: 77957204389     PISSN: 16624548     EISSN: 1662453X     Source Type: Journal    
DOI: 10.3389/neuro.01.009.2010     Document Type: Review

References (86)

1. Blau, V., van Atteveldt, N., Ekkebus, M., Goebel, R., and Blomert, L. (2009). Reduced neural integration of letters and speech sounds links phonological and reading deficits in adult dyslexia. Curr. Biol. 19, 503-508.
2. Britz, J., and Michel, C. M. (2010). Errors can be related to pre-stimulus differences in ERP topography and their concomitant sources. Neuroimage 49, 2774-2782.
3. Busch, N. A., Dubois, J., and VanRullen, R. (2009). The phase of ongoing EEG oscillations predicts visual perception. J. Neurosci. 29, 7869-7876.
4. Cappe, C., and Barone, P. (2005). Heteromodal connections supporting multisensory integration at low levels of cortical processing in the monkey. Eur. J. Neurosci. 22, 2886-2902.
5. Cappe, C., Morel, A., Barone, P., and Rouiller, E. M. (2009). The thalamocortical projection systems in primate: an anatomical support for multisensory and sensorimotor interplay. Cereb. Cortex 19, 2025-2037.
6. Cappe, C., Murray, M. M., Barone, P., and Rouiller, E. M. (2010). Multisensory facilitation of behavior in monkeys: effects of stimulus intensity. J. Cogn. Neurosci., published online 4 January.
7. De Lucia, M., Michel, C. M., Clarke, S., and Murray, M. M. (2007). Single-subject EEG analysis based on topographic information. Int. J. Bioelectromagnetism 9, 168-171.
8. De Lucia, M., Michel, C. M., and Murray, M. M. (2010). Comparing ICA-based and single-trial topographic ERP analyses. Brain Topogr. [in press.]
9. Foxe, J. J. (2009). Multisensory integration: frequency tuning of audio-tactile integration. Curr. Biol. 19, 373-375.
10. Foxe, J. J., Morocz, I. A., Murray, M. M., Higgins, B. A., Javitt, D. C., and Schroeder, C. E. (2000). Multisensory auditory-somatosensory interactions in early cortical processing revealed by high-density electrical mapping. Brain Res. Cogn. Brain Res. 10, 77-83.
11. Foxe, J. J., Wylie, G. R., Martinez, A., Schroeder, C. E., Javitt, D. C., Guilfoyle, D., Ritter, W., and Murray, M. M. (2002). Auditory-somatosensory multisensory processing in auditory association cortex: an fMRI study. J. Neurophysiol. 88, 540-543.
12. Fu, K. M., Johnston, T. A., Shah, A. S., Arnold, L., Smiley, J., Hackett, T. A., Garraghty, P. E., and Schroeder, C. E. (2003). Auditory cortical neurons respond to somatosensory stimulation. J. Neurosci. 23, 7510-7515.
13. Ghazanfar, A. A., and Schroeder, C. E. (2006). Is neocortex essentially multisensory? Trends Cogn. Sci. (Regul. Ed.) 10, 278-285.
14. Gillmeister, H., and Eimer, M. (2007). Tactile enhancement of auditory detection and perceived loudness. Brain Res. 1160, 58-68.
15. Gonzalez Andino, S. L., Murray, M. M., Foxe, J. J., and de Peralta Menendez, R. G. (2005a). How single-trial electrical neuroimaging contributes to multisensory research. Exp. Brain Res. 166, 298-304.
16. Gonzalez Andino, S. L., Michel, C. M., Thut, G., Landis, T., and Grave de Peralta, R. (2005b). Prediction of response speed by anticipatory high-frequency (gamma band) oscillations in the human brain. Hum. Brain Mapp. 24, 50-58.
17. Grave de Peralta Menendez, R., Murray, M. M., Michel, C. M., Martuzzi, R., and Gonzalez Andino, S. L. (2004). Electrical neuroimaging based on biophysical constraints. Neuroimage 21, 527-539.
18. Hackett, T. A., Smiley, J. F., Ulbert, I., Karmos, G., Lakatos, P., de la Mothe, L. A., and Schroeder, C. E. (2007a). Sources of somatosensory input to the caudal belt areas of auditory cortex. Perception 36, 1419-1430.
19. Hackett, T. A., De La Mothe, L. A., Ulbert, I., Karmos, G., Smiley, J., and Schroeder, C. E. (2007b). Multisensory convergence in auditory cortex, II. Thalamocortical connections of the caudal superior temporal plane. J. Comp. Neurol. 502, 924-952.
20. Hirokawa, J., Bosch, M., Sakata, S., Sakurai, Y., and Yamamori, T. (2008). Functional role of the secondary visual cortex in multisensory facilitation in rats. Neuroscience 153, 1402-1417.
21. Hugenschmidt, C. E., Mozolic, J. L., Tan, H., Kraft, R. A., and Laurienti, P. J. (2009). Age-related increase in cross-sensory noise in resting and steady-state cerebral perfusion. Brain Topogr. 21, 241-251.
22. Ilmoniemi, R. J., and Kičič, D. (2010). Methodology for combined TMS and EEG. Brain Topogr. 22, 233-248.
23. Jones, E. G., and Powell, T. P. (1970). An anatomical study of converging sensory pathways within the cerebral cortex of the monkey. Brain 93, 793-820.
24. Kayser, C., and Logothetis, N. K. (2007). Do early sensory cortices integrate cross-modal information? Brain Struct. Funct. 212, 121-132.
25. Kayser, C., Petkov, C. I., Augath, M., and Logothetis, N. K. (2005). Integration of touch and sound in auditory cortex. Neuron 48, 373-384.
26. Komura, Y., Tamura, R., Uwano, T., Nishijo, H., and Ono, T. (2005). Auditory thalamus integrates visual inputs into behavioral gains. Nat. Neurosci. 8, 1203-1209.
27. Lakatos, P., Chen, C. M., O'Connell, M. N., Mills, A., and Schroeder, C. E. (2007). Neuronal oscillations and multisensory interaction in primary auditory cortex. Neuron 53, 279-292.
28. Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., and Schroeder, C. E. (2008). Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320, 110-113.
29. Lakatos, P., O'Connell, M. N., Barczak, A., Mills, A., Javitt, D. C., and Schroeder, C. E. (2009). The leading sense: supramodal control of neurophysiological context by attention. Neuron 64, 419-430.
30. Lamarre, Y., Busby, L., and Spidalieri, G. (1983). Fast ballistic arm movements triggered by visual, auditory, and somesthetic stimuli in the monkey. I. Activity of precentral cortical neurons. J. Neurophysiol. 50, 1343-1358.
31. Laurienti, P. J., Burdette, J. H., Maldjian, J. A., and Wallace, M. T. (2006). Enhanced multisensory integration in older adults. Neurobiol. Aging 27, 1155-1163.
32. Lehmann, D. (1987). Principles of spatial analysis. In Handbook of electroencephalography and clinical neurophysiology, Vol. 1, Methods of analysis of brain electrical and magnetic signals, A. S. Gevins, and A. Remond, eds (Amsterdam, Elsevier), pp. 309-405.
33. Lickliter, R., and Bahrick, L. E. (2000). The development of infant intersensory perception: advantages of a comparative convergent-operations approach. Psychol. Bull. 126, 260-280.
34. Martuzzi, R., Murray, M. M., Maeder, P. P., Fornari, E., Thiran, J. -P., Clarke, S., Michel, C. M., and Meuli, R. A. (2006). Visuo-motor pathways in humans revealed by event-related fMRI. Exp. Brain Res. 170, 472-487.
35. Martuzzi, R., Murray, M. M., Michel, C. M., Thiran, J. -P., Maeder, P. P., Clarke, S., and Meuli, R. A. (2007). Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cereb. Cortex 17, 1672-1679.
36. Mathewson, K. E., Gratton, G., Fabiani, M., Beck, D. M., and Ro, T. (2009). To see or not to see: prestimulus alpha phase predicts visual awareness. J. Neurosci. 29, 2725-2732.
37. Michel, C. M., Koenig, T., Brandies, D., Gianotti, L. R. R., and Wackermann, J. (2009). Electrical Neuroimaging. Cambridge, UK, Cambridge University Press.
38. Michel, C. M., Murray, M. M., Lantz, G., Gonzalez, S., Spinelli, L., and Grave de Peralta, R. (2004). EEG source imaging. Clin. Neurophysiol. 115, 2195-2222.
39. Miller, J. (1982). Divided attention: evidence for coactivation with redundant signals. Cogn. Psychol. 14, 247-279.
40. Miller J., Ulrich R., and Lamarre Y. (2001). Locus of the redundant-signals effect in bimodal divided attention: a neurophysiological analysis. Percept. Psychophys. 63, 555-562.
41. Miniussi, C., and Thut, G. (2010). Combining TMS and EEG offers new prospects in cognitive neuroscience. Brain Topogr. 22, 249-256.
42. Murray, M. M., Brunet, D., and Michel, C. M. (2008). Topographic ERP analyses: a step-by-step tutorial review. Brain Topogr. 20, 249-264.
43. Murray, M. M., De Lucia, M., Brunet, D., and Michel, C. M. (2009). Principles of topographic analyses for electrical neuroimaging. In Brain Signal Analysis, T. C. Handy, ed. (Cambridge, MIT Press), pp. 21-54.
44. Murray, M. M., Foxe, J. J., Higgins, B. A., Javitt, D. C., and Schroeder, C. E. (2001). Visuo-spatial neural response interactions in early cortical processing during a simple reaction time task: a high-density electrical mapping study. Neuropsychologia 39, 828-844.
45. Murray, M. M., Molholm, S., Michel, C. M., Heslenfeld, D. J., Ritter, W., Javitt, D. C., Schroeder, C. E., and Foxe, J. J. (2005). Grabbing your ear: rapid auditory-somatosensory multisensory interactions in low-level sensory cortices are not constrained by stimulus alignment. Cereb. Cortex 15, 963-974.
46. Murray, M. M., and Spierer, L. (2009). Auditory spatio-temporal brain dynamics and their consequences for multisensory interactions in humans. Hear. Res. 258, 121-133.
47. Neil, P. A., Chee-Ruiter, C., Scheier, C., Lewkowicz, D. J., and Shimojo, S. (2006). Development of multisensory spatial integration and perception in humans. Dev. Sci. 9, 454-464.
48. Pogosyan, A., Gaynor, L. D., Eusebio, A., and Brown, P. (2009). Boosting cortical activity at Beta-band frequencies slows movement in humans. Curr. Biol. 19, 1637-1641.
49. Polley, D. B., Hillock, A. R., Spankovich, C., Popescu, M. V., Royal, D. W., and Wallace, M. T. (2008). Development and plasticity of intra- and intersensory information processing. J. Am. Acad. Audiol. 19, 780-798.
50. Raab, D. H. (1962). Statistical facilitation of simple reaction times. Trans. N Y Acad. Sci. 24, 574-590.
51. Ramos-Estebanez, C., Merabet, L. B., Machii, K., Fregni, F., Thut, G., Wagner, T. A., Romei, V., Amedi, A., and Pascual-Leone, A. (2007). Visual phosphene perception modulated by subthreshold cross modal sensory stimulation. J. Neurosci. 27, 4178-4181.
52. Romei, V., Murray, M. M., Cappe, C., and Thut, G. (2009). Preperceptual and stimulus-selective enhancement of low-level human visual cortex excitability by sounds. Curr. Biol. 19, 1799-1805.
53. Romei, V., Murray, M. M., Merabet, L. B., and 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.
54. Romei, V., Rihs, T., Brodbeck, V., and Thut, G. (2008). Resting electroencephalogram alpha-power over posterior sites indexes baseline visual cortex excitability. Neuroreport 19, 203-208.
55. Ross, L. A., Saint-Amour, D., Leavitt, V. M., Molholm, S., Javitt, D. C., and Foxe, J. J. (2007). Impaired multisensory processing in schizophrenia: deficits in the visual enhancement of speech comprehension under noisy environmental conditions. Schizophr. Res. 97, 173-183.
56. Rowland, B. A., Quessy, S., Stanford, T. R., and Stein, B. E. (2007). Multisensory integration shortens physiological response latencies. J. Neurosci. 27, 5879-5884.
57. Rowland, B. A., and Stein, B. E. (2007). Multisensory integration produces an initial response enhancement. Front. Integr. Neurosci. 1:4. doi:10.3389/neuro.07.004.2007.
58. Rowland, B. A., and Stein, B. E. (2008). Temporal profiles of response enhancement in multisensory integration. Front. Neurosci. 2, 218-224. doi:10.3389/neuro.01.033.2008.
59. Saron, C. D., Foxe, J. J., Simpson, G. V., and Vaughan Jr., H. G. (2003). Interhemispheric visuomotor activation: spatiotemporal electrophysiology related to reaction time. In The Parallel Brain, E. Zaidel and M. Iacoboni, eds (Cambridge, MA, MIT Press), pp. 171-219.
60. Schroeder, C. E., and Foxe, J. (2005). Multisensory contributions to low-level, 'unisensory' processing. Curr. Opin. Neurobiol. 15, 454-458.
61. Schroeder, C. E., and Lakatos, P. (2009). Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci. 32, 9-18.
62. Schroeder, C. E., Lakatos, P., Kajikawa, Y., Partan, S., and Puce, A. (2008). Neuronal oscillations and visual amplification of speech. Trends Cogn. Sci. 12, 106-113.
63. Schroeder, C. E., Lindsley, R. W., Specht, C., Marcovici, A., Smiley, J. F., and Javitt, D. C. (2001). Somatosensory input to auditory association cortex in the macaque monkey. J. Neurophysiol. 85, 1322-1327.
64. Schroeder, C. E., Smiley, J., Fu, K. G., McGinnis, T., O'Connell, M. N., and Hackett, T. A. (2003). Anatomical mechanisms and functional implications of multisensory convergence in early cortical processing. Int. J. Psychophysiol. 50, 5-17.
65. Senkowski, D., Molholm, S., Gomez-Ramirez, M., and Foxe, J. J. (2006). Oscillatory beta activity predicts response speed during a multisensory audiovisual reaction time task: a high-density electrical mapping study. Cereb. Cortex 16, 1556-1565.
66. Senkowski, D., Schneider, T. R., Foxe, J. J., and Engel, A. K. (2008). Crossmodal binding through neural coherence: implications for multisensory processing. Trends Neurosci. 31, 401-409.
67. Silvanto, J., and Pascual-Leone, A. (2008). State-dependency of transcranial magnetic stimulation. Brain Topogr. 21, 1-10.
68. Smiley, J. F., Hackett, T. A., Ulbert, I., Karmas, G., Lakatos, P., Javitt, D. C., and Schroeder, C. E. (2007). Multisensory convergence in auditory cortex, I. Cortical connections of the caudal superior temporal plane in macaque monkeys. J. Comp. Neurol. 502, 894-923.
69. Sperdin, H. F., Cappe, C., Foxe, J. J., and Murray, M. M. (2009). Early, low-level auditory-somatosensory multisensory interactions impact reaction time speed. Front. Integr. Neurosci. 3:2. doi:10.3389/neuro.07.002.2009.
70. Sperdin, H. F., Cappe, C., and Murray, M. M. (2010). Auditory-somatosensory multisensory interactions in humans and the role of spatial attention. Neuropsychologia, in revision.
71. Stein, B. E., and Meredith, M. A. (1993). The Merging of the Senses. Cambridge, Massachusetts, MIT Press.
72. Stein, B. E., and Stanford, T. R. (2008). Multisensory integration: current issues from the perspective of the single neuron. Nat. Rev. Neurosci. 9, 255-266.
73. Sumby, W. H., and Pollack, I. (1954). Visual contribution to speech intelligibility in noise. J. Acoust. Soc. Am. 26, 212-215.
74. Talsma, D., Doty, T. J., and Woldorff, M. G. (2007). Selective attention and audiovisual integration: is attending to both modalities a prerequisite for early integration? Cereb. Cortex. 17, 679-690.
75. Talsma, D., and Woldorff, M. G. (2005). Selective attention and multisensory integration: multiple phases of effects on the evoked brain activity. J. Cogn. Neurosci. 17, 1098-1114.
76. Tajadura-Jimenez, A., Kitagawa, N., Valjamae, A., Zampini, M., Murray, M. M., and Spence, C. (2009). Auditory-somatosensory multisensory interactions are spatially modulated by stimulated body surface and acoustic spectra. Neuropsychologia 47, 195-203.
77. Talairach, J., and Tournoux, P. (1988). Co-planar Stereotaxic Atlas of the Human Brain. New York, Thieme.
78. Thut, G., and Pascual-Leone, A. (2010). A review of combined TMS-EEG studies to characterize lasting effects of repetitive TMS and assess their usefulness in cognitive and clinical neuroscience. Brain Topogr. 22, 219-232.
79. Van Zaen, J., Uldry, L., Duchêne, C., Prudat, Y., Meuli, R. A., Murray, M. M., and Vesin, J. M. (2010). Adaptive tracking of EEG oscillations. J. Neurosci. Methods 186, 97-106.
80. Vaughan, H. G. Jr. (1969). The relationship of brain activity to scalp recordings of event-related potentials. In Averaged Evoked Potentials; Methods, Results, Evaluations, E. Donchin and D. B. Lindsley eds [Washington, D.C., National Aeronautics and Space Administration (NASA No. SP 191)], pp. 45-94.
81. Wallace, M. T. (2009). Dyslexia: bridging the gap between hearing and reading. Curr. Biol. 19, R260-R262.
82. Wallace, M. T., Carriere, B. N., Perrault, T. J. Jr., Vaughan, J. W., and Stein, B. E. (2006). The development of cortical multisensory integration. J. Neurosci. 26, 11844-11849.
83. Wallace, M. T., Ramachandran, R., and Stein, B. E. (2004). A revised view of sensory cortical parcellation. Proc. Natl. Acad. Sci. U.S.A. 101, 2167-2172.
84. Wang, Y., Celebrini, S., Trotter, Y., and Barone, P. (2008). Visuo-auditory interactions in the primary visual cortex of the behaving monkey: electrophysiological evidence. BMC Neurosci. 9, 79.
85. Yau, J. M., Olenczak, J. B., Dammann, J. F., and Bensmaia, S. J. (2009). Temporal frequency channels are linked across audition and touch. Curr. Biol. 19, 561-566.
86. Zampini, M., Torresan, D., Spence, C., and Murray, M. M. (2007). Auditory-somtosensory multisensory interactions in front and rear space. Neuropsychologia 45, 1869-1877.