Acoustic noise improves visual perception and modulates occipital oscillatory states

Journal of Cognitive Neuroscience

Volumn 26, Issue 4, 2014, Pages 699-711

  Gleiss, Stephanie ^a   Kayser, Christoph ^a,b  

^a MAX PLANCK INSTITUTE FOR BIOLOGICAL CYBERNETICS   (Germany)

^b UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ACOUSTICS; ADULT; ARTICLE; ELECTROENCEPHALOGRAPHY; EVOKED VISUAL RESPONSE; FACILITATION; FEMALE; HUMAN; HUMAN EXPERIMENT; MALE; NERVE EXCITABILITY; NEUROIMAGING; NOISE; NORMAL HUMAN; OCCIPITAL CORTEX; OSCILLATION; PRIORITY JOURNAL; PSYCHOMETRY; QUANTITATIVE ANALYSIS; SOUND; VISION; VISUAL STIMULATION;

ACOUSTIC STIMULATION; ADOLESCENT; ADULT; AUDITORY PERCEPTION; BRAIN; BRAIN WAVES; ELECTROENCEPHALOGRAPHY; EVOKED POTENTIALS, AUDITORY; EVOKED POTENTIALS, VISUAL; FEMALE; HUMANS; MALE; NOISE; PHOTIC STIMULATION; PSYCHOMETRICS; SENSORY THRESHOLDS; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84896812883     PISSN: 0898929X     EISSN: 15308898     Source Type: Journal    
DOI: 10.1162/jocn_a_00524     Document Type: Article

References (107)

1. Andersen, T. S., & Mamassian, P. (2008). Audiovisual integration of stimulus transients. Vision Research, 48, 2537-2544.
2. Angelaki, D. E., Gu, Y., & DeAngelis, G. C. (2009). Multisensory integration: Psychophysics, neurophysiology, and computation. Current Opinion in Neurobiology, 19, 452-458.
3. Banerjee, S., Snyder, A. C., Molholm, S., & Foxe, J. J. (2011). Oscillatory alpha-band mechanisms and the deployment of spatial attention to anticipated auditory and visual target locations: Supramodal or sensory-specific control mechanisms? Journal of Neuroscience, 31, 9923-9932.
4. Bolognini, N., Senna, I., Maravita, A., Pascual-Leone, A., & Merabet, L. B. (2010). Auditory enhancement of visual phosphene perception: The effect of temporal and spatial factors and of stimulus intensity. Neuroscience Letters, 477, 109-114.
5. Brainard, D. H. (1997). The Psychophysics Toolbox. Spatial Vision, 10, 433-436.
6. Bresciani, J. P., Ernst, M. O., Drewing, K., Bouyer, G., Maury, V., & Kheddar, A. (2005). Feeling what you hear: Auditory signals can modulate tactile tap perception. Experimental Brain Research, 162, 172-180.
7. Burr, D., & Alais, D. (2006). Combining visual and auditory information. Progress in Brain Research, 155, 243-258.
8. Busch, N. A., Dubois, J., & VanRullen, R. (2009). The phase of ongoing EEG oscillations predicts visual perception. Journal of Neuroscience, 29, 7869-7876.
9. Busch, N. A., & VanRullen, R. (2010). Spontaneous EEG oscillations reveal periodic sampling of visual attention. Proceedings of the National Academy of Sciences, U.S.A., 107, 16048-16053.
10. Caclin, A., Bouchet, P., Djoulah, F., Pirat, E., Pernier, J., & Giard, M. H. (2011). Auditory enhancement of visual perception at threshold depends on visual abilities. Brain Research, 1396, 35-44.
11. Calvert, G. A. (2001). Crossmodal processing in the human brain: Insights from functional neuroimaging studies. Cerebral Cortex, 11, 1110-1123.
12. Cameron, E. L., Tai, J. C., & Carrasco, M. (2002). Covert attention affects the psychometric function of contrast sensitivity. Vision Research, 42, 949-967.
13. Cappe, C., Thelen, A., Romei, V., Thut, G., & Murray, M. M. (2012). Looming signals reveal synergistic principles of multisensory integration. Journal of Neuroscience, 32, 1171-1182.
14. Carrasco, M., Penpeci-Talgar, C., & Eckstein, M. (2000). Spatial covert attention increases contrast sensitivity across the CSF: Support for signal enhancement. Vision Research, 40, 1203-1215.
15. Chen, Y. C., Huang, P. C., Yeh, S. L., & Spence, C. (2011). Synchronous sounds enhance visual sensitivity without reducing target uncertainty. Seeing and Perceiving, 24, 623-638.
16. Cohen, M. R., & Maunsell, J. H. (2011). When attention wanders: How uncontrolled fluctuations in attention affect performance. Journal of Neuroscience, 31, 15802-15806.
17. Corey, D. M., Dunlap, W. P., & Burke, M. J. (1998). Averaging correlations: Expected values and bias in combined Pearson rs and Fisher's z transformations. The Journal of General Psychology, 125, 245-261.
18. Dahl, C., Logothetis, N., & Kayser, C. (2009). Spatial organization of multisensory responses in temporal association cortex. Journal of Neuroscience, 29, 11924-11932.
19. Dalton, B. H., & Behm, D. G. (2007). Effects of noise and music on human and task performance: A systematic review. Occupational Ergonomics, 7, 143-152.
20. Delorme, A., & Makeig, S. (2004). EEGLAB: An open source toolbox for analysis of single-trial EEG dynamics. Journal of Neuroscience Methods, 134, 9-21.
21. Donner, T. H., Siegel, M., Oostenveld, R., Fries, P., Bauer, M., & Engel, A. K. (2007). Population activity in the human dorsal pathway predicts the accuracy of visual motion detection. Journal of Neurophysiology, 98, 345-359.
22. Downar, J., Crawley, A. P., Mikulis, D. J., & Davis, K. D. (2000). A multimodal cortical network for the detection of changes in the sensory environment. Nature Neuroscience, 3, 277-283.
23. Doyle, M. C., & Snowden, R. J. (2001). Identification of visual stimuli is improved by accompanying auditory stimuli: The role of eye movements and sound location. Perception, 30, 795-810.
24. Ernst, M. O., & Bulthoff, H. H. (2004). Merging the senses into a robust percept. Trends in Cognitive Sciences, 8, 162-169.
25. Fiebelkorn, I. C., Foxe, J. J., Butler, J. S., Mercier, M. R., Snyder, A. C., & Molholm, S. (2011). Ready, set, reset: Stimulus-locked periodicity in behavioral performance demonstrates the consequences of cross-sensory phase reset. Journal of Neuroscience, 31, 9971-9981.
26. Fiebelkorn, I. C., Snyder, A. C., Mercier, M. R., Butler, J. S., Molholm, S., & Foxe, J. J. (2013). Cortical cross-frequency coupling predicts perceptual outcomes. Neuroimage, 69, 126-137.
27. Foxe, J. J., & Snyder, A. C. (2011). The role of alpha-band brain oscillations as a sensory suppression mechanism during selective attention. Frontiers in Psychology, 2, 154.
28. Goksoy, C., Demirtas, S., & Ates, K. (2005). Effects of continuous conditioning noise and light on the auditoryand visual-evoked potentials of the guinea pig. Brain Research, 1061, 42-49.
29. Gross, J., Schmitz, F., Schnitzler, I., Kessler, K., Shapiro, K., Hommel, B., et al. (2004). Modulation of long-range neural synchrony reflects temporal limitations of visual attention in humans. Proceedings of the National Academy of Sciences, U.S.A., 101, 13050-13055.
30. Harper, D. W. (1979). Signal detection analysis of effect of white noise intensity on sensitivity to visual flicker. Perceptual & Motor Skills, 48, 791-798.
31. Henry, M. J., & Obleser, J. (2012). Frequency modulation entrains slow neural oscillations and optimizes human listening behavior. Proceedings of the National Academy of Sciences, U.S.A., 109, 20095-20100.
32. Herrmann, K., Montaser-Kouhsari, L., Carrasco, M., & Heeger, D. J. (2010). When size matters: Attention affects performance by contrast or response gain. Nature Neuroscience, 13, 1554-1559.
33. Hipp, J. F., Engel, A. K., & Siegel, M. (2011). Oscillatory synchronization in large-scale cortical networks predicts perception. Neuron, 69, 387-396.
34. Jausovec, N., & Habe, K. (2004). The influence of auditory background stimulation (Mozart's sonata K. 448) on visual brain activity. International Journal of Psychophysiology, 51, 261-271.
35. Jensen, O., Bonnefond, M., & VanRullen, R. (2012). An oscillatory mechanism for prioritizing salient unattended stimuli. Trends in Cognitive Sciences, 16, 200-206.
36. Jones, B. E. (2003). Arousal systems. Frontiers in Bioscience, 8, s438-s451.
37. Kayser, C., & Logothetis, N. K. (2007). Do early sensory cortices integrate cross-modal information? Brain Structure & Function, 212, 121-132.
38. Kayser, C., Petkov, C. I., Lippert, M., & Logothetis, N. K. (2005). Mechanisms for allocating auditory attention: An auditory saliency map. Current Biology, 15, 1943-1947.
39. Keil, J., Muller, N., Ihssen, N., & Weisz, N. (2012). On the variability of the McGurk effect: Audiovisual integration depends on prestimulus brain states. Cerebral Cortex, 22, 221-231.
40. Kitajo, K., Doesburg, S. M., Yamanaka, K., Nozaki, D., Ward, L. M., & Yamamoto, Y. (2007). Noise-induced large-scale phase synchronization of human-brain activity associated with behavioural stochastic resonance. EPL (Europhysics Letters), 80, 40009.
41. Klimesch, W., Sauseng, P., & Hanslmayr, S. (2007). EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews, 53, 63-88.
42. Lakatos, P., Karmos, G., Mehta, A. D., Ulbert, I., & Schroeder, C. E. (2008). Entrainment of neuronal oscillations as a mechanism of attentional selection. Science, 320, 110-113.
43. Lakatos, P., O'Connell, M. N., Barczak, A., Mills, A., Javitt, D. C., & Schroeder, C. E. (2009). The leading sense: Supramodal control of neurophysiological context by attention. Neuron, 64, 419-430.
44. Lange, J., Oostenveld, R., & Fries, P. (2013). Reduced occipital alpha power indexes enhanced excitability rather than improved visual perception. Journal of Neuroscience, 33, 3212-3220.
45. Lee, D. K., Itti, L., Koch, C., & Braun, J. (1999). Attention activates winner-take-all competition among visual filters. Nature Neuroscience, 2, 375-381.
46. Lee, S. H., & Dan, Y. (2012). Neuromodulation of brain states. Neuron, 76, 209-222.
47. Linkenkaer-Hansen, K., Nikulin, V. V., Palva, S., Ilmoniemi, R. J., & Palva, J. M. (2004). Prestimulus oscillations enhance psychophysical performance in humans. Journal of Neuroscience, 24, 10186-10190.
48. Lippert, M., Logothetis, N., & Kayser, C. (2007). Improvement of visual contrast detection by a simultaneous sound. Brain Research, 1173, 102-109.
49. Lovelace, C. T., Stein, B. E., & Wallace, M. T. (2003). An irrelevant light enhances auditory detection in humans: A psychophysical analysis of multisensory integration in stimulus detection. Brain Research, Cognitive Brain Research, 17, 447-453.
50. Lugo, E., Doti, R., & Faubert, J. (2008). Ubiquitous crossmodal stochastic resonance in humans: Auditory noise facilitates tactile, visual and proprioceptive sensations. PLoS One, 3, e2860.
51. Lugo, E., Doti, R., & Faubert, J. (2012). Effective tactile noise facilitates visual perception. Seeing Perceiving, 25, 29-44.
52. Luo, H., Liu, Z., & Poeppel, D. (2010). Auditory cortex tracks both auditory and visual stimulus dynamics using low-frequency neuronal phase modulation. PLoS Biology, 8, e1000445.
53. Manjarrez, E., Mendez, I., Martinez, L., Flores, A., & Mirasso, C. R. (2007). Effects of auditory noise on the psychophysical detection of visual signals: Cross-modal stochastic resonance. Neuroscience Letters, 415, 231-236.
54. Martuzzi, R., Murray, M. M., Michel, C. M., Thiran, J. P., Maeder, P. P., Clarke, S., et al. (2007). Multisensory interactions within human primary cortices revealed by BOLD dynamics. Cerebral Cortex, 17, 1672-1679.
55. Mathewson, K. E., Gratton, G., Fabiani, M., Beck, D. M., & Ro, T. (2009). To see or not to see: Prestimulus alpha phase predicts visual awareness. Journal of Neuroscience, 29, 2725-2732.
56. Mathewson, K. E., Prudhomme, C., Fabiani, M., Beck, D. M., Lleras, A., & Gratton, G. (2012). Making waves in the stream of consciousness: Entraining oscillations in EEG alpha and fluctuations in visual awareness with rhythmic visual stimulation. Journal of Cognitive Neuroscience, 24, 2321-2333.
57. McDonald, J. J., Teder-Salejarvi, W. A., & Hillyard, S. A. (2000). Involuntary orienting to sound improves visual perception. Nature, 407, 906-908.
58. McDonnell, M. D., & Ward, L. M. (2011). The benefits of noise in neural systems: Bridging theory and experiment. Nature Reviews Neuroscience, 12, 415-426.
59. Mercier, M. R., Foxe, J. J., Fiebelkorn, I. C., Butler, J. S., Schwartz, T. H., & Molholm, S. (2013). Auditory-driven phase reset in visual cortex: Human electrocorticography reveals mechanisms of early multisensory integration. Neuroimage, 79, 19-29.
60. Molholm, S., Ritter, W., Murray, M. M., Javitt, D. C., Schroeder, C. E., & Foxe, J. J. (2002). Multisensory auditory-visual interactions during early sensory processing in humans: A high-density electrical mapping study. Brain Research, Cognitive Brain Research, 14, 115-128.
61. Mori, T., & Kai, S. (2002). Noise-induced entrainment and stochastic resonance in human brain waves. Physical Review Letters, 88, 218101.
62. Moss, F., Ward, L. M., & Sannita, W. G. (2004). Stochastic resonance and sensory information processing: A tutorial and review of application. Clinical Neurophysiology, 115, 267-281.
63. Naue, N., Rach, S., Struber, D., Huster, R. J., Zaehle, T., Korner, U., et al. (2011). Auditory event-related response in visual cortex modulates subsequent visual responses in humans. Journal of Neuroscience, 31, 7729-7736.
64. Ng, B. S., Schroeder, T., & Kayser, C. (2012). A precluding but not ensuring role of entrained low-frequency oscillations for auditory perception. Journal of Neuroscience, 32, 12268-12276.
65. Noesselt, T., Tyll, S., Boehler, C. N., Budinger, E., Heinze, H. J., & Driver, J. (2010). Sound-induced enhancement of low-intensity vision: Multisensory influences on human sensory-specific cortices and thalamic bodies relate to perceptual enhancement of visual detection sensitivity. Journal of Neuroscience, 30, 13609-13623.
66. Odgaard, E. C., Arieh, Y., & Marks, L. E. (2003). Cross-modal enhancement of perceived brightness: Sensory interaction versus response bias. Perception & Psychophysics, 65, 123-132.
67. Odgaard, E. C., Arieh, Y., & Marks, L. E. (2004). Brighter noise: Sensory enhancement of perceived loudness by concurrent visual stimulation. Cognitive, Affective & Behavioral Neuroscience, 4, 127-132.
68. Palva, S., & Palva, J. M. (2012). Discovering oscillatory interaction networks with M/EEG: Challenges and breakthroughs. Trends in Cognitive Sciences, 16, 219-230.
69. Pelli, D. G. (1997). The VideoToolbox software for visual psychophysics: Transforming numbers into movies. Spatial Vision, 10, 437-442.
70. Perez-Bellido, A., Soto-Faraco, S., & Lopez-Moliner, J. (2013). Sound-driven enhancement of vision: Disentangling detection from decisional level contributions. Journal of Neurophysiology, 109, 1065-1077.
71. Reynolds, J. H., & Heeger, D. J. (2009). The normalization model of attention. Neuron, 61, 168-185.
72. Romei, V., Brodbeck, V., Michel, C., Amedi, A., Pascual-Leone, A., & Thut, G. (2008). Spontaneous fluctuations in posterior alpha-band EEG activity reflect variability in excitability of human visual areas. Cerebral Cortex, 18, 2010-2018.
73. Romei, V., Gross, J., & Thut, G. (2012). Sounds reset rhythms of visual cortex and corresponding human visual perception. Current Biology, 22, 807-813.
74. Romei, V., Murray, M. M., Cappe, C., & Thut, G. (2009). Preperceptual and stimulus-selective enhancement of low-level human visual cortex excitability by sounds. Current Biology, 19, 1799-1805.
75. Romei, V., Murray, M. M., Cappe, C., & Thut, G. (2013). The contributions of sensory dominance and attentional bias to cross-modal enhancement of visual cortex excitability. Journal of Cognitive Neuroscience, 25, 1122-1135.
76. Romei, V., Murray, M. M., Merabet, L. B., & Thut, G. (2007). Occipital transcranial magnetic stimulation has opposing effects on visual and auditory stimulus detection: Implications for multisensory interactions. Journal of Neuroscience, 27, 11465-11472.
77. Romei, V., Thut, G., Mok, R. M., Schyns, P. G., & Driver, J. (2012). Causal implication by rhythmic transcranial magnetic stimulation of alpha frequency in feature-based local vs. global attention. European Journal of Neuroscience, 35, 968-974.
78. Sauseng, P., Klimesch, W., Heise, K. F., Gruber, W. R., Holz, E., Karim, A. A., et al. (2009). Brain oscillatory substrates of visual short-term memory capacity. Current Biology, 19, 1846-1852.
79. Schroeder, C. E., & Lakatos, P. (2009). Low-frequency neuronal oscillations as instruments of sensory selection. Trends in Neurosciences, 32, 9-18.
80. Schroeder, C. E., Lakatos, P., Kajikawa, Y., Partan, S., & Puce, A. (2008). Neuronal oscillations and visual amplification of speech. Trends in Cognitive Sciences, 12, 106-113.
81. Seitz, A. R., Kim, R., & Shams, L. (2006). Sound facilitates visual learning. Current Biology, 16, 1422-1427.
82. Shams, L., & Seitz, A. R. (2008). Benefits of multisensory learning. Trends in Cognitive Sciences, 12, 411-417.
83. Siegel, M., Donner, T. H., Oostenveld, R., Fries, P., & Engel, A. K. (2008). Neuronal synchronization along the dorsal visual pathway reflects the focus of spatial attention. Neuron, 60, 709-719.
84. Sikstrom, S., & Soderlund, G. (2007). Stimulus-dependent dopamine release in attention-deficit/hyperactivity disorder. Psychological Review, 114, 1047-1075.
85. Soderlund, G., Sikstrom, S., & Smart, A. (2007). Listen to the noise: Noise is beneficial for cognitive performance in ADHD. Journal of Child Psychology and Psychiatry, 48, 840-847.
86. Spence, C. (2011). Crossmodal correspondences: A tutorial review. Attention, Perception, & Psychophysics, 73, 971-995.
87. Spence, C., & Santangelo, V. (2009). Capturing spatial attention with multisensory cues: A review. Hearing Research, 258, 134-142.
88. Spence, C., Senkowski, D., & Roder, B. (2009). Crossmodal processing. Experimental Brain Research, 198, 107-111.
89. Spierer, L., Manuel, A. L., Bueti, D., & Murray, M. M. (2013). Contributions of pitch and bandwidth to sound-induced enhancement of visual cortex excitability in humans. Cortex. doi: 10.1016/j.cortex.2013.01.001.
90. Stein, B. E., London, N., Wilkonson, L. K., & Price, D. D. (1996). Enhancement of perceived visual intensity by auditory stimuli: A psychophysical analysis. Journal of Cognitive Neuroscience, 8, 497-506.
91. Stein, B. E., & Stanford, T. R. (2008). Multisensory integration: Current issues from the perspective of the single neuron. Nature Reviews Neuroscience, 9, 255-266.
92. Teder-Salejarvi, W. A., Di Russo, F., McDonald, J. J., & Hillyard, S. A. (2005). Effects of spatial congruity on audio-visual multimodal integration. Journal of Cognitive Neuroscience, 17, 1396-1409.
93. Thorne, J. D., & Debener, S. (2008). Irrelevant visual stimuli improve auditory task performance. NeuroReport, 19, 553-557.
94. Thut, G., Miniussi, C., & Gross, J. (2012). The functional importance of rhythmic activity in the brain. Current Biology, 22, R658-R663.
95. Thut, G., Nietzel, A., Brandt, S. A., & Pascual-Leone, A. (2006). Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. Journal of Neuroscience, 26, 9494-9502.
96. Van der Burg, E., Olivers, C. N., Bronkhorst, A. W., & Theeuwes, J. (2008). Pip and pop: Nonspatial auditory signals improve spatial visual search. Journal of Experimental Psychology: Human Perception and Performance, 34, 1053-1065.
97. van Dijk, H., Schoffelen, J. M., Oostenveld, R., & Jensen, O. (2008). Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. Journal of Neuroscience, 28, 1816-1823.
98. VanRullen, R. (2011). Four common conceptual fallacies in mapping the time course of recognition. Frontiers in Psychology, 2, 365.
99. VanRullen, R., Busch, N. A., Drewes, J., & Dubois, J. (2011). Ongoing EEG phase as a trial-by-trial predictor of perceptual and attentional variability. Frontiers in Psychology, 2, 60.
100. von Stein, A., Chiang, C., & Konig, P. (2000). Top-down processing mediated by interareal synchronization. Proceedings of the National Academy of Sciences, U.S.A., 97, 14748-14753.
101. Ward, L. M., MacLean, S. E., & Kirschner, A. (2010). Stochastic resonance modulates neural synchronization within and between cortical sources. PLoS One, 5, e14371.
102. Watkins, S., Shams, L., Josephs, O., & Rees, G. (2007). Activity in human V1 follows multisensory perception. Neuroimage, 37, 572-578.
103. Werner, S., & Noppeney, U. (2010). Distinct functional contributions of primary sensory and association areas to audiovisual integration in object categorization. Journal of Neuroscience, 30, 2662-2675.
104. Wichmann, F. A., & Hill, N. J. (2001). The psychometric function: II. Bootstrap-based confidence intervals and sampling. Perception & Psychophysics, 63, 1314-1329.
105. Wiesenfeld, K., & Moss, F. (1995). Stochastic resonance and the benefits of noise. Nature, 373, 33-36.
106. Womelsdorf, T., & Fries, P. (2007). The role of neuronal synchronization in selective attention. Current Opinion in Neurobiology, 17, 154-160.
107. Zannoli, M., Cass, J., Mamassian, P., & Alais, D. (2012). Synchronized audio-visual transients drive efficient visual search for motion-in-depth. PLoS One, 7, e37190.