Entrainment of perceptually relevant brain oscillations by non-invasive rhythmic stimulation of the human brain

Frontiers in Psychology

Volumn 2, Issue JUL, 2011, Pages

  Thut, Gregor ^a   Schyns, Philippe G ^a   Gross, Joachim ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

Author keywords

Brain oscillations; Entrainment; Perception; Rhythmic brain stimulation

Indexed keywords

EID: 84858861207     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2011.00170     Document Type: Review

References (85)

1. Antal, A., Boros, K., Poreisz, C., Chaieb, L., Terney, D., and Paulus, W. (2008). Comparatively weak after-effects of transcranial alternating current stimulation (tACS) on cortical excitability in humans. Brain Stimul. 1, 97-105.
2. Basar, E. (1980). EEG-Brain Dynamics: Relation Between EEG and Brain Evoked Potentials. Amsterdam: Elsevier.
3. Bergmann, T. O., Groppa, S., Seeger, M., Molle, M., Marshall, L., and Siebner, H. R. (2009). Acute changes in motor cortical excitability during slow oscillatory and constant anodal transcranial direct current stimulation. J. Neurophysiol. 102, 2303-2311.
4. Bohorquez, J., and Ozdamar, O. (2008). Generation of the 40-Hz auditory steady-state response (ASSR) explained using convolution. Clin. Neurophysiol. 119, 2598-2607.
5. Buzsáki, G., and Draguhn, A. (2004). Neuronal oscillations in cortical networks. Science 304, 1926-1929.
6. Capilla, A., Pazo-Alvarez, P., Darriba, A., Campo, P., and Gross, J. (2011). Steady-state visual evoked potentials can be explained by temporal superposition of transient event-related responses. PLoS ONE 6, e14543. doi: 10.1371/journal.pone.0014543
7. David, O., Kilner, J. M., and Friston, K. J. (2006). Mechanisms of evoked and induced responses in MEG/EEG. Neuroimage 31, 1580-1591.
8. Ding, J., Sperling, G., and Srinivasan, R. (2006). Attentional modulation of SSVEP power depends on the network tagged by the flicker frequency. Cereb. Cortex 16, 1016-1029.
9. Feurra, M., Paulus, W., Walsh, V., and Kanai, R. (2011). Frequency specific modulation of human somatosensory cortex. Front. Psychol. 2:13. doi: 10.3389/fpsyg.2011.00013
10. Foxe, J. J., and Snyder, A. C. (2011). The role of alpha-band brain oscillations as a sensory suppression mecha-
11. nism during selective attention. Front. Psychol. 2:154. doi: 10.3389/ fpsyg.2011.00154
12. Freunberger, R., Werkle-Bergner, M., Griesmayr, B., Lindenberger, U., and Klimesch, W. (2011). Brain oscillatory correlates of working memory constraints. Brain Res. 1375, 93-102.
13. Fries, P. (2005). A mechanism for cognitive dynamics: neuronal communication through neuronal coherence. Trends Cogn. Sci. 9, 474-480.
14. Fuggetta, G., Fiaschi, A., and Manganotti, P. (2005). Modulation of cortical oscillatory activities induced by varying single-pulse transcranial magnetic stimulation intensity over the left primary motor area: a combined EEG and TMS study. Neuroimage 27, 896-908.
15. Glass, L. (2001). Synchronization and rhythmic processes in physiology. Nature 410, 277-284.
16. Gould, I. C., Rushworth, M. F., and Nobre, A. C. (2011). Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations. J. Neurophysiol. 105, 1318-1326.
17. Gouwens, N. W., Zeberg, H., Tsumoto, K., Tateno, T., Aihara, K., and Robinson, H. P. (2010). Synchronization of firing in cortical fast-spiking interneurons at gamma frequencies: a phase-resetting analysis. PLoS Comput. Biol. 6, e1000951. doi: 10.1371/journal.pcbi. 1000951
18. Hallett, M. (2007). Transcranial magnetic stimulation: a primer. Neuron 55, 187-199.
19. Herrmann, C. S. (2001). Human EEG responses to 1-100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena. Exp. Brain Res. 137, 346-353.
20. Hutcheon, B., and Yarom, Y. (2000). Resonance, oscillation and the intrinsic frequency preferences of neurons. Trends Neurosci. 23, 216-222.
21. Ilmoniemi, R. J., and Kicić, D. (2010). Methodology for combined TMS and EEG. Brain Topogr. 22, 233-248.
22. Izhikevich, E. M. (2010). Dynamical Systems in Neuroscience: The Geometry of Excitability and Bursting. Cambridge: MIT Press.
23. Jensen, O., and Mazaheri, A. (2010). Shaping functional architecture by oscillatory alpha activity: gating by inhibition. Front. Hum. Neurosci. 4:186. doi: 10.3389/fnhum.2010.00186
24. Johnson, J. S., Hamidi, M., and Postle, B. R. (2010). Using EEG to explore how rTMS produces its effects on behavior. Brain Topogr. 22, 281-293.
25. Kanai, R., Chaieb, L., Antal, A., Walsh, V., and Paulus, W. (2008). Frequency-dependent electrical stimulation of the visual cortex. Curr. Biol. 8, 1839-1843.
26. Kelly, S. P., Lalor, E. C., Reilly, R. B., and Foxe, J. J. (2006). Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. J. Neurophysiol. 95, 3844-3851.
27. Kim, Y. J., Grabowecky, M., Paller, K. A., Muthu, K., and Suzuki, S. (2007). Attention induces synchronizationbased response gain in steady-state visual evoked potentials. Nat. Neurosci. 10, 117-125.
28. Klimesch, W., Sauseng, P., and Gerloff, C. (2003). Enhancing cognitive performance with repetitive transcranial magnetic stimulation at human individual alpha frequency. Eur. J. Neurosci. 17, 1129-1133.
29. Klimesch, W., Sauseng, P., and Hanslmayr, S. (2007a). EEG alpha oscillations: the inhibition-timing hypothesis. Brain Res. Rev. 53, 63-88.
30. Klimesch, W., Sauseng, P., Hanslmayr, S., Gruber, W., and Freunberger, R. (2007b). Event-related phase reorganization may explain evoked neural dynamics. Neurosci. Biobehav. Rev. 31, 1003-1016.
31. 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.
32. 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.
33. Lorincz, M. L., Kékesi, K. A., Juhász, G., Crunelli, V., and Hughes, S. W. (2009). Temporal framing of thalamic relay-
34. mode firing by phasic inhibition during the alpha rhythm. Neuron 63, 683-696.
35. Makeig, S., Westerfield, M., Jung, T. P., Enghoff, S., Townsend, J., Courchesne, E., and Sejnowski, T. J. (2002). Dynamic brain sources of visual evoked responses. Science 295, 690-694.
36. Marshall, L., Helgadottir, H., Molle, M., and Born, J. (2006). Boosting slow oscillations during sleep potentiates memory. Nature 444, 610-613.
37. Mathewson, K. E., Fabiani, M., Gratton, G., Beck, D. M., and Lleras, A. (2010). Rescuing stimuli from invisibility: inducing a momentary release from visual masking with pre-target entrainment. Cognition 115, 186-191.
38. 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.
39. Mathewson, K. E., Lleras, A., Beck, D. M., Fabiani, M., Ro, T., and Gratton, G. (2011). Pulsed out of awareness: EEG alpha oscillations represent a pulsed inhibition of ongoing cortical processing. Front. Psychol. 2:99. doi: 10.3389/ fpsyg.2011.00099
40. Mazzoni, A., Whittingstall, K., Brunel, N., Logothetis, N. K., and Panzeri, S. (2010). Understanding the relationships between spike rate and delta/ gamma frequency bands of LFPs and EEGs using a local cortical network model. Neuroimage 52, 956-972.
41. Moliadze, V., Antal, A., and Paulus, W. (2010). Boosting brain excitability by transcranial high frequency stimulation in the ripple range. J. Physiol. 588, 4891-4904.
42. Morgan, S. T., Hansen, J. C., and Hillyard, S. A. (1996). Selective attention to stimulus location modulates the steady-state visual evoked potential. Proc. Natl. Acad. Sci. U.S.A. 93, 4770-4774.
43. Müller, M. M., Teder-Sälejärvi, W., and Hillyard, S. A. (1998). The time course of cortical facilitation during cued shifts of spatial attention. Nat. Neurosci. 1, 631-634.
44. Niedermeyer, E., and Silva, F. D. (2004). Electroencephalography: Basic Principles, Clinical Applications and Related Fields, 5th Edn. Philadelphia, PA: Lippincott Williams and Wilkins.
45. Nitsche, M. A., Fricke, K., Henschke, U., Schlitterlau, A., Liebetanz, D., Lang, N., Henning, S., Tergau, F., and Paulus, W. (2003). Pharmacological modulation of cortical excitability shifts induced by transcranial direct current stimulation in humans. J. Physiol. 553, 293-301.
46. Nobre, A. C. (2001). Orienting attention to instants in time. Neuropsychologia 39, 1317-1328.
47. Ozen, S., Sirota, A., Belluscio, M. A., Anastassiou, C. A., Stark, E., Koch, C., and Buzsaki, G. (2010). Transcranial electric stimulation entrains cortical neuronal populations in rats. J. Neurosci. 30, 11476-11485.
48. Palva, S., and Palva, J. M. (2007). New vistas for alpha-frequency band oscillations. Trends Neurosci. 30, 150-158.
49. Panzeri, S., Brunel, N., Logothetis, N. K., and Kayser, C. (2010). Sensory neural codes using multiplexed temporal scales. Trends Neurosci. 33, 111-120.
50. Parkkonen, L., Andersson, J., Hämäläinen, M., and Hari, R. (2008). Early visual brain areas reflect the percept of an ambiguous scene. Proc. Natl. Acad. Sci. U.S.A. 105, 20500-20504.
51. Paus, T., Sipila, P. K., and Strafella, A. P. (2001). Synchronization of neuronal activity in the human primary motor cortex by transcranial magnetic stimulation: an EEG study. J. Neurophysiol. 86, 1983-1990.
52. Picton, T. W., John, M. S., Dimitrijevic, A., and Purcell, D. (2003). Human auditory steady-state responses. Int. J. Audiol. 42, 177-219.
53. Pikovsky, A., Rosenblum, M., and Kurths, J. (2003). Synchronization: A Universal Concept in Nonlinear Sciences, 1st Edn. New York, NY: Cambridge University Press.
54. Purpura, D. P., and McMurtry, J. G. (1965). Intracellular activities and evoked potential changes during polarization of motor cortex. J. Neurophysiol. 28, 166-185.
55. Rager, G., and Singer, W. (1998). The response of cat visual cortex to flicker stimuli of variable frequency. Eur. J. Neurosci. 10, 1856-1877.
56. Regan, D. (1988). Human Brain Electrophysiology: Evoked Potentials and Evoked Magnetic Fields in Science and Medicine. New York, NY: Appleton & Lange.
57. Romei, V., Driver, J., Schyns, P., and Thut, G. (2011). Rhythmic TMS over right parietal cortex causally links distinct brain frequencies to global versus local visual processing. Curr. Biol. 21, 334-733.
58. Romei, V., Gross, J., and Thut, G. (2010). On the role of prestimulus alpha rhythms over occipito-parietal areas in visual input regulation: correlation or causation? J. Neurosci. 30, 8692-8697.
59. Rosanova, M., Casali, A., Bellina, V., Resta, F., Mariotti, M., and Massimini, M. (2009). Natural frequencies of human corticothalamic circuits. J. Neurosci. 29, 7679-7685.
60. Ross, B., Herdman, A. T., and Pantev, C. (2005). Stimulus induced desynchronization of human auditory 40-Hz steady-state responses. J. Neurophysiol. 94, 4082-4093.
61. Salinas, E., and Sejnowski, T. J. (2001). Correlated neuronal activity and the flow of neural information. Nat. Rev. Neurosci. 2, 539-550.
62. Sauseng, P., Klimesch, W., Heise, K. F., Gruber, W. R., Holz, E., Karim, A. A., Glennon, M., Gerloff, C., Birbaumer, N., and Hummel, F. C. (2009). Brain oscillatory substrates of visual shortterm memory capacity. Curr. Biol. 19, 1846-1852.
63. Sauseng, P., Klimesch, W., Stadler, W., Schabus, M., Doppelmayr, M., Hanslmayr, S., Gruber, W. R., and Birbaumer, N. (2005). A shift of visual spatial attention is selectively associated with human EEG alpha activity. Eur. J. Neurosci. 22, 2917-2926.
64. Sayers, B. M., Beagley, H. A., and Henshall, W. R. (1974). The mechanism of auditory evoked EEG responses. Nature 247, 481-483.
65. Schnitzler, A., and Gross, J. (2005). Normal and pathological oscillatory communication in the brain. Nat. Rev. Neurosci. 6, 285-296.
66. Schwiedrzik, C. M. (2009). Retina or visual cortex? The site of phosphene induction by transcranial alternating current stimulation. Front. Integr. Neurosci. 3:6. doi: 10.3389/neuro.07.006.2009
67. Shallice, T. (1988). From Neuropsychology to Mental Structure. Cambridge: Cambridge University Press.
68. Siebner, H. R., and Ziemann, U. (2010). Rippling the cortex with high-frequency (>100 Hz) alternating current stimulation. J. Physiol. 588, 4851-4852.
69. Singer, W., and Gray, C. M. (1995). Visual feature integration and the temporal correlation hypothesis. Annu. Rev. Neurosci. 18, 555-586.
70. Smith, M. L., Gosselin, F., and Schyns, P. G. (2005). Perceptual moments of conscious visual experience inferred from oscillatory brain activity. Proc. Natl. Acad. Sci. U.S.A. 103, 5626-5631.
71. Smith, M. L., Gosselin, F., and Schyns, P. G. (2007). From a brain to its category via a few information processing states in the brain. Neuroimage 37, 974-984.
72. Tass, P. A. (2002). Desynchronization of brain rhythms with soft phaseresetting techniques. Biol. Cybern. 87, 102-115.
73. Thut, G., and Miniussi, C. (2009). New insights into rhythmic brain activity from TMS-EEG studies. Trends Cogn. Sci. 13, 182-189.
74. Thut, G., Nietzel, A., Brandt, S. A., and Pascual-Leone, A. (2006). Alpha-band electroencephalographic activity over occipital cortex indexes visuospatial attention bias and predicts visual target detection. J. Neurosci. 26, 9494-9502.
75. 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.
76. Thut, G., Veniero, D., Romei, V., Miniussi, C., Schyns, P., and Gross, J. (2011). Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr. Biol. doi:10.1016/j. cub.2011.05.049. [Epub ahead of print].
77. Van Der Werf, Y. D., and Paus, T. (2006). The neural response to transcranial magnetic stimulation of the human motor cortex. I. Intracortical and cortico-cortical contributions. Exp. Brain Res. 175, 231-245.
78. VanRullen, R., Busch, N., Drewes, J., and Dubois, J. (2011). Ongoing EEG phase as a trial-by-trial predictor of perceptual and attentional variability. Front. Psychol. 2:60. doi: 10.3389/ fpsyg.2011.00060
79. Veniero, D., Brignani, D., Thut, G., and Miniussi, C. (2011). Alpha-generation as basic response-signature to transcranial magnetic stimulation (TMS) targeting the human resting motor cortex: a TMS/EEG co-registration study. Psychophysiology. doi: 10.1111/j.1469-8986.2011.01218.x. [Epub ahead of print].
80. von Stein, A., Chiang, C., and König, P. (2000). Top-down processing mediated by interareal synchronization. Proc. Natl. Acad. Sci. U.S.A. 97, 14748-14753.
81. Whittington, M. A., Stanford, I. M., Colling, S. B., Jefferys, J. G., and Traub, R. D. (1997). Spatiotemporal patterns of gamma frequency oscillations tetanically induced in the rat hippocampal slice. J. Physiol. 502, 591-607.
82. Winfree, A. T. (2001). The Geometry of Biological Time, 2nd Edn. Berlin: Springer.
83. Worden, M. S., Foxe, J. J., Wang, N., and Simpson, G. V. (2000). Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha-band electroencephalography increases over occipital cortex. J. Neurosci. 20, RC63.
84. Zaehle, T., Lenz, D., Ohl, F. W., and Herrmann, C. S. (2010a). Resonance phenomena in the human auditory cortex: individual resonance frequencies of the cerebral cortex determine electrophysiological responses. Exp. Brain Res. 203, 629-635.
85. Zaehle, T., Rach, S., and Herrmann, C. S. (2010b). Transcranial alternating current stimulation enhances individual alpha activity in human EEG. PLoS ONE 5, e13766. doi: 10.1371/journal. pone.0013766