Left parietal tACS at alpha frequency induces a shift of visuospatial attention


Autoři: Teresa Schuhmann aff001;  Selma K. Kemmerer aff001;  Felix Duecker aff001;  Tom A. de Graaf aff001;  Sanne ten Oever aff001;  Peter De Weerd aff001;  Alexander T. Sack aff001
Působiště autorů: Department of Cognitive Neuroscience, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, The Netherlands aff001;  Brain Imaging Center, Maastricht, The Netherlands aff002;  Department of Psychiatry and Neuropsychology, School for Mental Health and Neuroscience (MHeNs), Brain + Nerve Centre, Maastricht University Medical Centre+ (MUMC+), Maastricht, The Netherlands aff003
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0217729

Souhrn

Background

Voluntary shifts of visuospatial attention are associated with a lateralization of parieto-occipital alpha power (7-13Hz), i.e. higher power in the hemisphere ipsilateral and lower power contralateral to the locus of attention. Recent noninvasive neuromodulation studies demonstrated that alpha power can be experimentally increased using transcranial alternating current stimulation (tACS).

Objective/Hypothesis

We hypothesized that tACS at alpha frequency over the left parietal cortex induces shifts of attention to the left hemifield. However, spatial attention shifts not only occur voluntarily (endogenous/ top-down), but also stimulus-driven (exogenous/ bottom-up). To study the task-specificity of the potential effects of tACS on attentional processes, we administered three conceptually different spatial attention tasks.

Methods

36 healthy volunteers were recruited from an academic environment. In two separate sessions, we applied either high-density tACS at 10Hz, or sham tACS, for 35–40 minutes to their left parietal cortex. We systematically compared performance on endogenous attention, exogenous attention, and stimulus detection tasks.

Results

In the endogenous attention task, a greater leftward bias in reaction times was induced during left parietal 10Hz tACS as compared to sham. There were no stimulation effects in either the exogenous attention or the stimulus detection task.

Conclusion

The study demonstrates that high-density tACS at 10Hz can be used to modulate visuospatial attention performance. The tACS effect is task-specific, indicating that not all forms of attention are equally susceptible to the stimulation.

Klíčová slova:

Attention – Functional electrical stimulation – Reaction time – Sensory cues – Target detection – Vision – Transcranial alternating current stimulation – Parietal lobe


Zdroje

1. Posner MI. Orienting of attention. Q J Exp Psychol. 1980;32: 3–25. doi: 10.1080/00335558008248231 7367577

2. Kim H, Levine SC. Sources of between-subjects variability in perceptual asymmetries: A meta-analytic review. Neuropsychologia. 1991;29: 877–888. doi: 10.1016/0028-3932(91)90053-b 1834960

3. Duecker F, Schuhmann T, Bien N, Jacobs C, Sack AT. Moving Beyond Attentional Biases: Shifting the Interhemispheric Balance between Left and Right Posterior Parietal Cortex Modulates Attentional Control Processes. J Cogn Neurosci. 2017;29: 1267–1278. doi: 10.1162/jocn_a_01119 28294715

4. Shepherd M, Müller HJ. Movement versus focusing of visual attention. Percept Psychophys. 1989; doi: 10.3758/BF03204974 2762102

5. Cheal M Lou Lyon DR. Central and Peripheral Precuing of Forced-choice Discrimination. Q J Exp Psychol Sect A. 1991; doi: 10.1080/14640749108400960 1775667

6. Buxbaum LJ, Ferraro MK, Veramonti T, Farne A, Whyte J, Ladavas E, et al. Hemispatial neglect: Subtypes, neuroanatomy, and disability. Neurology. 2004;62: 749–756. doi: 10.1212/01.wnl.0000113730.73031.f4 15007125

7. Ringman JM, Saver JL, Woolson RF, Clarke WR, Adams HP. Frequency, risk factors, anatomy, and course of unilateral neglect in an acute stroke cohort. Neurology. 2004;63: 468–474. doi: 10.1212/01.wnl.0000133011.10689.ce 15304577

8. Vallar G. Spatial hemineglect in humans. Prog Neurobiol. 1998; doi: 10.1016/S0301-0082(00)00028-9

9. Smania N. The spatial distribution of visual attention in hemineglect and extinction patients. Brain. 1998;121: 1759–1770. doi: 10.1093/brain/121.9.1759 9762963

10. Marzi CA, Natale E, Anderson B. Mapping spatial attention with reaction time in neglect patients. The Cognitive and Neural Bases of Spatial Neglect. Oxford University Press; 2002. pp. 274–288. doi: 10.1093/acprof:oso/9780198508335.003.0020

11. Bartolomeo P, Sieroff E, Decaix C, Chokron S. Modulating the attentional bias in unilateral neglect: the effects of the strategic set. Exp Brain Res. 2001;137: 432–444. doi: 10.1007/s002210000642 11355388

12. Morrow LA, Ratcliff G. The disengagement of covert attention and the neglect syndrome. Psychobiology. 1988;16: 261–269. doi: 10.3758/BF03327316

13. Posner MI, Cohen Y. Components of visual orienting. J Cogn Neurosci. 1984;32: 531–556. doi: 10.1162/jocn.1991.3.4.335 23967813

14. Kerkhoff G. Spatial hemineglect in humans. Progress in Neurobiology. 2001. doi: 10.1016/S0301-0082(00)00028-9

15. Ros T, Michela A, Bellman A, Vuadens P, Saj A, Vuilleumier P. Increased Alpha-Rhythm Dynamic Range Promotes Recovery from Visuospatial Neglect: A Neurofeedback Study. Neural Plast. 2017;2017: 1–9. doi: 10.1155/2017/7407241 28529806

16. Finnigan S, van Putten MJAM. EEG in ischaemic stroke: Quantitative EEG can uniquely inform (sub-)acute prognoses and clinical management. Clin Neurophysiol. 2013;124: 10–19. doi: 10.1016/j.clinph.2012.07.003 22858178

17. Sainio K, Stenberg D, Keskimäki I, Muuronen A, Kaste M. Visual and spectral EEG analysis in the evaluation of the outcome in patients with ischemic brain infarction. Electroencephalogr Clin Neurophysiol. 1983;56: 117–124. doi: 10.1016/0013-4694(83)90066-4 6191943

18. Giaquinto S, Cobianchi A, Macera F, Nolfe G. EEG recordings in the course of recovery from stroke. Stroke. 1994;25: 2204–2209. doi: 10.1161/01.str.25.11.2204 7974546

19. de Weerd AW, Veldhuizen RJ, Veering MM, Poortvliet DCJ, Jonkman EJ. Recovery from cerebral ischaemia. EEG, cerebral blood flow and clinical symptomatology in the first three years after a stroke. Electroencephalogr Clin Neurophysiol. 1988;70: 197–204. doi: 10.1016/0013-4694(88)90080-6 2458226

20. Szelies B, Mielke R, Kessler J, Heiss W-D. Prognostic relevance of quantitative topographical EEG in patients with poststroke aphasia. Brain Lang. 2002;82: 87–94. doi: 10.1016/s0093-934x(02)00004-4 12174818

21. Başar E, Başar-Eroglu C, Karakaş S, Schürmann M. Are cognitive processes manifested in event-related gamma, alpha, theta and delta oscillations in the EEG? Neurosci Lett. 1999; doi: 10.1016/S0304-3940(98)00934-3

22. Klimesch W. Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci. 2012;16: 606–617. doi: 10.1016/j.tics.2012.10.007 23141428

23. Klimesch W, Sauseng P, Hanslmayr S. EEG alpha oscillations: The inhibition-timing hypothesis. Brain Research Reviews. 2007. doi: 10.1016/j.brainresrev.2006.06.003 16887192

24. Gould IC, Rushworth MF, Nobre AC. Indexing the graded allocation of visuospatial attention using anticipatory alpha oscillations. J Neurophysiol. 2011;105: 1318–1326. doi: 10.1152/jn.00653.2010 21228304

25. Händel BF, Haarmeier T, Jensen O. Alpha Oscillations Correlate with the Successful Inhibition of Unattended Stimuli. J Cogn Neurosci. 2011;23: 2494–2502. doi: 10.1162/jocn.2010.21557 20681750

26. Sauseng P, Klimesch W, Stadler W, Schabus M, Doppelmayr M, Hanslmayr S, et al. A shift of visual spatial attention is selectively associated with human EEG alpha activity. Eur J Neurosci. 2005;22: 2917–2926. doi: 10.1111/j.1460-9568.2005.04482.x 16324126

27. Thut G, Nietzel A, Brandt SA, Pascual-Leone A. -Band Electroencephalographic Activity over Occipital Cortex Indexes Visuospatial Attention Bias and Predicts Visual Target Detection. J Neurosci. 2006;26: 9494–9502. doi: 10.1523/JNEUROSCI.0875-06.2006 16971533

28. Antal A, Paulus W. Transcranial Alternating Current Stimulation. Front Hum Neurosci. 2013;7: 317. doi: 10.3389/fnhum.2013.00317 23825454

29. Neuling T, Rach S, Herrmann CS. Orchestrating neuronal networks: sustained after-effects of transcranial alternating current stimulation depend upon brain states. Front Hum Neurosci. 2013;7: 161. doi: 10.3389/fnhum.2013.00161 23641206

30. Zaehle T, Rach S, Herrmann CS. Transcranial Alternating Current Stimulation Enhances Individual Alpha Activity in Human EEG. Aleman A, editor. PLoS One. 2010;5: e13766. doi: 10.1371/journal.pone.0013766 21072168

31. Kasten FH, Dowsett J, Herrmann CS. Sustained Aftereffect of α-tACS Lasts Up to 70 min after Stimulation. Front Hum Neurosci. 2016;10: 245. doi: 10.3389/fnhum.2016.00245 27252642

32. Witkowski M, Garcia-Cossio E, Chander BS, Braun C, Birbaumer N, Robinson SE, et al. Mapping entrained brain oscillations during transcranial alternating current stimulation (tACS). Neuroimage. 2016;140: 89–98. doi: 10.1016/j.neuroimage.2015.10.024 26481671

33. Feurra M, Paulus W, Walsh V, Kanai R. Frequency Specific Modulation of Human Somatosensory Cortex. Front Psychol. 2011;2: 13. doi: 10.3389/fpsyg.2011.00013 21713181

34. Kanai R, Chaieb L, Antal A, Walsh V, Paulus W. Frequency-Dependent Electrical Stimulation of the Visual Cortex. Curr Biol. 2008;18: 1839–1843. doi: 10.1016/j.cub.2008.10.027 19026538

35. Schwiedrzik C. Retina or visual cortex? The site of phosphene induction by transcranial alternating current stimulation. Front Integr Neurosci. 2009;3. doi: 10.3389/neuro.07.006.2009 19506706

36. Wach C, Krause V, Moliadze V, Paulus W, Schnitzler A, Pollok B. Effects of 10Hz and 20Hz transcranial alternating current stimulation (tACS) on motor functions and motor cortical excitability. Behav Brain Res. 2013;241: 1–6. doi: 10.1016/j.bbr.2012.11.038 23219965

37. Wöstmann M, Vosskuhl J, Obleser J, Herrmann CS. Opposite effects of lateralised transcranial alpha versus gamma stimulation on auditory spatial attention. Brain Stimul. 2018;11: 752–758. doi: 10.1016/j.brs.2018.04.006 29656907

38. Veniero D, Benwell CSY, Ahrens MM, Thut G. Inconsistent Effects of Parietal α-tACS on Pseudoneglect across Two Experiments: A Failed Internal Replication. Front Psychol. 2017;8: 952. doi: 10.3389/fpsyg.2017.00952 28642729

39. Corbetta M, Kincade JM, Ollinger JM, McAvoy MP, Shulman GL. Voluntary orienting is dissociated from target detection in human posterior parietal cortex. Nat Neurosci. 2000;3: 292–297. doi: 10.1038/73009 10700263

40. Yantis S, Schwarzbach J, Serences JT, Carlson RL, Steinmetz MA, Pekar JJ, et al. Transient neural activity in human parietal cortex during spatial attention shifts. Nat Neurosci. 2002; doi: 10.1038/nn921 12219097

41. Antal A, Alekseichuk I, Bikson M, Brockmöller J, Brunoni AR, Chen R, et al. Low intensity transcranial electric stimulation: Safety, ethical, legal regulatory and application guidelines. Clin Neurophysiol. 2017;128: 1774–1809. doi: 10.1016/j.clinph.2017.06.001 28709880

42. Datta A, Elwassif M, Battaglia F, Bikson M. Transcranial current stimulation focality using disc and ring electrode configurations: FEM analysis. J Neural Eng. 2008;5: 163–174. doi: 10.1088/1741-2560/5/2/007 18441418

43. Heise KF, Monteiro TS, Leunissen I, Mantini D, Swinnen SP. Distinct online and offline effects of alpha and beta transcranial alternating current stimulation (tACS) on continuous bimanual performance and task-set switching. Sci Rep. 2019; doi: 10.1038/s41598-019-39900-0 30816305

44. Saturnino GB, Thielscher A, Madsen KH, Knösche TR, Weise K. A principled approach to conductivity uncertainty analysis in electric field calculations. Neuroimage. 2019;188: 821–834. doi: 10.1016/j.neuroimage.2018.12.053 30594684

45. Saturnino GB, Puonti O, Nielsen JD, Antonenko D, Madsen KHH, Thielscher A. SimNIBS 2.1: A Comprehensive Pipeline for Individualized Electric Field Modelling for Transcranial Brain Stimulation. bioRxiv. 2018; doi: 10.1101/500314

46. Boayue NM, Csifcsák G, Puonti O, Thielscher A, Mittner M. Head models of healthy and depressed adults for simulating the electric fields of non-invasive electric brain stimulation. F1000Research. 2018;7: 704. doi: 10.12688/f1000research.15125.2 30505431

47. Saturnino GB, Antunes A, Thielscher A. On the importance of electrode parameters for shaping electric field patterns generated by tDCS. Neuroimage. 2015; doi: 10.1016/j.neuroimage.2015.06.067 26142274

48. Watson AB, Pelli DG. Quest: A Bayesian adaptive psychometric method. Percept Psychophys. 1983;33: 113–120. doi: 10.3758/bf03202828 6844102

49. Brainard DH. The Psychophysics Toolbox. Spat Vis. 1997; doi: 10.1163/156856897X00357

50. Liu X, Zhang J. Analysis of ordinal repeated measures data using generalized estimating equation. Sichuan Da Xue Xue Bao Yi Xue Ban. 2006;37: 798–800. 17037756

51. Kincade JM. An Event-Related Functional Magnetic Resonance Imaging Study of Voluntary and Stimulus-Driven Orienting of Attention. J Neurosci. 2005; doi: 10.1523/jneurosci.0236-05.2005 15872107

52. Ozaki TJ. Frontal-to-parietal top-down causal streams along the dorsal attention network exclusively mediate voluntary orienting of attention. PLoS One. 2011; doi: 10.1371/journal.pone.0020079 21611155

53. Worden MS, Foxe JJ, Wang N, Simpson G V. Anticipatory Biasing of Visuospatial Attention Indexed by Retinotopically Specific α-Bank Electroencephalography Increases over Occipital Cortex. J Neurosci. 2018; doi: 10.1523/jneurosci.20-06-j0002.2000 10704517

54. Müller HJ, Rabbitt PMA. Reflexive and voluntary orienting of visual attention: Time course of activation and resistance to interruption. J Exp Psychol Hum Percept Perform. 1989;15: 315–330. doi: 10.1037//0096-1523.15.2.315 2525601

55. van der Lubbe RHJ, Postma A. Interruption from irrelevant auditory and visual onsets even when attention is in a focused state. Exp Brain Res. 2005;164: 464–471. doi: 10.1007/s00221-005-2267-0 15785951

56. Yantis S, Jonides J. Abrupt Visual Onsets and Selective Attention: Voluntary Versus Automatic Allocation. J Exp Psychol Hum Percept Perform. 1990;16: 121–134. doi: 10.1037//0096-1523.16.1.121 2137514

57. Ergenoglu T, Demiralp T, Bayraktaroglu Z, Ergen M, Beydagi H, Uresin Y. Alpha rhythm of the EEG modulates visual detection performance in humans. Brain Res Cogn Brain Res. 2004;20: 376–383. doi: 10.1016/j.cogbrainres.2004.03.009 15268915

58. Hanslmayr S, Aslan A, Staudigl T, Klimesch W, Herrmann CS, Bäuml K-H. Prestimulus oscillations predict visual perception performance between and within subjects. Neuroimage. 2007;37: 1465–1473. doi: 10.1016/j.neuroimage.2007.07.011 17706433

59. Shipp S, Zeki S. Segregation and convergence of specialised pathways in macaque monkey visual cortex. J Anat. 1995;187: 547–562. 8586555

60. Sincich LC. Input to V2 Thin Stripes Arises from V1 Cytochrome Oxidase Patches. J Neurosci. 2005;25: 10087–10093. doi: 10.1523/JNEUROSCI.3313-05.2005 16267215

61. Bartels A, Zeki S. The architecture of the colour centre in the human visual brain: new results and a review *. Eur J Neurosci. 2000;12: 172–193. doi: 10.1046/j.1460-9568.2000.00905.x 10651872

62. Brewer AA, Liu J, Wade AR, Wandell BA. Visual field maps and stimulus selectivity in human ventral occipital cortex. Nat Neurosci. 2005;8: 1102–1109. doi: 10.1038/nn1507 16025108

63. Ghose GM, Maunsell JHR. Attentional modulation in visual cortex depends on task timing. Nature. 2002;419: 616–620. doi: 10.1038/nature01057 12374979

64. Hopfinger JB, Parsons J, Fröhlich F. Differential effects of 10-Hz and 40-Hz transcranial alternating current stimulation (tACS) on endogenous versus exogenous attention. Cogn Neurosci. 2017;8: 102–111. doi: 10.1080/17588928.2016.1194261 27297977

65. Ruhnau P, Neuling T, Fuscá M, Herrmann CS, Demarchi G, Weisz N. Eyes wide shut: Transcranial alternating current stimulation drives alpha rhythm in a state dependent manner. Sci Rep. 2016;6: 27138. doi: 10.1038/srep27138 27252047

66. Marx E, Deutschländer A, Stephan T, Dieterich M, Wiesmann M, Brandt T. Eyes open and eyes closed as rest conditions: Impact on brain activation patterns. Neuroimage. 2004; doi: 10.1016/j.neuroimage.2003.12.026 15050602

67. Adrian ED, Matthews BHC. The berger rhythm: Potential changes from the occipital lobes in man. Brain. 1934; doi: 10.1093/brain/57.4.355

68. Capilla A, Schoffelen J-M, Paterson G, Thut G, Gross J. Dissociated α-Band Modulations in the Dorsal and Ventral Visual Pathways in Visuospatial Attention and Perception. Cereb Cortex. 2014;24: 550–561. doi: 10.1093/cercor/bhs343 23118197

69. Kim Y-H, Gitelman DR, Parrish TB, Nobre AC, LaBar KS, Mesulam M-M. Posterior Cingulate Activation Varies According to the Effectiveness of Attentional Engagement. Neuroimage. 2018; doi: 10.1016/s1053-8119(18)30900-5

70. Hopf J-M, Mangun G. Shifting visual attention in space: an electrophysiological analysis using high spatial resolution mapping. Clin Neurophysiol. 2000;111: 1241–1257. doi: 10.1016/s1388-2457(00)00313-8 10880800

71. Kato C, Matsuo K, Matsuzawa M, Moriya T, Glover GH, Nakai T. Activation during endogenous orienting of visual attention using symbolic pointers in the human parietal and frontal cortices: a functional magnetic resonance imaging study. Neurosci Lett. 2001;314: 5–8. doi: 10.1016/s0304-3940(01)02207-8 11698133

72. Kasten FH, Maess B, Herrmann CS. Facilitated Event-Related Power Modulations during Transcranial Alternating Current Stimulation (tACS) Revealed by Concurrent tACS-MEG. eneuro. 2018;5. doi: 10.1523/ENEURO.0069-18.2018 30073188

73. Kasten FH, Herrmann CS. Transcranial Alternating Current Stimulation (tACS) Enhances Mental Rotation Performance during and after Stimulation. Front Hum Neurosci. 2017;11: 2. doi: 10.3389/fnhum.2017.00002 28197084

74. Meyer KN, Du F, Parks E, Hopfinger JB. Exogenous vs. endogenous attention: Shifting the balance of fronto-parietal activity. Neuropsychologia. 2018;111: 307–316. doi: 10.1016/j.neuropsychologia.2018.02.006 29425803

75. Meehan TP, Bressler SL, Tang W, Astafiev S V., Sylvester CM, Shulman GL, et al. Top-down cortical interactions in visuospatial attention. Brain Struct Funct. 2017;222: 3127–3145. doi: 10.1007/s00429-017-1390-6 28321551

76. Brindley GS. The site of electrical excitation of the human eye. J Physiol. 1955;127: 189–200. doi: 10.1113/jphysiol.1955.sp005248 14354638

77. Kar K, Krekelberg B. Transcranial electrical stimulation over visual cortex evokes phosphenes with a retinal origin. J Neurophysiol. 2012; doi: 10.1152/jn.00505.2012 22855777

78. Schutter DJLG, Hortensius R. Retinal origin of phosphenes to transcranial alternating current stimulation. Clin Neurophysiol. 2010; doi: 10.1016/j.clinph.2009.10.038 20188625

79. Laakso I, Hirata A. Computational analysis shows why transcranial alternating current stimulation induces retinal phosphenes. J Neural Eng. 2013; doi: 10.1088/1741-2560/10/4/046009 23813466

80. Herrmann CS, Strüber D, Helfrich RF, Engel AK. EEG oscillations: From correlation to causality. Int J Psychophysiol. 2016;103: 12–21. doi: 10.1016/j.ijpsycho.2015.02.003 25659527

81. Veniero D, Vossen A, Gross J, Thut G. Lasting EEG/MEG Aftereffects of Rhythmic Transcranial Brain Stimulation: Level of Control Over Oscillatory Network Activity. Front Cell Neurosci. 2015;9. doi: 10.3389/fncel.2015.00477 26696834

82. Okamura H, Jing H, Takigawa M. EEG Modification Induced by Repetitive Transcranial Magnetic Stimulation. J Clin Neurophysiol. 2001;18: 318–325. doi: 10.1097/00004691-200107000-00003 11673697

83. Woźniak-Kwaśniewska A, Szekely D, Aussedat P, Bougerol T, David O. Changes of oscillatory brain activity induced by repetitive transcranial magnetic stimulation of the left dorsolateral prefrontal cortex in healthy subjects. Neuroimage. 2014;88: 91–99. doi: 10.1016/j.neuroimage.2013.11.029 24269574

84. Griškova I, Rukšėnas O, Dapšys K, Herpertz S, Höppner J. The effects of 10Hz repetitive transcranial magnetic stimulation on resting EEG power spectrum in healthy subjects. Neurosci Lett. 2007;419: 162–167. doi: 10.1016/j.neulet.2007.04.030 17478041

85. Herrmann CS, Rach S, Neuling T, Strüber D. Transcranial alternating current stimulation: a review of the underlying mechanisms and modulation of cognitive processes. Front Hum Neurosci. 2013;7: 279. doi: 10.3389/fnhum.2013.00279 23785325

86. Vossen A, Gross J, Thut G. Alpha Power Increase After Transcranial Alternating Current Stimulation at Alpha Frequency (α-tACS) Reflects Plastic Changes Rather Than Entrainment. Brain Stimul. 2015;8: 499–508. doi: 10.1016/j.brs.2014.12.004 25648377

87. Helfrich RF, Schneider TR, Rach S, Trautmann-Lengsfeld SA, Engel AK, Herrmann CS. Entrainment of brain oscillations by transcranial alternating current stimulation. Curr Biol. 2014; doi: 10.1016/j.cub.2013.12.041 24461998

88. Chan CY, Nicholson C. Modulation by applied electric fields of Purkinje and stellate cell activity in the isolated turtle cerebellum. J Physiol. 1986;371: 89–114. doi: 10.1113/jphysiol.1986.sp015963 3701658

89. Ozen S, Sirota A, Belluscio MA, Anastassiou CA, Stark E, Koch C, et al. Transcranial Electric Stimulation Entrains Cortical Neuronal Populations in Rats. J Neurosci. 2010;30: 11476–11485. doi: 10.1523/JNEUROSCI.5252-09.2010 20739569

90. Reato D, Rahman A, Bikson M, Parra LC. Low-Intensity Electrical Stimulation Affects Network Dynamics by Modulating Population Rate and Spike Timing. J Neurosci. 2010;30: 15067–15079. doi: 10.1523/JNEUROSCI.2059-10.2010 21068312

91. Johnson M, Alekseichuk I, Krieg J, Doyle A, Yu Y, Vitek J, et al. Dose-dependent effects of transcranial alternating current stimulation on spike timing in awake nonhuman primates. bioRxiv. 2019; 696344. doi: 10.1101/696344

92. Lorenz I, Müller N, Schlee W, Hartmann T, Weisz N. Loss of alpha power is related to increased gamma synchronization—A marker of reduced inhibition in tinnitus? Neurosci Lett. 2009;453: 225–228. doi: 10.1016/j.neulet.2009.02.028 19429040

93. Lundqvist M, Herman P, Lansner A. Theta and Gamma Power Increases and Alpha/Beta Power Decreases with Memory Load in an Attractor Network Model. J Cogn Neurosci. 2011;23: 3008–3020. doi: 10.1162/jocn_a_00029 21452933

94. Spaak E, Bonnefond M, Maier A, Leopold DA, Jensen O. Layer-Specific Entrainment of Gamma-Band Neural Activity by the Alpha Rhythm in Monkey Visual Cortex. Curr Biol. 2012;22: 2313–2318. doi: 10.1016/j.cub.2012.10.020 23159599

95. Mueller M, Bosch J, Elbert T, Kreiter A, Sosa M, Sosa P, et al. Visually induced gamma-band responses in human electroencephalographic activity ? a link to animal studies. Exp Brain Res. 1996; 112 doi: 10.1007/BF00227182

96. Tallon-Baudry C, Bertrand O, Delpuech C, Pernier J. Oscillatory γ-Band (30–70 Hz) Activity Induced by a Visual Search Task in Humans. J Neurosci. 1997;17: 722–734. doi: 10.1523/JNEUROSCI.17-02-00722.1997 8987794

97. Gruber T, Mueller MM, Keil A, Elbert T. Selective visual-spatial attention alters induced gamma band responses in the human EEG. Clin Neurophysiol. 1999;110: 2074–2085. doi: 10.1016/s1388-2457(99)00176-5 10616112

98. Wach C, Krause V, Moliadze V, Paulus W, Schnitzler A, Pollok B. The effect of 10 Hz transcranial alternating current stimulation (tACS) on corticomuscular coherence. Front Hum Neurosci. 2013;7. doi: 10.3389/fnhum.2013.00511 24009573

99. Kerkhoff G, Schenk T. Rehabilitation of neglect: An update. Neuropsychologia. 2012;50: 1072–1079. doi: 10.1016/j.neuropsychologia.2012.01.024 22306520

100. Rossetti Y, Rode G, Pisella L, Farné A, Li L, Boisson D, et al. Prism adaptation to a rightward optical deviation rehabilitates left hemispatial neglect. Nature. 1998;395: 166–169. doi: 10.1038/25988 9744273

101. Cappa S, Sterzi R, Vallar G, Bisiach E. Remission of hemineglect and anosognosia during vestibular stimulation. Neuropsychologia. 1987;25: 775–782. doi: 10.1016/0028-3932(87)90115-1 3501552

102. Rubens AB. Caloric stimulation and unilateral visual neglect. Neurology. 1985;35: 1019–1019. doi: 10.1212/wnl.35.7.1019 4010940

103. Fierro B, Brighina F, Bisiach E. Improving Neglect by TMS. Behav Neurol. 2006;17: 169–176. doi: 10.1155/2006/465323 17148837

104. Oliveri M, Bisiach E, Brighina F, Piazza A, La Bua V, Buffa D, et al. rTMS of the unaffected hemisphere transiently reduces contralesional visuospatial hemineglect. Neurology. 2001;57: 1338–1340. doi: 10.1212/wnl.57.7.1338 11591865

105. Antal A, Paulus W. Investigating Neuroplastic Changes in the Human Brain Induced by Transcranial Direct (tDCS) and Alternating Current (tACS) Stimulation Methods. Clin EEG Neurosci. 2012;43: 175–175. doi: 10.1177/1550059412448030 22956645


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