Local entrainment of alpha oscillations by visual stimuli causes cyclic modulation of perception

Journal of Neuroscience

Volumn 34, Issue 10, 2014, Pages 3536-3544

  Spaak, Eelke ^a   de Lange, Floris P ^a   Jensen, Ole ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

Author keywords

Alpha oscillations; Entrainment; Rhythmic stimulation; Visual perception

Indexed keywords

ADULT; ALPHA RHYTHM; ARTICLE; FEMALE; HUMAN; HUMAN EXPERIMENT; MAGNETOENCEPHALOGRAPHY; MALE; NORMAL HUMAN; PRIORITY JOURNAL; TASK PERFORMANCE; VISION; VISUAL CORTEX; VISUAL FIELD; VISUAL ORIENTATION; VISUAL STIMULATION; VISUAL THRESHOLD;

ALPHA OSCILLATIONS; ENTRAINMENT; RHYTHMIC STIMULATION; VISUAL PERCEPTION;

ADOLESCENT; ADULT; ALPHA RHYTHM; FEMALE; HUMANS; MALE; MIDDLE AGED; PERIODICITY; PHOTIC STIMULATION; VISUAL CORTEX; VISUAL PERCEPTION; YOUNG ADULT;

EID: 84895491403     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4385-13.2014     Document Type: Article

References (55)

1. Arnal LH, Giraud AL (2012) Cortical oscillations and sensory predictions. Trends Cogn Sci 16:390-398. CrossRef Medline
2. Bastiaansen MC, Knösche TR (2000) Tangential derivative mapping of axial MEG applied to event-related desynchronization research. Clin Neurophysiol 111:1300-1305. CrossRef Medline
3. Bollimunta A, Chen Y, Schroeder CE, Ding M (2008) Neuronal mechanisms of cortical alpha oscillations in awake-behaving macaques. J Neurosci 28:9976-9988. CrossRef Medline
4. Bollimunta A, Mo J, Schroeder CE, Ding M (2011) Neuronal mechanisms and attentional modulation of corticothalamic alpha oscillations. J Neurosci 31:4935-4943. CrossRef Medline
5. Bonnefond M, Jensen O (2012) Alpha oscillations serve to protect working memory maintenance against anticipated distracters. Curr Biol 22:1969-1974. CrossRef Medline
6. Busch NA, Dubois J, VanRullen R (2009) The phase of ongoing EEG oscillations predicts visual perception. J Neurosci 29:7869-7876. CrossRef Medline
7. Capilla A, Pazo-Alvarez P, Darriba A, Campo P, Gross J (2011) Steady-state visual evoked potentials can be explained by temporal superposition of transient event-related responses. PLoS One 6:e14543. CrossRef Medline
8. Capotosto P, Babiloni C, Romani GL, Corbetta M (2009) Frontoparietal cortex controls spatial attention through modulation of anticipatory alpha rhythms. J Neurosci 29:5863-5872. CrossRef Medline
9. Capotosto P, Babiloni C, Romani GL, Corbetta M (2012) Differential contribution of right and left parietal cortex to the control of spatial attention: a simultaneous EEG-rTMS study. Cereb Cortex 22:446-454. CrossRef Medline
10. Cousineau D (2005) Confidence intervals in within-subjects designs: a simpler solution to Loftus and Masson's method. Tutor Quant Methods Psychol 1:42-45.
11. Cravo AM, Rohenkohl G, Wyart V, NobreAC (2013) Temporal expectation enhances contrast sensitivity by phase entrainment of low-frequency oscillations in visual cortex. J Neurosci 33:4002-4010. CrossRef Medline
12. de Graaf TA, Gross J, Paterson G, Rusch T, Sack AT, Thut G (2013) Alphaband rhythms in visual task performance: phase-locking by rhythmic sensory stimulation. PLoS One 8:e60035. CrossRef Medline
13. Fiebelkorn IC, Saalmann YB, Kastner S (2013) Rhythmic sampling within and between objects despite sustained attention at a cued location. Curr Biol 23:2553-2558. CrossRef Medline
14. Fox J (1997) Applied regression analysis, linear models, and related methods. Thousand Oaks, CA: SAGE.
15. Gross J, Kujala J, Hamalainen M, Timmermann L, Schnitzler A, Salmelin R (2001) Dynamic imaging of coherent sources: studying neural interactions in the human brain. Proc Natl Acad SciU S A 98:694-699. CrossRef Medline
16. Haegens S, Händel BF, Jensen O (2011) Top-down controlled alpha band activity in somatosensory areas determines behavioral performance in a discrimination task. J Neurosci 31:5197-5204. CrossRef Medline
17. Halbleib A, Gratkowski M, Schwab K, Ligges C, Witte H, Haueisen J (2012) Topographic analysis of engagement and disengagement of neural oscillators in photic driving: a combined electroencephalogram/magnetoencephalogram study. J Clin Neurophysiol 29:33-41. CrossRef Medline
18. Händel BF, Haarmeier T, Jensen O (2011) Alpha oscillations correlate with the successful inhibition of unattended stimuli. J Cogn Neurosci 23: 2494-2502. CrossRef Medline
19. Hanslmayr S, Aslan A, Staudigl T, Klimesch W, Herrmann CS, Bäuml KH (2007) Prestimulus oscillations predict visual perception performance between and within subjects. Neuroimage 37:1465-1473. CrossRef Medline
20. Hanslmayr S, Volberg G, Wimber M, Dalal SS, Greenlee MW (2013) Prestimulus oscillatory phase at 7 Hz gates cortical information flow and visual perception. Curr Biol 23:2273-2278. CrossRef Medline
21. Hari R, Salmelin R (1997) Human cortical oscillations: a neuromagnetic view through the skull. Trends Neurosci 20:44-49. CrossRef Medline
22. Henry MJ, Obleser J (2012) Frequency modulation entrains slow neural oscillations and optimizes human listening behavior. Proc Natl Acad Sci U S A 109:20095-20100. CrossRef Medline
23. Herrmann CS (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. CrossRef Medline
24. Jaegle A, Ro T (2014) Direct control of visual perception with phase-specific modulation of posterior parietal cortex. J Cogn Neurosci 26:422-432. CrossRef Medline
25. Jensen O, Bonnefond M, VanRullen R (2012) An oscillatory mechanism for prioritizing salient unattended stimuli. Trends Cogn Sci 16:200-206. CrossRef Medline
26. Kelly SP, Lalor EC, Reilly RB, Foxe JJ (2006) Increases in alpha oscillatory power reflect an active retinotopic mechanism for distracter suppression during sustained visuospatial attention. J Neurophysiol 95:3844-3851. CrossRef Medline
27. Klimesch W (2012) Alpha-band oscillations, attention, and controlled access to stored information. Trends Cogn Sci 16:606-617. CrossRef Medline
28. Lakatos P, Karmos G, Mehta AD, Ulbert I, Schroeder CE (2008) Entrainment of neuronal oscillations as a mechanism of attentional selection. Science 320:110-113. CrossRef Medline
29. Landau AN, Fries P (2012) Attention samples stimuli rhythmically. Curr Biol 22:1000-1004. CrossRef Medline
30. Lisman JE, Jensen O (2013) The θ-γ neural code. Neuron 77:1002-1016. CrossRef Medline
31. Lopes Da Silva FH, Storm Van LeeuwenW (1977) The cortical source of the alpha rhythm. Neurosci Lett 6:237-241. CrossRef Medline
32. Lütkenhöner B (2003) Magnetoencephalography and its Achilles' heel. J Physiol Paris 97:641-658. CrossRef Medline
33. Maris E, Oostenveld R (2007) Nonparametric statistical testing of EEG-and MEG-data. J Neurosci Methods 164:177-190. CrossRef Medline
34. Mathewson KE, Gratton G, Fabiani M, Beck DM, Ro T (2009) To see or not to see: prestimulus α phase predicts visual awareness. J Neurosci 29:2725-2732. CrossRef Medline
35. Mathewson KE, Prudhomme C, Fabiani M, Beck DM, 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. J Cogn Neurosci 24:2321-2333. CrossRef Medline
36. Morey RD (2008) Confidence intervals from normalized data: a correction to Cousineau (2005). Tutor Quant Methods Psychol 4:61-64.
37. Nolte G (2003) The magnetic lead field theorem in the quasi-static approximation and its use for magnetoencephalography forward calculation in realistic volume conductors. Phys Med Biol 48:3637-3652. CrossRef Medline
38. Oostenveld R, Fries P, Maris E, Schoffelen JM (2011) FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011:156869. CrossRef Medline
39. Rihs TA, Michel CM, Thut G (2007) Mechanisms of selective inhibition in visual spatial attention are indexed by alpha-band EEG synchronization. Eur J Neurosci 25:603-610. CrossRef Medline
40. Rohenkohl G, Nobre AC (2011) α Oscillations related to anticipatory attention follow temporal expectations. J Neurosci 31:14076-14084. CrossRef Medline
41. Rohenkohl G, Cravo AM, Wyart V, NobreAC (2012) Temporal expectation improves the quality of sensory information. J Neurosci 32:8424-8428. CrossRef Medline
42. Romei V, Gross J, 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. CrossRef Medline
43. Romei V, Gross J, Thut G (2012) Sounds reset rhythms of visual cortex and corresponding human visual perception. Curr Biol 22:807-813. CrossRef Medline
44. Schroeder CE, Lakatos P (2009) Low-frequency neuronal oscillations as instruments of sensory selection. Trends Neurosci 32:9-18. CrossRef Medline
45. Schroeder CE, Wilson DA, Radman T, Scharfman H, Lakatos P (2010) Dynamics of active sensing and perceptual selection. Curr Opin Neurobiol 20:172-176. CrossRef Medline
46. Spaak E, Bonnefond M, Maier A, Leopold DA, Jensen O (2012) Layerspecific entrainment of gamma-band neural activity by the alpha rhythm in monkey visual cortex. Curr Biol 22:2313-2318. CrossRef Medline
47. Thut G, Veniero D, Romei V, Miniussi C, Schyns P, Gross J (2011) Rhythmic TMS causes local entrainment of natural oscillatory signatures. Curr Biol 21:1176-1185. CrossRef Medline
48. Thut G, Miniussi C, Gross J (2012) The functional importance of rhythmic activity in the brain. Curr Biol 22:R658-R663. CrossRef Medline
49. van Dijk H, Schoffelen JM, Oostenveld R, Jensen O (2008) Prestimulus oscillatory activity in the alpha band predicts visual discrimination ability. J Neurosci 28:1816-1823. CrossRef Medline
50. Van Rullen R, Koch C (2003) Is perception discrete or continuous? Trends Cogn Sci 7:207-213. CrossRef Medline
51. Van Rullen R, Macdonald JS (2012) Perceptual echoes at 10 Hz in the human brain. Curr Biol 22:995-999. CrossRef Medline
52. Watson AB, Pelli DG (1983) QUEST: a Bayesian adaptive psychometric method. Percept Psychophys 33:113-120. CrossRef Medline
53. Worden MS, Foxe JJ, Wang N, Simpson GV (2000) Anticipatory biasing of visuospatial attention indexed by retinotopically specific alpha-band electroencephalography increases over occipital cortex. J Neurosci 20:RC63. Medline
54. Yamagishi N, Callan DE, Goda N, Anderson SJ, Yoshida Y, KawatoM (2003) Attentional modulation of oscillatory activity in human visual cortex. Neuroimage 20:98-113. CrossRef Medline
55. Zauner A, Fellinger R, Gross J, Hanslmayr S, Shapiro K, Gruber W, Müller S, KlimeschW (2012) Alpha entrainment is responsible for the attentional blink phenomenon. Neuroimage 63:674-686. CrossRef Medline