Neurofeedback Tunes Scale-Free Dynamics in Spontaneous Brain Activity

Cerebral Cortex

Volumn 27, Issue 10, 2017, Pages 4911-4922

  Ros, T ^a   Frewen, P ^b   Theberge J ^c   Michela, A ^a   Kluetsch, R ^d   Mueller, A ^e   Candrian, G ^e   Jetly, R ^f   Vuilleumier, P ^a   Lanius, R A ^b  

^a UNIVERSITY OF GENEVA   (Switzerland)

^b UNIVERSITY OF WESTERN ONTARIO   (Canada)

^c LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF HEIDELBERG   (Germany)

^e Brain and Trauma Foundation Grisons   (Switzerland)

^f Directorate of Force Health Protection   (Canada)

Author keywords

alpha rhythm; criticality; EEG; Hurst exponent; long range temporal correlations; neurofeedback; PTSD; scale free dynamics

Indexed keywords

ADULT; AROUSAL; ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DYNAMICS; ELECTROENCEPHALOGRAM; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; MATHEMATICAL MODEL; NEUROFEEDBACK; OSCILLATION; POSTTRAUMATIC STRESS DISORDER; PRIORITY JOURNAL; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; FEMALE; MALE; NERVE CELL; NERVOUS SYSTEM FUNCTION; PATHOPHYSIOLOGY; PHYSIOLOGY; PROCEDURES; YOUNG ADULT;

ADULT; BRAIN; BRAIN MAPPING; ELECTROENCEPHALOGRAPHY; FEMALE; HUMANS; MALE; NERVOUS SYSTEM PHYSIOLOGICAL PHENOMENA; NEUROFEEDBACK; NEURONS; STRESS DISORDERS, POST-TRAUMATIC; YOUNG ADULT;

EID: 85021646245     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhw285     Document Type: Article

References (85)

1. American Psychiatric Association and Task Force on DSM-IV. 2000. Diagnostic and statistical manual of mental disorders: DSM-IV-TR. American Psychiatric Association.
2. Angelakis E, Stathopoulou S, Frymiare JL, Green DL, Lubar JF, Kounios J. 2007. EEG neurofeedback: A brief overview and an example of peak alpha frequency training for cognitive enhancement in the elderly. Clin Neuropsychol. 21: 110-129.
3. Arns M, de Ridder S, Strehl U, Breteler M, Coenen A, de Ridder S, Martijn A, Coenen T. 2009. Efficacy of neurofeedback treatment in ADHD: the effects on inattention, impulsivity and hyperactivity: A meta-analysis. Clin EEG Neurosci. 40: 180-189.
4. Bak P, Tang C, Wiesenfeld K. 1987. Self-organized criticality: An explanation of the 1/f noise. Phys Rev Lett. 59: 381-384.
5. Barttfeld P, Uhrig L, Sitt JD, Sigman M, Jarraya B, Dehaene S. 2015. Signature of consciousness in the dynamics of restingstate brain activity. Proc Natl Acad Sci. 112: 887-892.
6. Becerra J, Fernández T, Harmony T, Caballero MI, García F, Fernández-Bouzas A, Santiago-Rodríguez E, Prado-Alcalá RA. 2006. Follow-up study of learning-disabled children treated with neurofeedback or placebo. Clin EEG Neurosci. 37: 198-203.
7. Blake DD, Weathers FW, Nagy LM et al. 1995. The development of a clinician-administered PTSD scale. J Trauma Stress. 8: 75-90.
8. Bollimunta A, Mo J, Schroeder CE, Ding M. 2011. Neuronal mechanisms and attentional modulation of corticothalamic oscillations. J Neurosci. 31: 4935-4943.
9. Botcharova M, Farmer SF, Berthouze L. 2014. Markers of criticality in phase synchronization. Front Syst Neurosci. 8: 176.
10. Brunner C, Scherer R, Graimann B, Supp G, Pfurtscheller G. 2006. Online control of a brain-computer interface using phase synchronization. IEEE Trans Biomed Eng. 53: 2501-2506.
11. Chialvo DR. 2010. Emergent complex neural dynamics. Nat Phys. 6: 744-750.
12. Churchill NW, Cimprich B, Askren MK, Reuter-Lorenz PA, Jung MS, Peltier S, Berman MG. 2015. Scale-free brain dynamics under physical and psychological distress: pre-treatment effects in women diagnosed with breast cancer. Hum Brain Mapp. 36: 1077-1092.
13. Coburn KL, Lauterbach EC, Boutros NN, Black KJ, Arciniegas DB, Coffey CE. 2006. The value of quantitative electroencephalography in clinical psychiatry: A report by the Committee on Research of the American Neuropsychiatric Association. J Neuropsychiatry Clin Neurosci. 18: 460-500.
14. Collins PY, Patel V, Joestl SS, March D, Insel TR, Daar AS, Anderson W, Dhansay MA, Phillips A, Shurin S, et al. 2011. Grand challenges in global mental health. Nature. 475: 27-30.
15. Escolano C, Navarro-Gil M, Garcia-Campayo J, Congedo M, De Ridder D, Minguez J. 2014. A controlled study on the cognitive effect of alpha neurofeedback training in patients with major depressive disorder. Front Behav Neurosci. 8: 296.
16. First MB, Spitzer RL, Gibbon M, Williams JBW. 1995. Structured clinical interview for Axis I DSM-IV disorders-patient edition (SCID-I/P). New York, NY: American Psychiatric Press.
17. Friedrich EVC, Sivanathan A, Lim T, Suttie N, Louchart S, Pillen S, Pineda JA. 2015. An effective neurofeedback intervention to improve social interactions in children with autism spectrum disorder. J Autism Dev Disord. 45: 4084-4100.
18. Gevensleben H, Holl B, Albrecht B, Schlamp D, Kratz O, Studer P, Wangler S, Rothenberger A, Moll GH, Heinrich H. 2009. Distinct EEG effects related to neurofeedback training in children with ADHD: A randomized controlled trial. Int J Psychophysiol. 74: 149-157.
19. Haegens S, Nacher V, Luna R, Romo R, Jensen O. 2011. Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking. Proc Natl Acad Sci. 108: 19377-19382.
20. Harang R, Bonnet G, Petzold LR. 2012. WAVOS: A MATLAB toolkit for wavelet analysis and visualization of oscillatory systems. BMC Res Notes. 5: 163.
21. Hardstone R, Poil S-S, Schiavone G, Jansen R, Nikulin V V, Mansvelder HD, Linkenkaer-Hansen K. 2012. Detrended fluctuation analysis: A scale-free view on neuronal oscillations. Front Physiol. 3: 450.
22. Hardt JV, Kamiya J. 1978. Anxiety change through electroencephalographic alpha feedback seen only in high anxiety subjects. Science. 201: 79-81.
23. Hartmann T, Lorenz I, Müller N, Langguth B, Weisz N. 2013. The effects of neurofeedback on oscillatory processes related to tinnitus. Brain Topogr. 27: 149-157.
24. He BJ, Zempel JM, Snyder AZ, Raichle ME. 2010. The temporal structures and functional significance of scale-free brain activity. Neuron. 66: 353-369.
25. Heinrich H, Gevensleben H, Strehl U. 2007. Annotation: neurofeedback-train your brain to train behaviour. J Child Psychol Psychiatry. 48: 3-16.
26. Hengen KB, Torrado Pacheco A, McGregor JN, Van Hooser SD, Turrigiano GG. 2016. Neuronal firing rate homeostasis is inhibited by sleep and promoted by wake. Cell. 165: 180-191.
27. Hesse J, Gross T. 2014. Self-organized criticality as a fundamental property of neural systems. Front Syst Neurosci. 8: 166.
28. Hsu D, Beggs JM. 2006. Neuronal avalanches and criticality: A dynamical model for homeostasis. Neurocomputing. 69: 1134-1136.
29. Iyer KK, Roberts JA, Hellström-Westas L, Wikström S, Hansen Pupp I, Ley D, Vanhatalo S, Breakspear M. 2015. Cortical burst dynamics predict clinical outcome early in extremely preterm infants. Brain. 138: 2206-2218.
30. Jin Y, Potkin SG, Kemp AS, Huerta ST, Alva G, Thai TM, Carreon D, Bunney WE. 2006. Therapeutic effects of individualized alpha frequency transcranial magnetic stimulation (alphaTMS) on the negative symptoms of schizophrenia. Schizophr Bull. 32: 556-561.
31. Jokíc-Begíc N, Begíc D. 2003. Quantitative electroencephalogram (qEEG) in combat veterans with post-traumatic stress disorder (PTSD). Nord J Psychiatry. 57: 351-355.
32. Kamiya J. 2011. The first communications about operant conditioning of the EEG. J Neurother. 15: 65-73.
33. Kello CT, Brown GD, Ferrer-I-Cancho R, Holden JG, Linkenkaer-Hansen K, Rhodes T, Van Orden GC. 2010. Scaling laws in cognitive sciences. Top Cogn Sci. 14: 223-232.
34. Kitzbichler MG, Bullmore ET. 2015. Power law scaling in human and empty room MEG recordings. PLoS Comput Biol. 11: e1004175.
35. Kluetsch RC, Ros T, Théberge J, Frewen PA, Calhoun VD, Schmahl C, Jetly R, Lanius RA. 2014. Plastic modulation of PTSD resting-state networks and subjective wellbeing by EEG neurofeedback. Acta Psychiatr Scand. 130: 123-136.
36. Koprivová J, Congedo M, Raszka M, Praško J, Brunovský M, Horácek J. 2013. Prediction of treatment response and the effect of independent component neurofeedback in obsessivecompulsive disorder: A randomized, sham-controlled, doubleblind study. Neuropsychobiology. 67: 210-223.
37. Lai MC, Lombardo MV, Chakrabarti B, Sadek SA, Pasco G, Wheelwright SJ, Bullmore ET, Baron-Cohen S, Suckling J. 2010. A shift to randomness of brain oscillations in people with autism. Biol Psychiatry. 68: 1092-1099.
38. Leistedt S, Dumont M, Coumans N, Lanquart JP, Jurysta F, Linkowski P. 2007a. The modifications of the long-range temporal correlations of the sleep EEG due to major depressive episode disappear with the status of remission. Neuroscience. 148: 782-793.
39. Leistedt S, Dumont M, Lanquart J-P, Jurysta F, Linkowski P. 2007b. Characterization of the sleep EEG in acutely depressed men using detrended fluctuation analysis. Clin Neurophysiol. 118: 940-950.
40. Linkenkaer-Hansen K. 2001. Long-range temporal correlations and scaling behavior in human brain oscillations. J Neurosci. 21: 1370-1377.
41. Linkenkaer-Hansen K, Monto S, Rytsälä H, Suominen K, Isometsä E, Kähkönen S. 2005. Breakdown of long-range temporal correlations in theta oscillations in patients with major depressive disorder. J Neurosci. 25: 10131-10137.
42. Liu X, Ward BD, Binder JR, Li SJ, Hudetz AG. 2014. Scale-free functional connectivity of the brain is maintained in anesthetized healthy participants but not in patients with unresponsive wakefulness syndrome. PLoS One. 9: e92182.
43. Lomas T, Ivtzan I, Fu CHY. 2015. A systematic review of the neurophysiology of mindfulness on EEG oscillations. Neurosci Biobehav Rev. 57: 401-410.
44. Lubar JF. 1997. Neocortical dynamics: implications for understanding the role of neurofeedback and related techniques for the enhancement of attention. Appl Psychophysiol Biofeedback. 22: 111-126.
45. Marder E, Goaillard J-M. 2006. Variability, compensation and homeostasis in neuron and network function. Nat Rev Neurosci. 7: 563-574.
46. Meisel C, Olbrich E, Shriki O, Achermann P. 2013. Fading signatures of critical brain dynamics during sustained wakefulness in humans. J Neurosci. 33: 17363-17372.
47. Montez T, Poil SS, Jones BF, Manshanden I, Verbunt JP, van Dijk BW, Brussaard AB, van Ooyen A, Stam CJ, Scheltens P, et al. 2009. Altered temporal correlations in parietal alpha and prefrontal theta oscillations in early-stage Alzheimer disease. Proc Natl Acad Sci USA. 106: 1614-1619.
48. Monto S, Vanhatalo S, Holmes MD, Palva JM. 2007. Epileptogenic neocortical networks are revealed by abnormal temporal dynamics in seizure-free subdural EEG. Cereb Cortex. 17: 1386-1393.
49. Mulholland T, Runnals S. 1962. Evaluation of attention and alertness with a stimulus-brain feedback loop. Electroencephalogr Clin Neurophysiol. 14: 847-852.
50. Musall S, Von Pföstl V, Rauch A, Logothetis NK, Whittingstall K. 2014. Effects of neural synchrony on surface EEG. Cereb Cortex. 24: 1045-1053.
51. Nikulin VV, Brismar T. 2004. Long-range temporal correlations in alpha and beta oscillations: effect of arousal level and test-retest reliability. Clin Neurophysiol. 115: 1896-1908.
52. Nikulin VV, Jönsson EG, Brismar T. 2012. Attenuation of longrange temporal correlations in the amplitude dynamics of alpha and beta neuronal oscillations in patients with schizophrenia. Neuroimage. 61: 162-169.
53. Niv S. 2013. Clinical efficacy and potential mechanisms of neurofeedback. Pers Individ Dif. 54: 676-686.
54. Nolan H, Whelan R, Reilly RB. 2010. FASTER: Fully Automated Statistical Thresholding for EEG Artifact Rejection. J Neurosci Methods. 192: 152-162.
55. Palva JM, Zhigalov A, Hirvonen J, Korhonen O, Linkenkaer-Hansen K, Palva S. 2013. Neuronal long-range temporal correlations and avalanche dynamics are correlated with behavioral scaling laws. Proc Natl Acad Sci USA. 110: 3585-3590.
56. Parish LM, Worrell GA, Cranstoun SD, Stead SM, Pennell P, Litt B. 2004. Long-range temporal correlations in epileptogenic and non-epileptogenic human hippocampus. Neuroscience. 125: 1069-1076.
57. Plante DT, Goldstein MR, Landsness EC, Riedner BA, Guokas JJ, Wanger T, Tononi G, Benca RM. 2013. Altered overnight modulation of spontaneous waking EEG reflects altered sleep homeostasis in major depressive disorder: A highdensity EEG investigation. J Affect Disord. 150: 1167-1173.
58. Poil S-S, Hardstone R, Mansvelder HD, Linkenkaer-Hansen K. 2012. Critical-state dynamics of avalanches and oscillations jointly emerge from balanced excitation/inhibition in neuronal networks. J Neurosci. 32: 9817-9823.
59. Poil SS, Jansen R, van Aerde K, Timmerman J, Brussaard AB, Mansvelder HD, Linkenkaer-Hansen K. 2011. Fast network oscillations in vitro exhibit a slow decay of temporal autocorrelations. Eur J Neurosci. 34: 394-403.
60. Poil SS, Van Ooyen A, Linkenkaer-Hansen K. 2008. Avalanche dynamics of human brain oscillations: relation to critical branching processes and temporal correlations. Hum Brain Mapp. 29: 770-777.
61. Ros T, Baars BJ, Lanius RA, Vuilleumier P. 2014. Tuning pathological brain oscillations with neurofeedback: A systems neuroscience framework. Front Hum Neurosci. 8: 1008.
62. Ros T, Munneke MAM, Ruge D, Gruzelier JH, Rothwell JC. 2010. Endogenous control of waking brain rhythms induces neuroplasticity in humans. Eur J Neurosci. 31: 770-778.
63. Ros T, Théberge J, Frewen PA, Kluetsch R, Densmore M, Calhoun VD, Lanius RA. 2013. Mind over chatter: plastic upregulation of the fMRI salience network directly after EEG neurofeedback. Neuroimage. 65: 324-335.
64. Schabus M, Heib DPJ, Lechinger J, Griessenberger H, Klimesch W, Pawlizki A, Kunz AB, Sterman BM, Hoedlmoser K. 2014. Enhancing sleep quality and memory in insomnia using instrumental sensorimotor rhythm conditioning. Biol Psychol. 95: 126-134.
65. Shew WL, Plenz D. 2012. The functional benefits of criticality in the cortex. Neuroscience. 19: 88-100.
66. Smit DJ a, Linkenkaer-Hansen K, de Geus EJC. 2013. Longrange temporal correlations in resting-state oscillations predict human timing-error dynamics. J Neurosci. 33: 11212-11220.
67. Smit DJA, de Geus EJC, van de Nieuwenhuijzen ME, van Beijsterveldt CEM, van Baal GCM, Mansvelder HD, Boomsma DI, Linkenkaer-Hansen K. 2011. Scale-free modulation of resting-state neuronal oscillations reflects prolonged brain maturation in humans. J Neurosci. 31: 13128-13136.
68. Stam CJ, Montez T, Jones BF, Rombouts SA, van der Made Y, Pijnenburg YA, Scheltens P. 2005. Disturbed fluctuations of resting state EEG synchronization in Alzheimer's disease. Clin Neurophysiol. 116: 708-715.
69. Stepp N, Plenz D, Srinivasa N. 2015. Synaptic plasticity enables adaptive self-tuning critical networks. PLoS Comput Biol. 11: e1004043.
70. Sterman MB, Egner T. 2006. Foundation and practice of neurofeedback for the treatment of epilepsy. Appl Psychophysiol Biofeedback. 31: 21-35.
71. Strehl U, Birkle SM, Wörz S, Kotchoubey B. 2014. Sustained reduction of seizures in patients with intractable epilepsy after self-regulation training of slow cortical potentials-10 years after. Front Hum Neurosci. 8: 604.
72. Surmeli T, Ertem A, Eralp E, Kos IH. 2012. Schizophrenia and the efficacy of qEEG-Guided neurofeedback treatment: A clinical case series. Clin EEG Neurosci. 43: 133-144.
73. Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Jahnke K, Laufs H. 2013. Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep. Proc Natl Acad Sci USA. 110: 15419-15424.
74. Teixeira FPP, Shanahan M. 2015. Local and global criticality within oscillating networks of spiking neurons. International Joint Conference on Neural Networks (IJCNN); 2015 September. pp. 1-7.
75. Tomen N, Rotermund D, Ernst U. 2014. Marginally subcritical dynamics explain enhanced stimulus discriminability under attention. Front Syst Neurosci. 8: 151.
76. Tononi G, Edelman GM, Sporns O. 1998. Complexity and coherency: integrating information in the brain. Trends Cogn Sci. 2: 474-484.
77. Tumari SZM, Sudirman R, Ahmad AH. 2013. Selection of a suitable wavelet for cognitive memory using electroencephalograph signal. Engineering. 05: 15-19.
78. Uhlhaas PJ, Singer W. 2006. Neural synchrony in brain disorders: relevance for cognitive dysfunctions and pathophysiology. Neuron. 52: 155-168.
79. Van de Ville D, Britz J, Michel CM. 2010. EEG microstate sequences in healthy humans at rest reveal scale-free dynamics. Proc Natl Acad Sci USA. 107: 18179-18184.
80. Várkuti B, Guan C, Pan Y, Phua KS, Ang KK, Kuah CWK, Chua K, Ang BT, Birbaumer N, Sitaram R. 2013. Resting state changes in functional connectivity correlate with movement recovery for BCI and robot-assisted upper-extremity training after stroke. Neurorehabil Neural Repair. 27: 53-62.
81. Vossen A, Gross J, Thut G. 2015. Alpha power increase after transcranial alternating current stimulation at alphafrequency (-tACS) reflects plastic changes rather than entrainment. Brain Stimul. 8: 499-508.
82. Williams ST, Conte MM, Goldfine AM, Noirhomme Q, Gosseries O, Thonnard M, Beattie B, Hersh J, Katz DI, Victor JD, et al. 2013. Common resting brain dynamics indicate a possible mechanism underlying zolpidem response in severe brain injury. Elife. 2013: e01157.
83. Young BM, Nigogosyan Z, Walton LM, Song J, Nair VA, Grogan SW, Tyler ME, Edwards DF, Caldera K, Sattin JA, et al. 2014. Changes in functional brain organization and behavioral correlations after rehabilitative therapy using a brain-computer interface. Front Neuroeng. 7: 26.
84. Zhigalov A, Arnulfo G, Nobili L, Palva S, Palva JM. 2015. Relationship of fast-and slow-timescale neuronal dynamics in human MEG and SEEG. J Neurosci. 35: 5385-5396.
85. Zhigalov A, Kaplan A, Palva JM. 2016. Modulation of critical brain dynamics using closed-loop neurofeedback stimulation. Clin Neurophysiol. 127: 2882-2889.