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Noise-induced Entrainment & Stochastic Resonance in Human Brain Waves

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  1. Tass 1995 Noise-induced Entrainment & Stochastic Resonance in Human Brain Waves Toshio Mori & Shoichi Kai, 2002, PRL Tass 1995 Noise-induced Entrainment in Human EEG

  2. Mori & Kai IEICE 2002 Motivation • First demonstration of Stochastic Resonance in the human Steady State Evoked Response (SSER). ? • Stochastic Resonance– Enhanced response to a weak signal in the presence of noise. • SSER– A periodic EEG response to a periodic sensory stimulus, such as flickering light or click sounds. ________________________________ • First demonstrationthat sensory noise can enhance the periodic EEG response to a periodic sensory stimulus. Mori & Kai PRL 2002 Noise-induced Entrainment in Human EEG

  3. Agenda • Background~30 min. EEG, Steady State Evoked Response, Stochastic Resonance • What’s new ~15 min. Setup, results, discussion • What’s missing ~15 min. Mechanism,significance,data exclusion,dynamics, … Noise-induced Entrainment in Human EEG

  4. 1981 Benzi et al., Nicolis - Stochastic Resonance in climatic transitions. 1993 Douglass et al. - SR found in crayfish mechanoreceptors. 1995 Collins et al. predict neural SR can also enhance aperiodic signals. 1996 Cordo et al., Collins et al. – Psychopysical evidence for SR in human somatosensory perception. 1999 Russell et al. – Behavioural use of SR by paddle fish. 2001 Schmid et al. – SR as a collective property of ion channels. 1981 Galambos et al. first report 40 Hz Auditory Steady State Response. 1995-97 Peter Tass models evoked visual hallucinations. 1997 December 16th – Dennō Senshi Porygon incident. 1998 Narici et al. – MEG SSER for auditory, visual and somatosensory stimuli at 6-14 Hz. 2000 Herrmann reports 1-100 Hz Steady State Visual Evoked Response. Historical glance Stochastic Resonance Steady State Response • 2002 Mori & Kai – Stochastic Resonance demonstrated in SSVER Noise-induced Entrainment in Human EEG

  5. Wikimedia Reminder: EEG Ward et al. 2003 • Measures electrical potential differences between electrodes placed on the scalp. • The signal is mainly affected by radial extra-cellular currents near cohorts of cortical neurons. 1-100 μV amplitudes, resolution of centimeters and milliseconds. • Asynchronous activity cancels out. A small number of synchronously firing neurons may dominate the overall resulting signal. • ~1/f spectral distribution. Peaks during wakefulness at ~10 Hz (α), ~20 Hz (β), ~40 Hz (γ) and ~6 Hz (θ). Varies among individuals. • Exhibits developmental changes through infancy and childhood. • Many cognitive tasks elicit consistent variations in EEG spectral power distribution. Noise-induced Entrainment in Human EEG Wikimedia

  6. EEG & MEG Jargon • Synchronization - An amplitude enhancement at a given frequency band. • Spontaneous activity – Pre-stimulus activity. • Evoked response - Change in frequency band power that is both time-locked and phase locked to a given stimulus or event. • Induced response – A change in frequency band power that is time-locked to the stimulus, but jitters in phase between trials (Arieli et al.). The induced activity is usually not revealed by traditional averaging techniques. • Ongoing (‘undriven’) activity - Post-stimulus activity that is not time-locked to the stimulus. • At present, the extent to which stimulus locking and amplitude changes reflect distinct processes remains unclear. Rizzuto et al. 2003 Noise-induced Entrainment in Human EEG Mazaheri & Jensen 2005

  7. “… most subjects reported form (stars or stripes) and color (blue, red or purple) illusions at frequencies around 10-15 Hz”. (…) “The observed hallucinations could be due to the oscillating SSVEP propagating across retinotopic areas of visual cortex. One area then is successively excited and inhibited, thus leading to hallucinations. This phenomenon is known from certain kinds of epilepsies and has been simulated in mathematical models (Tass 1995, 1997). Some of our subjects were retrospectively shown the hallucinations calculated by Tass (1995) and reported them to be identical to the ones observed.” – Herrmann 2000 Herrmann 2000 (Rotated) Historical glance Ross et al. 2000 Steady State Response • 1981 Galambos et al. first report 40 Hz Auditory Steady State Response. (Leaping to 1998 and back to 1995) • 1998 Narici et al. – MEG SSER for auditory, visual and somatosensory stimuli at 6-14 Hz. • 2000 Herrmann reports 1-100 Hz Steady State Visual Evoked Response. • 1995-97 Peter Tass models evoked visual hallucinations. • 1997 December 16th – Dennō Senshi Porygon incident. Artieda et al. 2004 Narici et al. 1998 Noise-induced Entrainment in Human EEG

  8. Mori & Kai J. Bifur. 2002 Tass 1995 Historical glance “… most subjects reported form (stars or stripes) and color (blue, red or purple) illusions at frequencies around 10-15 Hz”. (…) “The observed hallucinations could be due to the oscillating SSVEP propagating across retinotopic areas of visual cortex. One area then is successively excited and inhibited, thus leading to hallucinations. This phenomenon is known from certain kinds of epilepsies and has been simulated in mathematical models (Tass 1995, 1997). Some of our subjects were retrospectively shown the hallucinations calculated by Tass (1995) and reported them to be identical to the ones observed.” – Herrmann 2000 Steady State Response • ~10 million viewers. • 685 children suffered epileptic seizures, ~200 hospitalized. In Aichi: 1:3500 girls, 1:7000 boys. • Induced by surprisingly weak stimulus (12 Hz, 625 nm red). • Retrograde amnesia was common. • 1981 Galambos et al. first report 40 Hz Auditory Steady State Response. (Leaping to 1998 and back to 1995) • 1998 Narici et al. – MEG SSER for auditory, visual and somatosensory stimuli at 6-14 Hz. • 2000 Herrmann reports 1-100 Hz Steady State Visual Evoked Response. • 1995-97 Peter Tass models evoked visual hallucinations. • 1997 December 16th – Dennō Senshi Porygon incident. Takahashi & Tshukahara 2000 Oriental Light and Magic 1997 Noise-induced Entrainment in Human EEG Kyushu U.

  9. 1981 Galambos et al. first report 40 Hz Auditory Steady State Response. 1995-97 Peter Tass evoked visual hallucinations. 1997 December 16th – Dennō Senshi Porygon incident. 1998 Narici et al. – MEG SSER for auditory, visual and somatosensory stimuli at 6-14 Hz. 2000 Herrmann reports 1-100 Hz Steady State Visual Evoked Response. 1981 Benzi et al., Nicolis - Stochastic Resonance in climatic transitions. 1993 Douglass et al. - SR found in crayfish mechanoreceptors. 1995 Collins et al. predict neural SR can also enhance aperiodic signals. 1996 Cordo et al., Collins et al. – Psychopysical evidence for SR in human somatosensory perception. 1999 Russell et al. – Behavioural use of SR by paddle fish. 2001 Schmid et al. – SR as a collective property of ion channels. Historical glance Stochastic Resonance Steady State Response • 2002 Mori & Kai – Stochastic Resonance demonstrated in SSVER Noise-induced Entrainment in Human EEG

  10. Wikimedia Historical glance Stochastic Resonance • 1981 Benzi et al., Nicolis - Stochastic Resonance in climatic transitions. • 1993 Douglass et al. - SR found in crayfish mechanoreceptors. • 1995 Collins et al. predict neural SR can also enhance aperiodic signals. • 1996 Cordo et al., Collins et al. – Psychopysical evidence for SR in human somatosensory perception. • 1999 Russell et al. – Behavioural use of SR by paddle fish. • 2001 Schmid et al. – SR as a collective property of ion channels. Benzi 2007 Rin(t) = R0+ R1cos(ωt) C*(dT/dt) = Rin – Rout C*(dT/dt) = [1 – a(T)] * Rin – bET a(T) = albedo, bE = Emission coef. • 2002 Mori & Kai – Stochastic Resonance demonstrated in SSVER Noise-induced Entrainment in Human EEG Wikimedia Benzi 2007

  11. Jiang et al. 2003 Simonotto et al. 1997 Wikimedia Russell et al. 1999 Sakmann 1991 Schmid et al. 2001 Russell et al. 1999 Historical glance Stochastic Resonance • 1981 Benzi et al., Nicolis - Stochastic Resonance in climatic transitions. • 1993 Douglass et al. - SR found in crayfish mechanoreceptors. • 1995 Collins et al. predict neural SR can also enhance aperiodic signals. • 1996 Cordo et al., Collins et al. – Psychopysical evidence for SR in human somatosensory perception. • 1999 Russell et al. – Behavioural use of SR by paddlefish. • 2001 Schmid et al. – SR as a collective property of ion channels. No Extrinsic Noise Intrinsic + Extrinsic Noise 1993 Douglass et al. Noise-induced Entrainment in Human EEG Moss et al. 2004

  12. Found in numerous nonlinear systems. Found in sensory receptors. Affects psychophysical performance (visual, auditory, somatosensory, vestibular). Used behaviourally (sparse evidence). Theoretically modeled with intrinsic and extrinsic noise. No clear mechanism. Induced by numerous periodic signals. Interacts with spontaneous activity. Similar spectrogram across modalities (visual, auditory, somatosensory). Might induce transient hallucinations (common) or seizures (rare). No clear mechanism. 2002 Status Summary Stochastic Resonance Steady State Response • 2002 Mori & Kai – Stochastic Resonance demonstrated in SSVER Noise-induced Entrainment in Human EEG

  13. Experimental setup – 1/2 • 3x3 cm2 LED screen, 15 cm from the eyes. • Stimulus parameters: • Illuminance: 0.04 cd/m2(vs. 10-20 cd/m2 by Takahashi & Tsukahara 1998) • Pulse width: 100 μsec • Repetition rate: 5 Hz • 10 iterations of (10 sec. stimulation + 20 sec. rest) Mori & Kai PRL 2002 Wikimedia Mori & Kai J. Bifur. 2002 Noise-induced Entrainment in Human EEG

  14. Experimental setup – 2/2 • Noise bandpassed at 15-60 Hz. • Noise always presented to the left eye. • EEG recording filtered: • 100-order LPF • Cutoff frequency fc = 25 Hz • 40 dB/Octave attenuation • FFT parameters: • Rectangular window • 4096 positions (8.192 seconds) • 0.12 Hz resolution Mori & Kai PRL 2002 Mori & Kai PRL 2002 Noise-induced Entrainment in Human EEG

  15. Binocular entrainment • The “entrainment” concept is ill-defined in general. • The same setup was also used for entrainment using binocular flicker stimulus. • Note Activity at occipital (bottom) electrode site. Mori & Kai 2001 Noise-induced Entrainment in Human EEG

  16. Setting the weak stimulus • Flicker alone at right eye. • Note heavy signal filtration (fc = 25 Hz, -40 dB/Octave, 100-order LPF). • Irradiance of weak stimulus set to non-entraining 30 μW/cm2 • This irradiance is >100 times weaker than reported by Takahashi & Tsukahara 1998 Mori & Kai PRL 2002 Mori & Kai J. Bifur. 2002 Spontaneous 10.7 Hz activity at O1 Evoked by 10.5 Hz flicker Noise-induced Entrainment in Human EEG

  17. Response Dynamics • SSVER first observed over occipital electrode sites, within ~200 milliseconds. • Frontal-Occipital phase inversion. Harada et al. 1991 Noise-induced Entrainment in Human EEG

  18. Response Dynamics • SSVER first observed over occipital electrode sites. • Frontal-Occipital phase inversion. Harada et al. 1991 Noise-induced Entrainment in Human EEG

  19. Birca et al. 2006 Preferential entrainment frequency • The preferential entrainment frequency is different than the spontaneous alpha frequency. • This finding is later corroborated by Birca et al. over 41 children and 10 adults. • No consistent relationship found between the spontaneous and entrainment frequencies. Nouha et al. 2001 Noise-induced Entrainment in Human EEG

  20. Noise-induced entrainment • Noise-induced entrainment was demonstrated both using a 5 Hz stimulus and using a 10 Hz stimulus. • Occipital dominance preserved. Noise-induced Entrainment in Human EEG Nouha et al. 2001

  21. Mori & Kai 2004 Harmonic Entrainment • Different papers give somewhat different reasons for using harmonic entrainment: • “Fundamental entrainment is often sensitive to uncontrollable factors such as the subject’s mental and physical conditions (e.g. stress) at the moment of testing, while harmonic entrainment is rather insensitive.” – Mori & Kai J. Bifur. 2002 • “When a periodic stimulus with a period close to that of the α-wave is applied, entrainment at the fundamental frequency is easily produced by a slight change of the physical or mental conditions, even if the stimulus is weak. Consequently, we investigate entrainment at the harmonic frequency, where the frequency is far from the α-wave frequency (fα) of the subject and entrainment is not easily induced by the above factors”. – Mori & Kai 2004 Noise-induced Entrainment in Human EEG Mori & Kai J. Bifur. 2002

  22. Exhibition of Stochastic Resonance • Suggested to be a universal effect. • Only observed at occipital electrode sites (for a visual stimulus). • Error bars not shown. Mori & Kai J. Bifur. 2002 Mori & Kai UPonN 2002 Noise-induced Entrainment in Human EEG

  23. So what’s missing in my opinion? • Mechanism • Inter-individual Variability • Significance • Data exclusion • Dynamics • Cognitive implication • Quantification Noise-induced Entrainment in Human EEG

  24. Mechanism? • “The optimum intensity of the noisy stimulus synchronizes more α oscillators in the human brain.” – Mori & Kai, PRL 2002 > Apparently, other methods than EEG are required to investigate the underlying mechanism. • “Thus, we bypass sensory organs and observe the SR in the visual cortex itself” – Mori & Kai, PRL 2002 > The cortical observations may stem from thalamic SR. This possibility is reflected in a later paper which puts it as: “a phenomenon produced in the visual information processing system following the optical chiasm”. – Mori & Kai 2004 Nouha et al. 2001 Noise-induced Entrainment in Human EEG

  25. Variability? • “The fact that the optimal noise intensity In* differs among individuals (Fig. 10) indicates that the potential barrier of the oscillators differs among individuals. The fact that the spectral peak Pe* differs indicates that different numbers of oscillators are concerned with entrainment.” –Mori & Kai 2004 • However, the individual In*, Pe* are not provided in fig. 10 or elsewhere, except for subject S. (In* = 54.5 μW/cm2, Pe* = 51.9 μV2/sec) • Error bars only shown for subject S, earlier. RANDOMLY GENERATED “DATA” FOR DEMONSTRATION ONLY Mori & Kai 2004 Noise-induced Entrainment in Human EEG Mori & Kai J. Bifur. 2002

  26. Reproducibility and Significance • 5 subjects (male, 22±2 years) • “We retested several of these subjects on subsequent days and obtained similar results. Although subjects are five in the present study, the obtained results therefore, have sufficient statistical significance.” – Mori & Kai J. Bifur. 2002 • However, statistical significance calculations are no where to be found, at least in English papers. • Such a strong effect has not been reproduced as yet (March 2008). Mori & Kai UPonN 2002 Noise-induced Entrainment in Human EEG

  27. Data exclusion • “Starting point of the photic stimulus was at zero-cross point in the α-wave changing from a positive to negative value. The data out of this definition and the data due to falling into a sleep were excluded” – Mori & Kai, J. Bifur. 2002 • What portion of the data has been excluded for each of these reasons? • This exclusion is not mentioned in the corresponding PRL paper. Nouha et al. 2001 Noise-induced Entrainment in Human EEG

  28. Spectral Dynamics? Skosnik et al. 2006 • Dynamics are not shown in this paper. • Older papers show some dynamics, but no time-frequency diagrams. • Only evoked activity is considered, while induced and ongoing activities may be of cognitive relevance as well. Noise-induced Entrainment in Human EEG

  29. Kitajo et al. 2003 What happened afterwards? • 2003 Kitajo et al. use a similar setup to demonstrate a mild but significant contribution of visual noise to psychophysical performance in a sensorimotor task. • 2007 Tanaka et al. report a weak SR in MEG 40 Hz ASSR – 3/9 amplitude, 3/9 phase, 3/9 null. Tanaka et al. 2007 Noise-induced Entrainment in Human EEG

  30. Highlights • First convincing evidence for occipital EEG entrainment by a weak visual stimulus, in the presence of visual noise. • Innovative methodology insures that SR also occurs beyond the sensory receptors. • Unclear mechanism. • Small sample size, significance not explicitly shown. • Not reproduced enough as yet. • Might explain the Dennō Senshi Porygon incident. • Unclear cognitive implication. Noise-induced Entrainment in Human EEG

  31. Acknowledgements I would like to thank Professor Shoichi Kai for his kind and helpful replies to my questions. Manuscripts of [4-7] were kindly provided by Professor Kai. Many thanks to my friends who reviewed this presentation: Ariel, Avshalom, Daniel, Julia & Maya. With ongoing gratitude to Dr. Daniel Levy. Thank you for coming! Noise-induced Entrainment in Human EEG

  32. Questions? Oriental Light and Magic 1997 Noise-induced Entrainment in Human EEG

  33. Bibliography – Mori & Kai • Mori T., Kai S., 'Noise-Induced Entrainment and Stochastic Resonance in Human Brain Waves', Phys. Rev. Lett. 88, 218101, 2002 http://dx.doi.org/10.1103/PhysRevLett.88.218101 • Mori T., Kai S., ‘The Human Brain Uses Noise’, in ‘Unsolved Problems of Noise Fluctuations’ UPonN 2002 :Third International Conference,Vol.665, pp.227-233, 2003 http://dx.doi.org/10.1063/1.1584895 • Mori T., Kai S., Stochastic Resonance in the Brain, IEICE Transactions, D-II Vol.J85-D-II, No.6(20020601) pp. 1093-1100 http://ci.nii.ac.jp/naid/110003184272/en/ • Mori T., Kai S., 'Stochastic resonance in the brain', Systems and Computers in Japan 35 11, Pages 39 - 47, 24 Aug 2004 http://dx.doi.org/10.1002/scj.10398 • Mori T., Kai S., ‘Stochastic Resonance in Alpha Oscillators in the Human Brain’, Int. J. Bifurcation and Chaos,Vol.12, No.11, pp.2631-2639, 2002 http://dx.doi.org/10.1142/S0218127402006151 • Mori T., Kai S., ‘Spatio-temporal map of α-wave entrainment in human brain by photic stimulus’, Jpn. J. Med. Elect. Biol. Engin. Vol.39, No.4, pp.284-91, 2001 • K. Harada, S. Nishifuji, S. Kai, K. Hirakawa, ‘Response of Alpha Wave to Flicker Stimulation’,IEICE Transactions ,Vol. E 74, No.6, P.1486-1491, 1991 http://search.ieice.org/bin/summary.php?id=e74-a_6_1486&category=A&lang=&year=1991 • 九大工,A 福工大  森 敏生,A 山崎 秀樹,甲斐 昌, Brain Wave Dynamics due to the light stimuli, http://www.e.ap.kyushu-u.ac.jp/ap/research/nouha/nouha.pdf Noise-induced Entrainment in Human EEG

  34. Bibliography – Stochastic Resonance • Sakmann B., 'Nobel Lecture. Elementary steps in synaptic transmission revealed by currents through single ion channels', EMBO J. 1992 Jun;11(6):2002-16 http://dx.doi.org/10.1007/BF01122797 • Douglass JK, Wilkens L, Pantazelou E, Moss F., Noise enhancement of information transfer in crayfish mechanoreceptors by stochastic resonance, Nature. 1993 Sep 23;365(6444):337-40 PMID: 8377824 • Cordo P, Inglis JT, Verschueren S, Collins JJ, Merfeld DM, Rosenblum S, Buckley S, Moss F., Noise in human muscle spindles, Nature. 1996 Oct 31;383(6603):769-70 PMID: 8892999 • Gammaitoni L., Hänggi P., Jung P., Marchesoni F., 'Stochastic Resonance', Rev. Mod. Phys. 70(1), 1998, pp. 223–287 http://dx.doi.org/10.1103/RevModPhys.70.223 • Russell DF, Wilkens LA, Moss F, Use of behavioural stochastic resonance by paddle fish for feeding, Nature. 1999 Nov 18;402(6759):291-4 PMID: 10580499 • Schmid G., Goychuk I., Haenggi P., 'Stochastic resonance as a collective property of ion channel assemblies', Europhys. Lett., 56 (1) , pp. 22-28 (2001) http://dx.doi.org/10.1209/epl/i2001-00482-6 • Collins J.J., Priplata A.A., Gravelle D.C., Niemi J., Harry J., Lipsitz L.A., 'Noise-enhanced human sensorimotor function', Engineering in Medicine and Biology Magazine, IEEE 22(2), March-April 2003 pp. 76 - 83 http://dx.doi.org/10.1109/MEMB.2003.1195700 • Kitajo K, Nozaki D, Ward LM, Yamamoto Y, 'Behavioral stochastic resonance within the human brain', Phys Rev Lett. 2003 May 30;90(21):218103. http://10.1103/PhysRevLett.90.218103 • Jiang Y, Lee A, Chen J, Ruta V, Cadene M, Chait BT, MacKinnon R., 'X-ray structure of a voltage-dependent K+ channel', Nature. 2003 May 1;423(6935):33-41 • Moss F., Ward L., Sannita W., 'Stochastic resonance and sensory information processing: a tutorial and review of application', Clin. Neurophys., Vol. 115(2), pp. 267-281, Feb. 2004 http://dx.doi.org/10.1016/j.clinph.2003.09.014 • Benzi R., ‘Stochastic Resonance: from climate to biology’http://arxiv.org/abs/nlin.CD/0702008 Noise-induced Entrainment in Human EEG

  35. Bibliography – Steady State Evoked Response • Galambos R., Makeig S., and Talmachoff P.J., 'A 40-Hz auditory potential recorded from the human scalp', PNAS 78(4), 1981 Apr, pp. 2643-7. http://www.pnas.org/cgi/content/abstract/78/4/2643 • Tootell RB, Silverman MS, Switkes E, De Valois RL, 'Deoxyglucose analysis of retinotopic organization in primate striate cortex', Science. 1982 Nov 26;218(4575):902-4 http://dx.doi.org/10.1126/science.7134981 • Tass P., ‘Cortical pattern formation during visual hallucinations’, J Biol Phys 21: 177-210, 1995 http://dx.doi.org/10.1007/BF00712345 • Tass P., 'Oscillatory Cortical Activity during Visual Hallucinations', J. of Bio. Physics, 23(1), Mar 1997, pp. 21 – 66 http://dx.doi.org/10.1023/A:1004990707739 • Narici L., Portin K., Salmelin R. and Hari R., 'Responsiveness of Human Cortical Activity to Rhythmical Stimulation: A Three-Modality, Whole-Cortex Neuromagnetic Investigation', NeuroImage, 7(3), April 1998, pp. 209-223 http://dx.doi.org/10.1006/nimg.1998.0323 • Ross B., Borgmann C., Draganova R., Roberts L.E., Pantev C., 'A high-precision magnetoencephalographic study of human auditory steady-state responses to amplitude-modulated tones', J. Acoust Soc. Am. 108(2), 2000 Aug, pp. 679-91 http://dx.doi.org/10.1121/1.429600 • Herrmann CS, 'Human EEG responses to 1–100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena', Exp. Brain Res., 137(3 – 4), Apr 2001, pp. 346 - 353, http://dx.doi.org/10.1007/s002210100682 • Bressloff PC, Cowan JD, Golubitsky M, Thomas PJ, Wiener MC, 'What geometric visual hallucinations tell us about the visual cortex', Neural Comput. 2002 Mar;14(3):473-91 http://dx.doi.org/10.1162/089976602317250861 • Rizzuto D.S., Madsen J.R., Bromfield E.B., Schulze-Bonhage A., Seelig D., Aschenbrenner-Scheibe R., and Kahana M.J., 'Reset of human neocortical oscillations during a working memory task', PNAS, Jun 2003; 100: 7931 -7936. http://dx.doi.org/10.1073/pnas.0732061100 • Ward L.M., 'Synchronous neural oscillations and cognitive processes', Trends Cogn Sci. 2003 Dec;7(12):553-9 http://dx.doi.org/10.1016/j.tics.2003.10.012 • Artieda J., Valencia M., Alegre M., Olaziregi O., Urrestarazu E. and Iriarte J., 'Potentials evoked by chirp-modulated tones: a new technique to evaluate oscillatory activity in the auditory pathway', Clinical Neurophysiology, 115(3), March 2004, pp. 699-709 http://dx.doi.org/10.1016/j.clinph.2003.10.021 • Mazaheri A. and Jensen O., 'Posterior alpha activity is not phase-reset by visual stimuli', PNAS, February 21,2006; 103(8): 2948 - 2952. http://dx.doi.org/10.1073/pnas.0505785103 • Skosnik PD, Krishnan GP, Vohs JL, O'Donnell BF, 'The effect of cannabis use and gender on the visual steady state evoked potential', Clin Neurophysiol. 2006 Jan;117(1):144-56 http://dx.doi.org/10.1016/j.clinph.2005.09.024 • Birca A., Carmant L., Lortie A. and Lassonde M., 'Interaction between the flash evoked SSVEPs and the spontaneous EEG activity in children and adults', Clin Neurophysiol. 2006 Feb;117(2):279-88. http://dx.doi.org/10.1016/j.clinph.2005.10.001 Noise-induced Entrainment in Human EEG

  36. Bibliography – Photosensitive Epilepsy • Oriental Light and Magic, ‘でんのうせんしポリゴン ‘, December 16th1997 • Jeavons PM, Harding GFA, 'Television Epilepsy', Lancet 296, Issue 7679,1970, P. 926 http://dx.doi.org/10.1016/S0140-6736(70)92092-1 • Stefánsson SB, Darby CE, Wilkins AJ, Binnie CD, Marlton AP, Smith AT, Stockley AV., 'Television epilepsy and pattern sensitivity', Br Med J. 1977 Jul 9;2(6079):88-90. PMID 871807 • Takahashi T, Tsukahara Y., 'Pocket Monster incident and low luminance visual stimuli: special reference to deep red flicker stimulation', Acta Paediatr Jpn. 1998 Dec;40(6):631-7 PMID: 9893306 http://dx.doi.org/10.1111/j.1442-200X.1998.tb02006.x • Taylor I, Hodgson B, Scheffer IE, Mulley J, Berkovic SF, Dibbens L., 'Is photosensitive epilepsy less common in males due to variation in X chromosome photopigment genes?', Epilepsia. 2007 Sep;48(9):1807-9, PMID: 17521342 http://dx.doi.org/10.1111/j.1528-1167.2007.01138.x • Pikachu dynamics and brain http://www.e.ap.kyushu-u.ac.jp/ap/research/nouha/index-j.html • Wikimedia Commons A low-quality version of the problematic Pokemon scene is available at: http://www.youtube.com/watch?v=t-Ybd0Yby68 But you better not watch it. Noise-induced Entrainment in Human EEG

  37. End Noise-induced Entrainment in Human EEG

  38. Jiang et al. 2003 Sakmann 1991 Schmid et al. 2001 Supplementary Jiang et al. 2003 Intrinsic noise Intrinsic+extrinsic noise 1993 Douglass et al. Noise-induced Entrainment in Human EEG Moss et al. 2004

  39. Supplementary Tass 1995 Noise-induced Entrainment in Human EEG

  40. Supplementary Takahashi & Tsukahara 1998 Noise-induced Entrainment in Human EEG

  41. Supplementary Nicolis 1993 Noise-induced Entrainment in Human EEG

  42. Supplementary Tootell et al. 1982 Bressloff et al. 2002 Ermentrout et al. 1979 Noise-induced Entrainment in Human EEG

  43. Supplementary Bressloff et al. 2002 Noise-induced Entrainment in Human EEG

  44. Supplementary Herrmann 2000 Noise-induced Entrainment in Human EEG