20.03.2008lior golgher noise-induced entrainment in human eeg noise-induced entrainment &...

20.03.2008 Lior Golgher Noise-induced Entrainment in Human EEG

Noise-induced Entrainment & Stochastic Resonance in Human Brain Waves

Toshio Mori & Shoichi Kai, 2002, PRL

Tass 1995

Tass 1995

20.03.2008 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 demonstration that sensory noise can enhance the periodic EEG response to a periodic sensory stimulus.

Mori & Kai PRL 2002


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, …


Historical glance

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.

2002 Mori & Kai – Stochastic Resonance demonstrated in SSVER

Stochastic Resonance Steady State Response


Reminder: EEGWikimedia

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.

Wikimedia


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.

Mazaheri & Jensen 2005

Rizzuto et al. 2003


Herrmann 2000 (Rotated)

Historical glance


(Leaping to 1998 and back to 1995) 1998 Narici et al. – MEG SSER for

auditory, visual and somatosensory stimuli at 6-14 Hz.




Steady State Response

Artieda et al. 2004

Narici et al. 1998

Ross et al. 2000

“… 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


Historical glance Steady State

Response

Tass 1995


(Leaping to 1998 and back to 1995) 1998 Narici et al. – MEG SSER for

auditory, visual and somatosensory stimuli at 6-14 Hz.




“… 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

Takahashi & Tshukahara 2000

Oriental Light and Magic 1997

~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.

Kyushu U.Mori & Kai J. Bifur. 2002



1995-97 Peter Tass evoked visual hallucinations.


1998 Narici et al. – MEG SSER for auditory, visual and somatosensory stimuli at 6-14 Hz.


Historical glance










Historical glance








Stochastic Resonance

C*(dT/dt) = Rin – Rout

C*(dT/dt) = [1 – a(T)] * Rin – bET

a(T) = albedo, bE = Emission coef.

Benzi 2007

Benzi 2007Wikimedia

Rin(t) = R0+ R1cos(ωt)

Wikimedia


Russell et al. 1999

Russell et al. 1999

Historical glanceStochastic Resonance

1993 Douglass et al.

Simonotto et al. 1997

Wikimedia

Moss et al. 2004Schmid et al. 2001

Jiang et al. 2003

Sakmann 1991





1999 Russell et al. – Behavioural use of SR by paddlefish.


No Extrinsic Noise Intrinsic + Extrinsic Noise


2002 Status Summary

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.




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 J. Bifur. 2002

Wikimedia

Mori & Kai PRL 2002


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 2002Mori & Kai PRL 2002


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


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 J. Bifur. 2002

Mori & Kai PRL 2002

Evoked by 10.5 Hz flickerSpontaneous 10.7 Hz activity at O1


Response Dynamics SSVER first observed over occipital

electrode sites, within ~200 milliseconds. Frontal-Occipital phase inversion.

Harada et al. 1991


Response Dynamics

Harada et al. 1991

SSVER first observed over occipital electrode sites.

Frontal-Occipital phase inversion.


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

Birca et al. 2006


Noise-induced entrainment was demonstrated both using a 5 Hz stimulus and using a 10 Hz stimulus.

Occipital dominance preserved.

Nouha et al. 2001

Noise-induced entrainment


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

Mori & Kai 2004


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 UPonN 2002


So what’s missing in my opinion? Mechanism Inter-individual Variability Significance Data exclusion Dynamics Cognitive implication Quantification


Mechanism?

Nouha et al. 2001

“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


Fictitious Figure - Inter-subject variability

0

10

20

30

40

50

60

70

01020304050607080

Optimal Noise Intensity In*

[μW/cm2]

Ma

xim

al P

ow

er

De

ns

ity

Pe*

[μ

V2/s

ec

]

STSKOTMKRK

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.


Mori & Kai 2004

RANDOMLY GENERATED “DATA ”

FOR DEMONSTRATION ONLY


Reproducibility and Significance

Mori & Kai UPonN 2002

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).


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


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.

Spectral Dynamics?


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.

Kitajo et al. 2003

Tanaka et al. 2007


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.


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!


Questions?

Oriental Light and Magic 1997


Bibliography – Mori & Kai

1. 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

2. 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

3. 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/

4. 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

5. 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

6. 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

7. 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

8. 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


Bibliography – Stochastic Resonance

9. 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

10. 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

11. 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

12. 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

13. 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

14. 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

15. 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

16. 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

17. 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

18. 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

19. Benzi R., ‘Stochastic Resonance: from climate to biology’ http://arxiv.org/abs/nlin.CD/0702008


Bibliography – Steady State Evoked Response20. 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

21. 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

22. Tass P., ‘Cortical pattern formation during visual hallucinations’, J Biol Phys 21: 177-210, 1995 http://dx.doi.org/10.1007/BF0071234523. 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:100499070773924. 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.1998.032325. 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

26. 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

27. 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

28. 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

29. 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

30. 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

31. 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

32. 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

33. 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


Bibliography – Photosensitive Epilepsy34. Oriental Light and Magic, ‘ でんのうせんしポリゴン ‘ , December 16th 199735. Jeavons PM, Harding GFA, 'Television Epilepsy', Lancet 296, Issue 7679,1970, P. 926

http://dx.doi.org/10.1016/S0140-6736(70)92092-136. 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

37. 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

38. 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

39. Pikachu dynamics and brain http://www.e.ap.kyushu-u.ac.jp/ap/research/nouha/index-j.html

40. Wikimedia Commons

A low-quality version of the problematic Pokemon scene is available at:

http://www.youtube.com/watch?v=t-Ybd0Yby68But you better not watch it.


End


Schmid et al. 2001

Jiang et al. 2003

Sakmann 1991

Supplementary

Intrinsic noise Intrinsic+extrinsic noise

1993 Douglass et al.

Moss et al. 2004

Jiang et al. 2003


Supplementary

Tass 1995


Supplementary

Takahashi & Tsukahara 1998


Supplementary

Nicolis 1993


Supplementary

Tootell et al. 1982 Ermentrout et al. 1979Bressloff et al. 2002


Supplementary

Bressloff et al. 2002


Supplementary

Herrmann 2000

20.03.2008lior golgher noise-induced entrainment in human eeg noise-induced entrainment &...

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