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ELECTROENCEPHALOGRAPHIC (EEG) COHERENCE STUDY OF WORKING MEMORY BRAIN OSCILLATIONS

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Title: ELECTROENCEPHALOGRAPHIC (EEG) COHERENCE STUDY OF WORKING MEMORY BRAIN OSCILLATIONS


1
ELECTROENCEPHALOGRAPHIC (EEG) COHERENCE
STUDY OF WORKING MEMORY BRAIN OSCILLATIONS
  • Dr. Simon Brežan
  • Institute of Clinical Neurophysiology,
  • University Medical Centre Ljubljana, Ljubljana,
    Slovenia
  • coauthors Vita Štukovnik, Veronika Rutar, Jurij
    Dreo, Vito Logar, Blaž Koritnik, Grega Repovš,
    Blaž Konec, Janez Zidar
  • INTERNATIONAL NEUROSCIENCE CONFERENCE, SINAPSA,
    LJUBLJANA 2005

2
WORKING MEMORY (WM)
  • memory processes encoding, storage, recall
  • memory structure sensory memory (attention)gt
    short-term memory (rehearsal/replacement)gt
    long-term memory
  • active role of short term memory working
    memory- central for intelligent goal-directed
    behaviour, coherent thoughts, language etc.
  • DEFINITION complex of cognitive processes for
    time- and capacity- limited maintenance,
    manipulation and utilization of mental
    representations

3
MODEL OF WORKING MEMORY (BADDELEY, 2000)
  • central executive (CE) attentional control of
    subsystems, manipulation of information,
    planning, strategy selection, inhibition
  • slave subsystems
  • phonological loop 2 separated components
    storage and rehearsal of verbal information
  • visuospatial sketchpad separated storage and
    rehearsal of visual and spatial information
  • episodic buffer integration of information from
    other subsystems and episodic long-term memory

4
NEUROPHYSIOLOGICAL AND NEUROANATOMICAL BASIS OF
WORKING MEMORY
  • NEUROPHYSIOLOGICAL VIEW
  • basic neurophysiological mechanism of WM
    repeated reverberations of electrical impulses in
    reverberational (feedback) loops (Štrucl, 1999)?
  • repeated excitation of a synapse in excitational
    loopgt increase of excitatory postsynaptic
    potential (EPSP) postsynaptic facilitation.
  • postsinaptic facilitation preservation/maintenan
    ce of specific information in WM?
  • role of active repeating?

5
  • NEUROANATOMICAL VIEW
  • Cell electrophysiological and functional brain
    imaging studies (Fletcher and Henson, 2001, etc.)
  • various components of working memory different
    anatomically separated neuronal networks
  • specific brain activity
  • (pre)frontal (VLFC, DLFC, AFC) cortex
  • premotor cortex
  • limbic cortex and other subcortical structures
  • posterior association parietal areas
  • hypothetical lateralization of functions (Postle
    et al., 2000)
  • verbal information (phonological loop) left
    hemisphere
  • visuospatial information (visuospatial
    sketchpad) right hemisphere
  • central executive heteromodal association cortex
    of (pre)frontal brain regions (Gathercole, 1999)?

6
BINDING PROBLEM
  • BINDING PROBLEM The mechanisms for functional
    integration (binding) of different brain areas,
    responsible for specific (WM) functions?
  • Paralell and distributed processing of
    information in the brain
  • Functional integration - coupling (visual
    perception, complex motor patterns, visuo-motor
    integration, cognitive functions) key for
    understanding brain functioning
  • The code for functional coupling synchronised
    oscillations of neuronal networks between
    anatomically separated brain areas?
  • Measure of synchronised brain oscillations EEG
    coherence

7
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8
ELECTROENCEPHALOGRAPHY (EEG), SIGNAL ANALYSIS
EEG COHERENCE AND POWER SPECTRA
  • EEG repeated, periodic electrical activity of
    (pyramidal) cortical neurons
  • activity of many neurons (synaptic EPSPs, IPSPs)
    ionic currentsgt field potentials, macropotential
    (EEG signal)
  • intrinsic qualities of neurons, dynamic
    interactions between neuronal networks- changing
    pattern of synchronization and desynchronization
    of regional brain cells- amplitude changes of
    specific frequency bands.
  • EEG - great time resolution (milisec), distinct
    patterns of activity
  • brain rhythms, frequency bands for oscillations
    (delta 0,5-4 Hz, theta 4-7 Hz,
    alpha 8-13 Hz, beta 13-30 Hz, gamma 30-50 Hz)
  • specific functional, behavioral, spatial
    correlates- switching neural networks between
    different functional states- activating or
    inhibiting neural systems?

9
EEG COHERENCE AND POWER SPECTRA
  • POWER SPECTRUM - degree of representation (power)
    of specific frequency band in the signal basic
    input data for coherence calculation
  • gt different levels of regional cortical activity
    or different level of regional synchronization-act
    ivation or inhibition of neural networks
  • EEG COHERENCE measure of degree of similarity,
    phase-locking (synchronization) of 2 distant
    signals for specific frequency band
  • gt different degrees of long-range
    synchronization of oscillations between separate
    cortical regions for specific frequency band
  • measure of functional coupling binding and
    communication between separated brain centers
  • 2 different operational systems of the brain

10
Cxy(?) coherence value between signals x and y
  • Fxy(?)- value of cross-correlation power spectrum
    of signals x, y
  • Fxx(?)- value of auto-correlation power spectrum
    of signal x
  • Fyy(?)- value of auto-correlation power spectrum
    of signal y

11
WORKING MEMORY AND SYNCHRONIZED BRAIN
OSCILLATIONS POWER SPECTRA AND EEG COHERENCE
STUDIES
  • synchronous oscillations- correlation with
    specific behavioural contexts and cognitive tasks
    numerous studies
  • The neurophysiological theory of (working)
    memory
  • Brain oscillations in different frequency bands
    subserve specific (memory) functions and operate
    over different spatial scales.
  • Multiple superimposed synchronized (coherent)
    oscillations in different frequency bands with
    different spatial patterns and functional
    correlates govern specific mental functions.

12
EEG WORKING MEMORY STUDIES
  • EEG COHERENCE changes
  • increases mainly in theta, alpha and gamma band
    (working memory processes) (Serrien et al., 2003
    Sauseng et al., 2004 Sarnthein et al, 1998
    Jensen et al., 2002, etc.)
  • changes of power spectra and coherence with
    different memory load (Gevins et al., 1997,
    Jensen, 2000, etc.)
  • POWER SPECTRA changes
  • decrease in lower alpha band (non-specific effect
    of attention, mental effort) (Klimesch et al.,
    1998, etc.)
  • decrease in upper alpha band (correlate of
    semantic processing) (Basar et al., 2000, etc.)
  • or increase in alpha band (active inhibition of
    disturbing neural networks not needed for the
    memory task) (Klimesch et al., 1998, etc.)
  • increase in theta band frontal midline theta
    rhythm (memory maintenance, attention, mental
    effort) (Klimesch et al. Gevins et al. 1997,
    etc.,)
  • increase in gamma band (sensory, perceptional,
    attentional, working memory processes) (Jensen,
    2000 Babiloni et al., 2004, etc.)

13
SPATIAL SCALES OF COHERENCE CHANGES IN WM TASKS
  • MAINLY (PRE)FRONTO- TEMPORO- PARIETAL INCREASES
    OF THETA, ALPHA COHERENCE
  • MAINLY FRONTOCENTRAL INCREASES OF THETA AND GAMMA
    OSCILLATIONS- POWER SPECTRUM INCREASES (FRONTAL
    MIDLINE THETA RHYTHM) THETA SOURCE??
  • ? IN ACCORDANCE WITH BADDELEYS MODEL OF WM
    SEPARATE SYSTEMS FOR STORAGE (POSTERIOR) AND
    ACTIVE MAINTENANCE, UPDATING OF INFORMATION
    (FRONTAL BRAIN AREAS) in modal specific
    subsystems
  • NEED FOR INFORMATION EXCHANGE, COOPERATION,
    FUNCTIONAL COUPLING BETWEEN ANTERIOR AND
    POSTERIOR BRAIN REGIONS
  • LONG RANGE- SLOW RHYTHMS, SHORT RANGE- FAST
    RHYTHMS
  • TOP-DOWN CONTROL- CENTRAL EXECUTIVE

14
OUR STUDY OF WORKING MEMORY AND BRAIN OSCILLATIONS
  • AIM
  • To examine the neurophysiological mechanisms of
    working memory processes
  • To investigate task-related coherence (and power
    spectra) changes for different EEG frequencies
    during the processes of working memory
  • Search for possible differences in coherence (and
    power spectra) changes between maintenance and
    manipulation processes in working memory.
  • HYPOTHESES
  • Increases in fronto-posterior coherence in
    working memory tasks
  • Increases in bilateral (pre)frontal coherence for
    manipulation vs. maintenance-only processes of
    working memory (prefrontal central executive?)

15
METHODS
  • PARTICIPANTS
  • 11 healthy right-handed volunteers (4 males, 7
    females) informed consent, aged between 20-35
  • average number of set repetition per each
    task/person 38
  • 10 min training of paradigm before recording
  • EEG RECORDING
  • Dark quiet room, projection of different tasks on
    computer screen- cca. 80 cm from the eyes
  • EEG cap (E1-S Electro-Cap) - 29 electrodes,
    standard 10-20 International electrode system
    with extra electrodes Fp1, Fp2, Fz, FCz, Cz,
    CPz, Pz impedance below 5kO
  • EEG aparat Medelec (Profile Multimedia EEG
    System, version 2.0, Oxford Instruments Medical
    Systems Division, Surrey, England)
  • EOG measurement (6 additional eye electrodes,
    Croft 2000)- 20 min calibration task
  • Synchroniztation signal between 2 computers
  • Presentation software for paradigm programming

16
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17
  • COGNITIVE WM PARADIGM
  • Modified Sternberg paradigm of working memory
  • CONTROL 2 EXPERIMENTAL CONDITIONS
  • alternating the type of task coincidentaly
    during recording sessions!
  • WAIT control task with no memory demands
    (ignore the set, fixate the cross, relax)
  • TASK matching the serial position of goal
    stimulus with simultaneosly presented set of
    letters
  • SET (M, D, O) TASK instruction (WAIT)
    FIXATION (5500ms) GOAL (3 D)
    ANSWER (NO)
  • ANALYSIS! SET (M D O)
  • MEMORIZE rehearsal (retention) of information
    in WM
  • TASK matching the serial position of goal
    stimulus with rehearsed originally presented set

18
DATA ANALYSIS
  • Special independent computer programmes were
    designed for coherence and power spectra
    analysis
  • Borland Delphi 7.0 (with EOG artefact correction-
    modified Croft correction procedure) and Matlab
    software (no EOG correction)
  • .edf conversion of EEG recordings
  • Analysis of 5500ms retention/fixation periods in
    all 3 types of tasks, selection of artefact-free
    epochs

19
Borland Delphi 7.0 data analysis
  • Our analytical procedure
  • Measuring EEG volatage and recording them in .EDF
    files
  • Correcting EEG voltages with the RAAA EOG
    correction method
  • Dividing the 5 secod retention periods for all
    sets of every task into five 1 second periods.
  • Transforming the time-domain EEG signal of all
    five 1 second periods into a frequency-domain
    signal via a Fast Fourier Transform alghoritm.
  • Averaging the frequency-domain EEG signals for
    all five 1 second periods for every set of every
    task to obtain the Average-frequency-domain
    signal for that set of that task for each person.
  • Calculating Power-Spectra and Coherence for every
    set of every task for each person.
  • Averaging of Power-Spectra and Coherence for
    every task from all the sets in that task for
    every person. Thus obtaining the Average-task PS
    and C for every person.
  • Averaging of Power-Spectra and Coherence for all
    persons for every task Thus obtaining the
    Average-person PS and C.
  • Averaging the Power-Spectra and Coherence in the
    desired frequency bands. Thus obtaining the
    Average-band PS and C that are displayed in our
    results.
  • Optionally comparing Average-band PS and C for
    two different tasks.

20
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21
Statistical analysis
  • To calculate the border coherence-difference
    values that are significant at desired p-levels
    we created from 50.000 to 100.000 (depending on
    the frequency band) randomly distributed
    simulated EEG measurements that fit our
    experimental design exactly
  • a total of 11 people, 4 with 56 sets per person,
    7 with 28 sets of one task per person
  • per each set an average of five 1 second
    retention periods
  • a 1 Hz resolution in the Fourier transform
  • From these simulations we obtained a sampling
    distribution curve that fits our experiment
    design as accurately as possible. The
    border-coherence values that are significant at
    desired p-levels were then estimated through a
    two-tailed t-test by calculating the area under
    the sampling distribution curve that fits the
    desired p-level.
  • FB 1 Delta (1-4 Hz), Theta (4-7 Hz), Alpha 1
    (7-10 Hz), Alpha 2 (10-13 Hz)
  • FB 2 Beta (13-30 Hz)
  • FB 3 Gamma (3050 Hz)

Border coherence-difference values at desired p-levels for different frequency bands Border coherence-difference values at desired p-levels for different frequency bands Border coherence-difference values at desired p-levels for different frequency bands Border coherence-difference values at desired p-levels for different frequency bands
p-level Coh. diff. FB 1 Coh. diff. FB 2 Coh. diff. FB 3
lt 0.5 gt 0.0186 gt 0.0091 gt 0.008
lt 0.1 gt 0.0452 gt 0.0221 gt 0.020
lt 0.05 gt 0.0542 gt 0.0263 gt 0.022
lt 0.01 gt 0.0722 gt 0.0348 gt 0.030
22
RESULTS
  • Increases and decreases of coherence for
    different frequency bands with differences
    between 3 tasks will be showed only for
    statistical significance p lt 0.1 FOR ALL IMAGES
  • New schematic model of the head with coherence
    value TASK DIFFERENCES presented
  • Colour scale
  • warm colours- coherence increases between
    electrodes
  • cold colours- coherence decreases between
    electrodes

23
COHERENCE CHANGESMEMORIZE VS. WAIT (CONTROL)
TASK (P lt 0.1)
  • ALPHA 1
  • EXPLAINATION OF SCHEME!
  • (Pre)fronto-central
  • fronto-parietal
  • fronto-occipital increases
  • Interhemispheric bitemporal increases
  • Temporo- parietal increases

24
MEMORIZE VS. WAIT
  • ALPHA 2
  • Fronto-central increases
  • interhemispheric frontotemporal increases
  • fronto-parieto-occipital increases
  • Temporo-parietal increases

25
MEMORIZE VS. WAIT
  • GAMMA
  • Less intensive increases, dominant
  • fronto-parietal
  • fronto-temporal
  • fronto-central increases

26
MEMORIZE VS. WAIT
  • THETA
  • Fronto- central increases
  • Fronto- occipital increases
  • Interhemispheric bitemporal increases
  • Frontotemporo-parietooccipital increases

27
REORDER VS. WAIT
  • ALPHA 1
  • (pre)fronto-centro-parietal increases
  • temporo- central
  • interhemisheric bitemporal
  • parieto-occipital increases

28
REORDER VS. WAIT
  • ALPHA 2
  • Prefronto-central increases
  • Fronto-centro-parietal
  • Fronto-temporal
  • Centro-temporal
  • Interhemispheric bitemporal
  • Temporo-occipital

29
REORDER VS. WAIT
  • GAMMA
  • Less intensive but
  • simmilar pattern of coherence increases

30
REORDER VS. WAIT
  • THETA
  • Fronto-central
  • Fronto-parietal
  • Frontotemporo-occipital increases

31
REORDER VS. MEMORIZE
  • ALPHA 1
  • Centro-temporal increase
  • Occipito-temporal increase
  • Decreases of coherence

32
REORDER VS. MEMORIZE
  • ALPHA 2
  • Fronto-central
  • Fronto-temporo-parietal
  • Parieto-occipital increases
  • Interhemispheric bitemporal increases
  • Decreases of coherence

33
REORDER VS. MEMORIZE
  • GAMMA
  • Less intensive increases
  • Prefronto-centro-parieto-occipital axis increases

34
REORDER VS. MEMORIZE
  • THETA
  • Mainly
  • (Pre)fronto-parietooccipital axis increases

35
ADDITIONAL DATA ANAYLSIS AND DIFFERENT WAY OF
DATA PRESENTATION
  • //MATLAB SOFTWARE (no EOG correction)
  • The influence of EOG correction procedures on EEG
    coherence?
  • gtgtSIMMILAR TRENDS IN COHERENCE VALUES

Memorise vs. wait task THETA coherence changes
36
  • Reorder vs. wait task
  • THETA coherence changes

37
Reorder vs. memorize task THETA coherence changes
38
SUMMARY OF RESULTS
  • WM TASKS COHERENCE INCREASES MAINLY IN ALPHA 2,
    ALPHA 1, THETA (AND ALSO GAMMA) FREQUENCY BANDS
  • FOR MEMORIZE (WM MAINTENANCE) VS. WAIT (CONTROL)
    TASK
  • FOR REORDER (WM MANIPULATION) VS. WAIT (CONTROL)
  • SPATIAL SCALES OF INCREASES MAINLY
    FRONTO-POSTERIOR, FRONTOTEMPORAL, BITEMPORAL
    LONG- RANGE CONNECTIONS IN THE BRAIN
  • REORDER (WM MANIPULATION) VS. MEMORIZE
    (MAINTENANCE-ONLY) COHERENCE INCREASES MAINLY IN
    ALPHA2 AND THETA BAND
  • SPATIAL SCALESALSO ANTERIO-POSTERIOR BRAIN AXIS,
    BITEMPORAL INTERHEMISPHERICALLY, BUT
    NO (PRE)FRONTAL INTERHEMISHERIC INCREASES
  • DECREASES OF COHERENCE OTHER AREAS

39
INTERPRETATION OF RESULTS
  • Greatest coherence (synchronization) increases
    -retention WM periods in ALPHA AND THETA (and
    gamma) frequency bands
  • widespread fronto-parietal association brain
    areas involved- in accordance with other studies
    and Baddeleys model of WM!
  • temporal interhemispheric connections?
  • Different EEG frequencies appear to have
    different functional correlates?
  • LIJ (Lisman, Idiart, Jensen, 1998) WM MODEL!!!
  • The increased theta coherence -working memory
    processes (storage, rehearsal and scanning)
  • Alpha band directly involved in memory processes
    or reflects increased mental effort, attention?
    Role not known yet, results contradictive in
    different studies
  • Gamma band is believed to be correlated with
    sensory processing and the very content of
    information processing, but could also reflect
    increased attentiveness.

40
  • The neuronal synchronization (increased
    coherence) functional coupling
  • role in interaction of posterior association
    cortex (where sensory information is stored), and
    (pre)frontal cortex, where relevant current
    information is held, rehearsed and updated
    (Baddeleys model, phonological loop)
  • Decreases of coherence functional decoupling of
    disturbing processes, selective attention?
  • LATERALIZATION?
  • Verbal memory tasks seem to activate primarly
    left brain hemisphere, but visuospatial memory
    tasks activate predominantly right brain
    hemisphere- we didnt demonstrate significant
    lateralization patterns!
  • possible reasons?volume conduction, low spatial
    resolution, visuospatial strategies

41
Manipulation- CE function
  • We found increases of coherence in fronto-
    parietal loops also compared to memorize only
  • Central executive also demands funtional
    integration of anterio-posterior neural circuits-
    brain regions and not primarily prefrontal
    interhemispheric communication?
  • Role of interhemispheric connections in temporal
    brain regions (alpha 2- semantic memory?)

42
LIJ NEUROPHYSIOLOGICAL MODEL OF WORKING MEMORY
(Lisman, Idiart and Jensen, 1998)
  • Figure --. Concept of LIJ working memory model.
  • Three memory items (A, B, C) are loaded in
    memory buffer, the theta period increases by one
    gamma period with each item added. In retention
    interval (delay period), items are maintained by
    activity-dependent intrinsic properties of the
    neurons coding these items. After probe
    presentation the items can be scanned compared
    with the probe as they are activated. After
    scanning, motor response and answer can be
    initiated. RT reaction time

43
  • Figure --. LIJ model as a multi-item short-term
    memory buffer.
  • Theta and gamma oscillations play an important
    role in the concept. An afterdepolarization (ADP)
    is triggered after a cell fires (sensory input)
    and it causes depolarizing ramp that serves to
    trigger the same cell to fire again after delay.
    These ramps are temporarily offset for different
    memories, an offset that causes different
    memories to fire in different gamma cycles. The
    key function of this buffer is to perpetuate the
    firing of cells in a way that retains serial
    order. The repeat time is determined by theta
    oscillations due to external input. Gamma
    oscillations arise from alternating global
    feedback inhibition and excitation (the cell with
    most depolarized ramp will fire again) because of
    separate firing of different memory codes.

44
DISCUSSION CRITICAL APPROACH
  • BETTER STATISTICAL SIGNIFICANCE?- PROBLEM OF
    CONTROL- WAIT TASK (absolute coherence values!)
    spontaneous non-intentional memory set
    repetition?- encoding before instruction
    inhibitory instruction context (WM?), working
    space preparation resting state correlated
    networks?
  • PROBLEM OF VOLUME CONDUCTION- electrical charge
    flowgt voltage/ signal masking effect
  • INFLUENCE OF EOG CORRECTION PROCEDURE?
  • LOW SPATIAL RESOLUTION IN EEG, occipital-parietal
    transfer of signal, interhemispherically?
    NO LATERALIZATION IN VERBAL
    TASK?
  • ELECTROMAGNETIC INFLUENCES, OTHER ARTEFACTS-
    SIGNAL TO NOISE RATIO

45
FUTURE PERSPECTIVES
  • LAPLACE CORRECTION (Nunez) FOR VOLUME
    CONDUCTION
  • ADDITION OF NEW PURELY SENSORY-PERCEPTIVE
    CONTROL TASK
  • ELECTRODE POSITIONING DETERMINATION
  • HIGHER SAMPLING RATE
  • choosing appropriate cognitive paradigms and
    neuropsychological tests- possible to study
    physiological and patophysiological aspects of
    cognitive, motor and sensory brain function!!!
  • new future perspectives for possible search of
    patophysiological mechanisms and etiological
    factors contributing to many different
    neurological diseases!

46
MAIN REFERENCES
  • Baddeley, A. (2000). The episodic buffer a new
    component of working memory? Trends in cognitive
    science, 4(11), 417-423.
  • Jensen O, Tesche CD (2002). Frontal theta
    activity in humans increases with memory load in
    a working memory task.. Eur J Neurosci.
    200215(8)1395-9.
  • Jensen, O. in Lisman, J.E. (1998). An oscillatory
    short-term memory buffer model can account for
    data on the Sternberg task. The journal of
    neuroscience, 18(24), 10688-10699.
  • Babiloni, C., Carducci, F., Vecchio, F., Rossi,
    S., Babiloni, F., Cincotti, F., Cola, B.,
    Miniussi, C. in Rossini, P.M. (2004). Functional
    frontoparietal connectivity during short-term
    memory as revealed by high resolution EEG
    coherence analysis. Behavioral neurosciencies,
    118(4), 687-697.
  • Klimesch W. Memory processes, brain oscillations
    and EEG synchronization. Internal journal of
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  • Klimesch, W., Doppelmayr, M., Schwaiger, P.
    Auinger in Winkler, Th. (1999). Paradoxical
    alpha synchonisation in memory task. Cognitive
    brain research, 7, 493-501.
  • Sarnthein, J., Petsche, H., Rappelsberger, P.,
    Shaw, G.L. in von Stein, A. (1998).
    Synchronization between prefrontal and posterior
    association cortex during human working memory.
    Neurobiology, 95, 7092-7096.
  • Sauseng, P., Klimesch W., Doppelmayr, M.,
    Hanslmayr, S., Schabus, M. in Gruber, W.R.
    (2004). Theta coupling in the human
    electroencephalogram during a working memory
    task. Neuroscience letters, 354, 123-126.
  • Serrien, D.J., Pogosyan A.H. in Brown, P. (2003).
    Influence of working memory on patterns of motor
    related cortico-cortical coupling. Experimental
    brain research. Dostopno na spletni strani
  • Stam, C.J., van Cappellen van Walsum, A.M. in
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    psychophysiology, 46, 53-66.

47
ABSOLUTE VALUES OF THETA COHERENCE-WAIT VS.
MEMORIZE TASK
48
ABSOLUTE VALUES OF THETA COHERENCE- WAIT VS.
REORDER TASK
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