event-related mu-rhythm desynchronization during movement observation

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  • 7/23/2019 Event-related Mu-rhythm Desynchronization During Movement Observation

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    Event-related mu-rhythm desynchronization during movement

    observation is impaired in Parkinsons disease

    T. Heida a,, N.R. Poppe a, C.C. de Vos b,c, M.J.A.M. van Putten b,c, J.P.P. van Vugt c

    a MIRA Institute for Biomedical Engineering and Technical Medicine, Faculty of Electrical Engineering, Mathematics and Computer Science, Biomedical Signals and Systems

    Group, University of Twente, Enschede, The Netherlandsb MIRA Institute for Biomedical Engineering and Technical Medicine, Faculty of Science and Technology, Department of Clinical Neurophysiology, University of Twente, Enschede,

    The Netherlandsc Medisch Spectrum Twente, Department of Neurology and Clinical Neurophysiology, Enschede, The Netherlands

    a r t i c l e i n f o

    Article history:

    Accepted 23 January 2014

    Available online 2 February 2014

    Keywords:

    Parkinsons disease

    Event-related synchronization

    Event-related desynchronization

    Mu-rhythm

    Mirror neuron system

    h i g h l i g h t s

    EEG alpha and beta band desynchronization (i.e. mu-rhythm ERD) during movement observation was

    largely absent in Parkinsons patients.

    Mu-rhythm ERD impairment may be a marker for Parkinsons disease.

    Evaluating mu-rhythm ERD functionality may reveal pathological processes.

    a b s t r a c t

    Objective: Patients with Parkinsons disease often experience difficulties in adapting movements and

    learning alternative movements to compensate for symptoms. Since observation of movement has been

    demonstrated to lead to the formation of a lasting specific motor memory that resembled that elicited by

    physical training we hypothesize that mu-rhythm desynchronization in response to movement observa-tion is impaired in Parkinsons disease.

    Method: In a pilot study with nine patients with Parkinsons disease at a Hoehn and Yahr stage of I or II

    and eleven age-matched controls, we tested this hypothesis by comparing the event related desynchro-

    nization (ERD) patterns from the EEGrecorded during theobservation of hand action and baseline videos.

    Results: Healthy subjects showed normal bilateral ERD of the mu-rhythm. In patients with Parkinsons

    disease this distinct ERD pattern was lacking.

    Conclusion: The results of this study suggest that event-related mu-rhythm desynchronization is

    impaired in Parkinsons disease, even at early stages of the disease.

    Significance: Studying event-related mu-rhythm desynchronization dysfunction in Parkinsons disease

    patients may enhance our understanding of symptoms as impaired motor learning.

    2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights

    reserved

    1. Introduction

    Idiopathic Parkinsons disease (PD) is a progressive neurodegen-

    erative disease resulting in multiple motor symptoms which differ

    in type and severity depending on disease progression, and show a

    large variability between patients. PD symptoms are associated

    with basal ganglia dysfunction caused by the loss of dopamine-

    producing cells in the substantia nigra pars compacta. The basal

    ganglia are involved in enabling practiced motor acts and in gating

    the initiation of voluntary movements by modulating motor

    programs stored in the motor cortex and elsewhere in the motor

    hierarchy (Marsden, 1982; Mink, 1996; OReilly and Frank, 2006).

    Parkinsons patients often experience difficulties in adapting

    movements and learning alternative movements to compensate

    for symptoms. Observation of movement has been demonstrated

    to lead to the formation of a lasting specific motor memory that

    resembled that elicited by physical training (Stefan et al., 2005).

    http://dx.doi.org/10.1016/j.clinph.2014.01.016

    1388-2457/2014 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved

    Corresponding author. Address: University of Twente, Biomedical Signals &

    Systems, Zuidhorst 214, P.O. Box 217, 7500 AE Enschede, The Netherlands. Tel.: +31

    53 4892759; fax: +31 53 4892287.

    E-mail address: [email protected](T. Heida).

    Clinical Neurophysiology 125 (2014) 18191825

    Contents lists available at ScienceDirect

    Clinical Neurophysiology

    j o u r n a l h o m e p a g e : w w w . e l s e v i e r . c o m / l o c a t e / c l i n p h

    http://dx.doi.org/10.1016/j.clinph.2014.01.016mailto:[email protected]://dx.doi.org/10.1016/j.clinph.2014.01.016http://www.sciencedirect.com/science/journal/13882457http://www.elsevier.com/locate/clinphhttp://www.elsevier.com/locate/clinphhttp://www.sciencedirect.com/science/journal/13882457http://dx.doi.org/10.1016/j.clinph.2014.01.016mailto:[email protected]://dx.doi.org/10.1016/j.clinph.2014.01.016http://-/?-http://-/?-http://-/?-http://-/?-http://-/?-http://crossmark.crossref.org/dialog/?doi=10.1016/j.clinph.2014.01.016&domain=pdfhttp://-/?-
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    We hypothesize that impaired motor learning in PD might partly

    reflect deficits in the neuronal responses to movement

    observation.

    Non-invasive studies using positron emission tomography and

    fMRI studies have found that action observation activates, often

    bilaterally, the rostral part of the inferior parietal lobule (IPL) and

    the posterior part of the inferior frontal gyrus (IFG) as well as the

    ventral premotor area (PMv) and the anterior intraparietal area

    (AIP) (Alegre et al., 2010; Cattaneo and Rizzolatti, 2009; Chaminade

    et al., 2005; Fogassi and Ferrari, 2011; Iacoboni and Dapretto,

    2006; Kessler et al., 2006; Keysers and Gazzola, 2006; Nishitani

    and Hari, 2000; Rizzolatti and Craighero, 2004). During electroen-

    cephalography (EEG) event related desynchronization (ERD) of

    mu-rhythm activity, i.e. a decrease in alpha (812 Hz) and beta

    power (1330 Hz), occurs over these areas during movement

    observation. Mu-rhythm ERD during observed movement has been

    suggested to be an indicator of activity in the so-called mirror neu-

    ron system (MNS) (Alegre et al., 2010; Pfurtscheller and Lopes da

    Silva, 1999). Mirror neurons are a class of neurons that become ac-

    tive both when individuals perform a specific motor act and when

    they observe a similar act performed by others (Di Pellegrino et al.,

    1992;Fadiga et al., 1995;Rizzolatti et al., 2009). The MNS has been

    implicated in several social behaviors varying from motor learning

    (e.g. through imitation) to social recognition and empathy (Iaco-

    boni and Dapretto, 2006). The MNS has been most widely studied

    in non-human primates using direct neuronal recordings. There is

    no consensus on the exact location of the MNS in humans; the

    areas mentioned above have been suggested to be part of this sys-

    tem. Subcortical areas involved in motor behavior such as basal

    ganglia and cerebellum were also found to be activated during

    observation of hand movements (Alegre et al., 2010; Decety

    et al., 1994; Devos et al., 2003; Frey and Gerry, 2006; Kessler

    et al., 2006; Khn et al., 2004). For example, local field potentials

    in the subthalamic nucleus, measured in PD subjects during sur-

    gery for deep brain stimulation, show changes in activity during

    movement observation coherent with changes occurring in the

    motor cortex (Fogassi and Ferrari, 2011; Marceglia et al., 2009).We tested the hypothesis that the neuronal response to move-

    ment observation is impaired in PD by comparing the amount of

    event related desynchronization (ERD) from the EEG recorded dur-

    ing the observation of hand action and baseline videos of PD pa-

    tients and age-matched healthy control subjects.

    2. Methods

    2.1. Study population

    In this pilot study 9 Parkinsons patients (7 males, 2 females,

    average age 67.1 8.6 years; the time since diagnosis ranged from

    6 months to about 14 years; Hoehn and Yahr stage 1 (n= 3), and 2(n= 6), seeTable 1) and 11 age-matched healthy control subjects

    (6 males, 5 females, average age 61.5 10.0 years) were included.

    All patients fulfilled the UK Brain Bank criteria for Parkinsons dis-

    ease (Hughes et al., 1992). Patients with severe tremor, dyskinesias

    or those treated with deep brain stimulation were excluded in or-

    der to prevent EEG artifacts. Patients with known PD related

    dementia according to the clinical diagnostic criteria (Emre et al.,

    2007) and those using sedative medication were also excluded. Pa-

    tients were allowed to take their usual anti-parkinsonian medica-

    tion on the day of the experiment. All procedures conformed to the

    Declaration of Helsinki and were approved by the Medical Ethical

    Committee of the Medisch Spectrum Twente in Enschede, the

    Netherlands. All subjects gave written informed consent prior to

    participation in the study.

    2.2. Measurement set up

    Subjects sat comfortably in an armchair in an electrically and

    sound-shielded room watching hand action and baseline videos.

    The EEG was recorded using ASA acquisition software (ANT Inter-

    national BV, the Netherlands); 64 Ag/AgCl electrodes were posi-

    tioned according the 10/10-system using a waveguard EEG cap.

    The signals were amplified, low-pass filtered (digital FIR filter

    1350 Hz cut off) and sampled at 5 kHz (Refa, Twente Medical Sys-tems International BV, the Netherlands).

    2.3. Experimental protocol

    A measurement consisted of six trials. During each trial, sub-

    jects watched a video consisting of eight fragments showing hand

    movements interspersed with seven baseline fragments. Subjects

    could rest between trials whenever desired. Presented hand ac-

    tions included pinching, grasping, ball grasping, finger tapping,

    and hand turning (supination/pronation), randomly executed with

    left or right hand. As an example,Fig. 1A shows three frames of the

    video showing pinching movements executed with the left hand. A

    moving red ball over a black background was used as baseline vi-

    deo (Fig. 1B). It was expected that during the observation of thisbaseline video the brain returned to a resting state in which mirror

    neurons are deactivated. Patients were carefully watched to not

    perform any voluntary movements.

    Each trial had a duration of approximately two and a half min-

    utes with the hand action and baseline fragments having a length

    varying from 8 to 12 s. The various types of hand actions were ran-

    domly distributed over the six trials to prevent predictability. Each

    hand action appeared several times in a number of trials up to a

    maximum of six times.

    2.4. EEG analysis

    All analyses were performed off-line in Matlab (the Mathworks,

    Inc., 2009b). EEGlab (http://sccn.ucsd.edu/eeglab/ ; Delorme andMakeig, 2004) was used to create topoplots (i.e. a topographic

    map of a scalp data field in a 2D circular view); ANT-Matlab scripts

    Table 1

    Patient details (time in years).

    Patient Sex Age Disease duration Hoehn & Yahr stage Dominant motor symptoms Antiparkinsonian medication

    1 F 49 5 I Tremor None

    2 M 62 4 II Bradykinesia Ropinirole

    3 F 54 10 II Tremor, bradykinesia Levodopa/benserazide, pergolide, amantadine

    4 M 72 2 I Tremor None

    5 M 72 8 II Tremor, rigidity Levodopa/benserazide, pramipexole

    6 M 68 7 II Tremor, freezing, bradykinesia Pramipexole

    7 M 75 12 II Freezing, bradykinesia Levodopa/benserazide, pramipexole

    8 M 73 7 II Rigidity, bradykinesia, akinesia Levodopa/benserazide

    9 M 74 4 III Tremor, bradykinesia Levodopa/carbidopa, entacapone

    1820 T. Heida et al. / Clinical Neurophysiology 125 (2014) 18191825

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    (ANT International BV, the Netherlands) were used to import EEG

    data into Matlab.

    2.4.1. Preprocessing

    The EEG data was down-sampled to 500 Hz and filtered using a

    band-pass filter of 170 Hz (4th order non-causal Butterworth fil-

    ter) to remove drift and noise. In addition, a 50 Hz notch-filter was

    used to remove power line noise. To be able to analyze local corti-

    cal activity and to limit volume conduction effects, source deriva-

    tion was applied (Defebvre et al., 1998): for each electrode the

    average of the signals of the neighboring electrodes was extracted.

    In a few occasions electrodes were malfunctioning during part of

    the experiment. These electrodes were excluded from the dataset and the source derivation was adapted accordingly.

    The EEG signals were split into five components by band-pass

    filtering the data (4th order non-causal Butterworth filter) accord-

    ing to the EEG frequency bands: delta (14 Hz), theta (48 Hz), al-

    pha (813 Hz), beta (1330 Hz), and gamma (3070 Hz) band. For

    artifact detection and removal the signal components of each video

    fragment were split into epochs of 500 ms, with 50% overlap. The

    mean signal power of each epoch was calculated by taking the

    mean of the squared voltage. For each electrode and for each signal

    component, a threshold level equal to the mean power of the total

    fragment plus two times the standard deviation was used to re-

    move epochs having a mean power exceeding this threshold. The

    remaining data from all repetitions of a single hand action video

    or baseline video were combined for further analyses.

    2.4.2. Evoked response (de)synchronization

    At each electrode position on the scalp, and for each frequency

    band the event-related desynchronization (ERD) or synchroniza-

    tion (ERS) was calculated as a power decrease or increase, respec-

    tively, compared to the corresponding baseline power. The evoked

    response is expressed as percentages of this baseline power:

    ER ppref

    pref 100%withPthe mean power of the EEG signal compo-

    nent recorded during the observation of a single hand action video

    andPrefthe average power of all baseline fragments; positive val-

    ues correspond to ERS, negative values correspond to ERD. By in-

    verse distance weighted interpolation grand average ERD/ERS

    topoplots were created for each frequency band and each hand ac-tion video, for both the PD and the control group.

    2.4.3. Statistical analysis

    Based on previous studies in humans, mu-rhythm ERD during

    observed movement is expected to be detected in the area covered

    by the electrodes C3, FC3, C5, CP3, and C1 for the left hemi sphere,

    and the electrodes C4, FC4, C2, CP4, and C6 for the right hemi-

    sphere, of a 64-channel 10/10 distributed EEG cap (Alegre et al.,

    2011; Babiloni et al., 2002; Buccino et al., 2001; Cattaneo and

    Rizzolatti, 2009; Fogassi and Ferrari, 2011; Iacoboni and Dapretto,

    2006). For the statistical analyses (SPSS Inc., 18) and comparison of

    mu-rhythm ERD in Parkinsons patients and healthy controls the

    evoked responses in these areas were determined by taking

    the maximum ERD of all five electrodes for each hemisphere. The

    ShapiroWilk test was used to determine whether the data sets

    were normally distributed. If not, log transformation was applied.The students t-test for independent samples was used to deter-

    mine if significant differences existed between the observation of

    hand actions performed with the left and right hand. To test

    whether the ERD in both hemispheres were not independent due

    to interhemispheric connections a paired-samples students t-test

    was performed. A repeated measures analysis of variance (ANOVA)

    with post hoc multiple comparisons was performed to test if

    specific types of hand actions were more effective in evoking

    mu-rhythm ERD than others. To test for band specificity of the ob-

    served ERD group comparison was performed for the ERD in the

    indicated areas for all frequency bands using the MannWhitney

    U test since the sample size was different for the two groups

    (n= 9 patient group;n = 11 control group), and the data was not

    in all cases normally distributed (even after log-transformation).ERD levels within each of the other frequency bands (i.e. delta, the-

    ta, and gamma) were determined according to the same method as

    used for determining mu-rhythm ERD in the area around C3 and

    C4: we have taken the maximum ERD level at one of five electrodes

    for each subject for each of the frequency bands.

    3. Results

    3.1. Mu-rhythm ERD in healthy subjects

    Fig. 2 shows the grand average ERD/ERS topoplots of the control

    group that resulted from the observation of the ball grasping

    movement performed by the right hand. The alpha and beta bandshow relatively similar ERD patterns in the area surrounding the

    Fig. 1. (A)Videoframes of thepinching movementperformed with theleft hand;the movementwas repeated several times duringthe video. (B)Three frames of thebaseline

    video;the redball movedacross the screen in a randomfashionwithvariablespeed. (For interpretationof thereferences to colorin this figure legend, thereader is referred to

    the web version of this article.)

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    electrodes C3 and C4 (i.e. C3, FC3, C5, CP3, C1, and C4, FC4, C2, CP4,

    C6, resp.), corresponding to the mu-rhythm desynchronization pat-

    terns. No statistical differences between the observation of the ac-

    tion performed by the left and right hand, or between the left and

    right hemisphere, were found. Furthermore, no age and gender re-

    lated effects were found.

    Besides the induced ERD patterns all observed hand actions re-

    sulted in a distinct alpha and beta band synchronization (ERS) area

    around electrodes Pz and POz, the central part of the parietal-

    occipital area. The level of synchronization in this area seemed to

    be related to the level of desynchronization in the area around

    C3 and C4: a high ERD level around C3/C4 was accompanied by a

    high ERS level around Pz/POz.

    3.2. Mu-rhythm ERD in Parkinsons patients

    Fig. 3 shows the grand average ERD/ERS topoplots of the Parkin-

    son group resulting from the observation of the ball grasping

    movement performed by the right hand. In contrast to the grand

    average topoplots of the control group the Parkinson group did

    not show distinctive desynchronization spots around C3 and C4

    in the alpha and beta band. Some types of hand actions did evoke

    ERD around C3/C4 (e.g. left hand pinching and right hand grasping)

    in the alpha band, but the effect was much smaller compared to

    the control group. No statistically significant difference was found

    between the observation of left and right hand actions for all types

    of hand actions (p> 0.05). In addition, no statistically significantdifference was found between the left and right hemisphere, and

    also no relatedness between the two hemispheres was found for

    all observed hand actions performed by either hand (p> 0.05).

    Similar to the healthy subjects alpha and beta band ERS in the

    central part of the parietal-occipital area were found in the PD

    patients.

    3.3. Group comparison of mu-rhythm ERD

    Fig. 4expresses the ERD differences in the area around C3 and

    C4 between the Parkinson and the control group for all observed

    hand actions (including left and right hand actions). The ERD level

    was significantly reduced in the Parkinson group compared to the

    control group for all observed hand actions in the beta band(p< 0.05). A similar result is observed for the alpha band except

    for the hand turning movement. All other frequency bands show

    less or no (gamma band) significant differences in ERD between

    the two groups.

    It should be noted that the mean EEG baseline level of the Par-

    kinson group was 0.45lV2 (95% confidence interval (CI): 0.31

    0.67 lV2) versus 0.31 lV2 (95% CI: 0.280.35 lV2) of the control

    group, indicating that the baseline EEG power in the Parkinson

    group was significantly higher than the control group baseline

    EEG power (p< 0.05).

    The ERS in the central parietal-occipital area was comparable

    for the control and PD group for each of the observed hand actions.

    However, when combining the responses to all types of observed

    hand actions the level of event related synchronization was signif-icantly higher in the PD group (p< 0.05).

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    Delta30 Hz

    Fig. 2. Grand average ERD topoplots of the control group (n= 11) resulting from the observation of the ball grasping movement performed by the right hand. Bilateral alpha

    and beta banddesynchronization (around C3 and C4) indicate mu-rhythm desynchronization. The high levels of desynchronization in the frontal areas in the delta, theta and,

    to some extent, the alpha band may be ascribed to eye blinking and eye movements.

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    4. Discussion

    The main finding of our study was that patients with PD did not

    show event-related mu-rhythm desynchronization in the area

    around electrodes C3 and C4 in response to movement observa-

    tion. Our experimental protocol was able to detect normal ERD

    (and also ERS) patterns in our healthy controls very similar to

    the patterns described in previous studies (Iacoboni and Dapretto,

    2006; Keysers and Gazzola, 2006; Rizzolatti et al., 2009), both with

    respect to magnitude and topographic distribution over the scalp.

    The ERD levels of the healthy control and PD group showed sig-

    nificant differences for the alpha and beta band for all observed

    movements (except one in the alpha band, see Fig. 4), while the

    other frequency bands did not show these clear differences. Itshould be noted that for all frequency bands ERD levels within

    the same area were compared, while we only expected to see clear

    mu-rhythm ERD, and thus desynchronization in the alpha and beta

    band. The level of ERD (or even ERS) and the spatial distribution

    may differ for the other frequency bands, and may be related to dif-

    ferent functions.

    The elevated overall baseline power and increased alpha and

    beta synchronization levels in the baseline EEG in PD may express

    overactivity of motor cortical areas and reduced inhibition of the

    motor cortex as a result of dopamine depletion (Seiss and Praamstra,

    2004; Stoffers et al., 2008). It has been found that increased resting

    state cortico-cortical coupling in the alpha range (810 Hz, i.e. al-

    pha1) is a feature of PD from the earliest clinical stages onward

    (Stoffers et al., 2008). With increasing disease duration and sever-ity of PD symptoms, neighboring frequency bands (i.e. theta

    (48 Hz), alpha2 (1013 Hz) and beta band (1330 Hz)) become

    increasingly involved in the off state (Stoffers et al., 2008;

    Silberstein et al., 2005). EEG-EEG coherence over 1035 Hz has

    been found to correlate with severity of disease symptoms in un-

    treated PD (Silberstein et al., 2005). Dopaminergic therapy reduces

    the coupling in parallel with motor improvement. The reduced mo-

    tor cortex inhibition in PD is proposed to reflect the loss of spatial

    and temporal selectivity in basal ganglia functioning that influence

    the selection and suppression of competing responses (Seiss and

    Praamstra, 2004). The desynchronization of these idling rhythms

    is impaired as well as the local synchronization at 3050 Hz (the

    gamma band), required for the execution of motor programs (De-

    vos et al., 2003; Salenius et al., 2002). This failure of high frequency

    synchronization is reflected downstream as the inability to gener-ate fused muscle contraction. Impairments in the degree of sup-

    pression of mu-power during movement have been shown to

    correlate with bradykinesia (Defebvre et al., 1993; Silberstein

    et al., 2005).

    A high baseline level may mean that it is easier to detect desyn-

    chronization. However, average levels of ERS/ERD were compara-

    ble for the PD group and the group of healthy subjects. Alegre

    et al. (2010)found a similar effect in STN activity: In STN record-

    ings in PD patients in which abnormal beta oscillatory activity is

    detected, movement-related decrease in beta activity is still pres-

    ent with the same relative intensity under medication on and off

    conditions, while after medication intake the oscillatory activity

    in the beta band is greatly attenuated (Alegre et al., 2010).

    In the central part of the parietal-occipital areas (around elec-trodes Pz and POz) synchronization was observed in the alpha

    noitazin

    orh

    cn

    ys

    no

    itazin

    orh

    cn

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    Delta30 Hz

    Fig. 3. Grand average ERD/ERS topoplots of the Parkinsongroup (n= 9) resulting from the observation of the ball grasping movement performed by the right hand. The alpha

    and beta band ERD levels around C3/C4 are much lower compared to the control group (p< 0.05).

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    and beta band for most of the hand action videos in the control

    group. A similar simultaneous contralateral localized mu rhythm

    ERD and an occipital localized alpha rhythm ERS was observed dur-

    ing the performance of self-paced hand movements in a group

    study of nine healthy subjects as described by Pfurtscheller and

    Lopes da Silva (1999). They explained this contrasting behavior

    as the expression of the activation of those cortical areas involved

    in a single motor program while areas that are not involved in the

    execution of this program are deactivated.

    ERS around the parietal-occipital electrodes Pz and POz may

    also be related to motion processing, since these electrodes are lo-

    cated in the region including the visual area V3A.Pfurtscheller and

    Lopes da Silva (1999) pose that gamma band oscillations (around

    40 Hz) may reflect a stage of active information processing sincethey appear appropriate to establish rapid coupling or synchroni-

    zation between spatially separated cell assemblies (Pfurtscheller

    and Lopes da Silva, 1999). A prerequisite for gamma band ERS

    may be the desynchronization in alpha and beta band rhythms

    (Pfurtscheller and Lopes da Silva, 1999). In almost all of the topo-

    plots from the control group alpha and beta band ERS in the pari-

    etal-occipital area was accompanied by gamma band ERD (see

    Fig. 2). The ERS around electrodes POz and Pz as observed in the

    control group was also present in the Parkinson group, at an even

    higher level. In most cases this ERS was not accompanied by a gam-

    ma band ERD pattern, which may indicate a dysfunction of visuo-

    motor integration as is often suggested to occur in PD (Devos et al.,

    2003; Labyt et al., 2003; Tropini et al., 2011).

    Another explanation for this elevated ERS level can be found inthe choice for the baseline movies. The moving ball movie could

    induce higher visual cortex activity due to the moving properties

    of the ball. Compared to the hand movies, that only show vertical

    movement, the red ball moves across the screen randomly in all

    directions (horizontally, vertically, and diagonally) with different

    speeds. This might induce more activity (desynchronization) in

    the visual cortex for the baseline movies. In general, the baseline

    movie should provide a baseline mu-rhythm that is strong enough

    to detect mu-rhythm desynchronization during movement obser-

    vation. It has recently been found, however, that the most effective

    baseline movie is subject specific, and can range from a static im-

    age (e.g. a static hand, (white stripes on) a black screen) to a dy-

    namic movie (e.g. bouncing ball(s), slowly moving flower)

    (Tangwiriyasakul et al., 2013).

    The number of patients included in this pilot study was rela-tively low, the clinical disability of the patients was only moder-

    ate (Hoehn and Yahr stage III), and the patients were not

    withdrawn from medication prior to participation in this study.

    Movement-related (de)synchronization patterns in the cortex

    have been found to be partially corrected by both chronic and

    acute administration of L-Dopa in mildly impaired PD patients

    (Brown and Marsden, 1998; Defebvre et al., 1998; Devos et al.,

    2003; Zaidel et al., 2010). Still, the event-related mu-rhythm

    ERD was found to be impaired in our group of patients. This sug-

    gests that impaired dopaminergic activity in the basal ganglia by

    itself is insufficient to explain the observed impairment of mu-

    rhythm ERD. Mu-rhythm ERD impairment may be a marker for

    Parkinsons disease. However, whether or not this mu-rhythm

    impairment can be ascribed to an impairment of the neuronalnetwork involved in movement observation or to a more global

    Fig. 4. Visualizationof thecomparisonof theERD level in thearea around electrodes C3and C4, of the PD group with thecontrolgroupfor each of theobserved hand actions,

    and for all frequency bands. The bars represent the mean SEM (standard error of the mean). Hand actions: FT = finger tapping; PC = pinching; HT = hand turning;

    GP = grasping; and BG = ball grasping. Indicates a statistically significant difference (p< 0.05).

    1824 T. Heida et al. / Clinical Neurophysiology 125 (2014) 18191825

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    7/7

    change in brain activation patterns related to PD requires further

    investigation.

    5. Conclusion

    This pilot study shows that event related mu-rhythm desyn-

    chronization during movement observation as measured with

    EEG is impaired in Parkinsons disease. This is in line with earlierfindings of impaired desynchronization of subthalamic nucleus

    activity during movement observation in Parkinsons disease. This

    impairment may play a role in symptoms such as impaired motor

    learning and programming.

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