Event Related Desynchronization (ERD) ofMu Rhythms During Concentric and

Eccentric Contractions

The Graduate School

Yonsei University

Department of Physical Therapy

Joohee Park

Event Related Desynchronization (ERD) ofMu Rhythms During Concentric and

Eccentric Contractions

Joohee Park

A Master ThesisSubmitted to the Department of Physical Therapy

and the Graduate School of Yonsei Universityin partial fulfillment of the requirements

for the degree of Master of Science

June 2014

This certifies that the masters thesis of Joohee Park is approved.

Thesis Supervisor: Hye-Seon Jeon

Kyung Hwan Kim: Thesis Committee Member #1

Heonseok Cynn: Thesis Committee Member #2

The Graduate SchoolYonsei University

June 2014

Acknowledgement

First, I want to thank Prof. Hyeseon Jeon. She has given me lifelong guidance and

encouragement during all phases of my graduate-school life. Most importantly, she

gave me an opportunity to improve myself and to study further. Without her, I would

not be who I am today. I would also like to thank the other members of my thesis

committee, Prof. Kyunghwan Kim and Prof. Heonseock Cynn. I deeply thank Prof.

Kyunghwan Kim. He gave me an opportunity to study electroencephalography and

helped me to arrange my thesis. Without his support, I would not have been able to

finish my thesis. I also gladly express my gratitude to Prof. Heonseock Cynn. I really

appreciate his thoughtfulness and encouraging advice to keep my mind straight. I also

wish to express my deep and sincere gratitude to Prof. Chunghwi Yi, Ohyun Kwon,

Sanghyun Cho, and Joshua Yoo.

Especially, I offer sincere thanks to Prof. Sagyeom Lee and Jiseong Kim of Suwon

Women’s College (Department of Physical Therapy) for their support and encour-

agement.

I really appreciate my senior graduate member, Sunyoung Kang. I thank her for

keeping a warm heart and cheery attitude toward me during my time at graduate

school. I will never forget your support—I love you so much. I additionally wish to

show my appreciation to Jaeik Song. I am really happy to have met him, and appreci-

ate the chance to thank him for his sacrifices and encouragement for my sake. Also, I

would like to thank laboratory member Boram Chai.

I deeply appreciate Sungdae Chuoung and Onebin Lim, who continuously motivat-

ed me and helped me adapt to life at graduate school. Woojeong Choi and Jeong-ah

Kim, I will never forget our “women” master’s degree meeting. I would also like to

express my gratitude to all the members of the graduate school Department of Physi-

cal Therapy.

In particular, I wish to express my deep appreciation for Kwang Su Cha, who has

supported this thesis. I was able to finish my graduate coursework because of him.

Thanks for his kind-heartedness and consideration. I also appreciate Jeong Woo Choi.

I gladly thank Juhee Kang, who is my best friend. Since our middle school years

together, she has always encouraged me in my choices. I wish to sincerely thank my

friends Yoonjung Choi, Yuri Park, Yeona Cho, and specially, Bomi choi. Thanks to

Seong uk Kim, who will be my best friend for the rest of my life.

Finally, this thesis is dedicated to my family, Ducksoo Park, Yongsoon Kim, and

Seongho Park. Without the support of my family, I would not have focused on my

studying and I would never have attempted this degree. I really love you. Most im-

portantly, I would like to thank Seongung Lee. I am fortunate to have met him during

my life.

I keep the words, no pain, no gain, in my mind, and work hard for further study.

Thank you.

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Table of Contents

List of Figures ···································································· iii

List of Tables ····································································· iv

Abstract ············································································ v

Introduction ······································································· 1

Method ············································································· 5

1. Subjects ······································································ 5

2. Instrumentation ····························································· 6

2.1 Electromyography ······················································ 6

2.2 Electroencephalography ··············································· 6

2.3 Isokinetic Device ······················································· 6

3. Experimental Procedure ······················································· 7

4. Data Analysis ······························································· 13

4.1 Electromyography Data ·············································· 13

4.2 Electroencephalography Data ········································ 14

5. Statistical Analysis ························································ 17

Results ············································································ 18

1. Fatigue Effects ····························································· 18

2. Chronological Events of the Trigger, EMG, and ERD Onset ········ 19

3. RT of EMG ································································· 21

4. ERD Onset Time of Mu Rhythms ······································· 23

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5. ERD Amplitude of Mu Rhythms ········································ 26

6. Topography of Averaged ERD Activity of Mu Rhythms ············· 29

Discussion ········································································ 30

1. Exclusion of Possible Influences of Fatigue Induced by Repetitive

Contractions ································································ 32

2. RT of EMG ································································· 33

3. ERD Onset Time of Mu Rhythms ······································· 34

4. ERD Amplitude of Mu Rhythm ··········································· 36

5. Limitations ··································································· 38

Conclusions ······································································ 39

References ········································································ 40

Abstract in Korean ······························································· 49

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List of Figures

Figure 1. Experimental procedure ·············································· 10

Figure 2. Participant on the isokinetic device ································· 11

Figure 3. Presentation of visual cues on the computer monitor ············· 12

Figure 4. Time frequency map in C4 ··········································· 16

Figure 5. Detection of the baseline, onset time, and amplitude of ERD

············································································ 16

Figure 6. Examples of Examples of joint angles, EMG (biceps brachii),

force, and ERD (C4) for concentric contractions (left) and

eccentric contractions (right) ········································· 20

Figure 7. Two-way interaction plot for RT ···································· 22

Figure 8. ERD onset time plot ·················································· 25

Figure 9. Time frequency map of contraction types and hemisphere ······· 28

Figure 10. Topography of average mu rhythm ERD in 1000 - 2000 ms

prior to the onset of EMG ··········································· 29

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List of Tables

Table 1. Median frequency and peak torque ··································· 18

Table 2. Results of two-way ANOVA for the RT of EMG ················· 22

Table 3. Results of three-way ANOVA for the onset of ERD ············· 24

Table 4. ERD onset time ························································ 24

Table 5. Results of three-way ANOVA for ERD amplitude ··············· 27

Table 6. ERD amplitude ························································ 27

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ABSTRACT

Event Related Desynchronization (ERD) of Mu rhythm

During Concentric and Eccentric Contraction

Joohee Park

Dept. of Physical Therapy

The Graduate School

Yonsei University

Concentric contractions are achieved by the shortening of muscle fibers when a

person performs movements against gravity and external force. Eccentric contractions

are achieved by the lengthening of muscle fibers when a person performs movements

in line with gravity or that lower the load. Previous studies using electroencephalog-

raphy (EEG) and functional magnetic resonance imaging (f-MRI) reveal differences

between the brain activities associated with these two types of contractions in patients.

This study designs an experiment to examine the changes in cortical activation pat-

terns as subjects undergo familiarization with tasks by repeating concentric and ec-

centric elbow flexor contractions. We speculate that previously observed differences

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in brain activities are possibilities induced by the level of required attention and fa-

miliarity with motor tasks, rather than due to fundamental differences in the biome-

chanical characteristics of the tasks. Accordingly, the purposes of our study are, first,

to compare the EEG patterns and reaction time (RT) of electromyographic (EMG)

between concentric and eccentric biceps brachii (BB) contractions under the RT para-

digm, and subsequently, to evaluate how the EEG patterns and RT of EMG change

after the same amount of practice.

Sixteen subjects performed three phases of 30 repetitions of submaximal voluntary

concentric and eccentric BB muscle contractions on a Biodex isokinetic dynamometer.

In all, the subjects performed a total of 90 eccentric and 90 concentric contractions.

EEG signals (32 channels) were obtained, together with force, joint angle, and biceps

EMG data. Event-related desynchronization (ERD) patterns of the mu rhythms (8 - 13

Hz) in the somatosensory cortex of bilateral hemispheres (C3 and C4) were selective-

ly analyzed. EMG onset times were compared using two-way repeated analysis of

variance (ANOVA) measures (contraction type x phase), and ERD onset and ERD

amplitudes were statically compared using three-way repeated ANOVA measures

(contraction type x phase x hemisphere).

There were several major findings, as follows. (1) The mean RT of EMG in phase I

of eccentric contractions was significantly longer than the mean RT of EMG in the

phase I of concentric contractions, and the RTs of both contraction types decreased

with practice. The mean RTs of EMG in phase III were not statistically different be-

tween contraction types. (2) The time of ERD onset relative to EMG onset came sig-

- vii -

nificantly earlier during eccentric contractions in both phase I and phase III. For both

contraction types, the onset was significantly faster in phase III. In phase III, however,

the difference between contraction types was maintained. (3) The ERD amplitude was

significantly lower in phase III than in phase I during both types of contractions.

However, no statistical difference was found between contraction types and hemi-

spheres. (4) Topography reveals that the mu rhythms in the sensorimotor cortex were

bilaterally deactivated during phase I, regardless of the type of contraction. In phase

III, however, the mu rhythm ERD was localized in the contralateral sensorimotor area

during concentric contractions. Phase III ERD patterns in the eccentric contractions

remained bilateral.

RT represents the amount of information to be processed by the central nervous

system (CNS) before initiation of a given motor action. In the same way, early ERD

onset of mu rhythms in the sensory motor cortex is related to less preparation required

for a given motor task. Therefore, these results seem to suggest that eccentric contrac-

tions require the brain to work harder in preparation for the task. Furthermore, in the

case of both types of muscle contraction herein, the mental demand decreased as fa-

miliarity with the motor action increased with practice, which supports the observed

changes in both ERD onset and amplitude in repetitive contractions. However, in con-

trast to our expectation, eccentric contractions still required more brain activity for

preparation and cognitive load, even after repetitive training to familiarize the sub-

jects with the task. Therefore, we conclude that the differences in brain activity during

- viii -

eccentric and concentric muscle activity do not disappear with motor learning or prac-

tice.

Keywords: Concentric contraction, Eccentric contraction, Electroencephalography,

Event related desynchronization, Practice.

- 1 -

Introduction

Human voluntary dynamic movements are largely classified into concentric and

eccentric contractions (Enoka 1996). Concentric contractions are achieved by the

shortening of muscle fibers when a person performs movements against gravity and

external force. During concentric contractions, the torque produced by contraction of

the muscle exceeds the force of the load torque, and accordingly, the load is raised.

For example, when the activation of the elbow flexor muscle is higher than the load

of the arm, the elbow resists external force and the elbow flexor muscle is shortened.

Eccentric contractions are achieved by the lengthening of muscle fibers when a per-

son performs movements in line with gravity or that lower the load. The muscle

torque generated during an eccentric contraction is lesser than the load torque. Ac-

cordingly, the load is lowered in line with the force of gravity. As an example, when

the torque generated by the elbow flexor muscle is smaller than the load of the arm,

the muscle undergoes a lengthening contraction (i.e., elbow extension) (Enoka 1996).

As another example, descending onto a step requires muscle lengthening, which is

associated with eccentric control of the quadriceps muscles, in order to load the

weight of a person to his or her standing leg, while his or her knee undergoes knee

flexion. Although eccentric contractions are involved in our ordinary muscle activities,

the concept of a “lengthening contraction” is unfamiliar and unusual.

- 2 -

Eccentric contractions are an efficient way of movement because eccentric contrac-

tions generate the same level of force at a given velocity with lower muscle activation

in comparison to concentric contractions (Bigland-Ritchie and Woods 1976; Bigland

and Lippold 1954; Steriade and Llinás 1988; Tesch et al. 1990). According to Enoka

(1996), concentric and eccentric contractions are controlled by different neural con-

trol mechanisms. This assertion is based on the evidence of different monosynaptic

reflex excitability (Abbruzzese et al. 1994; Duchateau and Enoka 2008) and altered

motor unit recruitment strategies (Howell et al. 1995; Nardone, Romano, and

Schieppati 1989). Increased smoothness in movement (Brown 2000) and increased

risk of muscle tissue damage during eccentric muscle performance are also reported

(Asmussen and Bonde‐Petersen 1974; Clarkson and Tremblay 1988; Mafi, Lorentzon,

and Alfredson 2001). These findings are partially related to the higher degree of diffi-

culty in controlling eccentric contractions, which is represented by the increased at-

tention and mental demands among individuals performing eccentric muscle activities

(Fang et al. 2004).

Recently, electroencephalography (EEG) and functional magnetic resonance imag-

ing (f-MRI) have been used to investigate the characteristics of eccentric muscle con-

tractions. According to an EEG study by Fang et al. (2001, 2004), executing eccentric

muscle contractions requires longer preparation time and a larger magnitude of brain

activity. The study reports that controlling eccentric contractions is more difficult

than controlling concentric contractions. Furthermore, according to an f-MRI study

by Olsson et al. (2012), activation of the prefrontal cortex is relatively higher during

- 3 -

imagery of the eccentric phase than during imagery of the concentric phase. To be fair,

however, the motor cortex is more heavily recruited during imagery of the concentric

phase than during imagery of the eccentric phase. It appears that mental planning for

eccentric contractions may require additional involvement of high-order central nerv-

ous system (CNS) areas such as the prefrontal cortex.

According to one study, the dorsal prefrontal cortex and the anterior cingulate cor-

tex are activated when subjects learn a new motor sequence and need to pay more

attention (Passingham 1997). A study by Raichle et al. (1994) reports that there is a

decrease in the activation of the prefrontal cortex as familiarity with a motor activity

increases due to repeated exposure to the same task. In addition, motor cortex activity

increases during tasks that require more attention, such as dual motor tasks (Johansen-

Berg and Matthews 2002). In a previous transcranial magnetic stimulation (TMS)

study (Pascual-Leone, Grafman, and Hallett 1994), the peak amplitudes of motor

evoked potentials (MEP) progressively increase as reaction time (RT) decreases. The

authors explained the mechanisms of this finding by stating that decreased inhibitory

control from higher-order brain areas over the motor cortex cause increased MEP. In

an existing EEG study, a progressive decline in RT during sequential learning is cou-

pled with a decrease in the 10-Hz event-related desynchronization (ERD) amplitude

in the sensorimotor area of the brain (Zhuang et al. 1997). In other words, as motor

tasks became more familiar, there is a decrease in the brain involvement associated

with the tasks.

- 4 -

Based on evidence from the studies above, we speculate that differences between

concentric and eccentric contractions can be explained by the level of attention re-

quired for subjects to perform the tasks and the level of familiarity with the tasks, ra-

ther than any fundamental differences in the biomechanical characteristics of each

type of contraction. Therefore, the purpose of our study is to compare the EEG pat-

terns and RT of muscle activation between concentric and eccentric biceps brachii

(BB) contractions under the RT paradigm. We also compare how changes in the EEG

patterns and RT are different between the types of contractions after the same amount

of training among subjects. This study hypothesizes that different EEG patterns will

result from concentric and eccentric contractions due to different levels of attention

involved in each type of contraction, and that, if the level of attention required by sub-

jects to perform the contractions becomes similar due to repeated practice, then the

two types of contractions will demonstrate similar EEG patterns.

- 5 -

Methods

1. Subjects

For this study, we recruited 16 volunteers (male = 12, female = 4; mean age ±

standard deviation = 22.43 ± 2.149). The minimum sample size was determined based

on power analyses using G-power software version 3.1.2 (Franz Faul, University of

Kiel, Kiel, Germany) with 3 subjects (calculated by partial η² of 0.689). The neces-

sary sample size for this study was calculated as 7 subjects.

The power was 0.95, effect size was 1.48, and α-level was 0.05. Inclusion criteria

were age (between 20 and 29 years), and dominant use of the right hand. That is, to

prevent the possible interference of age and dominance of the brain on EEG cortical

signals (Klimesch 1999), only right-handed young adults were included in this exper-

iment. Furthermore, anyone suffering from pain or with any history of psychiatric,

neurological, and/or musculoskeletal disorders was excluded from this experiment.

This study was approved by the Yonsei University Wonju Institutional Review Board.

Prior to conducting this study, the researchers explained the entire procedure to par-

ticipants, and collected written informed consent from the participants.

- 6 -

2. Instrumentation

2.1 Electromyography

Surface EMG data was collected using wireless Tele-Myo EMG instrument (Nor-

axon, Inc., Scottsdale, AZ, U.S.A.).

2.2 Electroencephalography

A 32-channel EEG instrument (10-10 system; American Electroencephalographic

Society, 1991) was used for collecting data, and data was recorded by an EEG record-

ing system (Brain Products GmbH, Munich, Germany). Thirty-two sintered active

Ag/AgCl electrodes (EASYCAP, FMS, Munich, Germany) were used.

2.3 Isokinetic Device

The Biodex System Isokinetic Dynamometer (Biodex Medical, Shirley, NY, USA)

was used to provide an objective and controlled environment for each type of isomet-

ric, concentric, and eccentric contraction.

- 7 -

3. Experimental Procedure

The experimental procedure is illustrated in Figure 1. The entire experiment con-

sisted of three phases. Each phase included 30 trials of concentric contractions and 30

trials of eccentric contractions, together with three maximum isometric contractions.

The order of muscle contractions was randomized within each phase using drawing

lots (eccentric → concentric or concentric → eccentric). Phase II was exclusively for

practice, and phase II data was not analyzed. Only data from phases I and III were

used for comparing concentric and eccentric contractions among participants. After

finishing the muscle contractions, three maximum isometric contractions were per-

formed at the end of each phase to determine whether fatigue was developed by the

repetitive muscle contractions. Ten-minute rests were given between phases.

The procedure began with subjects sitting on the Biodex dynamometer chair, after

which a researcher put an EEG electrode cap tightly on the head of each subject. Af-

ter pulling down the EEG cap, researchers prepared the scalp of each subject by in-

jecting gel (Electro-Gel™, Electro-Cap International, Eaton, OH, USA) on the scalp,

and connected each prepared scalp area with electrodes. Then, a researcher checked

an impedance map to set the impedance of all electrodes below 10 ㏀. The imped-

ance map represents the level of impedance by color. A red signal represents high

impedance (over 10 ㏀), indicating the need for researchers to inject more gel or as-

sert more pressure on the electrodes. After all of the color on this study’s impedance

map turned from red to green (representing levels of impedance under 10 ㏀), the

- 8 -

subjects sat quietly on the Biodex chair for 5 minutes to identify any other noises that

could potentially interrupt the EEG data. After completing EEG electrode attachment,

EMG electrodes were attached on the left cervical erector spinae (CES), the left upper

trapezius (UT), and the left BB of the subjects. Before placing the EMG electrodes,

researchers shaved the hair of the subjects and cleaned the skin of their scalps using

isopropyl alcohol to reduce the impedance of the skin. The inter-electrode distance

was 2 ㎝. The electrodes for the left CES were placed to the left of the center of the

cervical paraspinal muscle near C4. The electrodes for the left UT were located on the

left ridge of the shoulder, between the acromion and C7. The electrodes for the left

BB were placed on the medial part of the upper arms of subjects. In order to palpate

the muscle mass of the BB, subjects performed elbow supination and flexed their up-

per arms against the external load (Criswell 2010). Preparation procedures took ap-

proximately 30 to 40 minutes in all.

Before performing the elbow motions, subjects were positioned in the shape of an

X, and fastened in position with two seat belts to minimize unnecessary movement

during the procedure. Starting at the shoulder of the testing arm (i.e., the left shoul-

der), the shoulder was abducted and flexed 30° from the body, the elbow was flexed

45°, a neutral position of the wrist was maintained and supinated 90°, and then a fin-

ger grasped the handle of a lever-arm attachment on the isokinetic device according to

instruction from the Biodex manual (Biodex Application Manual, Shirley, NY) (Fig-

ure 2). At the beginning of data collection, EMG and torque values were obtained

while the subjects performed maximal voluntary isometric contractions three times in

- 9 -

60° elbow flexion. The target levels of submaximal concentric/eccentric contractions

were set at 50% of the averaged maximum isometric contraction value of the three

maximal isometric contractions. For concentric motions, the subjects moved their arm

toward the body from 30° to 90°. For eccentric motions, the subjects moved their arm

away from the body from 90° to 30°. The angular velocity of full ROM was set at

30°/second for both types of contraction (Fang et al. 2001; 2004). After 30 trials of

concentric and eccentric contractions (i.e., a total of 60 trials) per phase, the subjects

performed maximum isometric contractions three times to determine whether fatigue

was caused by the repetitive muscle contractions during each phase.

Subjects were asked to begin the elbow motions as soon as possible upon the

presentation of visual cues on the 17-inch LCD monitor (presentation version 16.3,

Neurobehavioral Systems Inc., Albany, CA, USA). A Ready signal (presented as a

cross mark) was followed by a Go signal (presented as a yellow circle) (Figure 3).

The EMG system, isokinetic dynamometer, and EEG devices were synchronized ac-

cording to the time of the Go signal. The average duration of presentation of the

Ready signal was 13 seconds, and was randomized (10 - 15 seconds). The duration of

presentation of the Go circle signal was two seconds. Movement was executed within

2 seconds, because subjects moved their arms for 2 seconds (60° of elbow flexion in

30°/second).

- 10 -

Figure 1. Experimental procedure.

- 11 -

Figure 2. Participant on the isokinetic device.

- 12 -

Figure 3. Presentation of the visual cues on the computer monitor:

“+” represents “ready” and “●” represents “go”.

- 13 -

4. Data Analysis

4.1 Electromyography Data

All the EMG and isokinetic data were processed and analyzed using MyoResearch

1.08 software. EMG signals were processed by band-pass filters from 10 Hz to 450

Hz, notch filters at 60 Hz, and a digitized 1000 Hz sampling rate. Root-mean square

(RMS) values were calculated with a moving window of 50 ms. Only BB EMG onset

and median frequency were analyzed in this study, because the EMG signals from the

CES and UT were biofeedback, which we utilized in order to prevent compensatory

movement and EEG interference. For analyzing EMG onset, 5 seconds of EMG activ-

ity were averaged and calculated as the EMG baseline in a position of rest. As calcu-

lated, the EMG onset determined that EMG amplitude increased over two standard

deviations in comparison to the baseline level for a minimum of 50 ms (Hodges and

Bui 1996). The median frequency of the left BB was analyzed by the fast Fourier

transform method.

Reaction time (RT) was defined as the duration of time between the Go signal (yel-

low circle) and the onset of BB EMG. The average RT of 30 trials for each type of

muscle contraction was used for interpretation of the data.

- 14 -

4.2 Electroencephalography Data

The MATLAB R2008a (MathWorks Inc. Natick, Massachusetts, USA) was used to

analyze recorded EEG data. Among the 32 electrodes, the C3 (left hemisphere) and

C4 (right hemisphere) were selected and analyzed. These areas represent the sen-

sorimotor cortex, and it is known that mu rhythms (8 - 13 Hz) are measured in these

areas of the brain (Marshall, Young, and Meltzoff 2011; Muthukumaraswamy, John-

son, and McNair 2004). Channels with noise contamination were excluded, and the

remaining channels in good condition were averaged and used as a reference.

The reference electrode was set by linked mastoid electrodes, with the ground

electrode placed between Fpz and Fz. The EEG signal was filtered by a band-pass

filter (0.03 - 100 Hz) and a notch filter at 60 Hz. Subsequently, the ocular and muscu-

lar artifacts were removed using independent component analysis (ICA). After re-

moving the artifacts, we performed further single-trial waveform analysis to prevent

high frequency signals such as muscular artifacts, which can contaminate EEG data.

To process the spectral analysis of EEG, each single-trial event-related potential

was applied using a continuous wavelet transform (CWT) of a complex Morlet wave-

let (Tallon-Baudry et al. 1996). The frequency ranged from 1 to 20 Hz. The CWT was

calculated according to the following equation (Figure 4).

- 15 -

Detections were made in the 8 - 13 Hz frequency range of mu rhythms (Braadbaart,

Williams, and Waiter 2013).

EMG onset was marked as 0 in a time frequency graph. The EEG data was seg-

mented into five-second intervals, before and after EMG onset. EEG data within a 10-

second window was analyzed in our research. The average value of a mu rhythm be-

tween -4 and -2 seconds before the EMG onset was determined as the baseline level

(Pfurtscheller and Aranibar 1977).

In mu rhythms, suppression occurs when the neurons in the somatosensory area re-

ceive inhibitory inputs from other areas of the brain, particularly during preparation

for motor acts. This phenomenon is called ERD (Braadbaart, Williams, and Waiter

2013). The variables of ERD onset and ERD amplitude of mu rhythms were used for

data analysis. The values of these variables are described in Figure 5. The onset of

ERD was defined as the moment in which the averaged curve of 8 - 13 Hz signal

crossed the baseline level (Van Winsun, Sergeant, and Geuze 1984). The amplitude of

ERD was defined as the average value of the ratio of spectral change from 1000 ms to

2000 ms, based on the baseline. This is represented in the following equation.

A: averaged alpha power decrease (1000~2000 ms)

B: mean alpha power at baseline

- 16 -

Time[ms]

Fre

quency[H

z]

-5000 0 5000

2

4

6

8

10

12

14

16

18

20

-0.5

0

0.5

Figure 4. Time frequency map in C4.

Figure 5. Detection of the baseline, onset time, and amplitude of ERD.

- 17 -

5. Statistical Analysis

PASW Statistics version 18 (SPSS, Inc., Chicago, IL, USA) was used for statistical

analyses of the data herein. The median frequency and peak torque values of the be-

fore phase (I) and after phase (III) were compared using paired t-tests to determine

whether fatigue was developed among the participants by repeated submaximal mus-

cle contractions. The RT was analyzed using two-way repeated analysis of variance

(ANOVA; phases x contraction types). Three-way repeated ANOVA (contraction

types x phases x hemisphere) was used to analyze ERD onset and ERD amplitude

(contraction type: concentric contractions and eccentric contractions, phase: phase I

and phase III, and hemisphere: C3 and C4). The Greenhouse-Geisser epsilon correc-

tion of degree of freedom was applied due to repetition of the measure. When interac-

tion effects were observed, the Bonferroni comparison was used as a post hoc test.

Statistical significance was set at 0.05.

- 18 -

Results

1. Fatigue Effects

To evaluate whether or not any fatigue of the BB developed among the partici-

pants, we compared the values of EMG median frequency and peak torque before

and after completion of the experimental procedures. Neither the EMG median fre-

quency nor peak torque values after completion of phase III were significantly

changed from the initial values (p > 0.05) (Table 1).

Table 1. Median frequency and peak torque. (N=16)

Phase I Phase III t p

Median Frequency 52.66 ± 16.41a 53.66 ± 17.98 -1.116 0.282

Peak Torque 43.63 ± 15.31 43.73 ± 15.63 -0.055 0.957

a Mean ± standard deviation

- 19 -

2. Chronological Events of the Trigger, EMG and ERD Onset

ERD onset was first activated at 100 - 200 ms before EMG onset. Torque was acti-

vated secondly, and movement was represented at 500 ms after EMG onset (Figure 6).

- 20 -

Figure 6. Examples of joint angles, EMG (biceps brachii), force, and ERD (C4) for concentric contractions (left) and eccentric contractions (right). Long dotted vertical lines indicate the timing of triggers. ERD: Event related desynchronization.

- 21 -

3. RT of EMG

RT data were analyzed using a two-way repeated ANOVA (phase ｘ contraction

type) (Table 2). Interaction effects were observed (p < 0.05). The results of the post

hoc test revealed that, in phase I, the RT was significantly longer in eccentric contrac-

tions than in concentric conditions (p < 0.05). In contrast, there was no significant

difference in RT between the two contraction types in phase III (p > 0.05). In the con-

centric condition, the RT in phase I was not significantly longer than the RT in the

concentric condition of phase III (p > 0.05). However, the RT of the eccentric con-

traction condition decreased significantly from phase I to phase III (p < 0.05) (Figure

7). Thus there was a significant main effect of phases (phase I > phase III), as well as

a main effect of type of contraction (eccentric > concentric) (p < 0.05).

- 22 -

Table 2. The results of two-way ANOVA for the reaction time of EMG (N=16)

Effect F p

Contraction type 27.345 0.001*

Phase 28.847 0.000**

Type ｘ Phase 6.654 0.030*

* p < 0.05

** p < 0.001

Figure 7. Two-way interaction plot for the RT (Contraction typeｘ Phase).

- 23 -

4. ERD Onset Time of Mu Rhythms

A three-way ANOVA for repeated measures (contraction type ｘ phase ｘ hem-

isphere) was performed with the data about ERD onset of mu rhythms (Tables 3 and

4). There were interaction effects between contraction types, phases, and hemispheres

(p < 0.05) (Figure 8). In the post hoc test, the ERD onset times were significantly

faster for eccentric contractions than the ERD onset times of concentric contractions

in both phases I and III (p < 0.05). While the ERD onset was faster in phase III than

phase I for both types of contractions, the difference was found to be statistically sig-

nificant only in the concentric contraction condition (p < 0.05). ERD onset times in

both C3 and C4 were significantly faster for eccentric contractions in comparison to

concentric contractions (p < 0.05). ERD onset in the performance of both concentric

and eccentric contractions occurred significantly earlier in C4 than C3 (p < 0.05).

- 24 -

Table 3. The results of three-way ANOVA for the ERD onset (N=16)

Effect F p

Contraction type 18.636 0.001*

Phase 3.652 0.074

Hemisphere 7.805 0.013*

Contraction typeｘ Phase 0.799 0.385

Contraction typeｘHemisphere 0.100 0.755

Hemisphereｘ Phase 0.102 0.754

Contraction typeｘHemisphereｘ Phase 4.817 0.043* * p < 0.05

Table 4. ERD onset time

Type Period Hemisphere Value (ms)

Concentric contraction

Phase I C3 -126.8 ± 143.03 a

C4 -141.2 ± 97.36

Phase III C3 -71.93 ± 60.84

C4 -97.86 ± 94.71

Eccentric contraction

Phase I C3 -154.93 ± 171.88

C4 -233.86 ± 142.33

Phase III C3 -135.00 ± 101.85

C4 -173.33 ± 107.93 a Mean ± standard deviation

- 25 -

Figure 8. ERD onset time plot A: Interaction between Contraction type and Phase B: Interaction between Contraction type and Hemisphere C: Interaction between Phase and Hemisphere

*p < 0.05 ERD: Event related desynchronization.

- 26 -

5. ERD Amplitude of Mu Rhythms

The ERD amplitudes of mu rhythms on EEG were analyzed by three-way repeated

ANOVA with factors of contraction type (concentric contractions and eccentric con-

tractions), phase (phase I and phase III), and hemisphere (C3 and C4) (Table 5). ERD

amplitude was significantly greater in phase III than phase I across both types of con-

tractions (Table 6). However, no interaction effects were observed between the three

factors (p > 0.05) (Figure 9).

- 27 -

Table 5. The results of three-way ANOVA for the ERD amplitude (N=16)

Effect F p

Contraction type 0.958 0.343

Phase 6.170 0.025*

Hemisphere 0.651 0.432

Contraction typeｘPhase 0.013 0.911

Contraction typeｘHemisphere 0.038 0.848

HemisphereｘPhase 0.001 0.980

Contraction typeｘHemisphereｘPhase 1.016 0.329 * p < 0.05

Table 6. ERD amplitude

Type Period Hemisphere Value (%)

Concentric contraction

Phase I C3 25.22 ± 15.50 a

C4 21.29 ± 18.74

Phase III C3 17.84 ± 19.65

C4 16.84 ± 14.92

Eccentric contraction

Phase I C3 21.88 ± 18.83

C4 21.65 ± 14.52

Phase III C3 16.96 ±16.85

C4 13.60 ± 17.58 a Mean ± standard deviation

- 28 -

Figure 9. Time frequency map of Contraction type (concentric and eccentric),

Phase (phase I and phase III), and Hemisphere (C3 and C4).

- 29 -

6. Topography of Averaged ERD Activity of Mu Rhythms

Each topography image in Figure 10 represents the ERD activity of mu rhythms in

the 1000 to 2000 ms window, prior to the onset of EMG. The data includes averaged

values of the 30 trials in each experimental condition. In phase I, substantial ERD was

observed bilaterally during both types of muscle contractions. In phase III, however,

bilateral ERD activity was observed only during eccentric contractions. ERD mu

rhythms tended to be localized in the C4 region (contralateral) during concentric con-

tractions.

Figure 10. Topography of averaged mu rhythm ERD in 1000 ~ 2000 ms prior to the

EMG onset

- 30 -

Discussion

This study designs an experiment to examine the changes in cortical activation pat-

terns as physical therapy subjects undergo familiarization with motor tasks by repeat-

ing concentric and eccentric elbow flexor contractions. The purposes of this thesis are,

first, to compare the EEG patterns and reaction times of EMG between concentric and

eccentric BB contractions under the RT paradigm, and second, to evaluate how the

EEG patterns and RT of EMG change after the same amount of practice. This result

partially supported the research hypothesis.

The four major findings of this study are as follows. (1) The mean RT of EMG in

phase I of eccentric contractions was significantly longer than the mean RT of EMG

in phase I of concentric contractions, and the RTs of both contraction types decreased

with practice. The mean RTs of EMG in phase III were not statistically different be-

tween contraction types. (2) The time of ERD onset relative to EMG onset, which is

related to the mental preparation of subjects to begin muscle movement, occurred sig-

nificantly earlier during eccentric contractions in both phases I and III. ERD onset

time was much more rapid in phase III than in phase I for both types of contractions.

In phase III, however, the difference in ERD onset time between contraction types

was maintained. (3) The ERD amplitude was significantly smaller in phase III than in

phase I during both types of contractions. However, no statistical difference was

found between contraction types and hemispheres. (4) The topography reveals that

the mu rhythms in the sensorimotor cortex were bilaterally deactivated during phase I,

- 31 -

regardless of the contraction type. In phase III, however, mu rhythm ERD was local-

ized in the contralateral sensorimotor area during concentric contractions. The ERD

patterns during phase III of the eccentric contractions remained bilateral.

- 32 -

1. Exclusion of Possible Influences of Fatigue Induced by Repetitive

Contractions

This experiment consisted of a total of 90 submaximal elbow flexor contractions

per each type of muscle contraction. A study by Gandevia (1998) states that muscle

fatigue is closely correlated with decreasing cortical activation in the motor cortex.

Therefore, we decided to set the intensity of muscle work as 50% maximal contrac-

tions. However, prior to comparing the obtained EMG, EEG, and torque data from the

three phases of the experiment, a procedure was required to clarify whether this data

was influenced by fatigue induced by 90 repetitions of 50% maximal contractions for

each contraction type.

Accordingly, we placed maximal voluntary isometric contraction (MVIC) periods

prior to phase I and immediately following the completion of phase III. Peak torque

and EMG median frequency values were compared before phase I and after phase III

using t-tests. Because no significant decrease was noted, we concluded that no mean-

ingful fatigue was induced among subjects by the number of repetitions (Gerdle et al.

2000; Kaiser, Birbaumer, and Lutzenberger 2001; Merletti, Lo Conte, and Orizio

1991).

- 33 -

2. RT of EMG

The degree of familiarity with and complexity of a motor task can be indirectly de-

termined by scrutinizing RT. RT represents the amount of information to be pro-

cessed by the CNS for a given motor action. If a subject is sufficiently familiar with a

movement due to practice or learning, then the RT decreases. On the other hand, RT

increases as the complexity and unfamiliarity of a motor task increases for the subject

(Shumway-Cook and Woollacott 1995).

In phase I, the RT of the eccentric contractions was longer than the RT of concen-

tric contractions. The longer RT implies that the performance of eccentric contrac-

tions is less familiar, and thereby, requires more attention from subjects than the per-

formance of concentric contractions. Furthermore, consistent with findings by Shum-

way-Cook and Woollacott (1995), this study finds that RT in phase III decreased as

the amount of practice increased in both types of muscle contractions. This finding is

suggestive of the effects of familiarization with or learning a motor task. However,

the magnitude of the RT decrease was greater in the performance of eccentric con-

tractions, which implies that more learning occurred in the eccentric condition during

the experimental procedure herein. The relatively small decrease in RT for concentric

contractions over the same number of repetitions suggests that the performance of

concentric movement was already more atomized and programed at the start.

- 34 -

3. ERD Onset of Mu Rhythm

According to prior EEG research regarding the time course of self-paced move-

ment-related EEG, the ERD of mu rhythms in the contralateral sensorimotor cortex

start approximately 1 - 2 s before the onset of the movement (Bigland and Lippold

1954; Defebvre et al. 1996; Leocani et al. 2001; Pfurtscheller and Berghold 1989). In

this study, the averaged ERD onset of mu rhythms was observed in the contralateral

sensorimotor area. The ERD started 150 - 200 ms prior to EMG onset during eccen-

tric contractions, and 70 - 120 ms prior to EMG onset during concentric contractions.

That is, the observed ERD onset was much faster in this study than it has been ob-

served in other studies. This finding can be partially explained by the differences in

the experimental paradigm. Because our experiment utilizes the RT paradigm, the

subjects were instructed to generate elbow movement as fast as they were able to,

following a Go signal. In addition, we determined the initiation of movement accord-

ing to EMG onset rather than the onset of movement itself.

In previous studies, ERD occurs earlier as the amount of information to be pro-

cessed increases, and ERD is closely related to motor preparation and completion of

cognitive processes (Pfurtscheller 1981; Pfurtscheller and Aranibar 1977; Pfurtschel-

ler and Aranibar 1979). The earlier onset of ERD suggests that the cortical activation

for planning begins earlier for eccentric movement than for concentric movement.

Therefore, it can be argued that eccentric contractions are a more complex motor task

than concentric contractions, and are possibly governed by a different controlling cen-

- 35 -

tral processing. Similarly, delays in ERD onset in phase III for both types of contrac-

tions may be the indirect consequence of decreased cortical demands secondary to

familiarity or learning by repetitive practice.

A study by Zhuang et al. (1997) reports that a short RT is correlated to delayed

ERD onset due to the time required to realize a movement and to process movement

information. In contrast to our expectation, the pattern of changes regarding ERD on-

set time did not follow a similar trend to the EMG RT. Even after repetitive practice

among participants, the onset of ERD for eccentric contractions occurred much soon-

er than the onset of ERD for concentric contractions. This result suggests that the ul-

timate difference between the two types of contractions does not disappear with the

practice of 90 repetitions.

- 36 -

4. ERD Amplitude of Mu Rhythm

ERD can be interpreted as an electrophysiological connection involved in the pro-

cessing of sensory or cognitive information for the production of motor behavior

(Pfurtscheller and Klimesch 1992). Thus it is commonly understood that increased

ERD amplitude in mu rhythms results from the increased cellular excitability in

thalamocortical feedback loops (Steriade and Llinás 1988). In our study, ERD ampli-

tude decreased after a great deal of repetitive practice by participants for both types of

contractions. This result corresponds to a previous study, which demonstrates that

progressive decline during motor learning processes occurs along with a decrease in

the mu band ERD amplitude (Zhuang et al. 1997). As with the results of ERD onset,

the amplitudes of both types of contractions changed significantly from phase I to

phase III.

In contrast to our hypothesis, the ERD amplitudes of concentric contractions tend

to be greater than the ERD amplitudes of eccentric contractions in all brain areas and

phases. This tendency is not consistent with our basic assumption that concentric con-

tractions are a more familiar type of movement to ordinary people than eccentric con-

tractions. Clear discussion regarding this issue is not possible given the large variabil-

ity in findings about ERD amplitude.

In our study, during eccentric and concentric contractions, the mu rhythms in the

ipsilateral sensorimotor area tended to be more desynchronized than the mu rhythms

in the contralateral area. Previously, it has been shown that ERD is dominant in the

- 37 -

contralateral brain area during the performance of ipsilateral hand movements

(Pfurtscheller 1977; Pfurtscheller 1981; Pfurtscheller 1989; Pfurtscheller and Arani-

bar 1977; Pfurtscheller and Aranibar 1979; Pfurtscheller and Berghold 1989). We

tested the non-dominant arm of subjects in this study. There are more recent studies

that are consistent with our findings, in which the authors state that the ipsilateral

brain area is more deactivated in non-dominant hand movements among subjects

(Dhamala et al. 2003; Kawashima et al. 1993; Sakai et al. 1999; Ziemann and Hallett

2001). Indeed, non-dominant hand movements would generate a greater processing

load on the ipsilateral left hemisphere, thereby resulting in greater activation. This is

possibly reflected in the greater ERD amplitude in this study (Bai et al. 2005; Dha-

mala et al. 2003). Furthermore, when the complexity of movement and processing

load on the contralateral hemisphere increases, it is theoretically conceivable that cor-

tical activation may “spill over” to the opposite ipsilateral hemisphere (Bai et al.

2005). Thus, because of significant activation of the ipsilateral area due to the unfa-

miliar conditions of isokinetic testing, the non-dominant arm movements may have

been assisted by the contralateral area of the brains of the subjects herein. In phase I,

ERD occurred bilaterally during both types of contractions. However, localization of

ERD in the contralateral hemisphere during concentric contractions in phase III oc-

curred, while bilateral ERD during eccentric contractions remained in phase III. This

finding suggests that greater familiarity was achieved for concentric contractions than

for eccentric contractions among participants in this study.

- 38 -

5. Limitations

There are limitations to an investigation of cortical control of muscle actions by

EEG. First, we should have applied the experiment to the dominant arm of subjects to

fulfill the basic assumption that performing concentric contractions is easier and more

familiar than performing eccentric contractions. Proficiency of movement with the

non-dominant limb might not be familiar even in terms of concentric contractions in

phase I. Furthermore, motor learning processes with the non-dominant arm may occur

more slowly than with the dominant arm. Consequently, the second limitation is that

subjects were unable to reach a status of having fully learned concentric and eccentric

contractions by way of 90 repetitions in a single day. In future studies, longer practice

periods are recommended to maximize motor learning among subjects.

- 39 -

Conclusions

The present study, involving EEG frequency analysis of concentric and eccentric

muscle contractions, confirms the results of previous investigations on the topic. Con-

centric contractions and eccentric contractions have different mechanisms of neural

control. In our study, even though the RTs of concentric contractions and eccentric

contractions are more similar in phase III than phase I, the ERD patterns (slower ERD

onset and lower ERD amplitude) remain different across phases in both types of con-

tractions. In observing these different patterns of ERD, we conclude that the brain

adapts to movement according to repetitions, and that the two types of contractions

have different ERD onset and amplitude tendencies regardless of whether or not simi-

lar levels of attention are required by subjects for the initiation of movement. This

seems to suggest that concentric contractions and eccentric contractions have differ-

ent mechanisms of neural control. Even though eccentric muscle control is a critical

part of our usual physical activity, clinicians often overlook the importance of eccen-

tric muscle training. Our results suggest that eccentric muscle training is a necessary

part of rehabilitation for athletes and neurologically impaired individuals due to in-

trinsic differences between eccentric and concentric control.

- 40 -

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국문 요약

구심성 운동과 원심성 운동하는 동안의 뮤리듬

시상관련 탈동기화 변화

연세대학교 대학원

물리치료학과

박 주 희

구심성 운동은 외부 힘과 반대되는 방향으로 일어나는 운동이며,

근육의 길이가 짧아지면서 일어나는 운동이다. 원심성 운동은 근육의

길이가 길어지면서 일어나는 운동으로 구심성 운동에 비해 우리에게 덜

익숙한 운동이다. 이 운동은 물건을 조절하면서 내려놓을 때 주로

나타난다. 이전 연구들은 이런 서로 다른 운동이 뇌에서 어떻게

조절되는지 확인하기 위해서 뇌파분석과 기능자기공명영상을 이용하여 두

운동을 비교하였다. 하지만, 우리는 이러한 이전 연구들의 결과가 원심성

운동이 구심성 운동보다 덜 익숙해서 나타난 것으로 가정하고, 팔굽관절의

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구심성 운동과 원심성 운동을 익숙화 시키는 과정을 실험에 포함시켜 두

운동의 뇌파를 비교하였다. 따라서, 연구의 목적은 익숙화 정도를

나타내는 구심성 운동과 원심성 운동의 반응시간을 측정하고, 구심성,

원심성 운동이 뇌파에서 어떻게 나타나는지, 익숙화 시키기 전의 구심성,

원심성 운동과 익숙화 시키고 난 후 두 운동의 뇌파가 어떻게 변화하는지

알아보려고 한다.

연구 대상자들은 16명의 오른손 잡이를 대상으로 수행하였다. 연구

설계는 준 최대의 팔굽관절 구심성, 원심성 운동과 최대 등척성 운동을

1~30번 (익숙화 시키기 전), 31~60번 (익숙화 단계), 61~90번 씩

(익숙화 시킨 후) 3단계에서 수행하도록 하였다. 뇌파분석은 32채널을

사용하였으며, 뇌파, 힘, 움직임 각도, 그리고 위팔 두갈래근의 근활성도를

동기화 시켜서 나타내었다. 특히 뇌파분석은 주파수 대역 분석을

수행하였는데, 뮤 리듬 대역에서 수행하였으며, 감각운동영역의 시상관련

탈동기화 (event-related desynchronization) 를 분석하였다. 반응시간은

이원 분산분석을 이용하였으며, 시상관련 탈동기화 개시 시간과 크기는

삼원 분산분석을 이용하여 분석하였다.

결과는 다음과 같다. 근전도 반응시간은 두 운동 모두 1~30번보다

61~90번에서 유의하게 감소하였다. 또한 원심성 운동이 구심성 운동보다

긴 반응시간을 가졌다. 시상관련 탈동기화 개시 시간은 원심성 운동에서

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유의하게 빠르게 나타났으며, 시상관련 탈동기화 개시 시간과 크기는 두

운동에서 모두 첫번째 30번 보다 세번째 30번에서 더 유의하게 느리게

나타났다.

반응시간은 길수록, 시상관련 탈동기화 개시시간은 느릴수록

중추신경계에서 많은 준비기간이 필요하다는 것을 의미한다. 그러므로

원심성 운동은 뇌에서 많은 준비기간이 필요하다는 것을 의미하고, 익숙해

짐에 따라 준비기간이 짧아지는 것을 확인할 수 있었다. 하지만, 90번

운동을 하면 익숙해져 두 움직임의 뇌파가 비슷해 질것이라는 우리의

예상과는 달리, 익숙해 진 후 에도 구심성, 원심성 운동 모두 서로

시상관련 탈동기화에서의 개시시간, 발생되는 위치와 크기가 차이 났다.

원심성 운동이 움직임에서 중요한 역할을 함에도 불구하고,

물리치료사들은 원심성 운동을 하는 것을 간과하는 경향이 있다. 하지만,

원심성 운동은 구심성 운동과는 다른 신경학적 전략을 가지고, 뇌에서 더

많은 준비기간이 필요함으로, 재활 과정에서 구심성 운동보다 더 많이

연습되어야 한다.

핵심 되는 말: 구심성 운동, 뇌파분석, 원심성 운동, 익숙화.