Shinshu University Institutional Repository SOAR-IR Title Changes in frequency properties of electroencephalograph and electromyography in motor learning process Author(s) 木村, 貞治; 藤原, 孝之; 西村, 尚志; 大平, 雅美; GOH, Ah Cheng; 神子嶋, 誠; 三好, 圭; 楊箸, 隆哉; 杉田, 勇; 許, 明峻 Citation Issue Date URL Rights 紀要 23: 25-36(1998) 1998-02-28 http://hdl.handle.net/10091/5220 25 信大・医短・紀要 Vo123, 1997 Changes in frequency properties of electroencephalograph and electromyography in motor learning process 木村貞治1),藤原孝之1),西村尚志1),大平雅美1), GOHAhChengl) 神子嶋誠1),三好 圭1),楊箸隆哉2),杉田 勇3),許 明唆4) Changes infrequency properties of electroencephalograph and eleetromyography in motor learmimg process The purpose of this study was to investigate the modifications of motor performance and changes in electrophysiological properties such as electroencephalogram (EEC) and electr0- myography (EMG). The subjects consisted of six healthy males aged 18 to 24 years (mean - 21.8 years). The task of motor learning was maximum reciprocal tapping of theNandVfinger in the non-dominant hand. Practices were executed 5 days per week for 4 weeks. Parame- ters of analysis were rate of tapping, median power frequency properties in EEC and EMG during 10 seconds. The results showed significant increases in the mean rate of tapping and median power frequencies in EEC. Correlation between rate of tapping and median power frequency of EEC on the motor cortex showed a gradual increase with each week. There was no significant cor- relation between rate of tapping and median power frequency properties of EMG. It is suggested that an increase of neural activities in the cortex may correlate with the evolution of motor learnlng. Key Words : Motorlearning (運動学習), EEC (脳波), EMG (筋電図) 1 )信州大学医療技術短期大学部理学療法学科; KIMURA Teiji. FUJIWARA Takayuki. NISHIMURA Naoshi, OHIRA Masayoshi, GOH Ah Cheng. KAMIKOJIMA Makoto. MIYOSHI Kei. Dept. of PhysicalTherapy. School of Allied Medical Sciences, Shinshu Univ. 2 )信州大学医療技術短期大学部看護学科; YANAGIHASHI Ryuya, DepL of Nursing. School of Allied Medical Sciences, Shinshu Univ. 3 )諏訪中央病院; SUGITA Isamu, DepL of Rehabilitation, Suwa Central Hospital 4 )順天郷大学校工科大学; FUR Myung Joon. Dept. of Electricalengineering, College of Electrical engineering. University of Sooncllunhyamg 26 learnlng in physical therapy. 1. lntroduction With regards to electrophysiological stud- ln physical therapy, some therapeutic in- ies related to motor control or motor learn- puts such as verbal orders, demonstrations. ing. Murthy and Fets8) indicated that the manual assistance and mechanical assistance band ratio of the β wave of electroencephalo一 are applied to the patients in order to im- gram was observed during tasks requlrlng prove the performance of motor control. fine finger movements and focused attention The series of processes concerned with in monkey motor cortical cells. Karni etal.9) relative permanent changes of motor per- reported that expansion of activated regions formance caused by these repetitive thera- in primary motor cortex during motor skill peutic Inputs is defined as motor learn- learning observed by functional magnetic ingl)2). resonance image (f-MRI) may be caused by The conceptual models of motor learning theory, such as closed loop theory3), schema the organization of synapse network related to the evolution of motor skill learnlng. theory4), impulse variability theory5)and Concerning the changes of cortical activity knowledge of results (KR) 6)7) have been when executing learned motor sequences. previously discussed. Lang et al.10) reported that in a learned se- Experimental approaches based on the quence of four movements (flex index finger, above motor learning theories have been de- extend hand. extend index finger,flex veloped from the fields of psychology, physi- hand) , large negative DC potentials were cal education, neuroscience, bio-information recorded in positions located above the me- engineering and othersl). sial fronto-central cortex (Cz) and sensori- In previous experimental studies, analyses motor hand areas of either hemisphere (C of motor learning have been executed based 3 andC 4 ) in the beginningofeachperiod. on the change of performance criteria such Furthermore, DC potentials were absent in as speed, accuracy ln movement, aS Well as Cz and the end of the period of execution. analyses based on the changes of electro- On the other hand, an electromyographical physiological properties such as EEC and study conducted by Sadoyama et al. ll) ex- EMG6). amined the modification of auricle muscles In physical therapy, both analyses of per- using EMG to evaluate the effect of motor formance and electrophysiologiCalproperties learnlng quantitatively. Since the results in- are important in order to prove the scientific dicated that the acquisition process of auricle evidence related to acquisition of motor skill movement was effectively shown, as demon- by therapeutic exercise. strated by the gradual increase in mean am- However there are only a few studies plitude of the EMGs of auricle muscles, they which attempt to explain the neuromuscular suggested that EMG signal processing changes which accompany skilled motor method has wider application in the field of Changes in frequency properties of electroencephalograph and electromyographyinmotor leaming process 27 neuromuscular rehabilitation and sports. 24 years (mean 21.8 years) who had no pre- Vallbo et al.12) investigated the human vious experiences about continuous skill mo- muscle spindle response in a motor learning tor learnlng Such as playlng the plan°. In- task by using microneurographic technique, formed consent to the experiment was taken and they concluded that focusing attention from all subjects. Subjects were all right on the kinaesthetic input during imposed handed. movement was not associated with a consis- 3. Methods tent increase of fusimotor drive. Although the above previous studies re- 1 ) Task of Motor Learning ported on the elecrophysiological evidences The maximal reclprOCal finger tapplng Of based on the analysis of EEC or EMG in mo- Ⅳ and V finger in the non-dominant hand tor control or motor learnlng process, with maximum veloclty Was Selected as a changes in the frequency properties of EEC motor learnlng task. The subjects were in- or EMG in motor learning processes have structed to execute maximum reclprOCal fin- not been discussed. Furthermore, correlation ger tapplng in N and V finger in the non- between evolution of motor performance and dominant hand, placing their left palms on changes in electrophysiologlCal properties the desk and observing their own move- have not been discussed. ments. Fets et al 13). reported that a cortical motor The task was selected because it is not neuron projects alpha motoneuron and it used in daily activity, and improvements of regulates the generation of muscle force. motor skill by practice can be expected. Consequently, lt appears that changes of 2 ) procedure frequency propel・tiesinEEG or EMG may During practice, subjects were seated on a reflect modification in cortical neuron activ- chair, with their back supported, and only ity and myoelectrical activity by motor their left hand was placed on the desk. learnlng. These quantitative analyses of mo- The task consisted of a block of50 trials tor learning may be necessary in order to per day, and one trial includes reclprOCal fin- clarify the effects of therapeutic exercises in ger tapping of leftⅣandVfinger for 10 sec- physicaltherapy. onds with maximal velocity and a rest period The purpose of this study was to investi- of 10 seconds. The practice was executed for gate the effect of motor learning based on 5 days (from Monday to Friday) per week the modification of motor performance and for 4 weeks. changes in frequency properties in EEC and EMG. The whole sequence of practice for a subject Was aS follows : 2. Subjects 1 block/day x5 daysx4 weeks- 1.000 trials. Subjects were six healthy males aged 18 to The practice of motor learning was limited 28 to only the practice time in a day to prevent and touch sensors were adjusted to position the bias induced by over training performed the ⅣandV丘nger pulpwithin the box. The by the subjects during their private time. touch sensor signals were amplified by a DC 3 ) Measurement The contents of measurement consisted of the rate of reciprocal tapping in Ⅳ and V fin- amplifier (Unipulse, Digital Indicator F 430), and were stored to a data recorder (Shinko, RCD-728). ger. electroencephalogram. and electr0- Recordings of EEC signals during tapping myographyinleft finger extensor and nexor were made by an EEC machine (NEC Sanei, during lOseconds. The trigger sound to MK - 930705) with 8 silver-silver chloride start and stop the tapping was generated by cup electrodes. The electrodes were placed a phono-stimulator (Sanei, 3 G 22) with lO- overthe scalp atFz', Cl',Cz,C2', RHM,P second intervals. Measurements were car- l', Pz', P2'based on the movement related ried out once per week. The data were cor- cortical potentials (MRCP) using a conduc- rected from 5 th to 7 th trials during a block tive electrode gel (Fig. 1). The electr0-ocu- in a day per week. logram (BOG) was recorded from an elec- Measurements were executed in a shielded room to prevent noise. trode placed 1.5cm below the right outer canthus in order to check the blinking. The The contact pressure of tapping by Ⅳ and subjects were required to keep their eyes V fingers was measured by using touch sen- opened during each trial in order to prevent sor equipment (ME, specially made) on the artifacts caused by blinking. desk. The touch sensor equipment was made by an aluminum box and two touch sensors, Two common reference electrodes were placed on the earlobe. EMG signals of left Extensor Digitorum Communis and Flexor Digitorum Sublimis during reciprocal finger tapping were de- tected by a telemetric EMG machine (NEC Sam-Ei. Multitelemeter 511) with surface electrodes. Before placing the silver-silver chloride disposal type electrode, the skin was first prepared with an abrasive alcohol prep- ping solution. and electrode impedance was always below 2 kEL A pair of electrodes were placed in the center of the muscle belly, parallel to the direction of muscle fibers. Detected EMG signals were stored on a Figt 1 Placementof Electrodes in EEG RHM was focused in this investigation. data recorder together with tapping signals and EEC signals. Changes in frequency properties of electroencephalograph and electromyography in motor learning process 29 by band-pass filter ranged from 0.5 Hz to 30 -EEG 占竿空-画亘] Hz. EMG signals were filtered by band-pass filter ranged from 10 Hz to 250 Hz14). Frequency properties of EEC signals and _.芳一--Ⅳ■V月qer.「耐DIR ■コD EMG signals were analyzed through Fast 欝≡ND (signalProcessor)CPU Fourier Transform (FFT) with Hanning window function, and median power freFig. 2 Block Diagram of Experiment quency (MdPF) was calculated using BIMU- 4 ) Data Analysis T A S-E. The analog data of tapping signals, EEC Data analyses of maximum tapplng, MdPF slgnals and EMG signals were converted to of EEC and EMG were performed using av- digital signals by an A/D converter with 1 eraglng Value of data in5th to7th trial of kHz sampling frequency from the data re- subjects in each week. Among the placement of scalp electrodes, corder. Signal processing was executed on a per- RHM was focused in this study since RHM sonal computer (NEC, PC-9821 Ⅹp) With a lies close to right primary motor cortex for software for processlng Of bi0-information finger movement15). signals (Kissei Comtec, BIMUTAS-E, ver. 5 ) Statistical Analysis 2.ll) (Fig.2,Fig.3). To test 4 weeks practice effects on maxi- Digital filters were used to reduce the mum tapping, MdPF of EEC and EMG, noise in each signals using BIMUTAS-E. The Friedman test was performed by using SPSS tapplng Slgnals were filtered by low pass fil- 6.1 for Windows (SPSS Inc. ) , because nor一 ter below 10 Hz. 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To test for difference among the4- Fig. 5 lndividual Difference in Rate ofTapplng weeks, Dunn test was used as a post hoc test. Although the mean rate of reciprocal tap- Statistical significance was accepted at less ping revealed an almost linear increase.indi- than 0.05 vidual differences were observed in the learning curve of individual subjects (Fig. 4. Results 5). 1 ) Modi丘cation of Motor Perfわrmance The mean number of times in reciprocal tapping of ⅣandV finger were increased in all subjects every week (Table 1, Fig. 4). Statistical significance was observed among weeks by Friedman test (p<0.01) 2 ) Changes in Median Power Frequency Properties in EEC Since subjects could keep their eyes open during data acquisition. prevention of arti- facts by blinking were confirmed by EOG. Mean value of MdPF on all electrodes in (Table 2). Dumm post hoc testing indicated EEC reveals a tendency to increase every significant difference between the 1 st week week (Table 1, Fig. 6). Friedman test showed and4thweek (p<0.01) significant increase of MdPF on all elec- Changes in kequency properties of electroencephalograph and clectromyography in motor learning process HZ6・04mo8 2O mean±SD 31 Hz 14.0 13.0 12.0 ll.0 10.0 9.0 1 W 2W 3W 4W 1 W 2W 3W 4W Fig.7 Changes of SpatlLal Distribution in EEG Fig.6 Changesof Mean MdPF in EPG on ALL on aH Electrode E lectrodes trodes in EEC (p<0.05) (Table2). Dunn H.0 Z mean±SD n"i nHi Ji JHi 6 4 2 ∩) 8 6 4 2 0 post hoe testing indicated significant differ- ence between the 1 st week and4th week (p< 0.05) In the change of MdPF among the place一 ment of electrodes, RHM revealed a steep increase of MdPF compared with other sites (Table 1, Fig.7). Friedman test showed signi丘cant increase 1 W 2W 3W 4W of MdPF on RHM (p<0.05) (Table2. Fig. Fig.8 Changes of Mean MdPF in EEG on 8). Dunn post hoe testing indicated signi丘- RHM cant difference between the 1 st week and 3 Table 2 ResultsofFriedman Test source of variation x r2 k N df P value 1) Rate of tapping between conditions 17.00 4 6 3 0.01 between subjects 16.00 6 4 5 0・001 2) MdPF in EEG (ATl) between conditjons 9.80 4 6 3 0[05 between subjects 1 1.29 6 4 5 0.05 between conditions 1 between subjects 1 3) MdPF in EEC (RHM) 1 L00 4 6 3 0.05 4.29 6 4 5 0.02 32 nificant increase every week. 0 0 ∩) 0 0 0 0 0 8 7 6 5 4 3 2 7 1 0 The motor task of present study was selected based on the comments that recipro- 「 cal tapping of Ⅳ and V丘nger in non-domi- nant hand is difficult to trainforflute players. However, the motor task in present 1 W 2W 3W 4W study does not have great benefit for the subjects. Also. knowledge of results were not Fig, 9 Changes of Coefficient of Corre一ation between Rate of Tapplng and MdPF of EEGin RHM rdweek (p<0.05). 3 ) Changes in Median Power Frequency Properties in EMG Friedman test indicated no significant informed to the subjects till completion of their practice period. Nevertheless, motor performance of the maximum reciprocaltapping of N and V finger in non-dominant hand were improved by practices during 4 weeks, as we expected. change of MdPF in EMG for both extensor This result indicates that new skilled mo- and flexor during4weeks (P>0.05) (Ta- tor task which has not been experienced pre- ble. 1). MdPF of EMGinfinger extensor viously has the possibility of modification in muscles were higher than flexor muscles at motor learnlng. the2nd, 3 rdand4thweeks. Change of dis- However, since we did not evaluate the charge pattern of both EMG was not ob- long term effect after completion of practice. served. it seemed that山rther study should be con- 4 ) Correlation between motor performance and electrophysiologlCal properties tinued. With regards to the phases of motor learn- Correlation coefficient between rate of tap- ing, Fitts16) classified cognitive phase, asso- ping and median power frequency proper- ciative phase and autonomous phase. Since ties on RHM in EEC were gradually in- content of task in the present study was sim- creased every week up to the 3 rd week ple reciprocal finger tapping, it seemed that the degree of participation of cognition may (Fig. 9). There were no slgnificant changes be- be small. But the discrimination between as- tween motor performance and EMG signals sociative phase and autonomous phase in or between extensor and flexor. present study may be difficult because we did not check the transfer trials. 5 l Discussion The eflects of knowledge of results (KR) ln the present study, it was demonstrated should also be investigated since it is consid- that motor performance in motor skill learn- ered that import, timing and frequency of ing was improved by daily practices, and KR may affect the motor performance7) 17) MdPF in EEC on all electrodes revealed sig- Although Busk and Galbraith18) pointed Changes in frequency properties of electroencephalograph and electromyography in motor learning process 33 out that skilled movements were not likely to seemed to be necessary to analyze the be reflected in the EEC, MdPF of EEC inall change of frequency properties in EEC dur- electrodes revealed significant increase, ac- ing motor learnlng Process. companied by the improvement of motor As a spatial property of frequency on all performance in present study. In particular, electrodes in EEC, EEC on RHM revealed RHM which lies over the prlmary motor cor- linear increases of median power frequency tex related to left finger movement revealed in motor learning process. This tendency on acute increase. Furthermore it was note- may suggest the increase of neuronal activi- worthy that the coefficient of correlation be- ties in the cortex included RHM. tween the rate of reclprOCal finger tapplng Tanji and Mushiake20) reported that pri一 and frequency properties of EEC on R班M mary motor cortex is mostly related to exe- were increased during motor learnlng prOC- cution of motor task, while neuronal actlVlty eSS. in the supplementary motor area exhibits a Gliner et al. 19) investigated changes in the variety of complex relationship to many dif- EEC power spectrum during repeated per- ferent aspects of motor task. Thach21) re- formances of the same task to determine ported that there are close relationship be- whether neurophysiologlCal correlates of at- tween neuronal actlVlty ln prlmary motor tention changed as a function of learnlng the cortex and motor parameters such as JOint task. His results indicated that mean alpha position, force, Velocity and acceleration of frequency increased slightly during the task movement generated by muscle contraction. while delta frequency decreased in electro- From these evidence, it is considered that encephalogram during perceptuaトmotor neuronal actlVlty ln prlmary motor cortex learning. He also reported that a decrease of may correlate with evolution of rate of reclp- duration in execution and decrease of error rocal finger tapplng aS a motor learning task in task were observed by motor learning. in present study, because simple reciprocal Since his report aimed to clarify the influ- finger tapplng Was used as a motor task in ence of attention in perceptual motor learn- this study. This speculation may be sup- ing based on the EEC, it is considered that di- ported by increase of coefficient of correla- rect comparison to the present study may be tion between rate of reciprocal finger tap- difiic ult. ping and median power frequency of EEC on Lang et al. 10) studied the changes of corti- R班M. cal activity when executing learned motor It is also suggested that correlation analy- sequence, and he concluded that the execu- sis between motor performance and cortical tion of a learned motor sequence task cannot activity seemed to be useful in quantitative be associated with a particular size and pat- evaluation of electrophysiological change in tern of cortical activity. Since they did not motor learnlng. analyze the frequency property in EEC, it In the present study, EMG of finger exten- 34 Sor revealed dominant activity ln late stage trot theories and motor learnlng theories. of motor learning process. However, there Furthermore he indicated that incorrect were no significant changes of MdPF in model of treatment can lead to inappropriate EMG on the finger muscles during motor expectations of the results. learnlng process. From these valuable information, it is con- Basmajian22) reported that properties of sidered that appropriate treatment program EMG activity in motor learning process is se- for motor learning in physical therapy should lective inhibition of unnecessary muscular be constructed by integration of both the sci- actlVlty rather than the activation of addi- entific investigation and clinical data in mo- tional motor units. He cited evidence that the tor learning. development of skill is accompanied by pro- The findings of the present study are lim- gressively more successful repression of un- ited in that the sample was small and only desired contractions and by a gradual in- short term effects were studied. Further- crease in the average duration and a de- more, since we did not analyze the ratio in crease in average frequency of potentials in frequency band in EEC, it is considered that the specific muscle under trainlng. analysis of the detailed frequency component Payton and Kelley23) investigated the of EEC in motor learnlng lS necessary. Fur- change of EMG activlty ln motor learnlng ther research is necessary to analyze motor process. They concluded that prlme muscles learning process in actual patients with mo- demonstrated significantly less totalelectri- tor disorders. cal activity during skilled movements than Acknowledgment during unskilled movements. From these evidence, dominant change of We would especially like to thank the col- frequency properties in extensor muscles lege students for their participation in this may suggest inhibition of the activity of study. We gratefully acknowledge the coop- nexor muscles. However. since integrated eration of the staff at Shinshu University, EMG was not calculated in present study, we School of Allied Medical Sciences. We also could not conclude the change of total electri- wish to express our thanks to Mr. Kazuo Ku- cal activity in EMG in motor learnlng prOC- doh, the staff of the ME corporation, for sup- eSS. porting this study. From above findings, it seemed that fur- REFERENCES ther electromyographical study in motor learning process should be continued. Crutchfield2) indicated that considerable portion of therapy is to teach the clients. It is also described that a large body of knowl- 1 ) Schmidt, R. A. : Motor learning and performance : from prlnClples to practice. Human Kinetics Books, Illinois, 1991. 2 ) Crutchfield. C.A.. Barnes, M. 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