Sequenced motor performance in patients with unilateral cerebral lesions

Neuropsychologla, 1971, VoL 9, pp. 445 to 449. Pergamon Press. Printed in England

SFQUENCED MOTOR PERFORMANCE IN PATIENTS WITH UNILATERAL CEREBRAL LESIONS AMIRAM

CARMON

Laboratory of Human Psychophysiology, Department of Neurology, Hebrew UniversityHadassah Medical School, and Hadassah University Hospital, Jerusalem, Israel (Received 18 June 1971) Abstract--Repetitive motor performance of groups of patients with right and with left hemispheric lesions and of control subjects was sequenced for locus and for pace in two separate experiments. The performance of the brain-damaged patients was inferior to that of the control subjects in the two tests. The side of the hemispheric lesions did not influence the performance of the patients when the locus was sequentially changed, but did affect it somewhat when the pace of tapping was constrained. When a fast pace of tapping was required, patients with lesions in the left hemisphere performed worse than patients with lesions in the right hemisphere. Under slow and moderate paces of tapping, a reverse trend occurred. The results give only partial support to the possibility that motor behaviour is differentially controlled by the two hemispheres, but are in general agreement with prior experiments. 1. I N T R O D U C T I O N AMONG the variety of perceptual a n d performance tasks used to investigate asymmetry of cerebral hemispheric functions, tests of m o t o r performance have n o t disclosed striking laterality differences. Simple m o t o r performances tests such as reaction time have n o t shown clear laterality effects [1]. WYKE [2] reported that repetitive alternation of h a n d m o v e m e n t with the ipsilateral h a n d was slow only in patients with left sided lesions. VAUGHAN and COSTA [3] found, however, no ipsilateral deficit either in patients with damage to the left or to the right hemispheres in a finger oscillation test. The two experiments differed as in the first one, the locus of performance was alternated, while in the second one, it was kept constant. The pace of performance was n o t constrained in the two experiments. The experiments reported here were designed in order to investigate the effects of a l t e r n a t i o n of locus a n d pace of repetitive rapid h a n d m o v e m e n t s on the level of m o t o r performance of patients with hemispheric lesions. 2. M E T H O D 2.1 Experiment I: Repetitive motor performance with alternation of hand position 2.1.1 Subjects. Thirty-eight patients with hemispheric lesions were investigated. Half had the lesions in the right (RH), and half in the left hemisphere (LH). Thirteen RH and 12 LH patients had localized vascular lesions. The rest of the patients had tumors in one of the hemispheres. The two patients groups did not differ markedly in mean age (49.5 years for RH patients and 53 years for the LH patients), nor in age range. In addition, 40 control Ss (mean age 51 years) free from any cerebral disease were examined. 2.1.2 Apparatus and procedure. The experimental task was tapping repetitively a microswitch for a predetermined time and then, following a visual cue, switching to another microswitch and continuing to tap. 445

446

AMIRAM CARMON

S was presented with a small box mounted parallely to him with two microswitches separated by 10 cm. The microswitches were equipped with 3 cm long arms and large buttons to ease performance. In front of the subject was a small light bulb (16V, 0.1 amp) which was illuminated for 70 msec when the microswitch was pressed. S had to tap repeatedly with the index finger one switch, and continue doing so as long as the bulb was illuminated. Once the light bulb stopped blinking, to the finger taps, S had to shift to the other switch and tap it. Alternation between the switches was made every time the light bulb stopped blinking to the closure of a switch. Tapping was recorded on electromechanical counter and alternation time on a BCD numeric printer (Massey-Dickinson). The experiment was made first for 6 alternations of 2.1 sec switch enabling durations, totaling 12.6 sec. Following this, 6 more switch alternations were made but this time the enabling period alloted for each switch was 6.1 sec, i.e. a total performance time of 36.6 sec. Patients with hemispheric lesions performed with the ipsilateral hand only. Half of the control Ss performed with the right, and half with the left hand only. Performance was scored for two measures: (1) The total time in which the correct switch was tapped; (2) The rate of tapping during the real time of performance (i.e. total number of correct taps divided by the time in which they were made). 2.2 Experiment 2: Repetitive motor performance to a pre-set pace 2.2.1 Subjects. Forty patients with localized lesions in one of the cerebral hemispheres were examined. Half had the lesion in the right, and half in the left hemisphere. The etiology was vascular in 10 R H and l l LH patients, and tumor in 8 patients in each group. The remaining 3 patients had localized atrophy. The control group was composed of forty patients free from any cerebral disease. The patients and control subjects were not the ones who participated in the first experiment. The mean age was 47.5 years in the control group, 48 years in the LH group and 50.5 in the R H group. 2.2.2 Apparatus and procedure. In this experiment the task was to tap one microswitch at the same pace as that at which a light bulb was turned on. The light bulb was programmed to be on for 50 msec and off for either 100, 200 or 400 msec. Thus, three tapping paces were set, a fast (6.7/sec), a moderate (4/sec) and a slow one (2.4/sec). Three trials, one for each pace, were given twice, using an ABCCBA order. Every trial lasted 15 sec. Programming of the equipment allowed recording of correct responses. Half of the control subjects performed with the right and half with the left hand. The patients with brain damage performed only with the hand ipsilateral to the lesion. Performance was scored for "efficiency" of repetitive tapping. This measure was the ratio of correct responses to the maximal number of possible correct responses in a given pace.

3. R E S U L T S Initial analysis by t-tests showed no significant difference in performance between the r i g h t a n d left h a n d s o f t h e c o n t r o l s u b j e c t s , i n a n y o f t h e t w o tests. T h e r e f o r e t h e r e s u l t s were pooled for the two hands of the controls. I n t h e t w o e x p e r i m e n t s a s i g n i f i c a n t d i f f e r e n c e i n p e r f o r m a n c e b e t w e e n t h e c o n t r o l Ss a n d t h e p a t i e n t s w i t h h e m i s p h e r i c l e s i o n s w a s f o u n d . I n t h e first e x p e r i m e n t , c o n t r o l Ss p e r f o r m e d a t a f a s t e r r a t e o f t a p p i n g , a n d s p e n t m o r e t i m e t a p p i n g t h a n d i d t h e p a t i e n t s , i.e. t h e y n e e d e d less t i m e t o c h a n g e f r o m o n e s w i t c h t o a n o t h e r (cf. Fig. 1). T h u s , t h e m e a n number of correct responses achieved by the control Ss was larger than that achieved by the patients with hemispheric lesions. Analysis of variance showed that the difference between the groups was significant. The between groups difference on rate yielded an F o f 13.96, f o r 1/65 d f ( p < O . 0 0 1 ) . F f o r d i f f e r e n c e i n t i m e o f p e r f o r m a n c e b e t w e e n t h e g r o u p s w a s 10.50 ( d f l / 6 5 , p < 0.005). H o w e v e r , t h e g r o u p s d i d n o t i n t e r a c t s i g n i f i c a n t l y w i t h r e g a r d t o t h e t w o c o n d i t i o n s , i.e. s l o w a n d f a s t s w i t c h a l t e r n a t i o n , e i t h e r b y r a t e o r b y t i m e . There was no significant difference between the performances of the two hemispheric groups, either in time spent in tapping or in the rate of tapping. Analyses of variance d o n e o n t h e t w o m e a s u r e s y i e l d e d n o n - s i g n i f i c a n t F ' s f o r all t h e m a i n effects i n v o l v i n g these groups.

SEQUENCED

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Total time and rate of tapping during fast and slow alternation of hand position.

In the second experiment the results were similar. The control Ss performed better than the brain-damaged patients in all three tapping paces (cf. Fig. 2). The difference in this respect was significant at the 0.05 level ( F = 3.02, df2/117). The interaction of groups on pace was not significant ( F = 2.30, df 2/234 p > 0.05). The two groups of patients, with right and with left sided lesions did not show, however, any difference in overall level of performance (F=0.03, df2/38). In spite of the lack of such a difference, there was a significant interaction between the two groups with lesions on pace ( F = 5.90, df 2/76, p < 0.05). The interaction was due to the fact that patients with left sided lesions performed better than patients with right sided lesions when slow and moderate paces of tapping were required and to a reversal of the between-group difference when fast tapping was required.

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448

AMIRAM CARMON

In order to evaluate further the performance of the brain-damaged patients in the two experiments an arbitrarily defined impaired performance score was used. This score was based on performance which fell below that of 90 per cent of the control group. Data in this form for the two experiments is presented in Table 1. Inspection of the table shows that the first experiment was of a questionable discriminative value for brain damage performance, as less than 50 per cent of the patients showed impaired performance in it. No clear difference was seen between the two patients groups with right and with left hemispheric lesions. In the second experiment, the number of patients with impaired performance was even smaller, and the distribution of impaired scores reflected the same interaction between the hemispheric lesions groups noted above. Table 1. Incidence of impaired performance

Experiment 1 Patients with right sided lesions (N=19) Patients with left sided lesions (N= 19) Experiment 2

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4. DISCUSSION In two experiments oil sequenced motor performance, patients with right and with left hemispheric lesions were compared with normal control subjects. The comparisons were made only with respect to tlle performance of the arm ipsilateral to the lesion in order to determine whether unilateral cerebral lesions produce general impairment of motor behaviour in the form of ipsilateral decrement in performance in addition to the specific motor impairment which is evident clinically in the form of contralateral paralysis. Ipsilateral impairment has been noted previously for somatosensory functions in a large proportion of patients with lesions localized in the right or in the left cerebral hemisphere [4-6]. The exact cause of the ipsilateral sensory deficit has not been determined. The possibility that ipsilateral motor impairment can exist as well in unilateral cerebral disease can be also entertained. Prior investigation indicated that such impairment exists under certain sensory feed-back conditions [7]. The results of the two experiments show that while ipsilateral motor deficit exists, its magnitude is not large. Another aim of the two experiments was to determine whether, under certain task requirements, motor performance of patients with right hemispheric lesions would be different from that of patients with left hemispheric lesions. Certain somatosensory functions were thought to be represented bilaterally in the left hemisphere [4, 8]. The possibility of left cerebral dominance for motor functions in the form of bilateral impairment

SEQUENCED MOTOR PERFORMANCE IN PA'IIENTS WITH UNILATERAL CEREr~RAL LESIONS

449

d u e to left sided lesions c o u l d also be d e r i v e d f r o m the results o f m o t o r p o s t u r a l a n d p u r s u i t m o t o r tests [9, 10]. T h e p r e s e n t i n v e s t i g a t i o n d o e s n o t give s t r o n g s u p p o r t for this h y p o t h e s i s . T h e results o f the first e x p e r i m e n t s h o w t h a t w h e n p e r f o r m a n c e is s p a t i a l l y d e t e r m i n e d t h e side o f the c e r e b r a l lesion d o e s n o t influence the level o f p e r f o r m a n c e . In the s e c o n d e x p e r i m e n t , p a c e k e e p i n g o f m o t o r p e r f o r m a n c e was differentially p e r f o r m e d in r e l a t i o n to the side o f the lesion. P a t i e n t s w i t h right sided lesions p e r f o r m e d b e t t e r t h a n p a t i e n t s with left sided lesions w h e n fast t a p p i n g rate was r e q u i r e d . Similarly, r a p i d finger o s c i l l a t i o n was f o u n d to be i m p a i r e d to a l a r g e r d e g r e e in p a t i e n t s w i t h left sided lesions [2]. T h e i m p a i r m e n t o f p a t i e n t s w i t h right h e m i s p h e r e lesions in a s l o w e r p a c e o f t a p p i n g , is in a g r e e m e n t with the results o f experinaents in w h i c h s l o w p a c e r e s p o n d i n g was r e q u i r e d like t h a t o f s i m p l e r e a c t i o n t i m e [1]. REFERENCES 1. DE RENZl, E. and FAGLIONI,P. The comparative efficiency of intelligence and vigilance tests in detecting hemispheric cerebral damage. Cortex 1, 410-433, 1965. 2. WYKE, M. Effect of brain lesions on the rapidity of arm movement. Neurology 17, 113-1120, 1967. 3. VAUGHAN, H. G. and COSTA, L. D. Performance of patients with lateralized cerebral lesions. Ii: Sensory and motor tests. J. herr. ment. Dis'. 134, 237-243, 1962. 4. SEMMES, J., WEINSTEIN, S., GHENT, L. and TEUBER, H. L. Somato-sensory Changes after Penetrating Brain Wounds in Man. Harvard University Press, Cambridge, 1960. 5. CARr~ION,A. Contralateral and ipsilateral tactile sensitivity in patients with unilateral cerebral lesions. Unpublished Ph.D. Thesis, Univ. of Iowa, 1969. 6. CARMON,A. and BENTON,A. L. Tactile perception of direction and number in patients with unilateral cerebral lesions. Neurology 19, 525-532, 1969. 7. CARMON,A. Impairment of kinesthetic feedback in patients with right hemispheric lesions. Possible implications to the pathophysiology of motor impersistence. Neurology 20, 1033-1038, 1970. 8. GOLDSTEIN,K. Die Lokalisation in der Grosshirnzinde. In Handbuch der Normalen undpatologischen physiologie, A. BETHE, A. BERGMAN,G. EMBELENand A. ELL1NGER(Editors), pp. 600-824. Springer, Berlin, 1927. 9. WYKE, M. Postural arm drift associated with brain lesions in man. Archs. Neurol. 15, 329-334, 1966. 10. WYKE, M. The effect of brain lesions on the performance of an arm-hand precision task. Neurapsychologia 6, 125-134, 1968. R6sum6--La performance motrice r6p6titive de groupes de malades atteints de 16sions h6misph6riques droites et gauches et de sujets de contr61e, 6tait 6tudi6e en s6quence pour le lieu et pour la vitesse dans deux expSri6nces s6par6es. La performance des sujets avec 16sions c6r6brales 6tait, dans les deux tests, inf6rieure b. celle des sujets de contrfle. La lat6ralisarion h6misph6rique des 16sions n'avait pas d'influence sur la performance des malades lorsque le lieu 6tait modifi6 de fagon successive, mais die l'affectait quelque peu lorsque la vitesse du "tapping" 6tuit command6e. Lorsqu'on r6clalnait une vitesse rapide du "tapping", les malades avec 16sions gauches avaient des performances inf6rieures h celles des malades avec 16sions droites. On constatait une tendance inverse avec des allures lentes et mod6r6es de "tapping". Ces r6sultats ne sont que partiellement en faveur d'un contr61e diff6rentiel du comportement moteur par l'un ou l'autre h6misph6re, en revanche, ils sont g6n6ralement en accord avec les exp6riences ant6rieures. Zusammenfassung--In zwei getrennten Experimenten wurden iterative motorische Handlungen bei Patientengruppen mit rechter und linkshemisph/irischer L/ision und bei Kontrollpersonen nacheinander fur Zielbewegungen und Klopfschritte geprtift. Die Leistung hirngesch/idigter Kranker war in beiden Testversucben schlechter als diejenige der Kontrollpersonen. Die Seite der Hemisphfirenltision hatte keinen EinfluB auf die Ausftihrung dieser Patienten, wenn man den Zielort regelm/iBig ~inderte, sir war aber von gewisser Bedeutung, falls man die Klopf-Schritt-Folge einschr/inkte. Wenn man eine rasche Klopf-Schritt-Folge verlangte, brachten Patienten mit linkshemisph~irischem Schaden eine schlechtere Leistung zustande als rechtshemisphfirisch Gesch/idigte. Bei langsamer und m~iBig schneller Folge war ein entgegengesetzter Trend zu beobachten. Die Ergebnisse liefern nur eine teilweise Best~.tigung der These, dab motorisches Verhalten von beiden Hemisph/aren unterschiedlich kontrolliert wird. Sie stimmen abet mit friiheren Experimenten im groBen und ganzen tiberein.