Effects of Unilateral Brain Damage on Contralateral and Ipsilateral Upper Extremity Function in Hemiplegia
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1 Effects of Unilateral Brain Damage on Contralateral and Ipsilateral Upper Extremity Function in Hemiplegia This article describes the long-term effects of unilateral penetrating hemispheric lesions on contralateral and ipsilateral upper extremity motor performance and functional outcome. Activities-of-daily-living skill and gross motor performance contralateral to the lesions were compared among 32 left-sided and 19 right-sided hemiplegic subjects using analysis of variance and chi-square techniques. Ipsilateral to the damaged hemisphere,finemotor tasks of simple visual motor reaction time, grip and pinch strength,fingertapping and Purdue Pegboard performance were tested. Analysis of covariance compared each ipsilateral task to performance in the corresponding hand of 70 matched controls. Results indicate similar long-term functional ADL outcome in right and left hemisphere-damaged subjects, despite more severe contralateral functional motor deficits following lesions of the left hemisphere. Right hemisphere lesions led to ipsilateral decrements in reaction time, and lesions of either hemisphere diminished grip or pinch strength,fingertapping, and pegboard performance ipsilaterally. These results demonstrate that unilateral brain damage involving the motor areas of either hemisphere has detrimental effects on ipsilateral upper extremity motor function. Findings are discussed and related to the concept that the left hemisphere is specialized or has greater neuronal representation for bilateral motor processes. Physical therapists involved in the treatment of patients with hemiplegia should be aware that motor functions of the ipsilateral, nonparetic upper extremity may also be affected adversely by unilateral brain lesions [Smutok MA, Grafman], Salazar AM, etal:effects of unilateral brain damage on contralateral and ipsilateral upper extremity function in hemiplegia. Phys Ther 69: , 1989.] Key Words: Brain injuries; Head injury; Hemiplegia, evaluation; Motor skills. Michael A Smutok Jordon Grafman Andres M Salazar Jane K Sweeney Bruce S Jonas Patrick J DiRocco The rehabilitation of patients with hemiplegia is a major challenge to many physical therapists. Within the first few months following a unilateral brain lesion, therapeutic efforts are aimed primarily at the restoration of motor function on the hemiplegic side. While attempting to facilitate motor activity in severely hemiplegic extremities, therapeutic techniques are often applied to the uninvolved extremities. Clinical experience and careful observation, however, sometimes suggest that the nonhemiplegic ("normal") extremities may not be functioning at a totally normal level. Deficits in extremities ipsilateral to the brain damage could result from impaired perception, aphasia, apraxia, or generalized weakness brought about by severe illness during the acute stages of brain injury, or they could relate to a more basic functional relationship between the motor cortex and the ipsilateral limbs. Hand function ipsilateral to the brain damage has been shown to be slower than normal hand function in patients suffering from cerebrovascular accident (CVA). 1,2 In a study of patients two years following stroke, Tsai and Lein reported that ipsilateral hand-speed performance was decreased more in right hemiplegia than in left hemiplegia. 3 The finding that lesions in the left hemisphere lead to greater decrements in ipsilateral (left) motor performance suggests this hemisphere may have greater neuronal representation of bilateral motor processes than the right hemisphere. Motor performance has been proposed to have unequal representation between the hemispheres on the basis of clinical 4 and experimental 5 research on brain-damaged patients without overt hemiplegia. Results have shown 26/195 Physical Therapy/Volume 69, Number 3/March 1989
2 that performance on certain distal motor measures, such as timed pegboard or maze stylus tasks, reveal an asymmetry of hemispheric functioning with left hemisphere lesions causing greater bilateral decrements in performance than right hemisphere lesions. 6-8 This left hemisphere observation does not hold for all studies 5,9,10 nor for all motor tasks. 7,11 Kimura and Archibald 7 and Kimura 12 have argued that the crucial role of the left hemisphere in motor functioning is subserving gestural (or symbolic) communications or, more precisely, control of changes in limb or articulatory posture. Thus, a motor task that contains a communicative component may demonstrate poorer performance following left hemisphere brain damage as compared with right hemisphere brain damage. Problems with respect to subject selection have emerged in interpreting the motor performance literature. Patient groups of varying ages with brain lesions dissimilar in etiology, testing at various times during the recovery period, and subjects with differing cognitive deficits or abnormal mood changes could influence motor performance. The effects of these factors often go unchallenged. These inconsistencies make interpretation of the literature on hemispheric representation of motor function difficult. A long-term outcome goal following hemiplegia is the attainment of independent living to the greatest extent possible. Independence in daily living is influenced by many factors including motor function, perception, communication, memory, information processing, and cognition. When differences in functional outcome are observed between right and left hemiplegia, the disparity can often be attributed to factors other than motor function. Left hemispheric specialization for language and right hemispheric specialization for visual, spatial, or perceptual processing often account for discrepant outcomes among hemiplegic patients with unilateral lesions of either right or left hemisphere. 13,14 As a result of these hemispheric asymmetries, the prediction of functional outcome also is often difficult. Reports of better outcome following right hemiplegia, 15,16 improved outcome in left hemiplegia, 17 and similar outcome regardless of hemiplegic side 18 have consequently surfaced in the literature. The conflicting reports demonstrate the difficulties inherent in the study of human brain function. We have had the unique opportunity of examining a group of hemiplegic men approximately 14 years after they sustained penetrating brain injuries as young adults. Differences with respect to age at injury, etiology, and recovery 7 time have been controlled to a great extent. Within this group, the effects of unilateral brain damage on contralateral gross motor and ipsilateral fine motor performance, as well as on overall function in daily activities, are of interest. We attempted to determine long-term motor outcome in right and left hemiplegia and also whether hemispheric asymmetries in motor function exist in this homogeneous brain-injured group. We hypothesized that fine motor deficits would be present ipsilateral to the brain injury (uninvolved side) and that these ipsilateral motor deficits would be similar among patients with right hemisphere brain damage (RHBD) and those with left hemisphere brain damage (LHBD). We also suspected that contralateral (hemiplegic side) gross motor performance and functional outcome would be similar in right and left hemiplegia. Improved insight into the effects of unilateral brain damage could influence physical therapists' treatment approaches as well as improve the ability to predict motor function outcome in hemiplegia. M Smutok, MS, LTC, Army Medical Specialist Corps, was Chief, Motor Performance Laboratory, Vietnam Head Injury Study, Department of Clinical Investigation, Walter Reed Army Medical Center, Washington, DC , when this study was conducted. He currently is a doctoral candidate, Department of Physical Education, University of Maryland at College Park, College Park, MD Address correspondence to Vietnam Head Injury Study, Department of Clinical Investigation, ATTN: HSHL-CI, Walter Reed Army Medical Center, Washington, DC (USA). J Grafman, PhD, is a Neuropsychologist, Clinical Neuropsychology Section, Medical Neurology Branch, National Institute of Neurological and Communicative Disorders and Stroke, Bldg 10, Rm 5N226, Bethesda, MD A Salazar, MD, COL, Medical Corps, is Director, Vietnam Head Injury Study, Department of Clinical Investigation, Walter Reed Army Medical Center. J Sweeney, PhD, PT, LTC, Army Medical Specialist Corps, is Chief, Army Medical Specialist Corps Clinical Investigation Service, Walter Reed Army Medical Center. B Jonas, PhD, is Statistician, Vietnam Head Injury Study, Department of Clinical Investigation, Walter Reed Army Medical Center. P DiRocco, PhD, is Assistant Professor, Department of Physical Education, University of Maryland at College Park. This study was conducted under the auspices of the Veterans Administration (VA Contract #V101 [91] M ) with the cooperation and support of the US Army, Navy, and Air Force and the American Red Cross. The views are those of the authors and not the US Department of Defense. This article was submitted January 29, 1988; was with the authors for revision for 22 weeks; and was accepted October 26, Method Subject Selection Subjects were chosen from the Vietnam Head Injury Study (VHIS) sample of 520 male veterans who suffered penetrating brain wounds while serving in Vietnam from 1967 to 1970 and from a group of 85 controls with no history of head injury. The study was approved by the human subject review board, and all subjects gave signed informed consent prior to participation. The VHIS involved an intensive, multidisciplinary, one-week, in-hospital evaluation at Walter Reed Army Medical Center, including neurological, motor, speech and language, and neuropsychological testing and computerized tomography (CT) scans of the brain. The participants in this Physical Therapy/Volume 69, Number 3/March /27
3 the Wechsler Adult Intelligence Scale (WAIS).20 The Beck Depression Inventory was administered for determination of mood, a variable that may affect performance.21 The Token Test, a measure of auditory-speech comprehension, was given to quantify the subjects' ability to follow verbal instructions.22 Functional and Gross Motor Performance Level of function (independent, supervised, assisted, or dependent) in activities of daily living was determined by assessment of self-care, mobility, home care, and community living skills as previously described.23 Present hand preference was determined by a 12-item, modified Edinburgh Fig. 1 Six representative cross-sectional computerized tomography scans of brain of Handedness Inventory.24 In addition, subject with left hemiplegia secondary to penetrating head injury. Lesion demonstrates unilateral right-cerebral parenchymal loss in superior temporal, lateral frontal, andgross motor and functional upper majority ofparietal lobe with damage to basal ganglia and internal capsule. No lesion extremity performance was tested exists in left hemisphere. bilaterally. Selective gross motor control was assessed by visual analysis Brain Lesion study included 19 right-hemiplegic of active, isolated movement ability at subjects with LHBD and 32 each joint in both upper extremities as left-hemiplegic subjects with RHBD. Lesion location was determined by a modified from the Bobath analysis of Seventy controls were stratifiedgeneral Electric Model 800 CT movement protocol for adult matched to the brain-injured subjects scanner* and a procedure and software hemiplegic individuals.25 Isolated for age, service in Vietnam, and program specifically devised for the movement was defined as the capacity premilitary service intelligence as VHIS. Cross-sectional CT scans were to move one joint of a limb without determined by a standard entrance taken at intervals of 0.5 cm with the simultaneously moving the other joints examination (Armed Forces subject positioned so that the plane of of that limb. Following a Qualification Test [AFQT]).19 All the scan was 25 degrees from the demonstration, subjects were asked to brain-injured subjects were currently orbital-meatal line. This procedure duplicate specific movements that diagnosed by clinical neurological yielded about 23 separate combined flexion and extension of examination as suffering from cross-sectional scans per subject (Fig. various joints of the arm. For example, hemiplegia (paresis, spasticity, or 1). Lesion location and size were coded one test of the ability to isolate elbow impaired selective movement), and all for computer entry using templates that flexion and extension involved were without apraxia. Mean age at assigned code numbers to the major observing the subject flex and extend injury was 21.3 ± 3.4 years. Duration of structures in each cross section. Total his elbow while maintaining fingers hemiplegia averaged approximately 14 brain lesion volume was calculated by extended, wrist at the neutral position, years. Extremities contralateral to the summing lesion volume for each forearm supinated, and shoulder hemiplegic side and all extremities in additional cross section. laterally (externally) rotated at 90 the controls had clinically normal gross degrees of flexion. One point was motor function. All subjects were Cognitive Measures scored if full elbow flexion and right-hand dominant prior to service in extension was completed without Vietnam. On the basis of a CT scan, For descriptive purposes, various changing the position of the other brain-injured subjects in the study were measures of cognitive performance joints. Upper limb movement determined to have no lesions in the were used to compare the three independent of any abnormal flexor hemisphere ipsilateral to the groups. The AFQT administered upon and extensor synergy patterns, hemiplegic side. entry into military service was used as a therefore, was examined. The summed measure of preservice intelligence. total score following observation of 122 Current intelligence was assessed with separate movements was taken as a measure of selective gross motor control. The influence of abnormal movement patterns was used to *General Electric Co, Medical Systems Group, PO Box 414, Milwaukee, WI /197 Physical Therapy/Volume 69, Number 3/March 1989
4 categorize each arm as functioning with 1) synergistic movement only, 2) a combination of synergistic and selective movements, or 3) normal selective movement. Finally, each upper extremity was grouped into one of four levels of functional use during ADL: 1) normal, independent selective function; 2) assister, or function to assist opposite upper extremity in two-handed activities only; 3) stabilizer, or only functional ability to stabilize objects against table or body; or 4) nonfunctional, or no use during activities. Grouping was based on observation during the ADL assessment. Ipsilateral Fine Motor Performance Longstanding hemiplegia in the brain-damaged groups prevented contralateral fine motor testing in a majority of subjects. Fine motor measures, therefore, were administered only on the ipsilateral side. The ipsilateral upper extremity fine motor test battery focused on five measures: 1. Simple visual reaction time was measured by having subjects press a hand-held button as rapidly as they could when they saw a brief flash of light presented on a small background darkened screen. Each subject performed 76 trials, and the mean reaction time was recorded. 2. Handgrip strength was measured with a Jamar adjustable hand-held dynamometer. The dynamometer grip width was adjusted to each individual's subjective comfort range. The elbow was maintained at 90 degrees, the forearm in the neutral position, and the wrist at approximately 45 degrees of extension while the subject remained seated. One submaximal trial grip was allowed. Strength was measured following one maximal handgrip trial on the dynamometer. Asimow Engineering Co, 1414 S Beverly Glen Blvd, Los Angeles, CA Pinch strength was measured using a Pinsco pinch gauge. The elbow was maintained at 90 degrees, the forearm in the neutral position, and the wrist in approximately 45 degrees of extension while the subject remained seated. Lateral pinch was used with the gauge between the pad of the thumb and the lateral border of the middle phalanx of the index finger while the middle, ring, and little finger pads touched the palm of the hand. Maximal pinch strength was measured following one submaximal trial on the gauge. 4. For rapid alternating movement, a finger-tapping test was used. Subjects were required to press a telegraph key-type apparatus with their forefinger while maintaining forearm contact on a horizontal tabletop. Each press was automatically recorded by a counter. The mean number of taps from three 10-second trials was recorded. 5. Manipulative hand dexteritycoordination skill was measured using the Purdue Pegboard. Subjects were instructed using standardized verbal instructions accompanied by a demonstration of the task. 26 One practice trial was allowed. The task required subjects to retrieve smooth pegs from a shallow cup one at a time, and place them in a row of holes in the board. The score was based on the number of pegs placed within a 30-second time limit. All functional and gross motor tests and ipsilateral fine motor tests of strength and hand dexterity were administered by two physical therapists. The therapists independently observed and scored the tests in four randomly chosen subjects prior to data collection. There was interrater agreement in 97% of 1,320 total recorded observations. Cognitive, visual reaction time, and finger-tapping tests were given by five B & L Engineering, 9618 Santa Fe Springs Rd, Ste 8, Santa Fe Springs, CA psychologists. These testers received standardized training by a neuropsychologist (JG) and met established criteria for test administration prior to data collection. Interrater reliability was not estimated among the psychologists. Scores were independently double-checked for accuracy of recording. Data Analysis Demographic, cognitive, lesion volume, and selective gross motor control measurements were compared among controls and the two brain-damaged groups using an analysis of variance. Pair-wise comparisons were made with Tukey's studentized range test when significant differences were found among the three groups. Contralateral functional motor performance between the subjects with RHBD and those with LHBD was compared by applying the chi-square test. An analysis of covariance was used to compare ipsilateral fine motor measures. Covariates included complex sensory impairment (proprioception, stereognosis, graphesthesia, tactile extinction, and finger agnosia) and simple sensory impairment (touch, pain, and vibration), as quantified by a clinical neurological examination. This technique accounted for any sensory system abnormality effects on fine distal motor measures of interest. The effects of unilateral brain damage on ipsilateral motor performance were tested by comparing 1) the right-hand scores of subjects with RHBD with those of the controls and 2) the left-hand scores of subjects with LHBD with those of the controls. A 5% level of significance was used in all statistical procedures. Results All subjects in the groups were ambulatory and independent in self-care, home care, and community living skills. Functional outcome in ADL was equal across all subjects. No subject exhibited a clinically apparent unilateral disregard. Table 1 lists demographic, cognitive, mood, and gross motor control data for comparison of controls and subjects Physical Therapy/Volume 69, Number 3/March /29
5 with RHBD and LHBD. Age, preservice intelligence (AFQT), education, and depression index data were similar in all three groups. Mean total brain volume loss was similar in both brain-injured groups. Current verbal IQ and auditory comprehension (Token Test) were lowest in the subjects with LHBD, whereas performance IQ was diminished in both hemiplegic groups. Although the mean Token Test score for the subjects with LHBD (92.0) was significantly lower than for the other two groups, it remains within a clinical range that is considered normal for speech comprehension. The Edinburgh Handedness Inventory revealed controls and subjects with RHBD had retained their right hand as dominant. Subjects with LHBD, who were also right-handed premorbidly, demonstrated stronger left-hand dominance as a result of their hemiplegia. Upper extremity gross motor control scores were maximal (maximum = 122) bilaterally in the controls and on the nonhemiplegic side of both brain-injured groups. The hemiplegic arm of the RHBD group had a slightly higher mean score on gross motor control (77.3) than the LHBD group's hemiplegic arm (66.9). Contralateral Function Functionally, both upper extremities of the controls and the noninvolved upper extremities of the hemiplegic subjects had full selective movement and normal functional use in ADL. A higher percentage of the RHBD group did not demonstrate any abnormal synergistic movement in the hemiplegic upper extremity (45%) than in the LHBD group (26%), but this difference was not significant (Tab. 2). Nevertheless, Table 2 reveals that a significantly higher number of subjects in the RHBD group functioned normally with their hemiplegic arm than in the LHBD group. Fifty percent of the subjects in the RHBD group used their contralateral, hemiplegic arm in a normal selective fashion contrasted to only 21% with normal hemiplegic arm use in the LHBD group. The subjects with RHBD apparently achieved better long-term contralateral function than those with Table 1. Group Characteristics and Cognitive, Mood, and Gross Motor Performance Variable Age (yr) Preservice AFQT C (%) Education (yr) Total lesion volume (cc) WAIS d Verbal IQ Performance IQ Token Test Beck Depression Inventory Edinburgh Handedness Inventory Right total Left total Gross motor control Right upper extremity Left upper extremity a Right hemisphere brain damage. b Left hemisphere brain damage. c Armed Forces Qualification Test. d Weschler Adult Intelligence Scale. Group Control (n = 70) e e Significantly different from other two groups (p <.05). s RHBD a (n = 32) e s LHBD b (n = 19) e e e 9.0 e 66.9 e Table 2. Functional Motor Performance of Contralateral Hemiplegic Upper Extremity Abnormal movement pattern (any synergistic movement) Normal movement pattern (no synergy) Abnormal functional use (assister, stabilizer, or no use) Normal functional use (selective use) Writing hand Right Left a Right hemisphere brain damage. b Left hemisphere brain damage. c p <.05. RHBD a (n = 32) n % LHBD b (n = 19) n % s x c 32.6 C 30/199 Physical Therapy/Volume 69, Number 3/March 1989
6 LHBD, even though the mean lesion volume of the RHBD group (67 cc) was similar to that of the LHBD group (60 cc) (Tab. 1). The range of lesion volumes was virtually identical in both groups (1-196 cc). In addition, 74% of the subjects with LHBD had changed their writing hand from right to left as a result of their right hemiplegia (Tab. 2). Ipsilateral Function The effects of unilateral brain damage on ipsilateral upper extremity performance in various fine motor measures are presented in Tables 3 and 4. A comparison of right arm performance between subjects with RHBD and controls demonstrated significant decrements in simple visual reaction time, grip strength, finger tapping, and pegboard performance (Tab. 3). The left arm of subjects with LHBD was deficient in pinch strength, finger tapping, and pegboard performance compared with the left arm of the controls (Tab. 4). The ipsilateral effects of brain injury on most motor tasks demonstrated deficiencies of approximately 7% to 13% in both brain-injured groups when compared with controls (Fig. 2). Complex sensory impairment used as a covariate resulted in a statistically significant negative effect on right pinch strength and pegboard performance in subjects with RHBD. Simple sensory impairment negatively affected left grip and pinch strength in subjects with LHBD. We found no other significant detrimental effects of sensory function on ipsilateral motor performance. Discussion Functional Activitiesof-Daily-Living Outcome Functional outcome, as measured by the level of independence in mobility, self-care, home care, and community living skills, was not different between the RHBD and LHBD groups. Both groups were fully independent. This observation was not unexpected given the young age of these men at the time of injury ( =21 years) and the long Table 3- Mean Performance and Analysis of Covariance Results of Right Arm Measure VRT b (sec) Grip strength (kg) Pinch strength (kg) FT C (taps/10 sec) Pegs d (number/30 sec) a Right hemisphere brain damage b Visual reaction time. c Finger-tapping test. d Purdue Pegboard test. Table 4. Measure VRT b (sec) Grip strength (kg) Pinch strength (kg) FT C (taps/10 sec) Pegs d (number/30 sec) Group Control (n = 70) RHBD a (n = 32) ss F Mean Performance and Analysis of Covariance Results of Left Arm a Left hemisphere brain damage. b Visual reaction time. c Finger-tapping test. d Purdue Pegboard test. Group Control (n = 70) intervening period following injury (14 years). Both factors probably contributed to the development of compensatory mechanisms and alternative abilities necessary for complete functional adjustment to their permanent disability. Studies that report differences in outcome between right and left hemiplegia often find these disparities in patient groups of advanced age 16 ; at much shorter follow-up periods 15 ; or when associated deficits such as aphasia, agnosia, or visuospatial disturbances are present. 17 As demonstrated by the demographic, cognitive, language, and mood data in LHBD a (n = 19) SS F P P Table 1, our groups displayed reasonable homogeneity. No functional differences existed between the groups on most of these measures. Lesion size and location (unilateral motor area) also demonstrate similarity. The hemisphere of damage, therefore, appears to have little influence on functional differences in ADL outcome between well-matched hemiplegic groups. This finding is in agreement with other studies involving older patients and much shorter time intervals following brain damage. 18,27 Physical Therapy/Volume 69, Number 3/March /31
7 Contralateral Gross Motor Function Our results demonstrate poorer contralateral functional motor performance following LHBD. The mean motor control score in subjects with LHBD was slightly lower (67) than for subjects with RHBD (77); however, the variability of motor control scores was large (Tab. 1). The proportion of subjects with LHBD with no evidence of abnormal synergistic movement patterns was lower than, but not statistically different from, the subjects with RHBD (Tab. 2). Nevertheless, fewer than one quarter of the subjects with LHBD had normal selective functional ADL use of the hemiplegic upper extremity, a significantly lower proportion as compared with one half of the subjects with RHBD (Tab. 2). From a functional motor performance standpoint, these results suggest that damage to the left hemisphere is more detrimental to the right arm than right hemisphere damage is to the left arm. The left hemisphere has been suggested to be the dominant hemisphere in right-handers. Previous research has shown performance of the right hand in nonhemiplegic subjects to be more diminished than that of the left hand when lesions of the contralateral hemisphere exist. 6,8,28 The results of our study also indicate greater contralateral motor effects in individuals with LHBD. If the left hemisphere contains greater neuronal representation of bilateral motor processes, as has been postulated, then our observations in hemiplegic subjects may be interpreted neuroanatomically. Following right hemisphere damage, the contralateral effects on the left arm may be compensated for by increased left-sided neuronal representation in the undamaged left hemisphere. In contrast, when left hemispheric function is impaired, there is less compensation for right-hand dysfunction by the right hemisphere. The right hemisphere may lack an adequate representation of ipsilateral (right) motor functions to overcome deficits on that side. Fig. 2. Ipsilateral hand performance in 32 left-hemiplegic subjects with right hemisphere brain damage (RHBD) and 19 right-hemiplegic subjects with left hemisphere brain damage (LHBD) relative to corresponding hand performance of 70 matched controls. (Hand performance = brain-injured performance control performance 100.) In a study of unilateral brain damage secondary to CVA, neoplasm, and trauma, Horn and Reitan reported that greater contralateral sensorimotor deficits were present in subjects with right hemisphere lesions, contrary to our finding. When the trauma group (similar in age and etiology to VHIS participants) was analyzed independent of the CVA and neoplasm groups, the right hemisphere contralateral effects were less pronounced. 29 In addition, the measures used by Horn and Reitan to assess sensorimotor performance were to a great extent sensoryperceptual and tactile-perceptual. It is not surprising that the right hemisphere may play a greater role than the left in more perceptually oriented motor tasks. Because of the severe sensorimotor deficits of hemiplegia, it was necessary to examine only the more gross measures of contralateral motor function in our groups. Comparisons with other reports involving nonparetic subjects in which complex fine motor measures were used, therefore, may not be valid. Ipsilateral Fine Motor Function A striking finding of this study is that damage to either hemisphere leads to longstanding decrements in motor performance in the ipsilateral upper extremity. The deficits, although mild, are nevertheless present and do not completely recover, even when increased ipsilateral arm use is functionally necessary because of contralateral hemiplegia. Simple visual reaction time, a task that requires visual perception and a rapid motor response, demonstrated a disparity between the right and left hemispheres. The visuoperceptual processing, an identified function of the right hemisphere that is required for rapid visual reaction time, was understandably decreased ipsilaterally in the RHBD group only. 27 Ipsilateral strength deficits (grip strength in the RHBD group and pinch strength in the LHBD group), rapid alternating movements (finger tapping), and dexterity (Purdue Pegboard test) occurred with lesions of either hemisphere. Similar decrements have previously been reported in hemiplegic patients /201 Physical Therapy/Volume 69, Number 3/March 1989
8 In this study, ipsilateral decrements appear to be similar in both brain-damaged groups on fine motor measures of pinch strength, finger tapping, and pegboard performance (Fig. 2). If, as suggested previously, the left hemisphere has greater bilateral motor representation than the right hemisphere, we would expect greater ipsilateral decrements following LHBD. Tsai and Lein, also observing ipsilateral motor processes in hemiplegia, reported that patients with left hemisphere brain damage had slower left-hand performance 18 months after stroke. 3 Our data suggest minimal hemispheric differences in ipsilateral motor performance 14 years after injury. Although our results seem to contradict the concept of left hemisphere dominance for bilateral motor representation, the lack of greater left hemisphere ipsilateral effect may be explained on the basis of present hand dominance. All brain-injured subjects and controls in this study were right-hand dominant prior to Vietnam service. At present, the controls and the subjects with RHBD remain right dominant. The subjects with LHBD, however, out of necessity have switched dominance to the left hand over the intervening 14 years, as confirmed by their higher left-hand Edinburgh Handedness Inventory scores (Tab. 1) and higher percentage of left-handed writing (Tab. 2). Because the statistical analysis of ipsilateral performance compares the left-hand (nondominant) performance of the controls with the present left-hand (dominant) performance of the subjects with LHBD, differences may be masked by longstanding increased use of the left hand in the subjects with LHBD. That is, the expected greater ipsilateral defects following LHBD may have been partially compensated for when right hemiplegia forced increased use and subsequently improved fine motor development of the left hand in this group. Controls who have retained right-hand dominance would not necessarily increase their left-hand use to this extent. The switch to left-hand dominance following right hemiplegia, therefore, could lessen an expected ipsilateral left hemispheric effect. It is interesting to note that, with the exception of grip strength, reliance on left-hand dominance in the LHBD group has not restored left-hand performance levels to that of controls (Fig. 2). The damaged brain's compensating abilities to change hand dominance do not reach the nondominant fine motor performance of the uninjured brain. We presume that retention of right-hand dominance in left hemiplegia following RHBD does not lead to a compensatory improvement in fine motor control of the right hand because it has remained the dominant hand throughout life. There is no necessity to develop dominant hand skills ipsilaterally following RHBD if the ipsilateral hand was dominant premorbidly. Our examination of a homogeneous sample of brain-injured adults supports the idea that the left hemisphere may have greater neuronal representation of motor processes, as previously reported. 3,4,6 We have suggested that the necessity to develop a previously nondominant hand into a dominant one may result in a partial compensation for loss of left hemisphere upper motoneurons by an adaptability of the brain to improve fine motor performance on the nondominant side. Tsai and Lein suggest a diminished adaptability of left-hand performance in 60-year-old right-hemiplegic patients approximately 18 months following stroke. 3 Fourteen years following penetrating head injury in 21-year-olds, our study shows no appreciable difference in ipsilateral performance between right and left hemisphere lesions. Both of our brain-injured groups had diminished fine motor performance; however, these deficits were similar between groups. Damage to the dominant (left) hemisphere may require a prolonged period greater than 18 months for compensatory ipsilateral fine motor development. The recovery of fine motor function may necessitate a longer time interval than previous research has investigated. A longitudinal examination of motor behavior following brain injury might provide evidence of continued improvement beyond what we have considered to be the termination of recovery. In addition, a nervous system not yet affected by advanced age may be necessary for this compensation to occur. The effects of age on motor performance are only beginning to be studied in healthy populations. Age-related changes in the damaged brain are largely unknown. At present, we can only speculate that the effects of aging are similar in both brain-injured and nonbrain-injured individuals. Further research into the consequence of brain lesions on motor function and also the recovery from motor deficits is necessary. Future study of hemiplegia must consider the influences of age and recovery time to gain meaningful interpretation about motor representation in the brain. Conclusions The major findings of this study regarding unilateral hemisphere damage in hemiplegia suggest: 1. Similar functional ADL recovery independent of hemiplegic side. 2. Greater long-term contralateral upper extremity functional motor deficits following left hemispheric damage. 3. Longstanding fine motor decrements of the ipsilateral upper extremity resulting from lesions involving the motor area of either hemisphere. Therapists involved in the treatment of patients with hemiplegia must be aware that the motor functions of the ipsilateral, uninvolved upper extremity may be affected adversely by a unilateral brain lesion. Therapy for the nonhemiplegic side should be incorporated into comprehensive treatment programs. In addition, hemiplegia secondary to LHBD may result in greater contralateral and, initially, ipsilateral motor deficits. Right hemiplegia, therefore, may require a more intensive approach in treatment and a more guarded prognosis than left hemiplegia. The communication abnormalities resulting from LHBD at times make rehabilitation difficult. It is Physical Therapy/Volume 69, Number 3/March /33
9 our contention that more severe functional motor abnormalities in these patients may also contribute to less complete and more prolonged recovery. Acknowledgments We thank the staffs of the Neurology Service and Department of Clinical Investigation at Walter Reed Army Medical Center for their help and advice; LTC Kurt Herzberger, MEd, PT, for assistance in data collection; and Pat West for her diligence preparing this manuscript. We acknowledge COL (Ret) Virginia A Metcalf, whose strong commitment to clinical research generated research positions for US Army physical therapists in the Vietnam Head Injury Study. Our deep appreciation goes to US Navy Master Chief (Ret) Herbert R Brown for his administrative expertise and for sharing his extensive knowledge of the history of this project with us. This article is dedicated to the memory of Dr William F Caveness: but for his foresight, tireless efforts, and determination, this research project would never have been possible. References 1 Thomas CW, Spangler DP, Izutsu S, et al: An analysis of psychomotor responses of adult hemiplegic patients. Arch Phys Med Rehabil 42: , Jebson RH, Griffith ER, Long EW, et al: Function of the "normal" hand in stroke patients. Arch Phys Med Rehabil 52: , Tsai LJ, Lein IN: The performance of the unaffected hand of stroke patients. Journal of the Formosan Medical Association 81: , Geschwind N: Disconnexion syndromes in animal and man. Brain 88: , Haaland KY, Delaney HD: Motor deficits after left or right hemisphere damage due to stroke or tumor. Neuropsychologia 19:17-27, Haaland KY, Cleeland CS, Carr D: Motor performance after unilateral hemisphere damage in patients with tumor. Arch Neurol 34: , Kimura D, Archibald Y: Motor functions of the left hemisphere. Brain 100: , Vaughan HG, Costa LD: Performance of patients with lateralized cerebral lesions: II. Sensory and motor tests. J Nerv Ment Dis 34: , Haaland KY, Porch BE, Delaney HD: Limb apraxia and motor performance. Brain Lang 9: , Jason GW: Hemispheric asymmetries in motor function: II. Ordering does not contribute to left hemisphere specialization. Neuropsychologia 21:47-58, Howes D, Boiler F: Simple reaction time: Evidence for focal impairment from lesions of the right hemisphere. Brain 98: , Kimura D: Acquisition of a motor skill after left hemisphere damage. Brain 100: , Bourestom NC: Predictors of long-term recovery in cerebrovascular disease. Arch Phys Med Rehabil 48: , Feigenson JS, McDowell FH, Meese P: Factors influencing outcome and length of stay in a stroke rehabilitation unit. Stroke 8: , Cassavan A, Ross PL, Dyer PR: Lateralization in stroke syndromes as a factor in ambulation. Arch Phys Med Rehabil 57: , Denes G, Semenza C, Stoppa E, et al: Unilateral spatial neglect and recovery from hemiplegia: A follow-up study. Brain 105: , Gordon EE, Drenth V, Jarvis L: Neurophysiologic syndromes in stroke as predictors of outcome. Arch Phys Med Rehabil 59: , Mills VM, DiGenio M: Functional differences in patients with left or right cerebrovascular accidents. Phys Ther 63: , Uhlander JE: Development of Armed Forces Qualification Test and predecessor Army screening tests, Washington, DC, US Dept of Defense, Personnel Research Branch Report No. 976, 1952, pp Wechsler D: Wechsler Adult Intelligence Scale Manual. New York, NY, Psychological Corp, Beck AT, Word CH, Mendleson M, et al: An inventory for measuring depression. Arch Gen Psychiatry 4: , DeRenzi E, Vignolo LA: The Token Test: A sensitive test to detect disturbances in aphasics. Brain 85: , Sweeney JK, Smutok MA: Vietnam Head Injury Study: Preliminary analysis of the functional and anatomical sequelae of penetrating head trauma. Phys Ther 63: , Oldfield RC: The assessment and analysis of handedness: The Edinburgh inventory. Neuropsychologia 9:97-113, Bobath B: Adult Hemiplegia: Evaluation and Treatment, ed 2. London, England, William Heinemann Medical Books Ltd, 1978, pp Tiffin J: Purdue Pegboard Examiner Manual. Chicago, IL, Science Research Associates, Inc, 1968, pp Wade DT, Hewer RL, Wood VA: Stroke: Influence of patient's sex and side of weakness on outcome. Arch Phys Med Rehabil 65: , Wyke M: The effects of brain lesions on the performance of bilateral arm movements. Neuropsychologia 90:33-42, Horn J, Reitan RM: Effect of lateralized cerebral damage upon contralateral and ipsilateral sensorimotor performances. Journal of Clinical Neuropsychology 4: , /203 Physical Therapy/Volume 69, Number 3/March 1989
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