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NeuroRehabilitation 9 (1997) 57-69

Sensory-motor control in the ipsilesional upper extremity after stroke Patricia S. Pohl a,*, Carolee J. Winstein b , Sompom Onla-or b aDepartment of Physical

Therapy £liucation and Center on Aging, University of Kansas Medical Center, 3901 Rainbow Boulevard, Kansas City, KS 66160-7601, USA bDepartment of Biokinesiology and Physical Therapy, University of Southern California, Los Angeles, CA, USA

Abstract There is substantial evidence to indicate that sensory-motor control of the ipsilesional upper extremity (UE) in adults after unilateral stroke is abnormal. Some of the sensory-motor deficits differ as a function of the side of the cerebral lesion. Rapid movements of the ipsilesional UE that require precise timing and sequencing are more affected in individuals with lesions in the left hemisphere. In contrast, ipsilesional movements that have constrained spatial requirements are more affected in those with lesions in the right hemisphere. Ipsilesional UE coordination of discrete tasks may be normal, but the coordination of continuous tasks is affected in adults with left stroke. Sensation in the ipsilesional UE appears to be unaffected, or minimally affected after stroke. Strength deficits have been demonstrated in the ipsilesional UE, but primarily in those with right sided lesions. Ipsi'lesional performance deficits are revealed in clinical tests of function that use time to completion as the measure of success. Ipsilesional performance deficits may reflect motor control deficits that are masked on the contralateral side by hemiplegia and hemisensory loss. Interventions that focus on specific motor control deficits, such as speed of sensory-motor processing, through practice with the ipsilesional UE, may result in functional improvements in both limbs. © 1997 Elsevier Science Ireland Ltd. Keywords: Stroke; Motor control; Rehabilitation

1. Introduction A unilateral stroke may result in sensorymotor control deficits; these deficits are

* Corresponding author. fax: [email protected]

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pronounced in the extremities contralateral to the lesion. Clinical measures of physical deficits after stroke focus on these contralateral deficits, however, evaluation of the 'uninvolved' extremities ipsilateral to the cerebral lesion may be included for comparison with the 'involved' extremities. Although it is unequivocal that the extremities contralateral to a unilateral cerebral lesion are

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more affected than the ipsilesional extremities, there is now a relatively large body of research that suggests that the ipsilesional extremities are not 'normal'. Particular to the upper extremity (UE), there is increasing evidence of sensorymotor control deficits on the ipsilateral side. These deficits have been identified in studies in which quantitative laboratory measures have been used, and, to a lesser extent, in studies in which standardized clinical measures have been used. Some studies have shown that the specific control deficits relate to the cerebral hemisphere affected by the ,stroke. Components of sensory-motor control in the ipsilesional UE may be affected after right hemispheric damage but not left or the reverse may be true. Admittedly, generalizations about ipsilesional UE control must be made with care due, in part, to inherent variability between subjects in lesion type, location and extent. Researchers have made some attempts to minimize this variability. The most frequent lesion in stroke is an infarction of the middle cerebral artery [1]. In many studies, attempts are made to restrict participants to individuals with lesions in the territory of the middle or anterior cerebral artery. Lesion location may be deduced from clinical data [2] or obtained from brain imaging techniques [3]. There are a few studies that have quantified lesion extent and location from computerized tomography (cr) scan, such as that by Haaland and Harrington [3], or provided qualitative analysis of lesion location from cr or magnetic resonance imaging (MRI), such as that by Winstein and Pohl [4]. Unfortunately in some cases, it is not clear how unilateral cerebral lesions were identified [5]. Given the subtlety of the control deficits of the ipsilesional extremities and in comparison to the magnitude of contralateral hemiparesis and hemisensory loss, the clinician may question what can be gained from examination of ipsilesional deficits. We suggest that identification of these ipsilesional sensory-motor control deficits provides information related to central sensory-motor processing that may be masked by profound hemiparesis and hemisensory loss in the contralateral extremities [6]. Sensory-motor control deficits that are identified in ipsilesional limb

performance may be a manifestation of the disrupted output from the damaged hemisphere that has broad effects on performance. Recent work using neuroimaging techniques has shown bilateral cerebral activation during the planning and execution of unimanual goal-directed actions [7-9]. For example, Dieber et al. [8] found significant regional cerebral blood flow (rCBF) increases bilaterally in frontal and parietallobes when subjects were required to select a particular movement from several choices and in response to a cue. Recently, we found significant increases in rCBF in ipsilateral dorsal pre-motor, contralateral inferior parietal, and bilateral occipital areas during continuous reciprocal aiming movements when task complexity was increased [9]. Thus, given the contributions from each hemisphere to these unilateral UE actions, if sensory-motor areas in one hemisphere are disrupted after unilateral stroke, manifestations of this disruption can be reflected in the movements of either limb, though the ipsilesional limb effect is decidedly more subtle. The recognition that unilateral hemispheric deficits can impact motor abilities of both the 'involved' and the 'uninvolved' extremities can provide direction for intervention designed to improve sensory-motor control. In addition to the evidence regarding bilateral activation during unilateral UE movements, there is some evidence of hemispheric asymmetry and handedness using functional MRI (fMRI). It has been demonstrated that the human motor cortex is asymmetrically activated during contralateral and ipsilateral finger movements, particularly in right-handed subjects [10]. As expected, motor cortical activation in the right hemisphere was greater for contralateral finger movements than for ipsilateral finger movements. In contrast, motor cortical activation in the left hemisphere was not significantly different for contralateral and ipsilateral finger movements. These results support the contention made in the early part of the 1900s that the left hemisphere has a specialized role in sensory-motor control for both UEs [11]. The primary purpose of this paper is to provide an overview of sensory-motor control deficits identified in the ipsilesional UE of individuals

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with unilateral cerebral damage. The table is a summary of the literature presented in this review. Control deficits identified through laboratory paradigms and through clinical tests are included. Secondarily, this overview highlights those ipsilesional deficits that are specific to the cerebral hemisphere affected-hemispheric asymmetries in sensory-motor control. Finally, implications of these findings for the physical rehabilitation of individuals with stroke are discussed. This overview is not an extant review of the literature. Clearly, the focus is on recent literature and work in progress. Further, the studies included in this review are restricted to those that examined the sensory-motor performance of adult humans after unilateral brain damage; the mechanisms of brain damage include stroke, traumatic brain injury, and tumor. Finally, the reader will observe that certain topics associated with sensory-motor control after stroke are omitted. Limb praxis and motor programming are discussed separately in this volume. Thus, studies which have concentrated on changes after stroke in reaction time, sequencing, and motor persistence are not emphasized in this review. 2. Ipsilateral UE sensory-motor control

2.1. Speed and accuracy

Speed and accuracy are explicit or implicit goals of many functional tasks. The challenge to the performer is to move as quickly as possible but remain within some precision constraint. The speed-accuracy trade-off was described almost 100 years ago [12], and tasks with these dual goals are often used to evaluate sensory-motor control. In general, investigators establish accuracy criteria and the performer is asked to move as rapidly as possible within those criteria. Hand asymmetry in performance is a common experience and is well-documented in the literature [13]. To control for handedness, some studies have limited subjects to right-hand dominant adults or those who were right-hand dominant pre-morbidly, and have limited comparisons to individuals performing with the same hand. Investigations into the speed

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and accuracy of performance of the ipsilesional VE have included tasks ranging from single target tapping to more complex tasks such as copying hand postures. The results of these studies suggest that when accuracy is constrained, ipsilesional speed deficits are not always apparent in the simples of these tasks (i.e. single target tapping), but are commonly reported in tasks that are more complex. 2.1.1. Single target tapping In single target tapping, the participant is required to move a finger or stylus up and down, tapping a single target as rapidly as possible for a pre-established amount of time (e.g. 10 s). Performance is measured as the number of target taps completed in the given time interval, or movement time (MT) /tap which can be calculated by dividing the duration of the tapping time by the number of taps completed. From a sensory-motor control perspective, single target tapping can be controlled primarily, if not solely, by open-loop processes [14]. Open-loop control means that sensory feedback, particularly visual feedback, is not essential for successful completion of the task. Certainly single target tapping can be completed rapidly and accurately for durations of 10-20 s with the eyes closed. The performance of single target tapping is not affected in the ipsilesional VE after right or left cerebral lesion [3,15-20]. The speed of single target tapping was normal, compared with controls, in both the ipsilateral and contralateral VE in a recent study that included individuals with small, well-defined cerebral lesions [21]. Given that single target tapping is controlled by openloop processes, the results of these studies suggest that open-loop control is preserved in the ipsilesional VE. However, ipsilesional slowing in single target tapping, regardless of lesion-side, has been reported in a sample population of adults with penetrating brain wounds [22], and in a sample population that included adults with stroke, traumatic brain injury, or neoplasms [23]. In contrast, studies that have included only those individuals with stroke have found slower single target tapping only for those with left lesions [4,24].

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Two variations of single target tapping were done by Carmon [5]. He required subjects to tap on a single target but switch to another target in response to a visual cue. Carmon reported that MT and the time spent switching from one target to the other increased for both those with right or left hemispheric lesions compared to controls. In a second experiment, subjects were required to tap on a single target under three different speeds of a paced task. Success was measured as efficiency, or the accuracy in timing the tap with the paced visual cue. In the fastest speed, those with left lesions were the least efficient. In contrast, in the slow and moderate paced conditions, those with right lesions were the least efficient (Fig. 1). 2.1.2. Aiming

Reciprocal or continuous aiming has been used to study the performance of the ipsilesional VE in individuals after stroke. In reciprocal aiming, the performer is required to move a stylus back and forth between two targets, hitting each target alternately, for a predetermined amount of time (e.g. 10 s). The sensory-motor control demands

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of the task can be altered in various ways, but one of the most obvious and well-studied manipulations is changing the precision requirement by varying the size of the target. Movements to wide targets can be controlled predominantly by openloop processes. Movements to narrow targets require sensory-based processing, primarily visual, to assure accuracy [25]. Ipsilesional VB performance deficits have been shown in both reciprocal aiming and in discrete aiming, in which the task is to move from a start position to a single target. Slower MTs for aiming with the ipsilesional VE have been found for those with right or left stroke compared to controls [4,19,26,27], or only for those with left stroke [28]. In this latter case, however, a large standard deviation in MT for those with right stroke may have contributed to the lack of a significant difference for those with right stroke compared to controls. Further, while individuals with right or left lesions are slower than controls in rapid aiming, it appears that the reason for slowing depends on the side of the lesion. Specifically, the performance of those with left lesions is particularly slowed, compared to controls, in conditions with low precision demands [4,19,20,29]. Compatible with results from single target tapping, this suggests that those with left sided lesions have difficulty in conditions that are controlled primarily by open-loop processes. In contrast, the performance of those with right lesions is particularly slowed, compared to controls, in conditions with high precision demands [4] or they are less accurate [28]. This suggests that those with right sided lesions have difficulty in conditions that have high visual-spatial processing demands. Further support for this right/left difference in motor control and thus, differences in ipsilesional performance that are side-related, comes from kinematic analyses of aiming movements. Openloop control has been operationalized as the time spent in acceleration (i.e. lift-off from one target to peak velocity) and the magnitude of peak velocity [4]. Haaland and Harrington [28] found that the accelerative portion of an aiming movement was prolonged for individuals with left, but not

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right,· stroke using the ipsilesional UE compared to controls. In this study, the decelerative portion of aiming was also prolonged for those with left stroke, however, as the authors suggest, this may have been due to the fact that the distance remaining to the target was larger. In other work, adults with left, but not right, stroke had lower peak velocities in the major plane of movement in reciprocal aiming to wide targets [4,30]. Sensory-based control has been operationalized as the time spent in deceleration as the target is approached (i.e. peak velocity to target hit) and the frequency of adjustments as the target is approached (i.e. stopping in the target approach such that vertical velocity becomes zero) [4]. As shown in Fig. 2, adults with right, but not left, stroke demonstrated longer absolute deceleration times with the ipsilesional UE compared to their controls in reciprocal aiming across three conditions of difficulty (i.e. low, medium, and high) [27]. Fig. 2 also illustrates the possible confound of hand asymmetry if comparisons were made across hands. The deceleration time of those with right stroke using their right, dominant VE is not different from controls using their left, non-dominant UE, but the deceleration time of those with

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right stroke is clearly prolonged when compared to controls using the same hand. It has also been shown that adults with right stroke tended to have a greater frequency of adjustments than controls in aiming to narrow targets. In contrast, there were no differences in the frequency of adjustments for those with left stroke compared to controls [4]. The sensory-motor control demands of aiming can also be altered by having a target appear suddenly, compared to a condition in which the targets are fixed. Fisk and Goodale [26] found that, compared to controls, ipsilesional performance for those with right or left lesions was slower in aiming to targets that suddenly appeared, but the reasons for the slowing differed depending on the side of the lesion. Individuals with left lesions had prolonged transport times, supporting the particular difficulty in open-loop control for those with left sided hemispheric damage. Those with right lesions had prolonged reaction times. When kinematic analyses were included in a similar task, it was noted that the accuracy of aiming for those individuals with right stroke was similar to that of controls but the trajectory deviated to the right [31]. Thus, adults with right sided lesions have particular difficulty in ipsilesional tasks with high visual-spatial processing demands.

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21.3. Other goal-directed movements The ipsilesional UE, regardless of lesion side, was slower in a rapid elbow flexion task [32], and less accurate in a pursuit rotor task [33,34]. Performance differences as a function of side have been reported. The ipsilesional VE of those with left sided cerebral lesions was slow in copying hand postures [2]. In summary, ipsilesional single target tapping may be unaffected in individuals with unilateral brain damage. If it is affected, it is more likely that slowed performance would be observed in those with left, but not right, brain damage. Further, sensory-motor deficits have been reported in studies that have examined aiming and other goal-directed movements that require speed and accuracy. Together, the results suggest that individuals with left lesions may have particular dif-

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ficulty in tasks that can be predominantly controlled by open-loop processing. Thus, rapid, ballistic movements may be problematic to those with left lesions. In contrast, individuals with right lesions may have particular difficulty in tasks that require visual-spatial processing. Slow, deliberate movements that require endpoint precision may be problematic to those with right lesions. There is some evidence to suggest that these control problems may be diminished with practice [30], however, further empirical work is needed to determine the potential for rehabilitation of these side-related motor control deficits.

2.2. Coordination Newell [35] defined coordination as the 'organization of the control of the motor apparatus'. Using this organization as a framework, the performer may scale a response to meet the specific demands of the task. For example, the basic rattern of a coordinated reach to get an apple out of a fruit basket is not unlike the pattern used to get a cherry out of a fruit basket, however these movements are scaled or parameterized to meet the differing precision demands caused by the size and characteristics of the fruit [36]. It is thought that once the coordination pattern is acquired, it is well retained. In contrast, the scaling characteristics are not easily retained and the performer may require practice to regain precise control [35]. Given this, we may expect that coordination is retained in the ipsilesional UE after stroke. Indeed, normal coordinated reaching with the ipsilesional UE has been described in studies of a few selected patients [37,38]. In discrete aiming, a normal uninterrupted movement [39,40] and a pattern of movement that is similar to controls [26] were demonstrated by subjects using the ipsilesional UE. In cyclical or continuous movements, coordination may be evaluated by the smooth linking of temporal phases of the movement which creates structural unity [35]. In other words, a continuous movement is not simply a concatenation of multiple discrete movements [41]. In reciprocal aiming,

MT has been partitioned into three temporal phases: (1) the accelerative phase - the time from lift-off from one target to peak velocity; (2) the decelerative phase - the time from peak velocity to target hit; and (3) the dwell phase the time from target-hit to lift-off [42]. Recently it was shown that across numerous practice trials of reciprocal aiming, the percentage of MT spent in each of these temporal phases is the same for adults with right stroke using their ipsilesional UE and controls using either UE [30]. Specifically, in a condition with a high precision requirement (i.e. to a 0.5 cm wide target) 32% of MT is spent in acceleration, 54% in deceleration, and 14% in the dwell phase. In contrast, the percentage of MT spent in the dwell phase is two times longer for those with left stroke using their ipsilesional UE (Fig. 3). It appears that those with left stroke fail to coordinate the phases of reciprocal aiming into a single unit. Each pass from one target to the other is performed in isolation with absolute dwell times on the order of 300 ms, more

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than twice that of all other subjects. The continuous nature of the task is lost and the movement resembles a series of discrete movements. One of the common clinical measures of coordination is the finger-to-nose test. In this test the patient is required to move the outstretched VE to touch the index finger to the nose and then return to an outstretched position. This is repeated a number of times with the eyes closed. Performance deficits in this test have been noted in the ipsilesional VE of those post-stroke [43]. It is arguable, however, that this clinical test does not provide the best characterization of coordinated movement. In summary, the literature suggests that coordination of discrete movements is normal in the ipsilesional VE. Basic patterns of limb coordination remain preserved in functional activities such as reaching or aiming to a single target. However, the coordination of cyclical or continuous movements may be impaired in the ipsilesional VE of those with left stroke. These individuals fail to link the temporal phases of a continuous movement into a single temporal unit. This suggests that the evaluation of the performance of cyclical and continuous functional activities may be particularly important for individuals with left sided stroke. 2.3. Sensory perception It is well known that sensory disturbances contribute to deficits in motor performance. For example, an adult with impaired proprioception due to large-fiber sensory neuropathy is unable to maintain force or position without visual feedback and displays a loss of dexterity in handling small objects [44]. It is reasonable, then, to suspect that performance deficits in the ipsilesional VE could be explained by ipsilesional sensory loss. However, the evidence to support this hypothesis is not compelling. Sensory deficits in the ipsilesional VE in those post-unilateral cerebral lesions have been found in some studies but not in others. Further, within subjects, sensory losses have been reported for some modalities but not others. For example, the ipsilesional hand was found to have normal joint

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proprioception [28,45], two-point discrimination [28,43] and touch/pressure sensation [15,43]. However, in subjects with normal two-point discrimination and touch-pressure, thumb kinesthesia was decreased [43]. Normal ipsilesional twopoint discrimination of the finger and position sense of the finger and forearm were reported by Haaland et al. [19,28]. These same subjects, however, had decreased two-point discrimination on the ipsilesional forearm. A few studies have shown differences in sensory loss in the ipsilesional VE that differed between those with right and left brain damage. Common among them, individuals with right lesions had greater ipsilesional UE sensory loss than those with left lesions. Tactile perception was more affected in those with right compared to left lesions [46,47], and two-point discrimination was decreased for those with right but not left lesions, compared to controls [15]. Similarly, there was a trend toward greater loss of point localization in patients post-right compared to left parietal cortex excision [48]. Ipsilesional elbow kinesthesia in adults with stroke was found to be normal when evaluated by clinical testing but impaired when evaluated by laboratory mechanical testing [49]. There was no effect of lesion side, however there appeared to be a positive relationship between the severity of the contralateral deficit and the severity of the ipsilesional deficit. A similar relationship between the severity of contralateral and ipsilateral sensory deficits has been documented previously [50,51]. Perhaps the most comprehensive sensory evaluation of the ipsilesional VE in recent literature was done by Robertson and Jones [52]. Individuals who were an average of 2-years post-left stroke were included in the experimental group. The left thumb and the left index finger of these individuals were normal in measures of pressure sensitivity, static two-point discrimination, moving twopoint discrimination, and object recognition. In fact, the only ipsilesional sensory deficit noted was that those with left stroke took longer than controls to differentiate between three textured materials. In summary, the literature suggests that ipsile-

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sional sensory loss is minimal, if present at all. Thus, the deficits in sensory-motor control in the ipsilesional UE cannot be explained by the presence of sensory deficits. It should be acknowledged that these aforementioned studies of sensation assess the perception of sensation. Ipsilesional UE sensory deficits may be present that are not uncovered within the constraints of clinical sensory testing. It remains to be seen if more extensive sensory deficits are present, and, if so, if they contribute to the control deficits identified in the ipsilesional UE of those after stroke. 2.4. Strength and muscle activity

A common measure of UE sensory-motor control is grip strength [53]. Most studies have reported that ipsilesional grip strength is preserved [3,16-21,43,54]. Although ipsilesional grip weakness has been reported in adults with right or left stroke, brain trauma, or neoplasm [23], the majority of studies that have reported a loss of ipsilesional grip strength have noted differences due to lesion side. Deficits in ipsilesional grip strength have been documented for individuals with right stroke but not left [24] and right penetrating brain wound but not left [22]. Jones et al. [45] found no statistical difference as a function of lesion side but described a 'marginal' deficit in ipsilateral grip strength in those with right stroke that was apparent 1-2 weeks post-onset but resolved at 1 year. Pinch strength has only been reported in a couple of studies that have looked at ipsilateral performance after cerebral lesion. The results have been mixed, leaving conclusions difficult to draw. Ipsilesional weakness in pinch has been documented by Smutok et al. [22] for those with left, but not right, brain damage. Robertson and Jones [52] included only individuals with left stroke and controls in their study and found no group difference in pinch strength. Jones et al. [45] reported weakness, as measured by the force imparted in turning a steering wheel, in the ipsilesional arm 11 days post-onset; this weakness was still present 1 year later. It should be noted that this study included only

eight individuals post-stroke; an insufficient number to make comparisons by lesion side. In another study, strength of ipsilesional abduction and adduction of the shoulder and flexion and extension of the elbow, wrist, fingers, and thumb was measured in individuals 8 weeks post-stroke. The strength of ipsilesional shoulder adduction was the most affected being 62% of that for controls [54]. When electromyography (EMG) is used to measure change in contralateral UE motor control, the 'normal' EMG activity of the ipsilesional UE may be used for comparison [55,56]. However, Hammond et al. [57] found that recruitment and termination times as measured from EMG during rapid ipsilesional wrist flexion and extension were affected after stroke. Specifically, there was a trend for the timing of the ipsilesional EMG to be 'intermediate' between contralateral and control values. In summary, the extent and magnitude of ipsilesional weakness after stroke are poorly defined. Ipsilesional UE weakness has been found in some, but not all, studies. Evidence exists that ipsilesional grip strength is affected in adults with right, but not left, cerebral lesions. There is, however, a paucity of literature describing proximal ipsilesional strength. Thus differences in results between studies and the absence of comprehensive strength evaluations of the ipsilesional UE make conclusions difficult to draw. At best, the normalcy of ipsilesional strength should be suspect. Careful evaluation of strength with comparisons to normative data, whenever possible, may prove the best strategy to defining strength deficits in the ipsilesional UE. 2.5. Clinical assessments of UE impairment and function

Sensory-motor control deficits in the ipsilesional UE often are not revealed through standard clinical testing. In fact, clinical tests of impairment such as the Fugl-Meyer Assessment [58] are usually not designed to identify deficits in the ipsilesional UE and, if the ipsilesional UE is tested, the scores may be used only for baseline

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comparisons. Further, gross measures of impairment or function are not sensitive to ipsilesional UE sensory-motor control deficits [22]. A common trait of those clinical tests that reveal ipsilesional performance deficits is that they assess speed of performance, using time to completion as the outcome measure. The Jebsen test is an UE assessment that was established to assess unilateral hand function in common activities [59]. It includes seven sub-tests, and the performance of each hand is timed in each subtest. In a study of ipsilesional performance on the Jebsen test of adults after stroke compared to controls, those with left stroke had prolonged MTs in five of the seven sub-tests; those with right stroke had prolonged MTs in two of the seven sub-tests [60]. Robertson and Jones [52] indicated that ipsilesional deficits were revealed by the Jebsen test although statistical analyses of these data were not included. Spaulding et a1. [61] found that those with stroke were slower with their ipsilesional UE compared to a normative data base in 27 of 28 comparisons within the Jebsen test. An effect of lesion side was only found in the writing sub-test, however, this comparison was made between those with left and those with right stroke. Thus, those with left stroke were slower using their non-dominant VE compared to those with right stroke using their dominant VE. Further, the results of this study must be examined cautiously because, as the authors acknowledge, multiple t-tests were used, creating a risk for Type II errors. Another common clinical VE functional test that uses time as a measure is the pegboard test. Although procedural variations exist, the general requirement is that the client move pins within a pegboard as fast as possible. Ipsilesional slowing in this task has been reported for those with cerebral damage regardless of the side of damage [3,15,18,19,22,43,62] or only for those with left hemisphere damage [16]. In an exception to these reports, however, ipsilesional slowing was not evident in a pegboard task in a comparison of 30 control subjects, 12 subjects with pre-motor cortex lesions, and two subjects with primary motor cortex lesions [21]. Other clinical tests that measure time to completion and have revealed ipsilesional deficits are

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the Box and Block test and the Upper Extremity Performance Evaluation Test for the Elderly [43] or the Test d'e'valuation des membres supe'rieurs des personees age'es (TEMPA). In the TEMPA only two of the four unilateral test components revealed ipsilesional slowing, specifically picking up a pitcher and pouring water into a glass and handling coins. A difference between those with right and left stroke was not evident, however, the sample size was too small to make lesion-side comparisons [43]. Ipsilesional slowing, with a tendency toward greater slowing compared to controls for those with left stroke, has been reported in other tests of manual dexterity such as the Minnesota Rate of Manipulation test and the O'Connor Finger and Tweezer Dexterity test [62]. In summary, clinical tests of UE function after brain damage are primarily designed to assess the contralateral VE. However, functional tests that measure speed of performance are sensitive to ipsilateral VE deficits. Compared to controls, the ipsilesional performance of adults with unilateral brain damage is slower in these timed tasks. There is some evidence that individuals with left sided lesions have more profound ipsilesional slowing than those with right sided lesions. 3. Considerations in applying research findings to the clinic Extrapolating results of research into the clinical domain is not an easy task. The clinician may wonder, will all stroke survivors have ipsilesional sensory-motor deficits, and if so, what components of control will be most affected? What should be expected? What if a client looks different than what the research has shown regarding ipsilesional deficits? In this light, there are a number of considerations. First, it should be kept in mind that the presence or absence of ipsilesional deficits is calculated using averaged group data. Group differences may not be significant, but this does not preclude a number of subjects within the sample population from demonstrating an ipsilesional deficit. For example, ipsilesional pressure sensation was normal in individuals with left lesions compared to controls as revealed from an Analy-

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sis of Variance using the median scores [15]. However, 50% of those with left lesions had ipsilesional pressure sensation deficits, defined by a score greater than 2.6 S.D. units from the mean of the control group. Second, inherent in the study of humans with pathology, there is a great deal of variability within the subject population. Within a study and between studies, subjects vary in the type of brain damage, the extent of the damage, the location of the damage, and the time since onset. Individual studies may attempt to control for some of these sources of variance. For example, Smutok et a1. [22] had a very circumscribed population of veterans, including only adults who were about 14 years post a penetrating brain injury. Other studies include individual descriptions of subjects regarding lesion location [4]. However, due to differences between studies, interpretation of findings across studies must be done with caution. On the other hand, when similar results are found among a number of studies, even in the presence of differences in subject samples, one can argue that the findings are quite robust. 4. Implications of ipsilesional deficits for physical rehabilitation Do ipsilesional deficits affect rehabilitation outcome after stroke? If so, it is logical to suggest that treatment should include interventions focused on these deficits. In a study of functional and motor recovery in 75 individuals post-stroke, Olsen [63] concluded that rehabilitation should focus on the ipsilesional as well as the contralateral extremities. Functional gains in UE activities have been observed in individuals whose contralateral VE remained useless [63-66], suggesting that improved ipsilesional control was responsible for greater functional independence. Individuals post-severe stroke may remain dependent in feeding and upper body dressing, tasks that should be possible with one arm and appropriate utensils [67]. A decrease in ipsilesional function is likely present and contributes to these functional deficits [63]. While numerous factors may contribute to compromised function of the ipsilesional VE including sensory-motor control

deficits, cognitive deficits, and depression, some have argued that training of the ipsilesional VE should be integrated into rehabilitation programs [62]. This may be particularly important for righthand dominant adults with left stroke who must train their non-dominant VE. In addition, it is possible that gains made in sensory-motor control in the ipsilesional UE may transfer to the contralateral VE, however this remains an empirical question. Does the side of lesion affect rehabilitation outcome after stroke? In a study which examined long-term ipsilesional deficits (i.e. 14 years after onset), there were no differences in functional outcome between those with right and left brain damage [22]. Other studies that have examined the relationship between lesion side and outcome have focused on contralateral deficits with little information about ipsilesional performance. In this literature, some studies have found that lesion side did not affect functional outcome [67-71], and others have found that individuals with right sided cerebral lesions had less favorable outcomes than those with left sided lesions [72-74]. Alexander [74], using a standardized and reliable indicator of disability outcome (Functional Independence Measure, FIM), reported an interaction between the FIM score at admission and the side of lesion. V sing the change in FIM score from admission to discharge (discharge FIM score minus admission FIM score) as the dependent measure, Alexander found that there was less change in FIM scores for those with right hemisphere stroke compared to those with left hemisphere stroke in the lowest admission FIM group (Fig. 4). Previous findings relating right hemisphere stroke with deficits in feedback-based motor control provide a plausible post-hoc explanation for this. In as much as the majority of motor activities scored on the FIM are primarily feedback-based tasks (they are guided by feedback from the moving limb and vision), an initial low capability in this area (low admission FIM) could be particularly difficult to overcome in those with a lesion in the area demonstrating feedback-based control specialization (i.e. right hemisphere). The clinical implication is that stroke subjects with a low admission FIM and a

P.S. Pohl et al. ! NeuroRehabilitation 9 (1997) 57-69

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This may be especially true in those stroke survivors who regain little use of the contralateral UE. Persistent, subtle sensoty-motor control deficits in the ipsilesional UE may retard independent function. Further, if the control deficits that are unmasked in the ipsilesional UE are also present in the hemiparetic UE, interventions which integrate training of the ipsilesional UE may improve the function of both UEs. While this proposal is intuitively appealing, further research is needed to test its efficacy. References

< 40

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61-80

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Fig. 4. Average Functional Independent Measure (FIM) change by stroke side and admission FIM class (adapted from Alexander).

right hemisphere lesion might benefit from training specifically emphasizing visual-spatial skills. The potential interaction of initial stroke severity, lesion side, and treatment intervention on functional outcomes is an important future research agenda. As aforementioned, a deficit in sensoty-motor control is only one factor that may contribute to compromised function of the ipsilesional UE. A comprehensive rehabilitation program should include, but certainly not restrict itself to, evaluation and treatment of sensoty-motor control in individuals after stroke. In addition to side-related sensoty-motor deficits of the ipsilesional VE, side-related cognitive deficits have been shown in individuals after stroke. For example, there is evidence to suggest that the right hemisphere has a specialized role in attention [75]. Functional deficits often reflect a complex interaction of sensoty-motor and cognitive skills. It may be argued that the optimal therapeutic regime provides the patient with experiences that focus on the interaction of sensoty-motor and cognitive deficits. As some have suggested, this may best be done by providing functional experiences in meaningful environments [76]. In summaty, ipsilesional VE performance deficits arguably impact rehabilitation outcomes.

[1) Brust JCM. Stroke: diagnostic, anatomical, and physiological considerations. In: Kandel ER, Schwartz JH, editors. Principles of neural science. NY: Elsevier! North-Holland, 1981:667-679. [2) Kimura D, Archibald Y. Motor functions of the left hemisphere. Brain 1974;97:337-350. [3) Haaland KY, Harrington D. The role of the hemispheres in closed loop movements. Brain Cognit 1989;9:158-180. [4) Winstein CJ, Pohl PS. Effects of unilateral brain damage on the control of goal-directed hand movements. Exp Brain Res 1995;105:163-174. [5) Carmon A. Sequenced motor performance in patients with unilateral cerebral lesions. Neuropsychologia 1971;9:445-449. [6) Haaland KY, Yeo RA. Neuropsychological and neuroanatomic aspects of complex motor control. In: Bigler ED, Yeo RA, Turkheimer E, editors. Neuropsychological function and brain imaging. NY: Plenum, 1989:219-244. [7) Colebatch JG, Dieber MP, Passingham RE, Friston KJ, Frackowiak RSJ. Regional cerebral blood flow during voluntary arm and hand movements in human subjects. J Neurophysiol 1991;65:1392-1401. [8) Dieber MP, Passingham RE, Colebatch JG, Friston KJ, Nixon PD, Frackowiak RSJ. Cortical areas and the selection of movement: a study with positron emission tomography. Exp Brain Res 1991;84:393-402. [9) Winstein CJ, Grafton ST, Pohl PS. Motor task difficulty and brain activity: an investigation of goal-directed reciprocal aiming using positron emission tomography (PET). J NeurophysioI1997;77:1581-1594. (10) Kim S-G, Ashe J, Hendrich K, Ellermann JM, Merkle H, Ugurbil K, Georgopoulos AP. Functional magnetic resonance imaging of motor cortex: hemispheric asymmetry and handedness. Science 1993;261:615-617. [11) Liepmann H. Motor aphasia, anarthria, and apraxia. Trans. 17th Int. Congr. Med. 1913 Section XI, Pt 2:97-106. [12) Woodworth RS. The accuracy of voluntary movement. Psychol Rev 1899;3:2, whole No. 13.

68 [13]

[14] [15]

[16]

[17] [18]

[19]

[20]

[21]

[22]

[23]

[24]

[25] [26]

[27]

[28]

[29] [30]

[31]

P.S. Pohl et al. / NeuroRehabilitation 9 (1997) 57-69 Roy EA, Kalbfleisch L, Elliott D. Kinematic analysis of manual asymmetries in visual aiming movement. Brain Cognit 1994;24:289-295. Schmidt RA. Motor control and learning. 2nd ed. IL: Human Kinetics, 1988. Vaughan Jr HG, Costa LD. Performance of patients with lateralized cerebral lesions. II: Sensory and motor tests. J Nerv Ment Dis 1962;134:237-243. Haaland KY, Cleeland CS, Carr D. Motor performance after unilateral hemisphere damage in patients with tumor. Arch Neurol 1977;34:556-559. Kimura D. Acquisition of a motor skill after left-hemisphere damage. Brain 1977;100:527-542. Haaland KY, Delaney HD. Motor deficits after left or right hemisphere damage due to stroke or tumor. Neuropsychologia 1981;19:17-27. Haaland KY, Harrington D, Yeo R. The effects of task complexity in left and right CVA patients. Neuropsychologia 1987;25:783-794. Haaland KY, Harrington D. Limb-sequencing deficits after left but not right hemisphere damage. Brain Cognit 1994;24:104-122. Halsband U, Ito N, Tanji J, Freund H-J. The role of premotor cortex and the supplementary motor area in the temporal control of movement in man. Brain 1993;116:243-266. Smutok MA, Grafman J, Salzar AM, Sweeney JI

Sensory-motor control in the ipsilesional upper extremity after stroke.

There is substantial evidence to indicate that sensory-motor control of the ipsilesional upper extremity (UE) in adults after unilateral stroke is abn...
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