62
ORIGINAL ARTICLE
Functional Significance of Ipsilesional Motor Deficits After Unilateral Stroke Caitilin Chestnut, MD, Kathleen Y. Haaland, PhD ABSTRACT. Chestnut C, Haaland KY. Functional significance of ipsilesional motor deficits after unilateral stroke. Arch Phys Med Rehabil 2008;89:62-8. Objective: To determine whether ipsilesional motor skills, which have been related to independent functioning, are present chronically after unilateral stroke and are more common in people with apraxia than in those without apraxia. Design: Observational cohort comparing the performance of an able-bodied control group, stroke patients with left- or right-hemisphere damage matched for lesion volume, and lefthemisphere stroke patients with and without ideomotor limb apraxia. Setting: Primary care Veterans Affairs and private medical center. Participants: Volunteer right-handed sample; stroke patients with left- or right-hemisphere damage about 4 years poststroke; a control group of demographically matched, ablebodied adults. Interventions: Not applicable. Main Outcome Measures: Total time to perform the (1) Williams doors test and the (2) timed manual performance test (TMPT), which includes parts of the Jebsen-Taylor Hand Function Test. Results: Ipsilesional motor deficits were present after left- or right-hemisphere stroke when using both measures, but deficits were consistently more common in patients with limb apraxia only for the TMPT. Conclusions: These findings add to a growing literature that suggests that ipsilesional motor deficits may have a functional impact in unilateral stroke patients, especially in patients with ideomotor limb apraxia. Key Words: Apraxia, ideomotor; Motor skills; Rehabilitation; Self care; Stroke. © 2008 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation ODERATE LIMITATIONS IN motor function affect 40% of stroke patients, and between 15% and 30% have M a severe motor disability. A majority of stroke patients report 1
that movement deficits have the greatest functional impact relative to other deficits.2 Contralateral motor deficits are emphasized after unilateral stroke, but there is also evidence that
From the University of New Mexico School of Medicine, Albuquerque, NM (Chestnut, Haaland); and Research Service & Behavioral Health Care Line, New Mexico VA Healthcare System, Albuquerque, NM (Haaland). Supported by a U.S. Department of Veterans Affairs Medical Merit Review Grant. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the author(s) or upon any organization with which the author(s) is/are associated. Reprint requests to Kathleen Y. Haaland, PhD, Behavioral Healthcare Line, NMVAHCS, 1501 San Pedro SE, Albuquerque, NM 87108, e-mail: khaaland@ unm.edu. 0003-9993/08/8901-00197$34.00/0 doi:10.1016/j.apmr.2007.08.125
Arch Phys Med Rehabil Vol 89, January 2008
more subtle ipsilateral deficits are present after damage to the left or right hemisphere.3-5 Some studies6-8 have found that ipsilesional deficits affect activities of daily living (ADLs), suggesting that they may influence the stroke patients’ ability to function independently. The importance of ipsilesional motor deficits in daily functioning is of particular clinical importance for patients who must use their ipsilesional limb because of hemiplegia because they use their ipsilesional limb 3 to 6 times more frequently than their contralesional limb.9 Despite the apparent practical importance of ipsilesional arm skills, little is known about its functional impact. Ipsilesional motor deficits after left- or right-hemisphere damage can be comparable3,10 or different.11-13 Although complex psychomotor skills are similarly impaired after left- or right-hemisphere damage,3,10 other motor tasks are differentially impaired after left- or right-hemisphere damage. For example, left-hemisphere damage often produces motor deficits, such as limb apraxia, impaired motor sequencing,14,15 and impaired rapid ballistic movements.16 In contrast, right-hemisphere damage often produces deficits in movements that require precise target localization16,17 with associated increases in final error.18 However, the functional relevance of these hemispheric asymmetries is unclear because most daily activities require various aspects of movement, some of which are controlled primarily by the right hemisphere and others are controlled primarily by the left hemisphere. Therefore, in most complex daily skills, one would expect comparable functional deficits after left- or right-hemisphere damage but potentially for different reasons. Few studies have examined the functional implications of ipsilesional deficits, but those that have usually report comparable ipsilesional deficits on functional tasks after left- or right-hemisphere damage. One study19 reported greater ipsilesional functional deficits after left- than right-hemisphere damage in acute stroke patients when errors were examined but comparable ipsilesional deficits when time was measured. Other studies7,19-21 have reported comparable ipsilesional deficits on functional tasks after left- or right-hemisphere damage. Several of these studies7,19 have shown that deficits were greater for left-hemisphere damage patients with limb apraxia and/or limb apraxia was the best predictor of daily activities after left- but not right-hemisphere damage. These results were in agreement with an earlier study8 that examined daily functioning not restricted to the ipsilesional limb and also emphasized the importance of limb apraxia as the best predictor of functioning after left-hemisphere damage but not right-hemisphere damage. We now examine this issue by using a motor sequencing task, the Williams doors test, and the timed manual performance test (TMPT), which is a combination of the Williams doors test and 5 items from the Jebsen-Taylor Hand Function Test (JTHFT). The TMPT has been shown to be an indicator of additional health care use and dependency in a large group of geriatric patients with multiple diagnoses.22,23 The purpose of this study was to determine (1) if left- and right-hemisphere damage produce ipsilesional deficits on these 2 measures, similar to previous findings by using some of the same simulated ADLs,7,19-21 and (2) if left-hemisphere damage patients with
63
IPSILESIONAL DEFICITS AFTER STROKE, Chestnut
limb apraxia show greater deficits than those who are not apraxic when lesion volume is controlled. Importantly, lesion location is also measured to ensure that performance differences between the left- and right-hemisphere– damage stroke groups cannot be attributed to intrahemispheric lesion location differences. METHODS Participants We examined 114 right-handed subjects, 31 patients with left-hemisphere damage caused by stroke, 21 patients with right-hemisphere damage caused by stroke, and 62 able-bodied control subjects (38 who performed with their left hand, 24 who performed with their right hand). The control subjects were volunteers recruited by advertisement, and their medical history and demographic measures were obtained from selfreport. Patients were included in the study if they had a radiologically confirmed stroke that damaged either the right or left cerebral cortex. Exclusion criteria included (1) neurologic diagnosis other than stroke; (2) neuroradiologic evidence of damage to the brainstem, cerebellum, or both hemispheres; (3) major psychiatric diagnosis; (4) hospitalization for substance abuse or dependence; or (5) peripheral neurologic disorders affecting sensation or movement of upper extremities. Control participants were excluded for the same reasons as well as any evidence of stroke. Informed consent was obtained from all study participants according to the Declaration of Helsinki, and the study was approved by the local institutional review board. In the group of patients with left-hemisphere damage, 11 were classified as apraxic and 20 as nonapraxic based on a wellvalidated battery.24 Demographic and descriptive features of the groups are presented in tables 1 and 2. Measures The neuropsychologic data obtained for all groups included ideomotor limb apraxia,24 aphasia (Western Aphasia Battery [WAB]25), spatial ability,26,27 and right and left motor ability Table 1: Demographic, Neurologic, and Neuropsychologic Variables for All Groups Characteristics
Control (n⫽62)
Age (y) Female sex, n (%) Education (y) Years poststroke Lesion volume (mL) Limb apraxia errors储 Aphasia quotient储 Spatial index储 Right motor index储 Left motor index储
64.6⫾12.0 27 (44) 14.5⫾2.4 NA NA 1.4⫾1.1 98.9⫾1.0§ 49.9⫾7.6 46.6⫾6.7 46.7⫾7.0
Left-Hemisphere Right-Hemisphere Damage (n⫽31) Damage (n⫽21)
60.6⫾12.4 6 (19) 13.7⫾3.5 5.1⫾6.6 77.1⫾78.3 3.0⫾2.5†¶ 76.1⫾29.6†¶ 45.2⫾10.5*¶ 28.0⫾16.8†¶ 45.7⫾7.5
66.6⫾11.9 9 (43) 13.6⫾2.8 4.2⫾3.9 98.2⫾127.3 1.5⫾1.5 97.3⫾2.8 36.3⫾13.8*‡¶ 42.4⫾8.9¶ 31.4⫾19.3‡¶
NOTE. Values are mean ⫾ standard deviation (SD) or as indicated. Spatial and motor indices are expressed as T scores with mean of 50 and an SD of 10 relative to the normative sample. Abbreviation: NA, not applicable. *One patient had missing data. † Left-hemisphere damage impaired relative to right-hemisphere damage (P⬍.05). ‡ Right-hemisphere damage impaired relative to left-hemisphere damage (P⬍.05). § Two subjects had missing data. 储 Significant group difference across 3 groups using ANOVA (P⬍.001). ¶ Impaired relative to control group.
Table 2: Demographic, Neurologic, and Neuropsychologic Variables for Able-Bodied Control and Left-Hemisphere–Damage Apraxic and Nonapraxic Groups Characteristics
Control (n⫽62)
Apraxic (n⫽11)
Nonapraxic (n⫽20)
Age (y) Female sex, n (%) Education (y) Years poststroke Lesion volume (mL3) Limb apraxia errors§ Aphasia quotient§ Spatial index§ Right motor index§储 Left motor index§
64.6⫾12.0 27 (44) 14.5⫾2.4 NA NA 1.4⫾1.1 98.9⫾1.0‡ 49.9⫾7.6 46.6⫾6.7 46.7⫾7.0
65.0⫾7.9 2 (18) 13.5⫾3.6 5.2⫾5.8 112.6⫾99.4 5.7⫾1.8†储 58.2⫾31.6†储 41.9⫾11.3储 25.3⫾17.0储 41.7⫾5.7
58.2⫾14.0 4 (20) 13.9⫾3.5 5.0⫾7.2 57.6⫾57.9 1.5⫾1.1 85.9⫾23.9储 47.0⫾9.9* 29.5⫾16.9储 47.8⫾7.6
NOTE. Values are mean ⫾ SD or as indicated. Spatial and motor indices are expressed as T scores with mean of 50 and an SD of 10 relative to the normative sample. *One patient had missing data. † Apraxic group impaired relative to nonapraxic group (P⬍.05). ‡ Two subjects had missing data. § Significant group difference across 3 groups using ANOVA (P⬍.002). 储 Impaired relative to control group.
(composite scores based on the mean standard score by using published normative data) for grip strength and finger tapping.28 The WAB25 is a well-known test of language (including language expression, auditory comprehension, confrontation naming). The spatial composite was comprised of the mean of standard T scores (based on the control group) for 3 tests: the block design subtest from the Wechsler Adult Intelligence Scale–Revised,26 which requires the construction of designs with blocks, and 2 tests of visual perception (facial recognition and judgment of line orientation tests),27 which require matching faces or the orientation of lines. The motor indices were based on the mean T score (derived from published normative data29) of finger tapping and grip strength for each arm. Grip strength was the maximum grip across 2 trials measured with a Smedley hand dynamometer, and the finger tapping score was based on the mean tapping rate of a telegraph key across five 10-second trials. Ideomotor limb apraxia was assessed by a published test with demonstrated interrater reliability30,31 that assesses the imitation of 15 gestures (5 meaningless, 5 intransitive movements [eg, gesture for “okay”], 5 transitive movements [eg, brush teeth]). When errors in internal hand position (eg, fist vs palm flat), hand orientation (eg, vertical vs horizontal), target (eg, brush nose, not teeth), and/or body part as object (eg, extend index finger to brush teeth) occurred, the item was scored as incorrect. Thus, more than 1 type of error could be made on a single gesture, but only 1 error per gesture was scored. Patients were considered apraxic if they made such errors on 4 or more of the 15 movements (2 standard deviations [SDs] greater than the healthy control group). The task was videotaped for later consensus scoring by 2 raters. Lesion size and location. Either magnetic resonance imaging (MRI) (Siemensa or Pickerb 1.5-T machines) or computed tomography (CT) scans (Siemens or Picker machines) were obtained at least 3 months poststroke. MRIs were obtained in 48 of the stroke patients, and CT scans were obtained in 4 of the stroke patients who had medical contraindications for MRI. CT slice thickness was 10mm without gaps between slices. MRI slice thickness was 10mm with a slice gap of 1.5 or 2mm. The lesion location was determined by a blinded Arch Phys Med Rehabil Vol 89, January 2008
64
IPSILESIONAL DEFICITS AFTER STROKE, Chestnut
ning when the examiner said “go” and stopping when the last door was closed. Timed manual performance test. This measure includes the Williams doors test and 5 items from the JTHFT.36 Subjects were timed as they (1) wrote a short sentence; (2) turned over five 3⫻5 cards; (3) picked up 2 paper clips, pennies, and bottle caps and placed them in an empty can; (4) stacked 4 checkers; and (5) transferred 5 kidney beans from the tabletop to a coffee can by using a spoon to simulate eating. The entire JTHFT data have been published previously.7
Fig 1. Williams doors test.
board-certified neurologist from T1-weighted MRI images for anatomic detail and T2-weighted images to specify lesion borders. These tracings were performed on 11 standardized MRI or CT horizontal sections based on the DeArmond atlas.32 Tracings were retraced and loaded into a computer program that used an algorithm to calculate lesion volume and location within each hemisphere.33 Williams doors test. The apparatus for this test is displayed in figure 1. The dependent measure is the total time to open and close 9 doors with various latches and handles with the ipsilesional limb only. This differs from previous studies, which measured the time for opening and closing each door separately and then summed those times or measured the repeated opening and closing of 1 door only.19 In addition, in some previous studies, subjects were allowed to perform the door task with 1 or both hands whichever way the subject believed would be most efficient,22,23,34 and in some only the dominant hand was used.35 Sequencing ability is emphasized in our modification by measuring the total time to open and close all 9 doors without stopping. All participants were asked to open and close all 9 doors in sequence as rapidly as possible. No practice was allowed. In the stroke patients, the speed of the ipsilesional limb was measured, and in the control group the left hand was assessed in 38 subjects and the right hand was assessed in 24. Time was measured by the examiner with a stopwatch begin-
Data Analysis First, demographic and clinical characteristics of the groups were examined by using analyses of variance (ANOVAs) or t tests for continuous variables and chi-square tests for nominal variables. We used t tests to show that there were no significant differences in the door scores between the 2 control groups who used their left or right hand. We then pooled the data from the 2 for comparison with the left- and right-hemisphere– damage stroke groups. To determine if there were group differences on the Williams test and the TMPT, we used 4 separate univariate ANOVAs to compare (1) the performance of the control and left- and right-hemisphere– damage groups and (2) the performance of the left-hemisphere– damage apraxic and nonapraxic groups and the control group for each measure. The Tukey least significant difference method was used for post hoc comparisons. When there were significant differences between the right- and left-hemisphere– damage groups or between the apraxic and nonapraxic groups, we performed analyses of covariance (ANCOVAs) controlling for lesion volume. In some cases, we also compared the incidence of deficits across groups using the chi-square test. RESULTS Hemispheric Differences Participant characteristics. There were no significant differences in age or education among the 3 groups (see table 1). There was a marginal sex difference across the groups with fewer women in the left-hemisphere– damage group relative to the right-hemisphere– damage and control groups with borderline significance (2 test⫽5.6, P⫽.06). However, performance on the door task did not differ significantly between the men and women in the control group, suggesting that sex should not explain any group differences in these measures. Lesion vol-
Fig 2. The overlap of lesions in stroke patients who have lefthemisphere damage (left side of sections) or right-hemisphere damage (right side of sections). Eight axial sections from the DeArmond atlas are displayed. Percentage of overlap is designated by colored bar to the right.
Arch Phys Med Rehabil Vol 89, January 2008
65
IPSILESIONAL DEFICITS AFTER STROKE, Chestnut
Fig 3. The mean time to open and close the 9 doors on the Williams doors test and to perform the TMPT for the control, lefthemisphere– damage (LHD), and right-hemisphere– damage (RHD) groups. Standard error bars displayed.
right motor index (P⬍.001) relative to the right-hemisphere– damage and the healthy control groups. The contralesional motor indices were comparable between the right- and left-hemisphere– damage groups. As can be seen in figure 3, Williams doors test performance differed across the 3 groups (F2,111⫽18.9, P⬍.001) with impairment for both the left- (P⬍.001) and right-hemisphere– damage (P⬍.001) groups relative to the control group but not relative to each other (P⫽.211). The pattern of results was the same for the TMPT (F2,111⫽21.9, P⬍.001) with both stroke groups performing worse than the control group (P⬍.002) but not relative to each other (P⫽.197). As can be seen in table 3, the incidence of impairment (2 SDs below the control group mean) data were more sensitive to group differences in the direction of the mean data in figure 3; for the Williams test, the incidence of impairment was significantly greater in the rightthan the left-hemisphere– damage group (2 test⫽8.3, P⬍.01), and for the TMPT there was marginal evidence for a higher incidence of impairment in the left-hemisphere– damage group (2 test⫽ 3.2, P⫽.074).
ume and years after a cerebrovascular accident (CVA) also did not differ significantly between the left- and right-hemisphere– damage groups (fig 2). In addition, the percentage of lefthemisphere– damage patients with anterior (19%), posterior (42%), and anteroposterior (39%) lesions and the percentage of right-hemisphere– damage patients with anterior (38%), posterior (33%), and anteroposterior (33%) lesions did not differ significantly (2 test⫽2.24, P⫽.325). The arterial distribution of the damage caused by stroke did not differ significantly between the left- and right-hemisphere– damage groups (2 test⫽3.31, P⫽.343) although most were in the middle cerebral artery territory (right-hemisphere damage, n⫽17 [81%]; lefthemisphere damage, n⫽29 [94%]). Finally, the incidence of cortical (right-hemisphere damage, 52%; left-hemisphere damage, 45%) and cortical plus subcortical (right-hemisphere damage, 48%; left-hemisphere damage, 55%) damage was comparable between the 2 groups (2 test⫽.26, P⫽.609), and intrahemispheric lesion location was fairly comparable across the 2 groups although the right-hemisphere– damage group showed a somewhat higher incidence of damage to motor and inferior parietal areas (see fig 2). Group differences on all other descriptive measures were in the expected direction. Significant differences were found among the 3 groups for limb apraxia (F2,111⫽9.83, P⬍.001), the aphasia quotient (F2,109⫽23.24, P⬍.001), the spatial index (F2,109⫽14.93, P⬍.001), the right motor index (F2,111⫽31.41, P⬍.001), and the left motor index (F2,111⫽17.73, P⬍.001). The pattern of these differences are summarized in table 1 with right-hemisphere– damage group impairment for the spatial index (P⬍.007) and the left motor index (P⬍.001) relative to the left-hemisphere– damage and the healthy control groups. The left-hemisphere– damage group was impaired for limb apraxia (P⬍.008), the aphasia quotient (P⬍.001), and the
Limb Apraxia Participant characteristics. When the left-hemisphere– damage apraxic and nonapraxic groups were compared with the control group, there were no significant differences in age or education among the 3 groups (see table 2). Sex differences were marginally significant (2 test⫽5.3, P⫽.07), with a tendency for a higher percentage of men than women in both the apraxic and nonapraxic groups relative to the control group. As noted earlier, there were no sex differences in the control group on the door task, suggesting that sex differences were not likely to account for group differences on this task. Lesion volume and years post-CVA, the spatial index, and the right and left motor indices did not differ significantly between the apraxic and nonapraxic groups. However, the apraxic group was more aphasic than the nonapraxic group (P⬍.001). As can be seen in figure 4, Williams doors test performance differed significantly across the 3 groups (F2,90⫽13.00, P⬍.001). Both the apraxic group (P⬍.001) and the nonapraxic group (P⬍.02) performed significantly worse than the control group, but the apraxic group’s performance was only marginally (P⫽.083) worse than the nonapraxic group. Although lesion volume did not differ significantly between the 2 groups, it is still possible that this finding could be caused by the apraxic groups’ larger absolute lesion volume. Therefore, we covaried lesion volume in an ANCOVA, which showed that there were no significant differences between the apraxic and nonapraxic group (F2,28⫽2.5, P⫽.127). To examine this marginal finding in another way, we compared the percentage of patients who were impaired (2 SDs below the control group mean) in each group. We again found evidence of only marginal differences between the apraxic and nonapraxic groups with impairment in 55% of the apraxic group and 25% of the nonapraxic group (2 test⫽2.7, P⫽.10), suggesting that per-
Table 3: Percentage of Impaired (2 SDs below the control group mean) Patients in Each Group Test
RHD (n⫽21)
LHD (n⫽31)
P*
Nonapraxic (n⫽20)
Apraxic (n⫽11)
P*
Williams doors test TMPT
76 24
36 48
⬍.001 .074
25 25
55 91
.10 ⬍.001
NOTE. Values are percent. Abbreviations: LHD, left-hemisphere damage; RHD, right-hemisphere damage. *Based on the chi-square test comparing the incidence of impaired and unimpaired performance for each of the 4 comparisons.
Arch Phys Med Rehabil Vol 89, January 2008
66
IPSILESIONAL DEFICITS AFTER STROKE, Chestnut
Fig 4. The mean time to open and close the doors on the Williams doors test and to perform the TMPT for the control group and the left-hemisphere– damaged apraxic and nonapraxic groups. Standard error bars displayed.
formance differences between these 2 groups were not statistically reliable (see table 3). TMPT performance also differed significantly across the 3 groups (F2,90⫽31.13, P⬍.001). Similar to the Williams doors test, TMPT performance was poorer for both the apraxic (P⬍.001) and nonapraxic (P⬍.001) groups relative to the control group. However, contrary to the door analyses, performance of the apraxic group was poorer than performance of the nonapraxic group (P⬍.005). In addition, the apraxic group continued to perform worse than the nonapraxic group when lesion volume was entered as the covariate in an ANCOVA (F1,28⫽4.6, P⬍.05). Finally, as can be seen in table 3, the incidence of impairment showed a similar pattern with a significantly higher incidence in apraxics than nonapraxics (2 test⫽12.3, P⬍.001). DISCUSSION Understandably, most of the previous studies37-39 have emphasized the influence of the contralesional limb on functional outcome after stroke. Our study shows that comparable ipsilesional deficits are present after left- or right-hemisphere damage caused by stroke on a motor task that has been related to functional independence.22,23 The same pattern of findings was found whether the Williams doors test was used alone or in combination with 5 simulated ADLs (TMPT); however, when we examined impairment incidence, there was evidence of greater right-hemisphere– damage impairment on the Williams doors test. Because the incidence figures could not be corrected for lesion volume differences, we are concerned that this may explain the different pattern of results. However, the lesion volume differences between the impaired and unimpaired groups were not statistically greater in the right- than left-hemisphere– damage groups when using either parametric (ANOVA) or nonparametric (Mann-Whitney U) analyses. For example, mean lesion volumes ⫾ SD for the right-hemisphere– damage impaired and unimpaired groups were 119.2⫾139.5 and 30.9⫾26.0mL3, respectively, whereas for the left-hemisphere– damage group, they were 70.9⫾59.4 and 80.5⫾88.3 for the impaired and unimpaired groups, respectively. These findings emphasize the potential importance of lesion volume effects in studies such as this. Arch Phys Med Rehabil Vol 89, January 2008
Therefore, although the incidence findings argue for greater impairment in the right- than the left-hemisphere– damage group on the Williams test, at this point it is most reasonable to rely on the initial analyses that show comparable deficits in both stroke groups. Most importantly, our results add to a growing literature6,7,19-21,40,41 suggesting that ipsilesional deficits after stroke have a functional impact. The current study is important because we show these findings in chronic left- or right-hemisphere stroke patients (mean years poststroke, 4 –5y) for whom lesion volume and location was comparable and controlled statistically. Other studies have not provided that information, which makes it difficult to know if the results might be influenced by such differences. Our findings are consistent with several other studies7,19-21 that have found comparable functional deficits after left- or righthemisphere damage. It is inconsistent with a previous study19 that used a composite measure that included a significant modification of the Williams doors test in which 1 door instead of 9 doors was used, the doors were opened and closed 3 times, and the writing task on the JTHFT was excluded. They found that acute stroke patients with left-hemisphere damage were significantly slower than those with right-hemisphere damage. Although our results show that the absolute time to complete the TMPT was greater in the left-hemisphere– damage than the right-hemisphere– damage group, the group differences were not statistically significant. Whether the differences are related to stroke chronicity, other differences between the 2 stroke groups, the dependent measures used, or potential differences in lesion size, lesion location, or both is not certain. This previous study19 emphasizes the potential utility of using an error analysis to identify different underlying mechanisms for deficits after right- or left-hemisphere damage. We did not examine error, which is a potential limitation because qualitative information about the types of errors that result in less efficient and potentially slower performance could help us understand the underlying mechanisms of performance on these tasks, as it has done with ideomotor limb apraxia studies24,42,43 and studies of sequencing.44-46 Our finding that the left-hemisphere– damage apraxic group performed marginally worse than the nonapraxic group (even with comparable ages and lesion volumes) on the Williams doors test was similar in direction but not degree to our previous findings46 that showed sequencing deficits in apraxics relative to nonapraxics. This difference in degree is likely related to the previous study’s use of an experimental paradigm that differentiated planning and implementation deficits and found particularly strong evidence for planning deficits in limb apraxics relative to nonapraxics. In contrast, the current study used a gross measure of sequencing, and, although the sequences were composed of different movements, we did not separate planning and implementation deficits and we did not compare performance on different types of sequences. In the previous study, deficits in the apraxic group were most apparent for sequences composed of different hand postures rather than sequences that repeated the same hand posture. However, the current paradigm has the advantage of being related to real-world consequences but suggests that apraxics show only marginally poorer ipsilesional deficits on such a task. Importantly, the apraxic group performed significantly worse than the nonapraxic group on the TMPT, which included the Williams doors test and 5 simulated ADLs from the JTHFT. These findings suggest that the TMPT is more sensitive to deficits of the apraxic patient. This is consistent with previous work using many of the same patients, which found ipsilesional deficits when the entire JTHFT was used, suggesting that these simu-
IPSILESIONAL DEFICITS AFTER STROKE, Chestnut
lated ADLs, which require manipulation of objects in space, are more affected by limb apraxia. Study Limitations As noted previously, we did not analyze errors, as has been done in a previous study.19 Such an analysis may have identified qualitative differences among the groups, which could delineate different underlying mechanisms for deficits across the groups. An additional and more important limitation is that the previous studies22,23 that have linked the TMPT to realworld functioning allowed participants to use either or both hands to perform the task. Because we restricted participants to using only 1 hand (the ipsilesional hand for the stroke groups), it is possible that the relationship between the TMPT and real-world functioning would be decreased. CONCLUSIONS Ideomotor limb apraxia is characterized by spatiotemporal deficits, especially for transitive movements that by definition are movements that use tools. These deficits can be seen whether the movement is performed with or without the object, and they have been identified by error analysis24,43 and by kinematic recording of the movement.42 The kinematic analyses show deficits in timing (eg, joint synchronization, relative joint amplitudes) and spatiotemporal (poor coupling of the spatial and temporal aspects of wrist trajectory) aspects of movement.42 Importantly, these spatiotemporal deficits can be seen even when the patient is manipulating the object, not only when they are pantomiming the movement without the object present, and they can affect movement efficiency. Given these types of deficits, it is not surprising that relative to the Williams doors test, the JTHFT, which is part of the TMPT and includes several items that depend on the temporal and spatial coordination of movement in space, is more sensitive to the deficits described in ideomotor limb apraxics. That is not to say that the Williams doors test, which has significant sequential hand position requirements, would not be impaired in apraxia. In fact, the present results show marginal impairment in apraxic relative to nonapraxic patients on that task, but the present results show that the deficits of the apraxic group were not as sensitively and consistently reflected by the Williams doors test as the TMPT. These conclusions are also consistent with previous findings that apraxics are particularly impaired when using implements to eat6 and when performing movements that require showing tool use relative to movements that do not require tools.24,47,48 Acknowledgment: We thank Robert T. Knight, MD, for neuroimaging consultation. References 1. Gresham GE, Duncan PW, Stason WB, Adams HP, Adelman AM, Alexander DN. Post-stroke rehabilitation. Clinical practice guideline no. 16. Rockville: U.S. Department of Health and Human Services, Public Health Service, Agency for Health Care Policy and Research; 1995. AHCPR publication no. 95-0662. 2. Chiou II, Burnett CN. Values of activities of daily living. A survey of stroke patients and their home therapists. Phys Ther 1985;65: 901-6. 3. Haaland KY, Delaney HD. Motor deficits after left or right hemisphere damage due to stroke or tumor. Neuropsychologia 1981; 19:17-27. 4. Wyke M. Effects of brain lesions on the rapidity of arm movement. Neurology 1967;17:1113-20. 5. Haaland KY, Harrington DL. Hemispheric asymmetry of movement. Curr Opin Neurobiol 1996;6:796-800.
67
6. Foundas AL, Macauley BL, Raymer AM, Maher LM, Heilman KM, Gonzalez Rothi LJ. Ecological implications of limb apraxia: evidence from mealtime behavior. J Int Neuropsychol Soc 1995; 1:62-6. 7. Wetter S, Poole JL, Haaland KY. Functional implications of ipsilesional motor deficits after unilateral stroke. Arch Phys Med Rehabil 2005;86:776-81. 8. Sundet K, Arnstein F, Rienvang I. Neuropsychological predictors in stroke rehabilitation. J Clin Exp Neuropsychol 1988;10:363-79. 9. Vega-Gonzalez A, Granat MH. Continuous monitoring of upperlimb activity in a free-living environment. Arch Phys Med Rehabil 2005;86:541-8. 10. Jones RD, Donaldson IM, Parkin PJ. Impairment and recovery of ipsilateral sensory-motor function following unilateral cerebral infarction. Brain 1989;112(Pt 1):113-32. 11. Fisk JD, Goodale MA. The effects of unilateral brain damage on visually guided reaching: hemispheric differences in the nature of the deficit. Exp Brain Res 1988;72:425-35. 12. Wyke M. The effects of brain lesions in the performance of an arm-hand precision task. Neuropsychologia 1968;6:125-34. 13. Winstein CJ, Pohl PS. Effects of unilateral brain damage on the control of goal-directed hand movements. Exp Brain Res 1995; 105:163-74. 14. Harrington DL, Haaland KY. Hemispheric specialization for motor sequencing: abnormalities in levels of programming. Neuropsychologia 1991;29:147-63. 15. Heilman KM, Rothi LJ, Kertesz A. Localization of apraxiainducing lesions. In: Kertesz A, editor. Localization in neuropsychology. New York: Academic Pr; 1983. p 371-92. 16. Haaland KY, Prestopnik JL, Knight RT, Lee RR. Hemispheric asymmetries for kinematic and positional aspects of reaching. Brain 2004;127:1145-58. 17. Carmon A. Sequenced motor performance in patients with unilateral cerebral lesions. Neuropsychologia 1971;9:445-9. 18. Schaefer SY, Haaland KY, Sainburg R. Ipsilesional motor impairments following stroke reflect lateralization of movement control. Brain 2007;130(Pt 8):2146-58. 19. Sunderland A, Bowers MP, Sluman SM, Wilcock DJ, Ardron ME. Impaired dexterity of the ipsilateral hand after stroke and the relationship to cognitive deficit. Stroke 1999;30:949-55. 20. Jebsen RH, Griffith ER, Long EW, Fowler R. Function of “normal” hand in stroke patients. Arch Phys Med Rehabil 1971;52: 170-4. 21. Spaulding SJ, McPherson JJ, Strachota E, Kuphal M, Ramponi M. Jebsen Hand Function Test: performance of the uninvolved hand in hemiplegia and of right-handed, right and left hemiplegic persons. Arch Phys Med Rehabil 1988;69:419-22. 22. Williams ME, Hadler NM, Earp JA. Manual ability as a marker of dependency in geriatric women. J Chronic Dis 1982;35:115-22. 23. Williams ME, Gaylord SA, Gerritty MS. The Timed Manual Performance test as a predictor of hospitalization and death in a community-based elderly population. J Am Geriatr Soc 1994;42: 21-7. 24. Haaland KY, Flaherty D. The different types of limb apraxia errors made by patients with left vs. right hemisphere damage. Brain Cogn 1984;3:370-84. 25. Kertesz A. Western Aphasia Battery. New York: Psychological Corp; 1982. 26. Wechsler D. Wechsler Adult Intelligence Scale–Revised. New York: Psychological Corp; 1981. 27. Benton AL, Hamsher K, Varney NR, Spreen O. Contributions to neuropsychological assessment. Oxford: Oxford Univ Pr; 1983. 28. Reitan RM, Davison LA. Clinical neuropsychology: current status and applications. Washington (DC): Winston; 1974. 29. Heaton RK, Grant I, Matthews CG. Comprehensive norms for an expanded Halstead-Reitan battery; demographic corrections, reArch Phys Med Rehabil Vol 89, January 2008
68
30. 31. 32. 33.
34.
35.
36.
37.
38.
39.
IPSILESIONAL DEFICITS AFTER STROKE, Chestnut
search findings, and clinical applications. With a supplement for the Wechsler Adult Intelligence Scale-Revised (WAIS-R). Odessa: Psychological Assessment Resources; 1991. Haaland KY. The relationship of limb apraxia severity to motor and language deficits. Brain Cogn 1984;3:307-16. Haaland KY, Harrington DL, Knight RT. Neural representations of skilled movement. Brain 2000;123:2306-13. DeArmond SJ, Fusco MM, Dewey MM. Structure of the human brain: a photographic atlas. 3rd ed. New York: Oxford Univ Pr; 1989. Frey RT, Woods DL, Knight RT, Scabini D, Clayworth C. Defining functional areas with averaged CT scans. Soc Neurosci 1987;13:1266. Gerrity MS, Gaylord S, Williams ME. Short versions of the Timed Manual Performance Test. Development, reliability, and validity. Med Care 1993;31:617-28. Hardin M. Assessment of hand function and fine motor coordination in the geriatric population. Top Geriatr Rehabil 2002; 18:18-27. Jebsen RH, Taylor N, Trieschmann RB, Trotter MJ, Howard LA. An objective and standardized test of hand function. Arch Phys Med Rehabil 1969;50:311-9. Kwakkel G, Kollen BJ, van der Grond J, Prevo AJ. Probability of regaining dexterity in the flaccid upper limb: impact of severity of paresis and time since onset in acute stroke. Stroke 2003;34:2181-6. Dromerick AW, Reding MJ. Functional outcome for patients with hemiparesis, hemihypesthesia, and hemianopsia. Does lesion location matter? Stroke 1995;26:2023-6. Mercier L, Audet T, Hebert R, Rochette A, Dubois MF. Impact of motor, cognitive, and perceptual disorders on ability to perform activities of daily living after stroke. Stroke 2001;32:2602-8.
Arch Phys Med Rehabil Vol 89, January 2008
40. Walker CM, Sunderland A, Sharma J, Walker MF. The impact of cognitive impairment on upper body dressing difficulties after stroke: a video analysis of patterns of recovery. J Neurol Neurosurg Psychiatry 2004;75:43-8. 41. Sunderland A. Recovery of ipsilateral dexterity after stroke. Stroke 2000;31:430-3. 42. Poizner H, Merians AS, Clark MA, Macauley B, Gonzalez Rothi LJ, Heilman KM. Left hemispheric specialization for learned, skilled and purposeful action. Neuropsychologia 1998;12:163-82. 43. Rothi L, Mack L, Verfaellie M, Brown P, Heilman KM. Ideomotor apraxia: error pattern analysis. Aphasiology 1988;2:381-8. 44. Kolb B, Milner B. Performance of complex arm and facial movements after focal brain lesions. Neuropsychologia 1981;19:491503. 45. Kimura D, Archibald Y. Motor functions of the left hemisphere. Brain 1974;97:337-50. 46. Harrington DL, Haaland KY. Motor sequencing with left hemisphere damage: are some cognitive deficits specific to limb apraxia? Brain 1992;115:857-74. 47. Buxbaum LJ, Veramonti T, Schwartz MF. Function and manipulation tool knowledge in apraxia: knowing ‘what for’ but not ‘how’. Neurocase 2000;6:83-97. 48. Buxbaum LJ, Saffran EM. Knowledge of object manipulation and object function: dissociations in apraxic and nonapraxic subjects. Brain Lang 2002;82:179-99. Suppliers a. Siemens, 51 Valley Stream Pkwy, Malvern, PA 19355. b. Picker International Inc, 595 Miner Rd, Cleveland, OH 44143.