(Stroke. 1999;30:1380-1383.)
© 1999 American Heart Association, Inc.
Original Contributions |
Middle Cerebral Artery Stroke That Includes the Premotor Cortex Reduces Mobility Outcome
Presented in preliminary form at the 50th annual meeting of the American Academy of Neurology, Minneapolis, Minn, April 29, 1998.
From the Department of Neurology, Toneyama National Hospital, Osaka, Japan (I.M., J.K.); Bobath Memorial Hospital, Osaka, Japan (T.S., K.K.); and the Department of Neurology, Cornell University Medical College, Burke Medical Research Institute, White Plains, NY (B.T.V.).
Correspondence to Ichiro Miyai, MD, PhD, Department of Neurology, Toneyama National Hospital, 5-1-1, Toneyama, Toyonaka City, Osaka 560-8552, Japan. E-mail webeo{at}ga2 so-net.ne.jp
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Abstract |
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Background and Purpose—The premotor cortex (PMC) (Brodmann 6) contributes uniquely to proximal upper and lower limb power and plays a role in the organization of motor behaviors. We assessed the degree to which PMC damage affected functional outcome.
Methods—We prospectively compared the functional outcome of patients with a first stroke in the middle cerebral artery distribution that either left the PMC intact (PMC-; n=19) or damaged the PMC (PMC+; n=12). The Functional Independence Measure for disability and the motor score of the Stroke Impairment Assessment Set for impairment assessed outcome.
Results—Demographic and clinical features and lesion volume were comparable for the PMC+ and PMC- groups. However, the PMC- group demonstrated significant gain in mobility and in proximal leg movement. This focal improvement contributed to the trend in the PMC- group toward greater independent ambulation.
Conclusions—Decreased motor recovery of proximal lower limbs in humans with PMC damage supports the idea that it is the origin of corticoreticulospinal pathways that subserve proximal lower extremity function. Furthermore, persistent proximal weakness after PMC damage may amplify other motor impairments, which include defects in planning, initiating, and sequencing. Neurorehabilitation outcomes may contribute to a more detailed functional anatomy after stroke and partial recovery.
Key Words: middle cerebral artery • stroke outcome • rehabilitation
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Introduction |
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We and others have demonstrated that patients with stroke confined to the basal ganglia (BG), including the internal capsule but sparing the cortex, had diminished response to rehabilitation compared with those with comparable damage to the BG and overlying cortex.1 2 To further specify these findings, in the present study we assessed the effect on outcome of ischemic damage in the premotor cortex (PMC or lateral premotor cortex, Brodmann area 6) or supplementary motor area (SMA or medial premotor cortex, Brodmann area 6).3 4 5 6 This study focused on patients with an initial single cerebral infarction in the territory of the middle cerebral artery (MCA). Since the SMA is supplied by the anterior cerebral artery, the target patients had BG and internal capsule damage with or without PMC damage.
Damage to the PMC disrupts sequential motor tasks and causes unilateral weakness of shoulder and hip muscles.7 8 Recent functional imaging has demonstrated that the recovery of sequential movements, limited by scan protocol demands to finger movements, in patients with stroke was associated with bilateral activation of the PMC.9 Other functional imaging and neurophysiological studies have suggested that the PMC mediates motor behavior that is dependent on environmental cues of the sort that occur commonly in rehabilitation environments.3 7 10 11 12 We examined whether these characteristics of the functional anatomy of PMC stroke would have an effect on rehabilitation outcome.
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Subjects and Methods |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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We examined 42 consecutive patients who had an initial single cerebral infarction with an ischemic lesion in the territory of the MCA, including the subcortical regions of the corona radiata, internal capsule, and the BG (mainly the putamen and the globus pallidus), as well as the overlying cortex, including the primary sensorimotor cortex. All patients were transferred to the Rehabilitation Division of Bobath Memorial Hospital after initial medical treatment followed by short-term physical therapy at acute care hospitals. On average, 4 months after the onset of stroke, patients who were still nonambulatory were referred to the hospital for multidisciplinary rehabilitation (Table 1
). Patients with severe medical
complications participated in abbreviated rehabilitation programs and
were not available for detailed weekly assessments; they were therefore
excluded from the protocol. These 11 patients had congestive heart
failure, myocardial infarctions, unremitting cardiac
arrhythmias, pneumonia, hip fracture, deep vein thrombosis, and
uncontrolled hypertension. Thirty-one patients were enrolled in the
study.
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MRI information was obtained on admission (on average, 4 months; Table 1
). The MRI protocol was identical for all patients in the
study: lesions were identified with the use of a 1.0-T superconductive
MRI system (Shimazu, MAGNEX Epios10). T2-weighted (repetition time,
3630 ms; echo time, 110 ms) axial spin-echo images as well as
T1-weighted (repetition time, 500 ms; echo time, 15 ms) axial spin-echo
images were obtained. Lesion density maps of each patient were plotted
on the standardized horizontal brain templates,13 and
digitalized files of the T2-weighted images were imported into the
measuring program (NIH Image 1.60). Lesion volume was estimated by
summing the area of the T2-identified infarct across contiguous slices.
The slice dimensions were 8.5 mm thick with a slice gap of
1.5 mm; there was no slice overlap. On the basis of the
distribution of cortical lesions, patients were divided into 2 groups:
12 patients were designated PMC+ and had damage in the subcortical
regions as defined above and the overlying cortex including PMC; 19
patients were designated PMC- and had damage in subcortical regions
and the overlying cortex other than PMC. No patient in either group had
a thalamic lesion.
All patients received multidisciplinary inpatient rehabilitation by the
neurodevelopmental technique of Bobath,14 including
45-minute sessions of physical therapy, 45-minute sessions of
occupational therapy, and 45-minute sessions of speech therapy as
needed, 5 days a week. At admission and discharge, functional outcome
was evaluated with the use of reliable and valid measures: the
Functional Independence Measure15 16 (FIM) for disability
and the motor subscore of the Stroke Impairment Assessment
Set17 (SIAS) for neurological impairment. We also
analyzed the change of activities of daily living (ADL),
mobility, and cognition subscores of FIM. The motor subscore of SIAS
(score range, 0 to 25) consists of 2 tests for upper extremity
(score range, 0 to 10) and 3 tests for lower
extremity (score range, 0 to 15). Details of SIAS are described
in Tables 2 and 3.
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FIM was rated by trained nursing staff who were blinded to sites of
lesions, and SIAS was rated by physicians who were also blinded to
sites of lesions. FIM evaluation was performed every 2 to 3 weeks, and
when the FIM score reached a plateau, a discharge plan was finalized.
Interrater reliability for individual items of SIAS and FIM was
estimated with the use of weighted 
18 (n=16). The
statistics for each SIAS item were 0.91 (95% CI, 0.77 to 1.07) for
knee-mouth test, 0.85 (95% CI, 0.65 to 1.04) for finger test, 0.69
(95% CI, 0.39 to 0.98) for hip flexion test, 0.70 (95% CI, 0.42 to
0.98) for knee extension test, and 0.71 (95% CI, 0.44 to 0.97) for
ankle dorsiflexion test. Thus, each item of the SIAS demonstrated
agreement (=0.69 to 0.91) across raters. The Spearman correlation
coefficient across raters for total SIAS, SIAS for upper extremity, and
SIAS for lower extremity was 0.980 (P=0.0001), 0.986
(P=0.0001), and 0.944 (P=0.0003), respectively.
Reliability for each FIM item also ranged from good to very good: 0.66
(0.38 to 0.95) for eating, 0.62 (0.37 to 0.88) for grooming, 0.71 (0.45
to 0.96) for bathing, 0.67 (0.43 to 0.91) for dressing upper body, 0.84
(0.65 to 1.04) for dressing lower body, 0.68 (0.41 to 0.95) for
toileting, 0.93 (0.79 to 1.06) for bladder management, 0.76 (0.50 to
1.01) for bowel management, 0.71 (0.47 to 0.96) for bed/chair transfer,
0.74 (0.49 to 0.99) for toilet transfer, 0.77 (0.55 to 0.99) for
tub/shower transfer, 0.77 (0.55 to 1.00) for walk/wheelchair, 0.81
(0.52 to 1.10) for stairs, 0.85 (0.66 to 1.04) for comprehension, 0.79
(0.58 to 1.00) for expression, 0.68 (0.41 to 0.94) for social
interaction, 0.72 (0.50 to 0.95) for problem solving, and 0.83 (0.60 to
1.05) for memory. The Spearman correlation coefficient for total FIM
(0.973; P<0.005), ADL subscale (0.912;
P<0.005), mobility subscale (0.987; P<0.005),
and cognition subscale (0.976; P<0.005) was
significant.
We used either a 
2 test or an unpaired
t test to compare demographic data of the groups.
Statistical analysis for functional outcome relied on the
nonparametric Wilcoxon rank sum test.
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Results |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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Table 1
demonstrates that the groups were similar in regard
to sex, age, days after stroke, length of stay, side of stroke, type of
deficits, Mini-Mental State Examination, and volume of lesion. Of note,
all patients had motor plus sensory plus visual deficits. Visual fields
were assessed by single and double confrontation with moving fingers
and by reaction to visual threat in globally aphasic patients All
patients were moderately or severely paralyzed, and no patients had
limb-kinetic apraxia, ideomotor apraxia, or ideational
apraxia.8 19 Although no patient met the criteria of the
Diagnostic and Statistical Manual of Mental
Disorders, Fourth Edition for organic mood disorder with
depression, 2 patients in each group were treated with antidepressants.
Lesion density maps of patients with cerebral infarction with and
without PMC lesion showed comparable lesion volume estimation for PMC+
and PMC- (Figure) (PMC+=72.9±8.0
cm3 [±SEM]; PMC-=65.9±8.0
cm3; P=0.2403).
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On admission, PMC- and PMC+ were comparable on total FIM and on the
mobility, ADL, and cognition subscores. PMC+ demonstrated a
significantly retarded mobility outcome on discharge (Table 4)
(P<0.05, Wilcoxon rank sum test). There was a trend
toward greater independence in ambulation (without physical assistance
or supervision) for the PMC- group (16 of 19 [84%] compared with 7
of 12 [58%] for the PMC+ group).
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To make comparisons in regions where the administrative rules for discharge vary, we calculated FIM efficiency for each patient (gain of FIM score/length of stay measured in days). The data (mean±SEM efficiency) demonstrate trends toward greater FIM efficacy for the PMC- group (PMC+/PMC-=0.085±0.024/0.141±0.036 for total FIM score; P=0.268). For purpose of comparison, these FIM efficacy scores are comparable to those of chronic stroke patients in Japan in other rehabilitation institutes.20
On admission, PMC- and PMC+ were comparable on total SIAS scores and
on the upper and lower extremity subscores (Table 5). There was
a significant difference between PMC+ and PMC- on the gains of SIAS
scores for proximal leg movement (P<0.05, Wilcoxon
rank sum test) (Table 6), but the overall gain in SIAS score for
upper and lower extremities was comparable.
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Finally, there was a significant correlation between disability (FIM) and impairment (SIAS) ratings on discharge for the hip (0.7; Z=4.41; P<0.0001) and proximal lower extremity mobility (0.7; Z=4.51; P<0.0001). In terms of disposition, there was a trend for the PMC- group to go home more often (17/19 [89%]) than the PMC+ group (8/12 [67%]).
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Discussion |
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TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
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In this prospective comparison of outcome in 2 groups of patients with ischemic cerebral infarction of MCA territory that differed only in lesion extension to the PMC (PMC+ or PMC-), there was a significant increase in the motor recovery of axial and proximal lower limb strength that contributed to a more favorable outcome in those without PMC damage (PMC-). These outcome differences are consistent with the current functional anatomy of stroke that damages PMC. It is crucial to note that all patients displayed comparable neurological deficits, which included hemiparesis, hemisensory loss, and homonymous hemianopia, and lesion volumes were comparable. There was no evidence for limb-kinetic apraxia, and despite a tendency of PMC+ patients to more often sustain left hemisphere damage, it was not significant (
2=3.3). The initial impairment and disability
levels were also comparable between the groups. Thus, the improved
axial and proximal lower limb improvement undoubtedly led to the
increase in acquisition of independent ambulation (84% of PMC-; 58%
of PMC+), a result that also contributed to a higher rate of returning
home in the PMC- group. On the basis of current functional neuroanatomy, there are several possible mechanisms that may underlie these findings. Parallel motor pathways among the primary motor cortex, the PMC, the SMA, and the final effectors in the spinal cord are known to exist,6 and the persistent weakness of the PMC+ group may reflect interruption of the output projections from the PMC via the reticulospinal tract.7 8 The PMC appears to participate in control of the contralateral proximal musculature and also of the axial musculature bilaterally. Evidence from functional neuroimaging and neurophysiological studies7 10 11 12 has demonstrated that the PMC mediates motor behavior that is dependent on environmental cues, especially visual cues. Thus, in the group with PMC+, there are additional reasons for the persistent motor impairment. Positron emission tomography studies in patients with ischemic subcortical strokes have suggested that the PMC ipsilateral to the infarct undergoes enhanced positron emission tomography activation on movement of the contralateral limb.21 Recent functional imaging has also demonstrated that the recovery of finger movements in patients with MCA infarction was associated with bilateral activation of the PMC.9 Intact PMC in the PMC- group likely contributed to the improved motor outcome. A final speculation depends on the finding that the PMC is involved in motor function, which includes braking, selection, initiation, planning, and sequencing.22 23 Disruptions of motor behavior at this level combined with the loss of power may have made the PMC+ group more tentative, particularly with regard to ambulation.24 25 This trend toward less independent ambulation contributed to the decreased rate of discharge to home.
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Acknowledgments |
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The authors acknowledge support from funds for the comprehensive research on aging and health from the Ministry of Health and Welfare in Japan. We thank Naomi Hoshina for assistance with data collection.
Received February 18, 1999; revision received April 7, 1999; accepted April 7, 1999.
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References |
|---|
|
TopAbstractIntroductionSubjects and MethodsResultsDiscussionReferences |
|---|
1. Miyai I, Blau AD, Reding MJ, Volpe BT. Patients with stroke confined to basal ganglia have diminished response to rehabilitation efforts. Neurology. 1997;48:95–101.
2.
Pantano P, Formisano R, Ricci M, Di Piero V, Sabatini
U, Barbanti P, Fiorelli M, Bozzao L, Lenzi GL. Prolonged muscular
flaccidity after stroke: morphological and functional alterations.
Brain. 1995;118:1329–1338.
3. Tanji J. The supplementary motor area in the cerebral cortex. Neurosci Res. 1994;19:251–268.[Medline] [Order article via Infotrieve]
4. Kurata K. Information processing for motor control in primate premotor cortex. Behav Brain Res. 1994;61:135–142.[Medline] [Order article via Infotrieve]
5.
Picard N, Strick PL. Motor areas of the medial wall: a
review of their location and functional activation. Cereb
Cortex. 1996;6:342–353.
6.
Fink GR, Frackowiak SJ, Pietrzyk U, Passingham RE.
Multiple nonprimary motor areas in the human cortex. J
Neurophysiol. 1997;77:2164–2174.
7.
Halsband U, Ito N, Tanji J, Freund HJ. The role of
premotor cortex and the supplementary motor area in the temporal
control of movement in man. Brain. 1993;116:243–266.
8.
Freund HJ, Hummelsheim H. Lesions of premotor cortex
in man. Brain. 1985;108:697–733.
9.
Seitz RJ, Höflich P, Binkofski F, Tellmann L,
Hezog H, Freund H-J. Role of premotor cortex in recovery from middle
cerebral artery infarction. Arch Neurol. 1998;55:1081–1088.
10. Passingham R. Functional organization of the motor system. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Mazziotta JC, eds. Human Brain Function. San Diego, Calif: Academic Press; 1997:243–274.
11.
Stephan KM, Fink GR, Passingham RE, Silbersweig D,
Ceballos-Baumann AO, Frith CD, Frackowiak RSJ. Functional
anatomy of the mental representation of upper extremity
movements in healthy subjects. J Neurophysiol. 1995;73:373–386.
12.
Schluter ND, Rushworth MFS, Passingham RE, Mills KR.
Temporary interference in human lateral premotor cortex suggests
dominance for the selection of movements: a study using
transcranial magnetic stimulation. Brain. 1998;121:785–799.
13. Matsui T, Hirano A. An Atlas of the Human Brain for Computerized Tomography. Tokyo, Japan: Igaku-shoin; 1978.
14. Bobath B. Adult Hemiplegia: Evaluation and Treatment. Rev ed 2. London, England: William Heinemann Medical Books Ltd; 1978.
15. Keith RA, Granger CV, Hamilton BB, Sherwin FS. The Functional Independence Measure: a new tool for rehabilitation. In: Eisenberg MG, Grzesiak RC, eds. Advances in Clinical Rehabilitation. Vol 2. New York, NY: Springer; 1987:6–18.
16. Ottenbacher KJ. Hsu Y, Granger CV, Fiedler RC. The reliability of the Functional Independence Measure: a quantitative review. Arch Phys Med Rehabil. 1996;77:1226–1232.[Medline] [Order article via Infotrieve]
17. Chino N, Sonoda S, Domen K, Saitoh E, Kimura A. Stroke Impairment Assessment Set (SIAS): a new evaluation instrument for stroke patients. Jpn J Rehabil Med. 1994;31:119–125.
18. Brennan P, Silman A. Statistical methods for assessing observer variability in clinical measures. BMJ. 1992;304:1491–1494.
19.
Pramstaller PP, Marsden CD. The basal ganglia and
apraxia. Brain. 1996;119:319–340.
20. Sonoda S, Chino N, Domen K, Saitoh E. Changes in impairment and disability from the third to the sixth month after stroke and its relationship evaluated by an artificial neural network. Am J Phys Med Rehabil. 1997;76:395–400.[Medline] [Order article via Infotrieve]
21. Weiller C, Chollet F, Friston KJ, Wise RJS, Frackowiak RSJ. Functional reorganization of the brain in recovery from striatocapsular infarction in man. Ann Neurol. 1992;31:463–472.[Medline] [Order article via Infotrieve]
22. Frackowiak RSJ. The cerebral basis of functional recovery. In: Frackowiak RSJ, Friston KJ, Frith CD, Dolan RJ, Mazziotta JC, eds. Human Brain Function. San Diego, Calif: Academic Press; 1997:275–299.
23. Mink JW. The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol. 1996;50:381–425.[Medline] [Order article via Infotrieve]
24. He SQ, Dum RP, Strick PL. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the lateral surface of the hemisphere. J Neurosci. 1993;13:952–980.[Abstract]
25. He SQ, Dum RP, Strick PL. Topographic organization of corticospinal projections from the frontal lobe: motor areas on the medial surface of the hemisphere. J Neurosci. 1995;15:3284–3306.[Abstract]
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