Damage to the motor cortex or corticospinal tract has long been known to produce weakness of the affected body parts. Because most of the descending corticospinal axons cross sides at the cervico-medullary junction, weakness appears in the limbs ipsilateral to a lesion in the spinal cord but contralateral to a lesion in the brain. This weakness is more profound in distal than in proximal muscles, and finger movements become particularly weak (Colebatch and Gandevia, 1989
). Above and beyond the degree of weakness, however, affected patients show a deficit of movement individuation. Voluntary movement of a particular digit is accompanied by more movement of adjacent digits, and the wrist, elbow and shoulder may move as well (Brunstrom, 1970
) (Zackowski et al., 2004
). Even when substantial strength recovers, a deficit of relatively independent finger movements that impairs tasks requiring fine manipulation typically persists, often permanently (Lawrence and Kuypers, 1968
We have investigated factors underlying this loss of individuation in human subjects with pure motor hemiparesis, a stroke syndrome in which weakness of the face, arm and leg occurs contralateral to a circumscribed infarction relatively restricted to corticospinal fibers in the posterior limb of the internal capsule, or in the basis pontis (Fisher, 1982
; Fisher and Curry, 1965
). These lesions typically produce no sensory, language or cognitive deficits. Changes in motor performance therefore can be attributed by and large to disruption of the corticospinal pathway and any subsequent reorganization. We evaluated 10 subjects selected for recovery sufficient to hold a pen with a precision grip and to walk short distances with an assistive device. Subjects were studied 2 to 34 months after stroke.
An instrumented glove recorded the motion of all the digits simultaneously as subjects performed cyclical flexion/extension or abduction/adduction movements of each digit. shows typical data from flexion/extension movements of the ring finger performed by a normal age-matched control subject, the affected hand of a subject with pure motor hemiparesis, and the unaffected hand of the same subject. In the control hand and in the patient’s unaffected hand, intentional movement of the ring finger was accompanied by low amplitude movement in the joints of the middle and little fingers. But in the affected hand, the accompanying movement of the middle and little fingers was much larger, and low amplitude movement was present as well in the thumb and index finger.
Figure 1 A. Single trials of joint position versus time for a control (left column), and the affected (middle column) and unaffected hand (right column) of a hemiparetic subject. In each case, the subject was instructed to flex and extend the ring finger cyclically (more ...)
We quantified the motion of the non-instructed digits using a previously described individuation index, which varies from 1 when there was no motion of non-instructed digits to 0 when all non-instructed digits moved as much as the instructed digit (Schieber, 1991
). As shown in , the individuation index of affected fingers was lower than that of fingers in normal controls or the unaffected hands of subject with pure motor hemiparesis (Lang and Schieber, 2003
). Similar deficits have been observed in the selectivity of isometric flexion force production at the fingertips following stroke (Li et al., 2003
). Abduction/adduction movements showed a greater loss of individuation than flexion/extension movements (Lang and Schieber, 2004a
Given that the motor cortex and corticospinal tract have a relatively magnified representation of the thumb compared to that of the other digits (Penfield and Rasmussen, 1950
) (Woolsey et al., 1952
), one might have expected that in patients with pure motor hemiparesis the thumb would show the most profound impairment. But instead the thumb showed the highest individuation index, both for flexion/extension and abduction/adduction movements. The higher degree of individuation of the thumb as compared to other digits in patients recovering from pure motor hemiparesis might reflect i) a larger reserve of thumb control in a partially damaged system, ii) greater reorganization of thumb control because of more emphasis on tasks that require use of the thumb during rehabilitation, and/or iii) greater biomechanical independence of the thumb and the muscles that move it.
Both passive (mechanical and involuntary) and active (voluntary) factors might contribute to the deficits in individuation that result from lesions of the motor cortex or corticospinal tract. To distinguish the contributions of passive and active factors, we splinted the proximal and distal interphalangeal joints (one finger at a time) to permit movement only at the metacarpophalangeal joint, and then asked subjects to perform flexion/extension movements of the splinted finger actively. Next, a motor rotated each splinted finger passively at the metacarpophalangeal joint, using a rate and range of motion similar to that produced by the subject actively. During both passive and active movements, the simultaneous motion of all finger joints was recorded with an instrumented glove (Lang and Schieber, 2004a
shows group data for the unaffected (A) and affected hands (B) of subjects with pure motor hemiparesis. In both unaffected and affected hands individuation indexes were higher during passive movement of the digits than during active movement. This indicates that even in normal hands, active, voluntary muscle contractions contribute to the concurrent low-amplitude movement of non-instructed digits along with the instructed digit, particularly in the more ulnar fingers (Lang and Schieber, 2004a
). In hands affected by corticospinal lesions, we thought it possible that the hyperreflexia, abnormal spread of reflexes among muscles, increased tone, and muscle contracture, all of which can accompany the weakness in hemiparesis (Given et al., 1995
; Kamper and Rymer, 2000
; O'Dwyer et al., 1996
; Vattanasilp et al., 2000
), might contribute to increased motion of the non-instructed digits in the passive condition. Such increased coupling produced by these involuntary factors would have been evident as a decrease in passive individuation indexes in the affected hands. But as shown in , the individuation indexes during passive motion of affected hands in our pure motor hemiparesis subjects were just as high as those of control hands. In contrast, during active movement the individuation indexes of the affected hands were significantly lower than those of the control hands. This active/passive difference indicates that the deficit of individuation reflects a change in active control of finger movements following corticospinal lesions.
Figure 2 Individuation indexes are shown for passive (open triangles) and active (filled squares) movements of each digit in unaffected (A) and affected (B) hands of patients with pure motor hemiparesis. Points represent group means ± standard error. For (more ...)
To examine this change in active control, we recorded surface EMG activity from three intrinsic muscles of the hand as subjects made abduction/adduction movements (Lang and Schieber, 2004b
). We recorded from the abductor pollicis brevis (APB), first dorsal interosseous (FDI) and abductor digiti quinti (ADQ), which act on the thumb, index finger and little finger, respectively. shows example recordings from the FDI of a control and of an affected hand during cyclical abduction/adduction movements of the thumb, index finger, ring finger and little finger. (Middle finger movements were not studied here because our instrumented glove did not transduce abduction/adduction movement of the middle finger independently.) Whereas FDI in the control hand was active only when the index finger was abducting, FDI in the affected hand was active as well during movement of the thumb or the ring finger. These inappropriate contractions of FDI in the affected hand would cause the index finger to move when the subject attempted to move only the thumb or the ring finger. The resulting inappropriate movement of the non-instructed index finger would lower the individuation index of thumb and ring finger movements.
Figure 3 Rectified surface EMG activity recorded from the first dorsal interosseous (FDI) muscle in the hand of a normal control subject (A) and the affected hand of a subject with pure motor hemiparesis (B) is shown from single trials in which the subjects were (more ...)
We quantified the degree to which each muscle was active selectively during movement of a single finger using an index of selective activation that could vary from 1 (contraction for only one movement) to 0 (equal contraction for all movements). presents the index of selective activation for each muscle averaged over the control, unaffected and affected hands. In subjects affected by pure motor hemiparesis, the index of selective activation was reduced in all three muscles. Hence when patients with corticospinal tract lesions attempt to move a particular digit, inappropriate contractions occur in muscles that move other digits. These other digits therefore move along with the intended digit to an abnormal degree. Such observations suggest that i) the corticospinal system normally acts to minimize muscle contractions that would move other digits, and/or ii) other descending systems (rubrospinal, reticulospinal) which may participate in compensating for the corticospinal lesion are unable to activate muscles as selectively as the normal corticospinal system.