Minimal forced use without constraint stimulates spontaneous use of the impaired upper extremity following motor cortex injury

Abstract

The purpose of this study was to determine if recovery of neurologically impaired hand function following isolated motor cortex injury would occur without constraint of the non-impaired limb, and without daily forced use of the impaired limb. Nine monkeys (Macaca mulatta) received neurosurgical lesions of various extents to arm representations of motor cortex in the hemisphere contralateral to the preferred hand. After the lesion, no physical constraints were placed on the ipsilesional arm/hand and motor testing was carried out weekly with a maximum of 40 attempts in two fine motor tasks that required use of the contralesional hand for successful food acquisition. These motor tests were the only "forced use" of the contralesional hand. We also tested regularly for spontaneous use of the contralesional hand in a fine motor task in which either hand could be used for successful performance. This minimal intervention was sufficient to induce recovery of the contralesional hand to such a functional level that eight of the monkeys chose to use that hand on some trials when either hand could be used. Percentage use of the contralesional hand (in the task when either hand could be used) varied considerably among monkeys and was not related to lesion volume or recovery of motor skill. These data demonstrate a remarkable capacity for recovery of spontaneous use of the impaired hand following localized frontal lobe lesions. Clinically, these observations underscore the importance of therapeutic intervention to inhibit the induction of the learned nonuse phenomenon after neurological injury.

Fig. 1

Recovery of contralesional hand performance in the mDB and nonuse tasks in four monkeys. Recovery of performance in the mDB task (solid circles) was computed as the percentage ratio of post-lesion performance score/average pre-lesion performance score (over the last five pre-lesion tests) on the well with highest pre-lesion skill. Recovery of spontaneous use of the contralesional hand (open triangles) is plotted as the percentage use of that hand in the post-lesion tests. The solid horizontal line represents average pre-lesion performance scores over the last five pre-lesion tests. The dashed horizontal line represents pre-lesion use of the preferred hand in the handedness test (note that the lesion was always made in the hemisphere contralateral to the preferred hand). Note that post-lesion performance score ratios of zero indicate no attempts in the testing session

Fig. 2

Scatter graphs showing post-lesion week of first attempt by the contralesional hand on the nonuse task versus post-lesion week of first attempt (a), first success (b) and five successes (c) on the best well of the mDB task. Post-lesion week of first attempt on the nonuse task is also plotted against total (gray matter + white matter) lesion volume in d. Each plotted symbol is data from a single monkey. Note that SDM56 was excluded from a, b, c and all regression analyses because he had no attempts on the nonuse task. SDM46 had no successes on the mDB task and thus is not included in b and c

Fig. 3

Scatter graphs showing post-lesion week of first attempt by the contralesional hand on the nonuse task versus post-lesion week of first attempt (a), first success (b) and five successes (c) on the best well of the mDB task. Post-lesion week of first attempt on the nonuse task is also plotted against total (gray matter + white matter) lesion volume in d. Each plotted symbol is data from a single monkey. Note that SDM56 was excluded from a, b, c and all these regression analyses because this monkey had no attempts on the nonuse task. SDM46 had no successes on the mDB task and thus is not included in b and c

Fig. 4

Scatter graphs showing average and highest percentage use on the nonuse test plotted against the ratio of post to pre-lesion manipulation skill (a, b), pre-lesion handedness index (c, d) and gray matter (GM) lesion volume (e, f). Each plotted symbol is data from a single monkey. Note that SDM49 was not included in these graphs or the associated regression analyses due to the short post-lesion observation period