Differential Poststroke Motor Recovery in an Arm Versus Hand Muscle in the Absence of Motor Evoked Potentials

Abstract

Background. After stroke, recovery of movement in proximal and distal upper extremity (UE) muscles appears to follow different time courses, suggesting differences in their neural substrates. Objective. We sought to determine if presence or absence of motor evoked potentials (MEPs) differentially influences recovery of volitional contraction and strength in an arm muscle versus an intrinsic hand muscle. We also related MEP status to recovery of proximal and distal interjoint coordination and movement fractionation, as measured by the Fugl-Meyer Assessment (FMA). Methods. In 45 subjects in the year following ischemic stroke, we tracked the relationship between corticospinal tract (CST) integrity and behavioral recovery in the biceps (BIC) and first dorsal interosseous (FDI) muscle. We used transcranial magnetic stimulation to probe CST integrity, indicated by MEPs, in BIC and FDI. We used electromyography, dynamometry, and UE FMA subscores to assess muscle-specific contraction, strength, and inter-joint coordination, respectively. Results. Presence of MEPs resulted in higher likelihood of muscle contraction, greater strength, and higher FMA scores. Without MEPs, BICs could more often volitionally contract, were less weak, and had steeper strength recovery curves than FDIs; in contrast, FMA recovery curves plateaued below normal levels for both the arm and hand. Conclusions. There are shared and separate substrates for paretic UE recovery. CST integrity is necessary for interjoint coordination in both segments and for overall recovery. In its absence, alternative pathways may assist recovery of volitional contraction and strength, particularly in BIC. These findings suggest that more targeted approaches might be needed to optimize UE recovery.

Keywords: motor cortex; motor evoked potential; neurorehabilitation; stroke recovery; transcranial magnetic stimulation.

Figure 1.

Lesion distribution on MRI. The lesion distribution from 43 subjects was mapped to JHU-MNI space and superimposed on one hemisphere, as described in Xu et al. The color bar denotes the number of subjects who shared the lesion location. Two missing subjects had striatocapsular lesions. All subjects had lesion involvement of the M1 and/or CST estimated by diffusion tensor imaging (results not shown.) Subjects with pontine lesions (n = 6) had FDI and BIC MEPs, indicating they did not specifically contribute to poorer recovery in the MEP− groups. MRI, magnetic resonance imaging; JHU-MNI, Johns Hopkins University–Montreal Neurological Institute; CST, corticospinal tract; FDI, first dorsal interosseous; BIC, biceps; MEP, motor evoked potential.

Figure 2.

Relationship of MEPs and volitional muscle contraction over time in the (A) paretic and (B) nonparetic FDI and BIC. At each time point, the presence/absence of an MEP and volitional muscle contraction in the same muscle were categorized for each subject, and the percentage of subjects with each category was calculated. Time courses of these proportions are shown for those with volitional contraction (upper panel) and no contraction (lower panel). The overall odds of MEP−/contraction+ in the paretic BIC were 4.6 times higher than the paretic FDI (P = .004) and 5.7 times higher than nonparetic BIC (P = .005). MEP, motor evoked potential; FDI, first dorsal interosseous; BIC, biceps.

Figure 3.

Effect of MEP status on (A) absolute and (B) normalized strength over time in the FDI and BIC. Single-subject data and average values with SEM are shown for each time point. (A) Absolute MVF is shown for the paretic and nonparetic sides for clinical reference. (B) Normalized MVF is shown for the paretic side. Normalization was within-subject, such that subjects’ paretic MVFs were normalized to their own highest nonparetic MVF value (nonparetic best), irrespective of MEP status. Both paretic hand and arm were weak following stroke, but having an MEP was associated with significantly greater strength than having no MEP, for both paretic FDI (P < .0001) and BIC (P < .001). Paretic BIC strength was less affected by MEP absence than paretic FDI strength (P = .002). Strength recovery curves ran in parallel for FDIs with and without MEPs, but began to converge for the paretic BIC groups (P = .008). This pattern of recovery in the presence/absence of MEPs was significantly different across the hand and arm (P = .047). MEP, motor evoked potential; FDI, first dorsal interosseous; BIC, biceps; SEM, standard error of the mean; MVF, maximum voluntary force.

Figure 4.

Effect of MEP status on absolute FMA scores over time in the paretic hand and arm. MEPs were assessed in the FDI and BIC. Absolute FMA subscores are shown for the nonparetic sides for clinical reference. Single-subject data and average values with SEM are shown for each time point. Both paretic hand and arm had reduced FMA scores following stroke, but having an MEP was associated with significantly higher FMA subscores than having no MEP, for both the hand (P < .0001) and arm (P < .0001). FMA recovery curves ran in parallel for paretic hands with and without MEPs. FMA recovery was steeper in arms without MEPs than with MEPs (P = .007). However, hand and arm recovery curves behaved in a largely similar fashion in the absence of MEPs, arriving at a recovery plateau at 12 weeks and not converging on their counterparts with MEPs. MEP, motor evoked potential; FMA, Fugl-Meyer Assessment; FDI, first dorsal interosseous; BIC, biceps; SEM, standard error of the mean.

Figure 5.

Effect of early MEP status on extent of (A) strength and (B) FMA recovery in paretic FDI and BIC. MEPs were assessed at W1. Recovery extent is the proportion of maximum potential change that is observed at 24 weeks after stroke, on average, for the group; graphically, it the slope of the regression fit. Shaded areas are 95% confidence intervals for the regression fits of the same color. The stippled line indicates perfect recovery; that is, if observed change = maximum potential change (slope = 1, intercept = 0). (A) FDIs with an early MEP had a greater extent of strength recovery than those without an MEP (P = .019). BICs with an initial MEP showed a trend for greater attainment of strength recovery than those without an MEP (P = .071). There was no significant difference in the influence of early MEP status on the extent of strength recovery in the FDI and BIC. (B) Hands with an initial FDI MEP showed a weak trend for attaining a greater extent of FMA recovery than those without an MEP (P = .095) (of note, recovery extent was not significantly different from zero in the FDI no-MEP group due to the variability of recovery, evidenced by its wide confidence intervals). Arms with and without initial BIC MEPs showed comparable extents of FMA recovery. There was no significant difference in the influence of early MEP status on the extent of FMA recovery in the hand and arm. MEP, motor evoked potential; FMA, FuglMeyer Assessment; FDI, first dorsal interosseous; BIC, biceps.