Bihemispheric brain stimulation facilitates motor recovery in chronic stroke patients

Abstract

Objective: Motor recovery after stroke depends on the integrity of ipsilesional motor circuits and interactions between the ipsilesional and contralesional hemispheres. In this sham-controlled randomized trial, we investigated whether noninvasive modulation of regional excitability of bilateral motor cortices in combination with physical and occupational therapy improves motor outcome after stroke.

Methods: Twenty chronic stroke patients were randomly assigned to receive 5 consecutive sessions of either 1) bihemispheric transcranial direct current stimulation (tDCS) (anodal tDCS to upregulate excitability of ipsilesional motor cortex and cathodal tDCS to downregulate excitability of contralesional motor cortex) with simultaneous physical/occupational therapy or 2) sham stimulation with simultaneous physical/occupational therapy. Changes in motor impairment (Upper Extremity Fugl-Meyer) and motor activity (Wolf Motor Function Test) assessments were outcome measures while functional imaging parameters were used to identify neural correlates of motor improvement.

Results: The improvement of motor function was significantly greater in the real stimulation group (20.7% in Fugl-Meyer and 19.1% in Wolf Motor Function Test scores) when compared to the sham group (3.2% in Fugl-Meyer and 6.0% in Wolf Motor Function Test scores). The effects outlasted the stimulation by at least 1 week. In the real-stimulation group, stronger activation of intact ipsilesional motor regions during paced movements of the affected limb were found postintervention whereas no significant activation changes were seen in the control group.

Conclusions: The combination of bihemispheric tDCS and peripheral sensorimotor activities improved motor functions in chronic stroke patients that outlasted the intervention period. This novel approach may potentiate cerebral adaptive processes that facilitate motor recovery after stroke.

Classification of evidence: This study provides Class I evidence that for adult patients with ischemic stroke treated at least 5 months after their first and only stroke, bihemispheric tDCS and simultaneous physical/occupational therapy given over 5 consecutive sessions significantly improves motor function as measured by the Upper Extremity Fugl-Meyer assessment (raw change treated 6.1 ± 3.4, sham 1.2 ± 1.0).

Figure 1 Representative individual lesion maps After spatial normalization to the Montreal Neurological Institute space using SPM5, individual lesion maps of patients in the real stimulation group (dual) and control group (sham) were drawn and superimposed onto a canonical T1-weighted image. The slice closest to the internal capsule level with the greatest lesion expansion is shown to illustrate each patient's lesion.

Figure 2 Change in motor impairment scores and fMRI laterality index (A) Proportional change of motor impairment scores from baseline to postintervention assessments ([post − pre]/pre × 100). Note that an increase in Upper Extremity Fugl-Meyer assessment (UE-FM) scores reflects an improvement in impairment of the affected limb and that a decrease in logarithmized Wolf Motor Function Test (WMFT) scores indicates a better function of the affected limb (i.e., shorter completion times). (B) Linear regression of change in the precentral gyrus activation laterality index (LI) and WMFT change (sec[log]) in the real stimulation group (Pearson coefficient r = 0.72, p = 0.029). No significant correlation between functional imaging measures and behavioral motor measures were found in the sham group.

Figure 3 Contrast of affected limb movements postintervention vs preintervention for the dual group Contrasting postintervention vs preintervention movements of the affected upper limb overlaid onto a standard anatomic template (p < 0.05, familywise error corrected; cluster extent threshold: 20 voxels). Both wrist (blue) and elbow (red) movements yielded stronger activations of ipsilesional primary motor/premotor cortex after the 5-day intervention. For the elbow movement task, the cluster was located in primary motor cortex (Talairach coordinates: x = −18, y = −23, z = 68; T = 5.39). For the wrist movement task, one cluster was located at the border between primary motor and premotor cortex (x = −40, y = −8, z = 60; T = 5.28); an additional positive activation change was found in the contralesional inferior frontal gyrus (x = 56, y = 29, z = 14; T = 5.66).