The role of the unaffected hemisphere in motor recovery after stroke

Abstract

The contribution of the ipsilateral (nonaffected) hemisphere to recovery of motor function after stroke is controversial. Under the assumption that functionally relevant areas within the ipsilateral motor system should be tightly coupled to the demand we used fMRI and acoustically paced movements of the right index finger at six different frequencies to define the role of these regions for recovery after stroke. Eight well-recovered patients with a chronic striatocapsular infarction of the left hemisphere were compared with eight age-matched participants. As expected the hemodynamic response increased linearly with the frequency of the finger movements at the level of the left supplementary motor cortex (SMA) and the left primary sensorimotor cortex (SMC) in both groups. In contrast, a linear increase of the hemodynamic response with higher tapping frequencies in the right premotor cortex (PMC) and the right SMC was only seen in the patient group. These results support the model of an enhanced bihemispheric recruitment of preexisting motor representations in patients after subcortical stroke. Since all patients had excellent motor recovery contralesional SMC activation appears to be efficient and resembles the widespread, bilateral activation observed in healthy participants performing complex movements, instead of reflecting maladaptive plasticity.

Figure 1

Axial T1‐weighted MRI scans at the level of maximum infarct volume for each patient performed at the time of fMRI. Patient numbers correspond with those in the Table I. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 2

Schematic representation of the experimental set‐up. (A) Time course of scan acquisition: Each box represents the measurements across one complete brain volume comprising 28 slices. Note the jittering effect between activation periods (gray‐shaded areas) and scanning intervals (white boxes). (B) Finger tapping task: Subjects performed acoustically paced movements of the right index finger at six different frequencies (2.0, 2.5, 3.0, 4.0, 5.0, and 6.0 Hz) 15 times each in a pseudo‐randomized order with onset‐to‐onset intervals ranging from 12–24 s.

Figure 3

Behavioral measures of healthy control subjects and patients during finger tapping with six frequencies. Actual tapping frequency performed by healthy controls and patients versus auditory cues (A); reaction time in (ms) (B); actual tapping intervals (s) performed by healthy controls and patients versus auditory cues (C); and error rates defined as a deviating number of taps compared to the number of cues (D). Values are mean ± SD. Black bars = auditory cues, white bars = healthy control subjects, gray bars = patients.

Figure 4

Statistical parametric maps of (1) the main effects for patients (A) and controls (B), (2) the positive linear BOLD signal changes along with increasing movement rates for patients (D) and controls (E) and (3) the results of the subtraction analysis of main effects (C) and positive linear BOLD signal changes (F) between the two groups. Red color indicates the significant activation patterns of the comparison controls > patients, green color indicates the significant activation patterns of the comparison patients > controls. L, left; R, right; z, distance to the intercommissural plane. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]

Figure 5

Parametric changes of BOLD signal intensity along with increasing movement rate of the right index finger in control subjects (A) and patients (B; size of effect and variance of BOLD signal intensity within the respective voxels calculated in arbitrary units by SPM5). SMA, supplementary motor area; PMC, premotor cortex; SMC, sensorimotor cortex; L, left; R, right; z, distance to the intercommisural plane;

Figure 6

The upper panel displays the results of a quantitative functional connectivity analysis: computed correlation coefficients across the time series of the blood oxygen level‐dependent (BOLD) signal within the volumes of interest. The diagram depicts very high (>0.9), high (>0.8), and intermediate correlations (>0.6). Low correlations are not displayed. The lower panel shows the correlation coefficients for both groups displayed as grey scale values. Note: The averaged gray scale values (lower panel) are in accordance with the results from the Mann‐Whitney‐U‐Test demonstrating higher correlation coefficients between SMA proper and right SMC, between SMC of both sides and between the right PMC and SMC in patients compared to controls. Vice versa, higher correlation coefficients were seen in controls compared with patients between SMA proper and left‐sided SMC. [Color figure can be viewed in the online issue, which is available at www.interscience.wiley.com.]