Elsevier

NeuroImage

Volume 34, Issue 1, 1 January 2007, Pages 322-331
NeuroImage

The relationship between motor deficit and hemisphere activation balance after stroke: A 3T fMRI study

https://doi.org/10.1016/j.neuroimage.2006.08.026Get rights and content

Abstract

Functional imaging during movement of the hand affected by a stroke has shown excess activation of the contralesional motor network, implying less physiological hemisphere activation balance. Although this may be adaptive, the relationship between the severity of motor deficit and the hemisphere activation balance for the four major cortical motor areas has not been systematically studied. We prospectively studied 19 right-handed patients with first-ever stroke (age range 61 ± 10 years) in the stable phase of recovery (> 3 months after onset), using auditory-paced index–thumb (IT) tapping of the affected hand at 1.25 Hz as the fMRI paradigm. The hemisphere activation balance for the primary motor (M1), primary somatosensory (S1), supplementary motor (SMA) and dorsal premotor (PMd) areas was measured by a modified weighted laterality index (wLI), and correlations with motor performance (assessed by the affected/unaffected ratio of maximum IT taps in 15 s, termed IT-R) were computed. There were statistically significant negative correlations between IT-R and the wLI for M1 and S1, such that the more the hemispheric balance shifted contralesionally, the worse the performance. Furthermore, worse performance was related to a greater amount of contralesional, but not ipsilesional, activation. No significant correlation between IT-R and the wLI was obtained for the SMA and PMd, which functionally have stronger bilateral organization. These findings suggest that the degree of recovery of fine finger motion after stroke is determined by the extent to which activation balance in the primary sensory motor areas – where most corticospinal fibers originate – departs from normality. This observation may have implications for therapy.

Introduction

Stroke is a leading cause of long-term physical, especially motor, disability, so to better understand the mechanisms underlying recovery is important as improved rehabilitative and/or pharmacological strategies might derive. Functional imaging techniques offer the opportunity to investigate neuronal reorganization directly in stroke victims (Chollet et al., 1991). In partially recovered stroke patients, one consistently reported and intriguing finding with affected hand movement is enhanced activation of the contralesional motor network, including the primary sensorimotor (SM1) cortex, resulting in a shift of activation balance towards the unaffected side (Baron et al., 2004, Calautti and Baron, 2003).

One extensively used approach to assess the hemisphere activation balance, in both motor and language studies is the laterality index (LI) (Cramer et al., 1997). The LI ranges from + 1 (activation only on the side contralateral to hand movement) to − 1 (only ipsilateral activation). After stroke, therefore, enhanced contralesional activation translates as reduced or even negative LI, and accordingly the LI for SM1 is on average significantly lower in chronic stroke patients than in normal subjects (Calautti and Baron, 2003, Foltys et al., 2003). However, the range of LI values is wide and strikingly overlaps with that of healthy age-matched subjects, and a close look at the literature suggests that this enlarged variance in the LI after stroke may be subtended by differences in severity of motor deficit. For instance, Cramer et al. (1997) and Pineiro et al. (2001) reported higher LI values for SM1 than Carey et al. (2002), and their patients had less severe residual deficit (Calautti and Baron, 2003). Accordingly, Johansen-Berg et al. (2002) reported a significant negative though weak, correlation between motor impairment (assessed by the reaction time in a tapping task) and the LI for the primary motor cortex (M1), with a similar trend for the dorsal premotor cortex (PMd), in 10 right hemiparetic patients studied with fMRI 4–40 months after subcortical stroke. Confirming and expanding these findings would constitute key information about a potentially important aspect of plasticity, and in turn potential interventions. Furthermore, the relationship between hemisphere activation balance and motor deficit for two other major cortical areas, namely the primary sensory cortex (S1), and the supplementary motor area (SMA) has not been studied. Although all four areas contribute fibers to the corticospinal tract (CST), the PMd and SMA have very dense transcallosal connections and operate under a bilateral functional mode (Rouiller et al., 1994, Schubotz and von Cramon, 2003), as compared to M1 and S1. Thus, any relationship between motor deficit and the LI would be expected to be much stronger for the latter two areas.

In the present prospective fMRI investigation, we systematically assessed, in a large sample of chronic stroke patients, the relationship between motor performance and the LI for each of these four areas using, for both the activation paradigm and the clinical assessment of performance, an active task highly dependent on CST integrity, namely index finger–thumb tapping (Chollet et al., 1991). We tested the hypothesis that the more severe the deficit the more reduced the LI would be for both M1 and S1, but not for the PMd and SMA.

Section snippets

Patients

Patients for this study were prospectively selected based on strict criteria. Inclusion criteria were a single ischemic or hemorrhagic stroke more than 3 months before, with initial motor deficit lasting at least 2 weeks; SM1 hand area intact or largely preserved on structural imaging; ability to perform the fMRI activation task; right-handedness (based on the Laterality Quotient [L.Q.] of the Edinburgh Inventory test (Oldfield, 1971)); and age over 40 years. Exclusion criteria were as follows:

Motor performance

The IT-max for each patient is shown in Table 1. The median and range of the IT-max in the group of age-matched healthy subjects was 52 (38–58) and 48 (32–62) for the right and left hands, respectively. A comparison between the IT-max of the affected hand in patients and the IT-max for the same proportion of right and left hand values in controls showed a statistically significant decrease in patients (p = 0.004, Mann–Whitney test), but no significant difference for the unaffected hand.

wLI results

The wLI

Discussion

In agreement with our hypothesis, we found that the more the hemispheric balance for M1 and S1 shifted towards the contralesional hemisphere the worse the finger-tapping deficit, while no such relationship existed for the PMd and SMA.

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