Multimodal imaging of brain reorganization in motor areas of the contralesional hemisphere of well recovered patients after capsular stroke

Abstract

Clinical recovery after stroke can be significant and has been attributed to plastic reorganization and recruitment of novel areas previously not engaged in a given task. As equivocal results have been reported in studies using single imaging or electrophysiological methods, here we applied an integrative multimodal approach to a group of well-recovered chronic stroke patients (n = 11; aged 50-81 years) with left capsular lesions. Focal activation during recovered hand movements was assessed with EEG spectral analysis and H2(15)O-PET with EMG monitoring, cortico-cortical connectivity with EEG coherence analysis (cortico-cortical coherence) and corticospinal connectivity with transcranial magnetic stimulation (TMS). As seen from comparisons with age-matched controls, our patients showed enhanced recruitment of the lateral premotor cortex of the lesioned hemisphere [Brodmann area (BA) 6], lateral premotor and to a lesser extent primary sensorimotor and parietal cortex of the contralesional hemisphere (CON-H; BA 4 and superior parietal lobule) and left cerebellum (patients versus controls, Z > 3.09). EEG coherence analysis showed that after stroke cortico-cortical connections were reduced in the stroke hemisphere but relatively increased in the CON-H (ANOVA, contrast analysis, P < 0.05), suggesting a shift of functional connectivity towards the CON-H. Nevertheless, fast conducting corticospinal transmission originated exclusively from the lesioned hemisphere. No direct ipsilateral motor evoked potentials (MEPs) could be elicited with TMS over the contralesional primary motor cortex (iM1) in stroke patients. We conclude that (i) effective recovery is based on enhanced utilization of ipsi- and contralesional resources, (ii) basic corticospinal commands arise from the lesioned hemisphere without recruitment of ('latent') uncrossed corticospinal tract fibres and (iii) increased contralesional activity probably facilitates control of recovered motor function by operating at a higher-order processing level, similar to but not identical with the extended network concerned with complex movements in healthy subjects.

Imaging correlates of motor recovery from cerebral infarction and their physiological significance in well-recovered patients

“…From these studies, it seems that inhibiting the contralesional M1 is one way to improve function of the lesional M1. Yet, we know from our results and others (Gerloff et al, 2006) that the uncrossed corticospinal tract from the contralesional M1 is not directly involved in the return of motor activity in the recovered hand, because MEPs were not recorded in the ipsilateral (recovered) FDI while stimulating the contralesional hemisphere using TMS, even at maximal stimulator output (Foltys et al, 2003) (despite contralesional M1 activation during wrist and index finger tasks in patients).…”

“…An alternative explanation is that contralesional M1 activation arises from top-down activation from higher order areas, and is an epiphenomenon not contributing to recovery. Gerloff et al (2006) using EEG coherence analysis recently showed that after stroke, corticocortical connections were reduced in the stroke-affected hemisphere but increased in the contralesional hemisphere, suggesting a shift of functional connectivity towards the contralesional side. Short and long-range connectivity from within (Fridman et al, 2004) and across the hemisphere (Johansen-Berg et al, 2002b) is known to affect the excitability of the cortex and hence contribute to motor recovery.…”

Multiscale topological properties of functional brain networks during motor imagery after stroke

“…Beta rhythms during MI have been correlated to sensorimotor processes in healthy subjects (McFarland et al, 2000) and stroke patients (Gerloff et al, 2006). In the latter, the relative asymmetry between ipsilesional and contralesional hemispheres during contralateral MI and its relationship with functional motor impairment remain debated (Graziadio et al, 2012;Shahid et al, 2010).…”

The behavioral significance of coherent resting-state oscillations after stroke

“…For instance, all measures of FC are sensitive to noise and the alpha band tends to have a greater signal-to-noise ratio, especially compared to faster rhythms. Furthermore, our analyses were restricted to the resting-state whereas other EEG frequencies may be more implicated during tasks (Gerloff et al, 2006).…”