Post-stroke reorganization of hand motor area: a 1-year prospective follow-up with focal transcranial magnetic stimulation

Abstract

Objective: Focal transcranial magnetic stimulation was used to test prospectively corticospinal excitability changes and reorganization of first dorsal interosseous (FDI) motor cortical representation in 31 patients who experienced a first ischemic stroke in the middle cerebral artery territory. All had severe hand palsy at onset.

Methods: Patients were assessed clinically with the Medical Research Council, Rankin, the National Institutes of Health stroke scales and Barthel Index at days 1, 8, 30, 90, 180 and 360 after stroke.

The following parameters of FDI motor evoked potential (MEPs) to focal transcranial magnetic stimulation were measured at the same delays: motor threshold, MEP amplitude, excitable cortical area, hot spot and center of gravity of FDI motor maps on affected and unaffected hemispheres. Correlations were sought between clinical and electrophysiological parameters.

Results: In patients whose affected motor cortex remained excitable at day 1, motor thresholds were not significantly different between sides and were similar to those of controls. Persistence of MEP on the affected side at day 1 was a strong predictor of good recovery. If present at day 1, MEPs recorded in affected FDI were significantly smaller than of the opposite side or in normals and progressively recovered up to day 360. In these patients, area of excitable cortex remained stable throughout the entire study. At day 1, amplitudes of MEPs obtained in unaffected FDI were significantly larger than later. Between days 1 and 360, we observed a significant displacement of center of gravity of motor maps towards more frontal regions on the affected side while no change was noted on the unaffected side.

Conclusions: Our data confirm the early prognosis value of transcranial magnetic stimulation in stroke. They indicate that the brain insult induces a transient hyperexcitability of the unaffected motor cortex. The evolution of FDI motor maps along the course of recovery mostly reflect corticospinal excitability changes but might also reveal some degree of brain plasticity. Most modifications observed occurred within 3 months of stroke onset.

Introduction

Motor recovery after stroke is largely variable and often difficult to predict from clinical and imaging findings. Among other paraclinical methods, transcranial magnetic stimulation (TMS) has been proposed to predict motor outcome after a stroke (Catano et al., 1995, Rapisarda et al., 1996, Bastings et al., 1997, Escudero et al., 1998, Pennisi et al., 1999). Most authors agree that persistent response to TMS in the early days after ischemic stroke is an indicator of good motor outcome. Recent studies outlined the existence of ‘a plastic’ reorganization of the cortical motor output that still operates between 2 and 4 months after an acute mono-hemispheric stroke (Trompetto et al., 2000). A contribution of the so-called unaffected hemisphere through ipsilateral pathways has been proposed based on clinical (Fisher, 1992), neurophysiological (Trompetto et al., 2000, Alagona et al., 2001), and neuro-imaging data (Chollet et al., 1991, Weiller et al., 1992, Silvestrini et al., 1995). Other mechanisms have been advocated: motor messages from motor cortex could be conveyed to spinal motor neurons through reticulospinal pathways whose connections are bilateral at the spinal cord level (Fries et al., 1991, Meyer et al., 1991) but their functional role in recovery from stroke remains controversial. The recovery process may also involve distinct mechanisms at different times after the brain injury. Some discrepancies among previous reports may be due to inclusion in some series of patients with different motor deficits at stroke onset, variable localizations of the infarcts and electrophysiological testing at different stages.

The aims of the present study were to investigate the neural mechanisms underlying functional recovery following stroke and to confirm the usefulness of early TMS in predicting motor outcome after stroke. The nature of recovery processes may also change along the course of the illness. Studying patients over a long period of time after stroke (more than 4 months after stroke as previously reported (Trompetto et al., 2000) may thus provide useful information. Therefore, we undertook a 1 year follow-up study of clinical and electrophysiological parameters of stroke patients with severe hand palsy at onset. All had a single ischemic lesion in the middle cerebral artery (MCA) territory.