Motor disinhibition in affected and unaffected hemisphere in the early period of recovery after stroke

Abstract

Objectives: To investigate motor disinhibition in affected and unaffected motor areas in the acute stage after stroke and during the early period of recovery.

Methods: Fifteen patients with moderate to severe hemiparesis after acute unilateral stroke were compared with 10 healthy age-matched controls. We used paired transcranial magnetic stimulation to study intracortical inhibition and facilitation from the thenar eminence muscles on both sides. F-wave from the median nerve on both sides were recorded. The recordings were performed 5–7 days (T1) and 30 days after stroke.

Results: In 10 patients who showed the presence of reliable motor evoked potentials on the affected side, intracortical inhibition was significantly reduced. On the unaffected side intracortical inhibition (ICI) was significantly reduced in all patients. Patients who presented significant motor recovery after 30 days showed persistence of abnormal disinhibition in the affected hemisphere but a return to normal ICI in the unaffected hemisphere. Patients with poor motor recovery showed persistence of abnormal disinhibition on both sides. No significant changes were observed in F-wave amplitude.

Conclusions: Motor disinhibition occurs on both sides after stroke in all acute stage patients. Changes in motor disinhibition on unaffected side also are related to motor recovery.

Introduction

It has been documented in animal models that acute focal brain damage is often followed by functional cortical motor and sensory reorganization close to the damaged areas and associated with behavioural motor recovery (Nudo et al., 1996, Xerri et al., 1998). Recent research has demonstrated enhanced excitability in the neighbourhood of the damaged area after ischaemic lesions in rats (Schiene et al., 1996, Buchkremer-Ratzmann et al., 1996, Buchkremer-Ratzmann and Witte, 1997). Involvement of cortical inhibition has also been found in remote areas to the lesions and in the contralateral unaffected hemisphere in animal models (Buchkremer-Ratzmann and Witte, 1997, Reinecke et al., 1999). In these brain areas, paired pulse inhibition studies including γ-amino butyric acid (GABA) receptor investigation, indicate a decrease in GABAergic inhibition (Mittmann et al., 1994, Schiene et al., 1996, Neumann-Haefelin et al., 1995, Luhmann, 1996). Functional imaging studies in patients recovering from hemiparetic stroke have described an enlarged activation volume in brain regions close and remote to the lesion, including the contralateral hemisphere (Weiller et al., 1992, Weiller et al., 1993, Cramer and Bastings, 2000). These studies, however, which yield information regarding changes in areas of the motor cortex, provide no information on the inhibitory and facilitatory mechanisms underlying these plastic changes.

Transcranial magnetic stimulation (TMS) is an important tool for exploring the excitability of the human motor cortex in vivo. TMS permits non-invasive painless evaluation of the cortical representation areas of muscles by mapping the motor cortex. Enlargement of motor areas has been documented using TMS in stroke patients during recovery (Traversa et al., 1997, Traversa et al., 1998, Traversa et al., 2000) and after specific rehabilitative treatment (Liepert et al., 1998). As regards the functional imaging, TMS maps, which inform about changes in areas of the motor cortex, provide no information on inhibitory and facilitatory mechanisms underlying these modifications in motor areas. The technique of paired magnetic stimulation is particularly sensitive in detecting intracortical mechanisms. Several studies have found that intracortical inhibition (ICI) and intracortical facilitation (ICF) reflect the excitability of distinct inhibitory and excitatory interneuronal circuits within the motor cortex (Kujirai et al., 1993, Ziemann et al., 1996a, Ziemann et al., 1996b). Liepert et al. have documented in a first study (Liepert et al., 2000a) the absence of motor inhibition by paired TMS in stroke patients in the acute stage only in the affected hemisphere and in a second study he reported the reduced motor inhibition in the unaffected hemisphere (Liepert et al., 2000b). The authors postulated that this disinhibition might be indicative of compensatory mechanisms involved in recovery-related reorganization.

The main objective of the present study was to test changes in intracortical excitability in patients in close and remote areas to the cerebrovascular lesion. We investigated the excitability of the hand motor cortex in both hemispheres by paired magnetic stimulation in patients with moderate to severe hemiparesis after an acute cerebrovascular monohemispheric lesion in order to verify involvement of the unaffected hemisphere in the early period of functional recovery.