On the reorganization of sensory hand areas after mono-hemispheric lesion: a functional (MEG)/anatomical (MRI) integrative study

Abstract

The topography of primary sensory cortical hand area following a monohemispheric lesion (sudden=stroke; progressive=neoplasm) was investigated in relationship with clinical recovery of sensorimotor deficits. Twenty seven patients with monohemispheric lesions were studied in a clinically stabilized condition. Functional informations from magnetoencephalography (MEG) were integrated with anatomical data from magnetic resonance imaging (MRI). MEG localizations of the neurons firing at early latencies in primary sensory cortex after separate stimulation of median nerve, thumb and little fingers of each hand were carried out. Characteristics of cerebral equivalent current dipoles (ECDs) activated by each contralateral stimulation, the `hand extension' (i.e., the distance in millimetres between ECDs of first and fifth digits), as well as interhemispheric differences of the tested parameters were investigated. Finally, ECDs' locations were integrated with MRI. Lesions involving cortical (C) or subcortical (SC) areas receiving sensory input from the hand were often combined to increase interhemispheric asymmetry of the tested parameters (22% for C and 49% for SC lesions). This might be due to an activation of neuronal districts which in the affected hemisphere (AH) differ from those normally activated in the unaffected hemisphere (UH) and in the control population. Moreover, the `hand extension' was enlarged on the AH—more frequently after a SC lesion—mainly due to a medial shift of the little finger ECD, combined to a tendency of both finger ECDs to shift frontally. After a C lesion, responses from the AH were often stronger than normal. Spatial reorganizations were also seen in the UH (7% of C and 14% of SC lesions). `Hand extension' in the UH was selectively enlarged for the P30m only when combined with a similar enlargement in the AH. Significant interhemispheric asymmetries due to neuronal reorganization in the AH were associated with worse clinical outcomes compared to patients without asymmetries.

Introduction

Conventional clinical sensory testing is often insufficient to precisely assess the amount of patient's sensory dysfunction following a hemispheric stroke 47, 4, 31. In a clinical context, (i.e., after a stroke) the estimation of discriminative sensory impairment is important because subtle sensory disturbances might be related to clinical outcome 6, 42as well as to functional reorganization of the sensory areas adjacent to the lesioned tissue. Thalamic afferents to sensorimotor brain areas as well as to postcentral parietal structures might play an important role in the mechanism of motor recovery as emphasized by studies both in animal models and in humans 6, 16, 5. Moreover, subdural grid electrodes recordings show that motor and sensory cortices overlap and are not simply separated by the central sulcus [39].

A robust bulk of experimental evidences supports the hypothesis that neuronal aggregates adjacent to a lesion in the sensorimotor brain areas can be progressively vicarious to the function of the damaged neurones 52, 9, 56, 26. Such a reorganization—if occurring in the affected hemisphere of patients with a monohemispheric lesion—should significantly modify the interhemispheric symmetry of somatotopic organization of the sensorimotor cortices. A roughly symmetrical organization of sensorimotor areas in right and left hemispheres has been repeatedly confirmed in healthy humans by different methods of functional brain imaging including positron emission tomography (PET), functional magnetic resonance imaging (fMRI) 25, 17, 23and MEG 24, 46. MEG represents a noninvasive technique able to spatially identify (using appropriate models) the synchronous neuronal firing of small cortical or subcortical areas in relation to spontaneous cerebral activity or in response to an external stimulus. In particular, it is ideal for the present study because neoplastic or gliotic tissues near the region where cerebral activation takes place has little effect on the spatial reconstruction of the source location 53, 54. Moreover, recent studies have demonstrated that MEG recordings are of great utility for noninvasive, presurgical discrimination of the spatial relationship between the neoplasm and the sensorimotor brain areas 19, 38, 40.

Few studies following monohemispheric lesions have been previously reported with MEG aiming to investigate the problem of the anatomo-functional substrate of sensorimotor recovery 54, 18, 35; in none of them interhemispheric differences were evaluated. Sensory perception following the amputation of a given body district has been recently investigated through MEG technique in amputees suffering from phantom limb pain [14]. It was suggested that such distressing pain is based upon `plastic' rearrangements of cortical somatotopy in which previously functionally silent or differently operating neuronal pools are vicarious to the lost sensory information.

We recently investigated the right/left interhemispheric differences of the hand primary sensory cortex in the healthy subjects by localizing the cerebral sources of brain responses (namely waves N20m–P30m) which follow between 20 and 30 ms median nerve stimulation at wrist, as well as separate stimulation of the thumb and little finger 46, 51. The `hand extension' was also calculated as the distance in millimetres between the generators activated by stimulation of fifth and first fingers of the contralateral hand. Despite the relative variability of absolute values due to inter-individual anatomical differences, it was found that interhemispheric differences of such parameters are restricted both intra- and inter-individually.

The aim of the present study is to investigate by means of the technique described above, patients with a monohemispheric lesion inducing sensorimotor deficits of the contralateral hand, followed by total, partial or no recovery. This is to check for possible changes in the topography of hand primary sensory areas, both in the affected and unaffected hemispheres, and to correlate them with clinical outcome and with the location and extension of the brain lesion.