Hemispheric asymmetry of hand representation in human primary somatosensory cortex and handedness

doi:10.1016/j.clinph.2008.04.300

Clinical Neurophysiology

Volume 119, Issue 11, November 2008, Pages 2579-2586

https://doi.org/10.1016/j.clinph.2008.04.300 Get rights and content

Abstract

Objective

To evaluate interhemispheric differences of hand representation in primary somatosensory (SI) and motor (MI) cortices and its relation to handedness.

Methods

MRI-based EEG dipole source analysis was performed separately for early (P14, N20, P22) and middle/late latency (P30, N60, N110) SEP components after left and right median nerve stimulation. In addition, the location of the MI hand area (Ω region) and handedness were determined.

Results

Equivalent current dipoles (ECDs) of N20, P30 and N60 SEP components were localized in contralateral SI (area 3b, N20 and P30; area 1, N60), the mean P22 ECD localization was in area 4 of contralateral MI. In contrast to the Ω region and the precentral P22 component, ECDs in both areas 3b and 1 were located more laterally in the right than in the left hemisphere. ECDs in the right SI lay more laterally than the ipsilateral Ω region. Asymmetry in SI was not correlated with handedness.

Conclusions

The data demonstrate that the location of hand representation shows relevant hemispheric asymmetry in human SI, both in areas 3b and 1.

Significance

Hemispheric asymmetry in SI must be considered in the studies on cortical reorganization and plasticity in SI as well as for transcranial magnetic stimulation (TMS) over SI.

Introduction

For studies investigating cortical reorganization and plasticity of the primary sensorimotor cortex (SMI), it is fundamental to know to what extent hemispheric asymmetry of functional SMI representations (e.g. hand) exists in healthy subjects. Lesions of peripheral nerves (Karl et al., 2001), CNS lesions (Rossini et al., 1998) and post-stroke rehabilitation therapy (Liepert et al., 2000) are capable to induce cortical reorganization in terms of spatial shifts or enlargements of SMI representations in the affected hemisphere. In addition, neurological and psychiatric diseases might be accompanied by abnormal hemispheric asymmetry of functional representations in primary motor (MI) and primary somatosensory (SI) cortices (Altamura et al., 2007, Reite et al., 2003). In the case of hemispheric homology of functional representations in MI and SI cortices, findings of relevant interhemispheric differences in patients may well be interpreted as the result of cortical reorganization processes. This interpretation would be misleading if asymmetric topography of MI and SI representations existed. The data currently available about interhemispheric differences of hand representation in SI are inconsistent. EEG and MEG studies provide both the evidence of non-significant (Rossini et al., 1994, Tecchio et al., 1997) and significant interhemispheric differences of equivalent current dipole (ECD) locations in area 3b of SI (Jung et al., 2003, Sutherland and Tang, 2006, Wikström et al., 1997). In the latter ones, ECDs are located 2.5–7.5 mm more laterally in the right than in the left SI.

In the axial plane, a knob-like structure of the precentral gyrus is regarded as the anatomical landmark of the hand area in MI (Yousry et al., 1997). In 90% of subjects, it has the shape of an inverted omega (Ω region). The Ω region is used as a target and routing structure in anatomical magnetic resonance imaging (MRI)-guided frameless stereotaxic neuronavigation (Sparing et al., 2007). It has been frequently assumed that the postcentral hand area of SI is located strictly opposite to the precentral Ω region (Hirayama et al., 2006). But if hand representations of MI and SI were not on the same level on mediolateral and ventrodorsal axes, it would comprise suboptimal focal transcranial magnetic stimulation (TMS) for the induction of plasticity (Tegenthoff et al., 2005, Wolters et al., 2005) and “virtual lesions” (Pascual-Leone et al., 1999) in SI.

In this study, an intra- and interhemispheric comparison of ECD localizations of major somatosensory evoked potential (SEP) components was performed, utilizing MRI-coregistered EEG dipole source analysis. In contrast to the previous studies (Jung et al., 2003, Sutherland and Tang, 2006, Tecchio et al., 1997, Wikström et al., 1997), our analysis included area 1 of SI and was not limited to area 3b. In addition, we investigated the spatial relation between the hand area in MI (Ω region) and in SI (ECD localizations) in both hemispheres for the first time.

Section snippets

Subjects

We investigated 16 healthy subjects (ages ranged from 23 to 28 years, mean age: 24.3 years; 8 female). According to the Edinburgh Inventory, the average handedness score was 70 ± 12, and two of the subjects were considered as left-handers (score < 0). All subjects gave their written informed consent to participate in the study. The study was approved by the local ethics committee.

Subjects were comfortably seated in an electrically shielded, noise- and light-reduced room which had a constant

Localization of SMI dipole generators

Both the dipole model of early and of middle/late latency SEP components contained two ECDs close to the central sulcus (N20, P22 and P30, N60, respectively) in each hemisphere (Fig. 1). The estimated ECD locations showed considerable interindividual consistency as indicated by the rather small variations of spatial ECD coordinates (all SEM < 3 mm). Projected onto individual AC–PC aligned MR images using BrainVoyager QX, ECDs of N20, P30, N60 SEP components were located postcentrally in most cases

Discussion

The main findings in this study are the more lateral (about 7 mm) localizations of ECDs (N20, P30, N60) in the right than in the left SI, both in area 3b (N20, P30) and in area 1 (N60), in contrast to symmetric locations of the presumably precentrally generated P22 source and the Ω region. As a consequence, ECDs of the SI hand area are localized about 7 mm lateral to the Ω region in the right hemisphere whereas MI and SI hand areas are on a level in the left hemisphere.

Acknowledgements

This study was supported by the Deutsche Forschungsgemeinschaft (Tr236/13). Thanks to Barbara Bliem for the attentive revision of the manuscript.

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Hemispheric asymmetry of hand representation in human primary somatosensory cortex and handedness

Abstract

Objective

Methods

Results

Conclusions

Significance

Introduction

Section snippets

Subjects

Localization of SMI dipole generators

Discussion

Acknowledgements

Electroencephalogr Clin Neurophysiol

Exp Neurol

Neuroimage

Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Comput Biomed Res

Electroencephalogr Clin Neurophysiol

Clin Neurophysiol

Brain Lang

Pain

Neuroimage

Neurosci Res

Electroencephalogr Clin Neurophysiol

Clin Neurophysiol

Neuropsychologia

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Neurosci Lett

Neuroimage

Brain Res

Neuroimage

Clin Neurophysiol

Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Electroencephalogr Clin Neurophysiol

Human cortical potentials evoked by stimulation of the median nerve. I. Cytoarchitectonic areas generating short-latency activity

J Neurophysiol

Potentials evoked in human and monkey cerebral cortex by stimulation of the median nerve. A review of scalp and intracranial recordings

Brain