Hand cortical representation at rest and during activation: Gender and age effects in the two hemispheres

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Abstract

Objective

To characterize the age- and gender- dependence of sensory hand cortical representation in the two hemispheres in healthy population.

Methods

In 57 adults, the cerebral activity from rolandic areas as detected by magnetoencephalography was considered both in a resting state (spectral power properties) and in response to the electrical stimulation of the contralateral median nerve (M20 and M30 cortical sources).

Results

We found a dependence of rest and evoked activity on age (alpha rhythm slowing, high frequency power increase, M20 latency increase, M20 strength increase, no change in M30) and on gender (higher alpha frequency, higher beta power, higher spectral entropy, lower M20 amplitude in women). These changes were quite symmetrical in the two hemispheres, making the interhemispheric differences non-dependent on age and gender. Moreover, lower total power and faster alpha rhythm appeared in the dominant hemisphere.

Conclusions

Age and gender have a significant effect on spontaneous and evoked activity at the primary sensorimotor cortex.

Significance

The results consolidate the reference base in healthy population, to study pathological conditions. Inter-hemispheric asymmetries are confirmed as a sensitive indicator for the early identification of possible neuronal rearrangements due to unilateral brain injuries.

Introduction

Cortical primary sensorimotor areas devoted to hand control have been amply studied through neurophysiological techniques (Allison, 1987, Desmedt and Cheron, 1981, Hallet, 1996, Rossini et al., 1987, Tecchio et al., 1997): in fact, the understanding of neural hand control organization in physiological situations is an essential step for identification of possible rearrangements that contribute to functional recovery in pathological conditions, such as stroke, dystonia, brain trauma, carpal tunnel syndrome and multiple sclerosis.

Magnetoencephalography (MEG) is a non-invasive technique, which detects at the cranial surface magnetic fields generated by post-synaptic currents associated with synchronous neuronal firing in the brain at rest or in response to an external stimulus. Because of its physical properties, MEG signals are not influenced by extra-cerebral intervening tissues and do not need any reference electrodes; they therefore, localize accurately the brain sources of stimulus-related electromagnetic activities (for a review see Del Gratta et al., 2001).

The neurophysiological responses to electrical median nerve stimuli as detected by electroencephalography (EEG, Somatosensory Evoked Potential, SEP) or MEG (Somatosensory Evoked Fields, SEF) have been widely described in healthy subjects with respect to age and gender (Allison, 1987, Hume et al., 1982, Huttunen et al., 1999, Shaw, 1992, Strenge and Hedderich, 1982, Tanosaki et al., 1999) and are currently used in clinical practice to identify and monitor abnormalities (Mauguiere, 1996). The spectral content of the neuronal oscillatory activity ‘at rest’ (quantitative EEG, Nuwer, 1988), providing a brain-state measure that reflects complex thalamo-cortical and cortico-cortical functional connectivity (Steriade, 2001, Steriade et al., 1990), has been widely studied in normal populations (for a review, see Van Sweden et al.,1997), leading to the identification of alterations of the cerebral background activity in different neurological diseases, like brain trauma, stroke or Alzheimer disease (Jeong, 2004, Niedermeyer, 1997a).

The anatomical and functional organization of primary sensorimotor areas was found to be fairly symmetric in both hemispheres by different morphological, functional metabolic and neurophysiological techniques (Hallet, 1996, Puce et al., 1995, Rossini et al., 1994, Tecchio et al., 1997, Wikstrom et al., 1997). The quantitative description of the asymmetries has shown an increased sensitivity of the neurophysiological characterization in the case of unilateral impairments (Oliviero et al., 2004, Rossini et al., 2001, Tecchio et al., 2005a, Wikstrom et al., 1999). There is evidence from EEG studies about a mild asymmetry in occipital alpha, with a higher voltage in the right hemisphere (Kellaway and Maulsby, 1996, Kiloh et al., 1972, Simon, 1977, Wieneke et al., 1980). No studies investigated the dependence of resting state inter-hemispheric asymmetries on age and gender.

In the present study, the neural activity properties as detected by MEG were considered both in resting state and in response to electrical stimulation of the median nerve, to evaluate: if any ‘age’ marker could be identified, possibly differentiated by the two genders, and to consolidate the normative base to study pathological conditions. The parameters describing the sensorimotor organization were quantified in terms of both absolute values and their inter-hemispheric differences.

Section snippets

Subjects

MEG recordings were performed in 57 right-handed healthy volunteers (31 males, mean age 44±22 years, range 23–95; 26 females, mean age 46±22 years, range 24–91; t test between the age of male and female group P=0.668). Handedness was evaluated by means of the Edinburgh Manuality test (Oldfield, 1971); the average score across subjects was 85±17. All subjects resulted normal at neurological exam and did not receive any pharmacological treatment at the time of recordings. All subjects above 55

Rest activity

A strong inter-individual variability in the PSD shape and in the amount of absolute and relative band power was found. In Fig. 1, the principal classes of rPSD typology are shown. In 5 subjects, we observed strong representation of rPSD in low-frequency bands and the absence of alpha peaks, with distribution of power (of low amplitude) in beta band (Fig. 1 a1): all subjects were younger than 35 (f, 26; f, 26; f, 34; m, 23; m 24). In the other subjects, alpha and beta band activity was clearly

Inter-hemispheric asymmetries

Results on evoked activity confirmed the physiological symmetries of left and right somatosensory hand representation previously reported (Tecchio et al., 1997, Wikstrom et al., 1997). A strong inter-hemispheric symmetry of rolandic resting activity was observed. The inter-hemispheric asymmetries did not show any dependence on demographical factors, although some parameters, related both to rest and evoked activity, varied with age and gender. For this reason they could be considered more

Acknowledgments

This work has been partially supported by the RBNE01AZ92_003, PNR 2001–2003, Fondi di Investimento per la Ricerca di Base (FIRB), by the European IST/FET Integrated Project NEUROBOTICS- The fusion of NEUROscience and roBOTICS (Project no. 001917 under the 6th Framework Programme) and by RF2003 conv. PS/03/10 of the Italian Department of Health.

The Authors thank Prof. Gian Luca Romani for his continuous support.

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