Combined MEG and EEG methodology for non-invasive recording of infraslow activity in the human cortex

Abstract

Objective

Periinfarct depolarisation and spreading depression represent key mechanisms of neuronal injury after stroke. Changes in cortical electrical potentials and magnetic fields in the very low frequency range are relevant parameters to characterize these events, which up to now have only been recorded invasively. In this study, we proved whether a non-invasive combined MEG/EEG recording technique is able to quantitatively monitor cortical infraslow activity in humans.

Methods

We used repetitive very slow and slow right finger movements as a physiological motor activation paradigm to induce cortical infraslow activity. Infraslow fields were recorded over the left hemisphere using a modulation-based MEG technique. EEG was performed using 16 standard Ag-Cl electrodes that covered the left motor cortex.

Results

We recorded stable focal motor-related infraslow magnetic field changes in seven out of seven subjects. We also found correlating infraslow electrical potential changes in three out of seven subjects. Slow finger movements generated significantly stronger field and potential changes than very slow movements.

Conclusions

This study demonstrates the technical feasibility of combined non-invasive electrical potential and magnetic field measurements to localize and quantitatively monitor physiological, low amplitude, infraslow cortical activity in humans. This specific combination of simultaneous recording techniques allows to benefit from the specific physical advantages of each method.

Significance

This combined non-invasive MEG–EEG methodology is able to provide important information on infraslow neuronal activity originating from tangentially and radially oriented sources. Moreover, this dual approach has the potential to separate neuronal from non-neuronal DC-sources, e.g., radially to the head orientated DC-currents across the skin/scalp/skull/dura occurring during cerebral hypercapnia or hypoxia.

Introduction

Slowly changing depolarisations of the cerebral gray matter are observed in border zones of ischemic foci. These slow potential shifts are referred to as periinfarct depolarisations (PID) and cortical spreading depressions (CSD). PID and CSD caused infarct expansion in animal models of focal cerebral ischemia (Hossmann, 1994). Experimental neuroprotective treatments for stroke decreased the incidence of PID and CSD (Williams et al., 2003). Advances in non-invasive measurements of infraslow potential shifts, as surrogates of PID and CSD, are likely to support the design of novel diagnostic and therapeutic strategies in the treatment of stroke. To date, CSD measurements are restricted to invasive techniques, such as recordings with subdural electrocorticographic strip electrodes (Strong et al., 2002, Fabricius et al., 2006, Dreier et al., 2006). However, these invasive techniques are only possible in very few human individuals after craniotomy.

Cerebral infraslow electrical activity can be measured non-invasively with two different techniques: Direct Current-Magnetoencephalography (DC-MEG) and Direct Current-Electroencephalography (DC-EEG). In this study, the term “infraslow” activity is used to describe very slow current changes or field changes in the range below 0.1 Hz (Vanhatalo et al., 2005). In the past, non-invasive recordings of very slowly changing cortical depolarisations were compromised by large baseline drift artefacts, which were much higher than the biological signals of interest (Barkley et al., 1991). First experimental non-invasive infraslow magnetic field recordings in humans were reported by employing a modulation-based MEG technique (Cohen, 1969). Over the last decade, MEG techniques have been refined. Now, these techniques enable the measurement of pathological infraslow magnetic field changes (Bowyer et al., 2005), as well as physiological infraslow magnetic field changes (Mackert et al., 1999, Mackert et al., 2001). The detection of slow electrical potential shifts requires a direct coupled (DC) EEG with a bandwidth starting from 0 Hz (Vanhatalo et al., 2003). Recent advances in amplifier technique and electrode design now allow the detection of infraslow potential shifts in humans non-invasively (Vanhatalo et al., 2003, Tallgren et al., 2005).

MEG and EEG are sensitive to different orientations of source generators (Barkley et al., 1991). The human cortex is folded forming fissures with dipole layers orthogonal to the cortex surface. MEG is insensitive to radial dipoles, but sensitive to dipoles that are tangential to the scalp, such as currents in the wall of fissures. By contrast, EEG is most sensitive to dipoles that are oriented radially to the scalp, e.g., sources generated by dipoles in the crown and floor of fissures.

In the present study, we aimed to detect, localize and quantitatively monitor cortical infraslow activity in the human cerebral cortex using simultaneous MEG and EEG measurements. This specific combination allows to benefit from the physical advantages of each method. To induce changes in focal cortical infraslow activity, a physiological motor activation paradigm was used, in which subjects performed self-paced repetitive slow and very slow finger movements.