Elsevier

NeuroImage

Volume 26, Issue 1, 15 May 2005, Pages 302-308
NeuroImage

Communication
GLM-beamformer method demonstrates stationary field, alpha ERD and gamma ERS co-localisation with fMRI BOLD response in visual cortex

https://doi.org/10.1016/j.neuroimage.2005.01.050Get rights and content

Abstract

Recently, we introduced a new ‘GLM-beamformer’ technique for MEG analysis that enables accurate localisation of both phase-locked and non-phase-locked neuromagnetic effects, and their representation as statistical parametric maps (SPMs). This provides a useful framework for comparison of the full range of MEG responses with fMRI BOLD results. This paper reports a ‘proof of principle’ study using a simple visual paradigm (static checkerboard). The five subjects each underwent both MEG and fMRI paradigms. We demonstrate, for the first time, the presence of a sustained (DC) field in the visual cortex, and its co-localisation with the visual BOLD response. The GLM-beamformer analysis method is also used to investigate the main non-phase-locked oscillatory effects: an event-related desynchronisation (ERD) in the alpha band (8–13 Hz) and an event-related synchronisation (ERS) in the gamma band (55–70 Hz). We show, using SPMs and virtual electrode traces, the spatio-temporal covariance of these effects with the visual BOLD response. Comparisons between MEG and fMRI data sets generally focus on the relationship between the BOLD response and the transient evoked response. Here, we show that the stationary field and changes in oscillatory power are also important contributors to the BOLD response, and should be included in future studies on the relationship between neuronal activation and the haemodynamic response.

Introduction

Functional magnetic resonance imaging (fMRI) (Ogawa et al., 1993) has revolutionised the field of cognitive neuroscience by providing a non-invasive means of mapping human brain function. However, blood oxygenation level dependent (BOLD) fMRI, the most widely applied method, and the more quantitative MRI measurements of cerebral blood flow (CBF) or volume (CBV) are indirect measures of brain activity. It is generally assumed that these haemodynamic responses are driven by the increased metabolic demand during activation, though this is not universally accepted. Ultimately, the success of fMRI will be limited by its ability to provide a quantitative measure of brain activity, and this will depend on a full understanding of the link between the haemodynamic response and neuronal activity. Valuable insight has been gained by comparing fMRI BOLD responses with simultaneous microelectrode recordings (Heeger and Ress, 2002, Logothetis et al., 2001), but the invasive nature of this approach restricts its use to animal studies.

Magnetoencephalography (MEG) provides a direct, non-invasive measure of neuronal activity by sampling the magnetic fields arising (mainly) from post-synaptic current flow within neurons (Hamalainen et al., 1993). Comparison between fMRI and MEG data should therefore shed light on the neural basis of fMRI. Existing literature (Dale et al., 2000) focuses on a comparison between the MEG ‘evoked response’ and the fMRI BOLD response. This evoked response is usually time-locked and phase-locked to the applied stimulus and comprises transients at or near the onset and offset of the applied stimulation period. However, a number of other effects have recently been detected using MEG, all of which may be relevant if a truly accurate model of the relationship between neuronal activity and the BOLD response is to be derived.

Sustained fields comprise what appears to be a baseline shift throughout the period of stimulation (i.e., between transient spikes at stimulus onset and offset). Such fields are not generally observed in MEG because in order to suppress 1/f noise, it is normal practice to apply a high-pass filter prior to data processing. Sustained fields have also remained largely undetected in electroencephalography (EEG) since in addition to 1/f amplifier noise (similar to that observed in MEG), EEG is also subject to 1/f electrode noise (due to electro-chemical instabilities at the electrode skin interface (Mackert et al., 1999)). This leads to MEG being an improved technique with which to detect a sustained field compared to EEG. Despite these difficulties, sustained fields have been documented in primary auditory cortex using both EEG (Picton et al., 1978, Picton et al., 1980) and MEG (Hari et al., 1980, Lammertmann and Lutkenhoner, 2001) and in the primary somatosensory cortex using MEG (Forss et al., 2001).

In addition to the phase-locked transient and sustained evoked MEG responses, oscillatory effects comprising time-locked but non-phase-locked event-related synchronisation (ERS) and desynchronisation (ERD) have also been recorded using MEG (Pfurtscheller and Lopes da Silva, 1999). Further, a paper by Singh et al. (2002) has demonstrated a striking co-localisation of ERD and (positive) BOLD effects in language and visual tasks. If such oscillatory effects represent a change in the overall level of activity, it would be expected that this would be reflected in an altered metabolic requirement and hence a BOLD response, whereas, if as their names imply, they represent primarily synchronisation/desynchronisation without a change in neuronal firing rate, it is possible that they could be largely fMRI silent. In either event, they are likely to be associated with neuronal responses that do alter metabolic state and thus give rise to BOLD effects.

Recently, we have developed a new ‘GLM-beamformer’ technique (Brookes et al., 2004), that enables accurate localisation of both phase-locked and non-phase-locked neuromagnetic effects in MEG, and their representation as statistical parametric maps (SPMs). This provides an ideal framework for comparison of the full range of MEG responses with fMRI BOLD results. Here, we present the first proof of principle for this technique using a simple visual paradigm (static checkerboard). We use this new technique to demonstrate the presence of a sustained (DC) field in the visual cortex, and its co-localisation with the visual BOLD response. We also use it to investigate the main non-phase-locked oscillatory effects, as identified using a standard synthetic aperture magnetometry (SAM) metric (Robinson and Vrba, 1998), and demonstrate co-localisation of both alpha ERD and gamma ERS with the BOLD response.

All of the neuromagnetic and BOLD effects are temporally correlated with the visual paradigm [inherent to their identification by the general linear model (GLM)], and hence also with each other. We use virtual electrodes, placed at the foci of each of the neuromagnetic statistical parametric maps to investigate the detailed temporal profiles of the MEG responses. In this way, we identify a close temporal correlation between all three neuromagnetic effects. Taken together, the spatial and temporal correlations suggest that each of the neuromagnetic effects are closely associated with the fMRI BOLD response.

Section snippets

Methods

Five healthy volunteers (3 male, 2 female, age 27 ± 4 years) with no known neurological disorders, head trauma, contraindication to MR, or medication were recruited to the study, which was approved by the Ethical Committees of Aston and Nottingham Universities. Each subject participated in both MEG and fMRI studies.

Results

Table 1 summarises the results of the MEG time frequency analysis using the traditional SAM methodology. It is clear that consistent effects across subjects are observed in the 5–15 Hz band and the 55–70 Hz band. Although other effects are apparent, they are not consistent across subjects, and for this reason, the frequency bands for GLM-beamformer analysis were selected to be the alpha band (8–13 Hz) and gamma band (55–70 Hz). Fig. 1 shows the spatial distribution of the sustained field, alpha

The neuromagnetic effects

Alpha band ERD is thought to originate from the involvement of a large neural network of cell assemblies in information processing, and is a suspected prerequisite to gamma band ERS which reflects the co-operative or synchronised behaviour of a large number of neurons within a network (Pfurtscheller, 1992, Pfurtscheller and Lopes da Silva, 1999, Pfurtscheller et al., 1993). Recent findings suggest that the alpha band ERD is both increased in amplitude and spatially more widespread in tasks of

Conclusion

Using a simple visual paradigm, we have demonstrated the use of the recently introduced GLM-beamformer method of MEG analysis for identifying and mapping heterogeneous neuromagnetic effects across a wide frequency spectrum, from DC to the high gamma band. This methodology provides an ideal framework for comparison of MEG and fMRI data sets. We have demonstrated, for the first time, the presence of a stationary field in the visual cortex, and shown that it, together with alpha ERD and gamma ERS,

Acknowledgments

We are grateful to the Wellcome Trust for a Major Equipment Grant, and for continuing support of the MEG laboratory at Aston University and G.R.B. We are also grateful to the Medical Research Council for Programme Grant support (Grant Number G9900259) and a research studenship for M.J.B.

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