High-frequency brain activity and muscle artifacts in MEG/EEG: A review and recommendations

In recent years high-frequency brain activity in the gamma-frequency band (30–80 Hz) and above has become the focus of a growing body of work in MEG/EEG research. Unfortunately, high-frequency neural activity overlaps entirely with the spectral bandwidth of muscle activity (~20–300 Hz). It is becoming appreciated that artifacts of muscle activity may contaminate a number of non-invasive reports of high-frequency activity. In this review, the spectral, spatial, and temporal characteristics of muscle artifacts are compared with those described (so far) for high-frequency neural activity. In addition, several of the techniques that are being developed to help suppress muscle artifacts in MEG/EEG are reviewed. Suggestions are made for the collection, analysis, and presentation of experimental data with the aim of reducing the number of publications in the future that may contain muscle artifacts

BOLD responses in human primary visual cortex are insensitive to substantial changes in neural activity

The relationship between blood oxygenation level dependent-functional magnetic resonance imaging (BOLD-fMRI) and magnetoencephalography (MEG) metrics were explored using low-level visual stimuli known to elicit a rich variety of neural responses. Stimuli were either perceptually isoluminant red/green or luminance-modulated black/yellow square-wave gratings with spatial frequencies of 0.5, 3, and 6 cycles per degree. Neural responses were measured with BOLD-fMRI (3-tesla) and whole head MEG. For all stimuli, the BOLD response showed bilateral activation of early visual cortex that was greater in the contralateral hemisphere. There was variation between individuals but weak, or no evidence, of amplitude dependence on either spatial frequency or the presence of luminance contrast. In contrast, beamformer analysis of MEG data showed activation in contralateral early visual cortex and revealed: (i) evoked responses with stimulus-dependent amplitude and latency; (ii) gamma and high-beta oscillations, with spatial frequency dependent peaks at approximately 30 and 50 Hz, but only for luminance-modulated gratings; (iii) The gamma and beta oscillations appeared to show different spatial frequency tuning profiles; (iv) much weaker gamma and beta responses, and at higher oscillation frequencies, for isoluminant compared to luminance-modulated gratings. The results provide further evidence that the relationship between the fMRI-BOLD response and cortical neural activity is complex, with BOLD-fMRI being insensitive to substantial changes in neural activity. All stimuli were clearly visible to participants and so the paucity of gamma oscillations to isoluminant stimuli is inconsistent with theories of their role in conscious visual perception

Acute effects of alcohol on stimulus-induced gamma oscillations in human primary visual and motor cortices

Alcohol is a rich drug affecting both the γ-amino butyric acid (GABA) and glutamatergic neurotransmitter systems. Recent findings from both modeling and pharmacological manipulation have indicated a link between GABAergic activity and oscillations measured in the gamma frequency range (30–80 Hz), but there are no previous reports of alcohol’s modulation of gamma-band activity measured by magnetoencephalography (MEG) or electroencephalography (EEG). In this single-blind, placebo-controlled crossover study, 16 participants completed two study days, on one day of which they consumed a dose of 0.8 g/kg alcohol, and on the other day a placebo. MEG recordings of brain activity were taken before and after beverage consumption, using visual grating and finger abduction paradigms known to induce gamma-band activity in the visual and motor cortices respectively. Time–frequency analyses of beamformer source reconstructions in the visual cortex showed that alcohol increased peak gamma amplitude and decreased peak frequency. For the motor task, alcohol increased gamma amplitude in the motor cortex. These data support the notion that gamma oscillations are dependent, in part, on the balance between excitation and inhibition. Disruption of this balance by alcohol, by increasing GABAergic inhibition at GABAA receptors and decreasing glutamatergic excitation at N-methyl-D-aspartic acid receptors, alters both the amplitude and frequency of gamma oscillations. The findings provide further insight into the neuropharmacological action of alcohol

Orientation discrimination performance is predicted by GABA concentration and gamma oscillation frequency in human primary visual cortex

Neuronal orientation selectivity has been shown in animal models to require corticocortical network cooperation and to be dependent on the presence of GABAergic inhibition. However, it is not known whether variability in these fundamental neurophysiological parameters leads to variability in behavioral performance. Here, using a combination of magnetic resonance spectroscopy, magnetoencephalography, and visual psychophysics, we show that individual performance on a visual orientation discrimination task is correlated with both the resting concentration of GABA and the frequency of stimulus-induced gamma oscillations in human visual cortex. Behaviorally, a strong oblique effect was found, with the mean angular threshold for oblique discrimination being five times higher than that for vertically oriented stimuli. Similarly, we found an oblique effect for the dependency of performance on neurophysiological parameters. Orientation detection thresholds were significantly negatively correlated with visual cortex GABA concentration for obliquely oriented patterns (r = −0.65, p < 0.015) but did not reach significance for vertically oriented stimuli (r = −0.39, p = 0.2). Similarly, thresholds for obliquely oriented stimuli were negatively correlated with gamma oscillation frequency (r = −0.65, p < 0.017), but thresholds for vertical orientations were not (r = −0.02, p = 0.9). Gamma oscillation frequency was positively correlated with GABA concentration in primary visual cortex (r = 0.67, p < 0.013). These results confirm the importance of GABAergic inhibition in orientation selectivity and demonstrate, for the first time, that interindividual performance on a simple visual task is linked to neurotransmitter concentration. The results also suggest a key role for GABAergic gamma oscillations in visual discrimination tasks

Elevating endogenous GABA levels with GAT-1 blockade modulates evoked but not induced responses in human visual cortex

The electroencephalographic/magnetoencephalographic (EEG/MEG) signal is generated primarily by the summation of the postsynaptic currents of cortical principal cells. At a microcircuit level, these glutamatergic principal cells are reciprocally connected to GABAergic interneurons. Here we investigated the relative sensitivity of visual evoked and induced responses to altered levels of endogenous GABAergic inhibition. To do this, we pharmacologically manipulated the GABA system using tiagabine, which blocks the synaptic GABA transporter 1, and so increases endogenous GABA levels. In a single-blinded and placebo-controlled crossover study of 15 healthy participants, we administered either 15 mg of tiagabine or a placebo. We recorded whole-head MEG, while participants viewed a visual grating stimulus, before, 1, 3 and 5 h post tiagabine ingestion. Using beamformer source localization, we reconstructed responses from early visual cortices. Our results showed no change in either stimulus-induced gamma-band amplitude increases or stimulus-induced alpha amplitude decreases. However, the same data showed a 45% reduction in the evoked response component at ~80 ms. These data demonstrate that, in early visual cortex the evoked response shows a greater sensitivity compared with induced oscillations to pharmacologically increased endogenous GABA levels. We suggest that previous studies correlating GABA concentrations as measured by magnetic resonance spectroscopy to gamma oscillation frequency may reflect underlying variations such as interneuron/inhibitory synapse density rather than functional synaptic GABA concentrations

Broadband Cortical Desynchronization Underlies the Human Psychedelic State

Psychedelic drugs produce profound changes in consciousness, but the underlying neurobiological mechanisms for this remain unclear. Spontaneous and induced oscillatory activity was recorded in healthy human participants with magnetoencephalography after intravenous infusion of psilocybin—prodrug of the nonselective serotonin 2A receptor agonist and classic psychedelic psilocin. Psilocybin reduced spontaneous cortical oscillatory power from 1 to 50 Hz in posterior association cortices, and from 8 to 100 Hz in frontal association cortices. Large decreases in oscillatory power were seen in areas of the default-mode network. Independent component analysis was used to identify a number of resting-state networks, and activity in these was similarly decreased after psilocybin. Psilocybin had no effect on low-level visually induced and motor-induced gamma-band oscillations, suggesting that some basic elements of oscillatory brain activity are relatively preserved during the psychedelic experience. Dynamic causal modeling revealed that posterior cingulate cortex desynchronization can be explained by increased excitability of deep-layer pyramidal neurons, which are known to be rich in 5-HT2A receptors. These findings suggest that the subjective effects of psychedelics result from a desynchronization of ongoing oscillatory rhythms in the cortex, likely triggered by 5-HT2A receptor-mediated excitation of deep pyramidal cells

The use of magnetoencephalography in the study of psychopharmacology (pharmaco-MEG)

Magnetoencephalography (MEG) is a neuroimaging technique that allows direct measurement of the magnetic fields generated by synchronised ionic neural currents in the brain with moderately good spatial resolution and high temporal resolution. Because chemical neuromodulation can cause changes in neuronal processing on the millisecond time-scale, the combination of MEG with pharmacological interventions (pharmaco-MEG) is a powerful tool for measuring the effects of experimental modulations of neurotransmission in the living human brain. Importantly, pharmaco-MEG can be used in both healthy humans to understand normal brain function and in patients to understand brain pathologies and drug-treatment effects. In this paper, the physiological and technical basis of pharmaco-MEG is introduced and contrasted with other pharmacological neuroimaging techniques. Ongoing developments in MEG analysis techniques such as source-localisation, functional and effective connectivity analyses, which have allowed for more powerful inferences to be made with recent pharmaco-MEG data, are described. Studies which have utilised pharmaco-MEG across a range of neurotransmitter systems (GABA, glutamate, acetylcholine, dopamine and serotonin) are reviewed

Functional properties of human primary motor cortex gamma oscillations

Gamma oscillations in human primary motor cortex (M1) have been described in human electrocorticographic and noninvasive magnetoencephalographic (MEG)/electroencephalographic recordings, yet their functional significance within the sensorimotor system remains unknown. In a set of four MEG experiments described here a number of properties of these oscillations are elucidated. First, gamma oscillations were reliably localized by MEG in M1 and reached peak amplitude 137 ms after electromyographic onset and were not affected by whether movements were cued or self-paced. Gamma oscillations were found to be stronger for larger movements but were absent during the sustained part of isometric movements, with no finger movement or muscle shortening. During repetitive movement sequences gamma oscillations were greater for the first movement of a sequence. Finally, gamma oscillations were absent during passive shortening of the finger compared with active contractions sharing similar kinematic properties demonstrating that M1 oscillations are not simply related to somatosensory feedback. This combined pattern of results is consistent with gamma oscillations playing a role in a relatively late stage of motor control, encoding information related to limb movement rather than to muscle contraction

Primary motor cortex activation during action observation revealed by wavelet analysis of the EEG

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