High-Frequency Brain Activity and Muscle Artifacts in MEG/EEG: a Review and Recommendations
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View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Online Research @ Cardiff REVIEW ARTICLE published: 15 April 2013 HUMAN NEUROSCIENCE doi: 10.3389/fnhum.2013.00138 High-frequency brain activity and muscle artifacts in MEG/EEG: a review and recommendations Suresh D. Muthukumaraswamy* CUBRIC, School of Psychology, Cardiff University, Cardiff, UK Edited by: In recent years high-frequency brain activity in the gamma-frequency band (30–80 Hz) Markus Butz, University College and above has become the focus of a growing body of work in MEG/EEG research. London, UK Unfortunately, high-frequency neural activity overlaps entirely with the spectral bandwidth Reviewed by: of muscle activity (∼20–300 Hz). It is becoming appreciated that artifacts of muscle activity Sylvain Baillet, McGill University, Canada may contaminate a number of non-invasive reports of high-frequency activity. In this Joerg F. Hipp, University of review, the spectral, spatial, and temporal characteristics of muscle artifacts are compared Tübingen, Germany with those described (so far) for high-frequency neural activity. In addition, several of *Correspondence: the techniques that are being developed to help suppress muscle artifacts in MEG/EEG Suresh D. Muthukumaraswamy, are reviewed. Suggestions are made for the collection, analysis, and presentation of CUBRIC, School of Psychology, Cardiff University, Park Place, Cardiff experimental data with the aim of reducing the number of publications in the future that CF10 3AT, UK. may contain muscle artifacts. e-mail: [email protected] Keywords: high-frequency activity, muscle artifacts, gamma-band activity, magnetoencephalography, electroencephalography In recent years high-frequency brain activity in the gamma- Unfortunately, high-frequency neural activity overlaps entirely frequency band (30–80 Hz) and above has become the focus of with the spectral bandwidth of muscle activity (∼20–300 Hz). a growing body of work in MEG/EEG1 research. Although this It is becoming appreciated that artifacts of muscle activity may focus is relatively recent, over 60 years ago, the pioneering work contaminate a number of non-invasive reports of high-frequency of Moruzzi and Magoun (1949) demonstrated that stimulation activity. Moreover, insufficient reporting of scientific data in some of the brainstem reticular formation leads to suppression of slow publications make it virtually impossible to tell post-hoc whether EEG rhythms and the emergence of low-voltage fast waves; they a particular reported effect is high-frequency activity of neural termed this phenomenon an “activated” EEG state. This concep- origin. In this review, the spectral, spatial, and temporal char- tualization of the frequency characteristics of cortical activation acteristics of muscle artifacts are compared with those described is still present in modern neuroimaging (Kilner et al., 2005; (so far) for high-frequency neural activity. In addition, several of Mukamel et al., 2007; Magri et al., 2012). With a few notable the techniques that are being developed to help suppress muscle exceptions, such as Freeman’s studies of high-frequency wave artifacts in MEG/EEG are reviewed. As will be shown, no single packets in the olfactory cortex of rabbits (Freeman, 1975)and, technique can suppress all muscle artifacts, nor does there exist later, monkey visual cortex (Freeman and van Dijk, 1987), and a single data feature that allows easy discrimination of brain and Chatrian’s observation of 50 Hz oscillations in human calcarine muscle activity. Suggestions are made for the collection, analysis, cortex during visual stimulation (Chatrian et al., 1960), higher and presentation of experimental data with the aim of reduc- frequency activity was relatively unstudied until the influential ing the number of publications in the future that may contain work of Gray and Singer (Gray et al., 1989; Gray and Singer, 1989) artifacts. suggested that these frequencies play an important role in cortical information processing. Following this suggestion, the low-pass THE CHARACTERISTICS OF MUSCLE ARTIFACTS IN MEG/EEG filters—traditionally set in EEG at around 30 Hz (Niedermeyer A good starting point is a consideration of the basic spec- and Lopes Da Silva, 2005; Fries et al., 2008)tohelpprevent tral properties of the muscles that are most likely to interfere aliasing and suppress muscle artifacts—have been increasingly with MEG/EEG recordings. It is well-known that the power elevated in an attempt to characterize high-frequency activity spectrum of contracting striated muscle, measured with surface non-invasively. As was predicted (Bressler, 1990), high-frequency electromyography, shows a bandwidth of 20–300 Hz and that activity has now been found across the neocortex and has been most of the power is in the lower end of this frequency range shown to be involved in a plethora of functions, including (Criswell, 2011) (although the higher end can extend up to 600 Hz sensory processing, movement control, memory and attention. forsomefacialmusclesduetotheirsmallersizeandhigher innervation ratio). Specifically, relevant to MEG/EEG record- ings, O’Donnell et al. (1974) found that the peak frequency of 1Note: Various frequency-band definitions exist in the literature for gamma, the masseter muscle, involved in chewing, is around 50–60 Hz, low-gamma, high-gamma, high-frequency activity, as well as fast oscillations, etc. For the purposes of this review, high-frequency activity is defined as neu- whereas for frontalis, the muscle which controls wrinkling of ral activity >∼30 Hz, and as much as possible specific numerical frequencies the brow, it is 30–40 Hz. The lower band-limit of the activity are used rather than somewhat arbitrary frequency-band categorizations. of these muscles is around 15 Hz, while the high-end activity Frontiers in Human Neuroscience www.frontiersin.org April 2013 | Volume 7 | Article 138 | 1 Muthukumaraswamy High-frequency activity and artifacts extends to well above 100 Hz (O’Donnell et al., 1974). Similarly, been described in simultaneous MEG/EEG recordings following Goncharova et al. (2003) report frequencies around 20–30 Hz for administration of the benzodiazepine secobarbitol (Claus et al., frontal muscles and 40–80 Hz for temporal muscles. For poste- 2012) where EEG showed heavy contamination with muscle arti- rior head muscles—sternocleidomastoids, splenius capitus, and facts, particularly in frontal–temporal sensors, while the MEG trapezius—higher peak frequencies (∼100 Hz) are reported, but was relatively clean, with some relatively localized peripheral these differ between muscles, direction and force of contraction contamination. as well as participants’ sex (Kumar et al., 2003). The extraocular muscles that contain both striate and smooth fibres and con- THE CHARACTERISTICS OF HIGH-FREQUENCY NEURAL trol saccadic eye movements produce activity that peaks around ACTIVITY IN MEG/EEG/iEEG 65 Hz (Yuval-Greenberg et al., 2008; Carl et al., 2012). Although Having defined the basic characteristics of muscle artifacts peak frequencies of the various head muscles differ between mus- in MEG/EEG, we now consider properties of neuronal high- cles, the types of contraction and participants, one key feature to frequency activity. The following summary is not a comprehen- note is that in general the spectral bandwidth of muscle activity is sive review of all high-frequency MEG/EEG/iEEG papers; rather, broad. it provides indicative examples that demonstrate the known The amplitude of muscle activity when recorded in tem- diversity of high-frequency responses observed in the brain [other poral MEG/EEG electrodes and sensors can be ∼1000 fT and useful review articles the reader may wish to consult include 100 µV, respectively. This is several orders of magnitude larger (Fries, 2009; Jerbi et al., 2009b; Donner and Siegel, 2011)]. A par- than what one might expect from high-frequency activity, which ticular emphasis is made on the studies that use intracranial EEG can be less than 20 fT and 1 µV in MEG and EEG, respectively (iEEG), because in comparison to MEG/EEG studies, iEEG tends (Herrmann and Demiralp, 2005). The tiny size of these neu- to be significantly less affected by artifacts, and can therefore indi- ral oscillations relative to the size of potential muscle artifacts cate the morphology of responses that MEG/EEG studies might is highly problematic. While large muscle artifacts can easily be characterize. That said, because the transfer function between screened and removed from data, small muscular artifacts can iEEG to MEG/EEG is not completely understood, it may be that pass such screening and remain present in so-called artifact-free some activity present in the iEEG is absent from the MEG/EEG. MEG/EEG recordings. The existence of muscular contamination of the EEG has been empirically shown in several elegant experi- TYPES OF HIGH-FREQUENCY ACTIVITY ments that used neuromuscular blockade (Whitham et al., 2007, It is useful to first define four types of high-frequency activity that 2008). In this experimental model, EEG recordings were made are commonly described in the literature. Firstly, there is resting during complete neuromuscular blockade with cisatracurium high-frequency activity, which is usually based on the frequency (which is functionally similar to curare). This allowed the EEG spectrum of the MEG/EEG measured while participants passively to be recorded with no EMG artifacts and to be compared to sit with their eyes open