Magnetoencephalography (MEG) and Its Clinical Applications: Comparison
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MEG has two clinical applications, i.e., localization of epileptic foci and pre-operative evaluation for brain surgery candidates. MEG is also an important neuroimaging tool for the therapeutic planning of several mental disorders and abnormality analysis such as epilepsy, autism, schizophrenia, stroke, head trauma, and monitoring of drug administration

  • magnetoencephalography (MEG)
  • clinical application

1. Introduction

A systematic analysis for the Global Burden of Disease (GDB) study reveals that, as of Y2016, neurological disorders were the major cause of Disability Adjusted Life Years (DALYs) and are the second leading cause of deaths [1]. Neurological disorders are associated with structural and functional abnormalities and can be identified by several diagnostic imaging tools. Generally, the decrease in brain volume as a result of cerebral atrophy is one of the common characteristics associated with structural abnormalities of brain for many neurological disorders. As an example, patients diagnosed with Parkinson’s disease show a slight decrease in substantia nigra in comparison with normal control subjects [2]. However, the degeneration of neurons of substantia nigra is significantly higher in patients with chronic Parkinson’s disease in comparison to the early stage of the disease.
Other main neurological disorders manifest in specific ways. Memory loss is the vital symptom of Alzheimer’s disease, affects older adults, and is the common cause of dementia. Epilepsy is characterized by random seizures and complex seizures involving loss of consciousness. Schizophrenia is a mental disorder that affects the way a person thinks, acts, expresses emotions, perceives reality, and relates to others, and the symptoms appear early in men. Autism is a mental disorder that sways how a person perceives and socializes with others, causing problems in social interaction and communication.
Multiple neuroimaging approaches, viz., magnetic resonance imaging (MRI), functional magnetic resonance imaging (fMRI), positron emission tomography (PET), electroencephalography (EEG), and magnetoencephalography (MEG) are used as diagnostics tool in medical imaging. These neuroimaging tools are used to identify the structural and functional changes in the brain, and can therefore assist in early diagnosis and disease prognosis. MRI, which offers a high spatial resolution (on a scale of millimetres), is used extensively as a clinical neuroimaging tool to identify both the structural and functional changes associated with neurological disorders. The temporal resolution of MEG was found to be better than fMRI and PET, since their resolution is on the order of seconds. MEG picks the fields generated by intraneuronal currents and hence provides a direct index of neuronal activity and synaptic current [3]. The neuroimaging tools of MEG and EEG are generally coupled together since they both reflect the electrophysiological phenomena occurring in the brain. They do not only provide direct structural information about the brain but also create a direct environment for understanding functional aspects of the brain with a high temporal resolution (on a scale of milliseconds).
The human brain is a complex organ that consists of about 86 billion neurons and over (2.42 ± 0.29) × 1014 synapses that assist in communication between the neurons [4]. The top layer of the brain, the cerebral cortex, is about 2–4 mm thick. Neuronal activity within the cerebral cortex is associated with action potentials in axons, neurotransmitters synapses, and postsynaptic currents in post-synaptic dendrites of the pyramidal cells. Post-synaptic primary currents, elicited by neuronal activity, are the primary sources of MEG and EEG signals [5]. Thus, associated electromagnetic fields are direct ways to monitor and evaluate cortical processing in resting-state or challenge conditions [6].
Oscillatory brain activity, i.e., brain waves, are generated as a result of synchronized neuronal activity which could potentially be a biomarker for various physiological functions and behavioural states. The cortical rhythms can be categorized in several ways [7]. Brain waves are classified into five major types based on their frequencies: Delta (0.5–4 Hz), Theta (4 Hz), Alpha (8–12 Hz), Beta (12–35 Hz), and Gamma (>35 Hz) [8]. MEG is used to detect the brain waves generated across different regions of the brain, and its amplitude can be calculated by Power Spectral Density (PSD) analysis.
MEG is an ideal candidate for clinical applications in patients who cannot undergo a stringent clinical procedure before and during imaging. The first MEG signal was measured in 1968 at the University of Illinois by physicist David Cohen using the copper induction coil as detector, which resulted in MEG signals [9] with inadequate signal to noise ratio (SNR). Later, the Super Conducting Quantum Interference Device (SQUID), developed by Zimmerman, was used, which increased the SNR of the MEG signals and thereby paved the way to acquire the MEG signals without signal averaging [10][11]. In commercial MEG equipment, several sensors were placed as an array, like a helmet model, which enhanced the effective measurement and the spatial resolution of the MEG signals. With the technological advancements over the last decades, e.g., whole head coverage, sophisticated noise suppression algorithms, and zero boil-off helium systems, MEG has been evolved as a multichannel whole-head MEG system and finds its application in clinical imaging. Modern MEG systems are equipped, e.g., with 306 sensors (Figure 1). One of the current designs includes sensors comprising magnetometers and gradiometers within one sensor element. Such a design facilitates improved signal-to-noise for nearby cortical sources, suppression of ambient noise, and even suppression of nearby artifacts produced by, e.g., vagus nerve stimulators, cardiac pacemakers, and deep-brain stimulators.
 
 

2. Clinical Application

2.1. Epilepsy

According to WHO, around 50 million people across the globe are affected by epilepsy—a chronic non-communicable brain disease. The symptoms include recurrent seizures and involve either the whole brain (generalized) or part of the brain (focal), accompanied by loss of consciousness and control of bowel or bladder function in certain cases.
The functional neural network topology for epilepsy subjects is different from the healthy subjects, especially in the theta band. In epilepsy, some regions of the brain generate abnormal electrical signals, which in turn create magnetic signals and therefore can be detected by MEG. Scott B. Wilson et al. performed a detailed study on the detection of a spike in neuro signals [12]. The spatial accuracy of MEG is good since distortion is less in MEG signals when compared with the EEG signals. The EEG and MEG epileptic spikes are identified in the time and frequency domain methods [13]. MEG finds its application in the detection of interictal epileptiform discharges and localizing functional cortices, to guide neurosurgical procedures [14]. The linear discriminant analysis (LDA) classifier was used for the classification of MEG data obtained from 15 healthy subjects and 18 epilepsy patients [15]. A two-stage algorithm comprising beamforming by virtual sensors and time-frequency analysis by Stockwell transform was used to detect the high-frequency signals that help in the presurgical planning [16]. The structural images from imaging modalities, viz., MRI, PET, and SPECT data of the patients, are usually co-registered with MEG for the epilepsy surgery evaluation [17]. The genetic algorithm with K- nearest neighbor was used for the classification of epileptical MEG spikes [18]. In [19], coherence analysis for epilepsy patients was performed on MEG data. The nonlinear signal analysis was found to be effective in the analysis of Idiopathic Generalized Epilepsy (IGE) and from healthy volunteers of 10 subjects [20]. MEG, being a non-invasive technique, is a potential tool for epilepsy surgery evaluation and can determine the abnormalities observed in structural and functional mapping [21]. MEG is an effective tool for children with intractable focal epilepsy to determine the surgical candidacy and focal cortical resection to stop seizures [22]. Recently [23] an optically pumped MEG (OPM) has been used to study epilepsy. The OPM, a cryogen-free MEG system, can be directly placed over the scalp and is invariant to head motion. The performance of OPM was found to be similar to EEG in the detecting the markers of epilepsy. The OPM, on the other hand, utilizes only 20–50 sensors placed over the suspected region; therefore, this method does not provide whole head coverage. (Figure 2)
 
 

2.2. Alzheimer’s Disease (AD)

AD is one of the common neurodegenerative diseases that affects over 60–70% of the 47.5 million people with dementia across the globe, according to Dementia fact sheet WHO. The onset of the disease happens several years before it is clinically diagnosed. AD is characterized by three stages. The first stage is a pre-clinical phase, which lasts for over a decade. During this stage, an abnormal biomarker pattern is exhibited and low amyloid β42 in cerebrospinal fluid (CSF) or increased tracer detection is shown in PET imaging. Towards the end of the first stage, neurodegeneration or injury is found. The second phase exhibits Mild Cognitive Impairment (MCI) and the third state is Alzheimer’s dementia. Therefore, there is need for the early intervention during the pre-dementia phases.
The identification of biomarkers for the neurodegenerative diseases will help in early diagnosis or the onset of the disease. For AD, Amyloid-β deposition is a well-established clinical biomarker, which starts several decades before the onset of the AD [24][25][26]. However, several research studies are being conducted in search of electrophysiological/electromagnetic markers for AD, which could assist in evaluating the early diagnosis of the pre-dementia phases. The report by [27] had identified a relation between the Amyloid-β deposition and the changes in the regional brain wave patterns, using resting state MEG as a technique. Briefly, the findings are: (a) there is an increase in alpha band activity in the medial frontal area, which reflects the Amyloid-β deposition (b) there is an increase in delta band power in the medial frontal area, showing that there is a regional decrease in glucose metabolism and showing a symptom of disease progression within the AD phases, (c) a global decrease in theta band activity only exhibits a general cognitive decline, not specific to AD. Thus, these findings are promising in that MEG could be a potential tool to provide electrophysiological biomarkers for the determination of predementia phases of AD.
In [28], the spectral property of MEG signals was utilized to distinguish between control, MCI, and Alzheimer’s disease (AD) subjects. In this study, a mean frequency approach was adapted before which the power spectral density of the MEG signals was calculated by the Fourier Transform of the autocorrelation function. The mean frequency is shown to decrease significantly in MCI patients and the values are intermediate between controls and AD patients. Another approach based on the MEG background activity was performed in [29]. In this study nonlinear techniques based on sample entropy (SampEn) and Lempel Ziv (LZC) complexity were used for the analysis of AD and control subjects using a 148-channel whole-head MEG system. The results suggest that for the AD subjects the MEG background activity revealed an increase in regularity and decrease in complexity, demonstrating that the neuronal dysfunction in AD can be identified by MEG background activity. Another study based on a missing stimulus paradigm was conducted in [30]. In this study, the subjects were exposed to short beep tones at certain intervals, and the tones were omitted randomly in the 160-channel MEG system. One of the advantages of the missing stimulus paradigm is the subjects need not pay attention to the stimuli. It was found that the amplitude of the average waveform is lower for AD subjects when compared with the control group. The study also concludes that the absence of the response to the omitted tone event could be an index for the early diagnosis of AD.
The MEG provides a 3D mapping of the brain so that functional connectivity of regions of the brain can be analyzed for the diagnosis of disorders [31]. The spectral coherence and cross mutual information function (CMIF) properties of the MEG waveform were used for the brain connectivity analysis in AD subjects [32]. The spectral entropy and statistical complexity measures were used for the analysis of MCI and AD subjects. The MCI subjects depict the intermediate pattern of abnormalities between control and AD subjects [33]. The MEG delta mapping was used for the analysis of 35 AD patients, 23 MCI patients, and 24 healthy control patients [34]. The Bayesian factor analysis algorithm was used for the analysis of MEG signals, using the Hadoop ecosystem [35]. The multilayer neural network was used for the classification of AD subjects with classification accuracy (78.39%) and sensitivity (91.11%) [36]. The MEG was found to be effective in the differential diagnosis of AD and major depression-related cognitive decline in the elderly subjects [37]. (Figure 3)
 
 

2.3. Schizophrenia

Schizophrenia is a severe mental disorder that has affected over 20 million people worldwide. A person affected by schizophrenia often exhibits the following symptoms: distortions in thinking, emotions, perception, language, behavior, sense of self, delusions, and hallucinations. Several research studies have been conducted to identify the region of the brain that is related to the symptoms of Schizophrenia, but the neural mechanism for the disease is yet to be identified. MEG can act a potential tool in identifying the electrophysiological marker for Schizophrenia. The disturbances in the oscillatory wave patterns can provide some insight regarding the symptoms or onset of the disease. Resting state MEG had been used to study schizophrenia and the findings suggests that the pathophysiology of schizophrenia can be correlated to the neural abnormalities in synchronized oscillatory activity [38]. This is complemented by EEG studies that the increase in delta, theta, and beta waves and the decrease in alpha power patterns had been identified in Schizophrenic patients [39]. However, there is poor reproducibility because of the sample characteristics, techniques adapted, and spatial distribution across the studies conducted [40][41]. Maor Zeev-Wolf et. al. [42] had employed the resting-state MEG to study the wave patterns in control and schizophrenic patients. Their findings suggest that high alpha power was negatively correlated with positive symptoms and beta power was positively correlated with the negative symptoms (Figure 4). The study concludes that different neural mechanisms may underplay in positive and negative symptomatic patients.
 
 
The MEG signal pattern was able to discriminate the schizophrenia patients from healthy subjects; 248-channel MEG signal analysis was performed on six healthy and six abnormal cases [43]. The gamma band activity can significantly differentiate healthy and schizophrenic patients, and a MEG measurement was taken on 15 schizophrenia and 15 healthy subjects. The recording was made while performing a complex mental arithmetic task and at rest. The gamma power was observed as high in healthy cases when subjected to the mental arithmetic task, while in the case of schizophrenia patients, less gamma power was observed regardless of the task. In [44], two techniques were used to analyze healthy and schizophrenia cases, based on the estimation of a number of dipoles in the delta and theta frequency and distribution, sources of slow wave activity. The beta and theta band activity were low in schizophrenia subjects and a higher number of slow wave generators was observed in certain areas of the brain. The dipole density plot was determined for healthy and schizophrenia cases, and for the diseased subjects there was an increase in the absolute dipole values in both the hemispheres [45]. The mismatch negativity is defined as the brain response subjected to deviations within a sequence of repetitive auditory stimuli and it was found to be absent in patients with schizophrenia. The fMRI and MEG data were combined for the analysis of healthy and affected subjects [46]. The diminishing alpha waves is a symptom of schizophrenia based on the analysis of 10 patients with schizophrenia and 18 healthy subjects [47]. The neuronal dynamics plays a vital role in the analysis of schizophrenia and neural synchrony was impaired in the schizophrenia subjects [48].
The MEG recordings of the gamma band activity of schizophrenia patients reveal the overactivity in the right frontal and right frontotemporal regions under cognitive demands (45 ± 71 Hz) (Figure 8. The gamma band activity was poor in frontotemporal, posteriotemporal, and occipital sites for the 60 to 71 Hz irrespective of the task [43]. The schizophrenic patients exhibited more enhanced activity in the low frequency bands (within the delta and theta frequency ranges) than the control subjects. Using the dipole density plot (DDP) method, the dipole localization was determined, and the results were superimposed on the MR images as isocontour lines [45]. The absolute dipole values measured in both hemispheres in schizophrenic patients were found to be high. The MEG and fMRI were coupled to study the altered neural responses to basic sound processing at the level of planum temporale in a group of schizophrenic patients and to correlate with the morphological changes in this region [45]. The MEG recording was done on schizophrenic patients during an auditory oddball task to investigate alpha brain activity related to selective attention to target stimuli and selective inhibition of irrelevant stimuli. The MEG-coherence source imaging (CSI) technique was employed to study and compare the brain oscillations (biomarkers) in normal subjects, and the schizophrenia patients were found to have an increased region of coherence [49]. The EEG and MEG focus on five measures: P50 auditory sensory gating, pre-pulse inhibition of the startle response (PPI), mismatch negativity (MMN), auditory P300, and gamma band oscillations. The measure indicates neuro defects such as inhibitory failure, aberrant salience detection, and impaired neural synchrony, which support the presence of higher-order cognition [50]. The static and dynamic connectivity measurements have been made by MEG-fMRI and the combined features have been used for the classification of schizophrenia subjects [51]. A pico-Tesla (pT) (1pT-10-12T)-TMS electronic device was developed to increase the (2–7 Hz) abnormal frequencies of the recorded MEG for patients with migraine, depression, or schizophrenia towards frequencies of less or equal to its frequencies of the alpha frequency range (8–13 Hz) [52]. The resting-state MEG can distinguish the different types of schizophrenia. The significant dysfunction in resting state connectivity is correlated with cognitive dysfunction and may cause differences in behavior and clinical presentation between subtypes of schizophrenia [53]. Although the alpha-band and baseline spectrum remain intact, gamma-band power at sensor level in schizophrenia patients during stimulus processing was found to be reduced. In schizophrenia subjects, high-frequency oscillations during visual processing were identified [54].
 
 

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