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Magnetoencephalography for Brain Electrophysiology and Imaging

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Magnetoencephalography for Brain Electrophysiology and Imaging F O C U S O N H U MA N B R A I N M A P P I N G R EVIEW Magnetoencephalography for brain electrophysiology and imaging Sylvain Baillet We review the aspects that uniquely characterize magnetoencephalography (MEG) among the techniques available to explore and resolve brain function and dysfunction. While emphasizing its specific strengths in terms of millisecond source imaging, we also identify and discuss current practical challenges, in particular in signal extraction and interpretation. We also take issue with some perceived disadvantages of MEG, including the misconception that the technique is redundant with electroencephalography. Overall, MEG contributes uniquely to our deeper comprehension of both regional and large-scale brain dynamics: from the functions of neural oscillations and the nature of event-related brain activation, to the mechanisms of functional connectivity between regions and the emergence of modes of network communication in brain systems. We expect MEG to play an increasing and pivotal role in the elucidation of these grand mechanistic principles of cognitive, systems and clinical neuroscience. After 45 years of its development and use1–3, we reflect here on the communication in brain systems. As the function and dynamical position of MEG among the techniques available to explore and principles of the signal components present in the volumes of dense resolve brain function and dysfunction. This review focuses on the and intricate MEG data become better understood, we explain how aspects that uniquely characterize MEG. We emphasize the specific MEG plays an increasing and pivotal role toward the elucidation of strengths of the modality, such as its source imaging capabilities. We the grand mechanistic principles of cognitive, systems and clinical also identify and discuss practical challenges, in particular in signal neuroscience. To this end, we emphasize that MEG is particularly extraction and interpretation. equipped to bridge human data with animal and computational mod- Because MEG and electroencephalography (EEG) appear to be els of electrophysiology in health and disease. sister electrophysiological techniques that are both sensitive to the We also review the principles of MEG signaling and the state of electrochemical current flows within and between brain cells, MEG the art of the technology, with a perspective on innovations on the is sometimes thought to be equivalent to EEG, with limited scientific horizon. We then highlight key MEG contributions to neuroscience added value. We refute this misconception and explain how distinct and discuss translations to clinical practice. Along the way, while physical principles make these two modalities complementary in we discuss limitations, current difficulties and uncertainties asso- many respects, rather than purely redundant. In particular, we argue ciated with the technique, we also wish to correct some mistaken that MEG is the modality with the best combination of direct and perceptions of MEG. noninvasive access to the electrophysiological activity of the entire brain, with sub-millisecond temporal resolution and ability to resolve Measurement principles and instrumentation activity between cerebral regions with often surprising spatial and The basic principles of MEG are simple; the sophistication lies in spectral differentiation and minimum bias. Indeed, unlike EEG, the sensing technology involved and the methodology required to the accuracy of MEG source mapping is immune to the signal dis- extract relevant signal information in the widest variety of experi- tortions caused by the complex layering of head tissues, with highly mental contexts. Fundamentally, any electrical current produces heterogeneous conductivity profiles that cannot be measured with magnetic induction (often popularly confounded with a magnetic 4 © 2017 Nature America, Inc., part of Springer Nature. All rights reserved. All rights part Nature. of Springer Inc., America, Nature © 2017 precision in vivo. field ), whose strength can be measured remote from the current We explore these ideas herein in details and conclude that MEG, source—for example, with a pick-up coil. The magnetic flux across used independently or in combination with other brain imaging tech- the coil surface induces an electrical current in the coil wiring mate- niques, contributes uniquely to our deeper comprehension of both rial, whose amplitude is instantaneously proportional to that of the the regional and large-scale neural dynamics of the brain: from the magnetic induction and is readily measurable. clarification of the nature of spontaneous and event-related brain activation to the elucidation of the mechanisms that yield functional Basic signal origins. In MEG, the electrochemical currents circulat- connectivity between regions and the emergence of modes of network ing within and between neurons generate the magnetic induction. Postsynaptic potentials (PSPs) are considered the main generators 3,5 McConnell Brain Imaging Centre, Montreal Neurological Institute, McGill of these ionic currents . There is also convincing though limited University, Montreal, Quebec, Canada. Correspondence should be addressed to evidence that fast ripples present in MEG signals in the range of S.B. ([email protected]) 500–1,000 Hz could be related to cell discharges6,7. Yet they may also Received 14 November 2016; accepted 17 January 2017; published online be explained by large spike components of PSP activity due to voltage- 23 February 2017; doi:10.1038/nn.4504 dependent channel conductance8 (Fig. 1). The useful frequency band NATURE NEUROSCIENCE VOLUME 20 | NUMBER 3 | MARCH 2017 327 R EVIEW of MEG signals is about 0.5–1,000 Hz, with 1–80 Hz being the most a Sodium spikes b 9 typical . We discuss below the possible functions and interdepend- Postsynaptic 10 mV Net PSP 10 potential 10 ms ence across this wide spectral range of brain signals . ––––––––– – – –– ––– Individual 100 mV Apical dendrites PSPs Instrumentation: innovations on the horizon. In practical terms, the 10 ms Time magnetic signal produced by neural currents in the nanoampere (10−9 A) Magnetic Primary current induction range is formidably weak. Extracranial magnetic inductions are typically 10,000– measured on a scale of femtoteslas (10−15 T), about 10 to 100 million 50,000 cells times smaller than the Earth’s static magnetic field. This reality imposes a need for sensitive sensor technology. The present industry standards Basal dendrites 30 mV Individual rely on pick-up coils coupled with superconducting interference devices ++ + + + + +++++ AP (SQUIDs)2,3. SQUIDs exploit the principles of quantum physics for the Net AP 100 mV detection of small electrical currents, like those induced by weak mag- Action potential 1 ms 10 ms Time Debbie Maizels/Springer Nature netic signals, with high sensitivity and large dynamic ranges. State-of-the-art commercial systems feature coil magnetometers Figure 1 Cellular origins of MEG signals. (a) For simplicity, we take the arranged in whole-head arrays of about 300 independent channels, cortical pyramidal neuron to epitomize the elementary cellular generator of MEG signals. All physiological currents from all cell types generate a sampled at up to 30 kHz simultaneously. Magnetic induction travels magnetic induction; the elongated morphology of the pyramidal neuron through the air: MEG sensors are not attached to the scalp, as the constrains the net primary current circulation along the cell, which is entire sensing apparatus is embedded in a thermally insulated tank, a factor in creating greater signal strength in comparison to those from called a dewar, filled with 70–100 L of liquid helium. Superconducting more stellate cellular morphologies. The primary current results from an temperatures minimize thermal noise and therefore optimize data imbalance in electrical potentials between the apical dendritic arborescence quality. Consequently, subject preparation times are much shorter of the cell and its soma and more basal dendrites. The magnetic induction than in EEG, as the contactless and gel-free sensors do not need to isolines in purple are perpendicular to the primary current flow and can be picked up outside the head. The sources are twofold: the postsynaptic be positioned and carefully verified manually. potentials (PSPs), including fast, large-amplitude sodium spikes, and Another distinctive property of MEG is that magnetic induction is axonal discharges (action potentials, AP). The slower components of the a vector signature of electrodynamics. In concrete terms, MEG sig- PSPs are substantially smaller in amplitude than the APs. (b) At the scale nals depend on the location and orientation of the pick-up coils with of cell assemblies, the mass effect of slower PSPs is stronger than that respect to neural sources, which vary between system manufacturers of APs owing to their greater overlap in time without requiring rigorous and are relative to the subject’s head position in the helmet. synchronization. Computational models and empirical evidence show that a minimum of 10,000 to 50,000 cells are required to produce a signal This represents a clear practical difference from EEG, which meas- detectable with MEG8. It is possible, in principle, that fast PSP spiking ures differences of scalar electrical potentials between electrodes activity, and possibly shadows of APs, are detectable in MEG. attached to the scalp. Although the head’s shape and size obviously vary between individuals, the standardization
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