Can the Recording of Motor Potentials Evoked by Transcranial Magnetic Stimulation Be Optimized?

摘要

Introduction Transcranial magnetic stimulation (TMS) combined with surface electromyography (sEMG) has been for a long time an important non-invasive tool to investigate and better understand how brain controls the skeletal muscles. However, the present literature still lacks standardization protocols and comprehensive discussions about possible influences of sEMG electrode placement and montages on TMS evoked responses. With the advent of TMS by Barker et al. ( 1985 ), several advances have been made in basic and clinical neurophysiology (Rossini et al., 2015 ). In TMS, a high-intensity brief magnetic pulse applied with a coil over the subject's scalp, induces an electric field across the cortical tissue that depolarizes a group of neuronal pools. Therefore, if a single pulse is applied over a particular spot of the primary motor cortex (M1), the generated action potentials travel down the corticospinal tract reaching a specific muscle or group of muscles, which in turn can be achieved by recording their myoelectric activities. Such myoelectric activity may contain potentials varying from a few micro to millivolts and are recognized as motor evoked potentials (MEPs). MEPs can be recorded by means of sEMG with different electrode types, e.g. surface or indwelling, and montages, e.g. mono and bipolar. Most TMS applications take advantage of MEP amplitude and latency to evaluate the integrity and/or excitability of the motor corticospinal pathway to study normal and abnormal aspects of neurophysiology, including the pathophysiology of many neurological and motor disorders. Some may believe that differences in electrode arrangement for recording MEPs can offer a small impact in data quality; in this case he/she may be a victim of an ordinary pitfall. Thus, we may ask and discuss along this manuscript, what are the disadvantages and advantages of recording MEPs from different surface electrode montages? Do they provide a robust and similar comprehension of motor corticospinal excitability? The compound surface EMG signal Two basic mechanisms regulate muscle force generation from the motor units (MUs): spatial and temporal summation. Considering an increase in muscle force, spatial summation refers to the recruitment of MUs following the size principle (Henneman et al., 1965 ) while temporal summation accounts to an increase in the firing rate (De Luca and Erim, 1994 ). Moreover, muscle fibers that belong to a MU may be sparsely—or heterogeneously—clustered throughout the muscle volume (Bodine-Fowler et al., 1990 ). Consequently, MUs action potentials (MUAPs) recorded over the skin surface may not be uniformly distributed in space as muscle force varies (Merletti and Parker, 2004 ; Rosa et al., 2008 ; Garcia and Vieira, 2011 ; Hodson-Tole et al., 2013 ). Therefore, sEMG amplitude arising from the algebraic temporal and spatial summation of the action potentials that emanate from the underlying recruited MUs may exhibit different spatial distributions throughout the muscle extent. Previous studies based on mathematical modeling reinforce the need of always considering the inhomogeneous nature of a muscle due to its architecture and MU recruitment when considering the sEMG signal properties (Mesin and Farina, 2005 ; Messaoudi and Bekka, 2015 ). Moreover, such properties have been better described in the last years in several superficial muscles with the advent of multi-electrode arrays for high-density sEMG (HD-sEMG) (Holtermann, 2008 ). For instance, different levels of myoelectric activity may be observed for a same contraction force depending on the site of electrode placement (Rojas-Martinez et al., 2012 ). In turn, different TMS pulse intensities may lead to distinct distributions of MEP in forearm muscles. Specifically, lower stimulation intensities seem to yield to MEPs spatial distribution like those observed in voluntary contractions (Van Elswijk et al., 2008 ). Altogether, these few studies exemplify the idea that even though recommendations were conceived to provide robust and representative electrode placement instructions, recording the myoelectric activity under distinct conditions may not be a straightforward task depending on the purpose of the investigation, especially for MEPs elicited with TMS. Guidelines for sEMG signal recording: do they fit with MEP acquisition? Among other methodological issues, there seemed to be lack of consensus regarding the sEMG acquisition and processing since few decades ago (see Zipp, 1982 ). Consequently, various European groups developed recommendations on how to apply the sEMG. The European concerted action named Surface ElectroMyoGraphy for the Non-Invasive Assessment of Muscles (SENIAM), carried out between the years 1996 and 1999, provides very important guidelines concerning electrode size and placement (see details on http://www.seniam.org ). Thereafter, many authors started to follow those recommendations that allowed comparisons among different studies. SE