Elsevier

Clinical Neurophysiology

Volume 112, Issue 10, October 2001, Pages 1781-1792
Clinical Neurophysiology

Transcranial magnetic stimulation coregistered with MRI: a comparison of a guided versus blind stimulation technique and its effect on evoked compound muscle action potentials

https://doi.org/10.1016/S1388-2457(01)00633-2Get rights and content

Abstract

Introduction and methods: Compound muscle action potentials (CMAPs) elicited by transcranial magnetic stimulation (TMS) are characterized by enormous variability, even when attempts are made to stimulate the same scalp location. This report describes the results of a comparison of the spatial errors in coil placement and resulting CMAP characteristics using a guided and blind TMS stimulation technique. The former uses a coregistration system, which displays the intersection of the peak TMS induced electric field with the cortical surface. The latter consists of the conventional placement of the TMS coil on the optimal scalp position for activation of the first dorsal interossei (FDI) muscle.

Results: Guided stimulation resulted in significantly improved spatial precision for exciting the corticospinal projection to the FDI compared to blind stimulation. This improved precision of coil placement was associated with a significantly increased probability of eliciting FDI responses. Although these responses tended to have larger amplitudes and areas, the coefficient of variation between guided and blind stimulation induced CMAPs did not significantly differ.

Conclusion: The results of this study demonstrate that guided stimulation improves the ability to precisely revisit previously stimulated cortical loci as well as increasing the probability of eliciting TMS induced CMAPs. Response variability, however, is due to factors other than coil placement.

Introduction

Transcranial magnetic stimulation (TMS) was developed and introduced in 1985 by Barker and coworkers as a safe and painless means for stimulating the human cortex (Barker et al., 1985). When TMS is applied to restricted loci on the scalp it elicits compound muscle action potentials (CMAPs) from discrete skeletal muscles. Several investigators have produced maps of the location and extent of the motor cortical outputs. This has been done by plotting the TMS elicited CMAPs' amplitude or area as a function of stimulated scalp areas (Levy et al., 1991, Cohen et al., 1991a, Wassermann et al., 1992, Brasil-Neto et al., 1992a, Mortifee et al., 1994, Thickbroom et al., 1999). The studies of both normal and pathological motor control as well as brain plasticity have resulted from the utilization of TMS in medical research (Levy et al., 1990, Cohen et al., 1991a, Cohen et al., 1991b, Cohen et al., 1993, Traversa et al., 1997). However, knowledge of the specific cortical region stimulated by using focal TMS (as opposed to the scalp location of the coil) may in addition lead to the creation of functional cortical maps useful for preoperative evaluation for planning neurosurgical procedures near eloquent cortical areas (Krings et al., 1997a, Grimson et al., 1999).

One problem common to TMS studies is the enormous variability of the CMAPs. This variability has been attributed to numerous neurophysiological factors that have a potential impact on membrane excitability levels of cortical and/or spinal cord neurons (Brasil-Neto et al., 1992a, Mortifee et al., 1994, Fadiga et al., 1995, Izumi et al., 1995, Brouwer and Qiao, 1995, Nielsen and Petersen, 1995, Ellaway et al., 1998). It is to be noted that most studies have not taken into account the degree of precision attainable in placing and repositioning the TMS stimulating coil on the scalp for exciting restricted cortical surface loci. Specifically, several studies have shown that at the microstimulation level, motor cortex organization consists of spatially discrete redundant clusters of neurons primarily responsible for the activation of specific lower motoneurons (Asanuma et al., 1976, Asanuma, 1981, Cheney and Fetz, 1984). Nevertheless, neurons on the fringe of these clusters show divergence with respect to lower motor neurons in the spinal cord. Therefore, as the focus of neurostimulation is remote from the coil, even small errors in its placement on the scalp might lead to a difference in the neurons excited in cortical neuronal clusters and thereby contribute to the variability of CMAPs.

In a previous report we introduced a coregistration system, which can be used to relate actual scalp locations to virtual cortical surface loci below (Ettinger et al., 1996). The virtual cortical surface is derived from a 3-dimensional brain reconstructed from magnetic resonance images (MRIs). We assume that the peak electric field induced by a figure of 8 coil is generated along an axis that goes through the center and is perpendicular to the plane defined by the figure of 8 coil (Cohen et al., 1990, Cohen and Cuffin, 1991). Using this assumption, the coregistration system is capable of tracking the peak stimulating electric field as it intersects the underlying cortical surface (Gugino et al., 1999).

Our hypothesis was that precise tracking of the location and orientation of a TMS coil relative to the cortical area intersected by the assumed peak electric field would allow us to reproducibly perform stimulation of targeted neocortical areas. In addition, we wanted to compare the results of guided stimulation to conventional blind TMS where the experimenter relies on a marked grid drawn on a cap placed on a subject's head for determining placement of the coil. A subsidiary goal of this study was to evaluate differences in the variability of TMS induced CMAPs using a guided versus blind stimulation technique of increasing stimulus intensities.

Section snippets

Subjects

Informed written consent was obtained from 5 subjects for this prospective study approved by the Human Research Committee and covered by an Investigational Device Exemption (IDE) from the Food and Drug Administration (FDA). The 5 subjects (4 males and one female) were normal volunteers aged 22–46 years. All of them were familiar with TMS. All were right handed according to the Edinburg Handedness inventory (Oldfield, 1974).

MRI acquisition

MRIs were acquired using a 1.5 T General Electric Sigma System scanner

Results

The first hypothesis, that the image guided system, compared to blind stimulation, would improve the accuracy revisiting a known optimum cortical location during TMS, was confirmed. The ANOVAs revealed that there was no interaction between experimenters for any of the variables analyzed. The spatial distribution of stimulated loci acquired for each volunteer across the 4 experimenters was analyzed (Fig. 4). It was found that greater spatial area resulted from blinded stimulation trials. A

Discussion

The use of the guided technique in our study was initially developed to aid preoperative planning for patients undergoing neurosurgical procedures. Previous studies using direct electrical stimulation of discrete cortical areas intraoperatively have shown the unreliability of using surface blood vessels and cortical sulci patterns for identifying functional motor cortex. This is a result of the variability in the relationship between cortical surface anatomy and functional cortex (Penfield and

Acknowledgements

This research was supported in part by funds from the National Institute of Mental Health Career Investigator Award, including grants K02MH-01110, R01 MH-50747, and by the Scottish Rite Foundation (M.E.S.); by grants PO1 CA67165, R01RR11747 and P41RR13218 (R.K.), and by grant R03 MH60272, and a NARSAD Young Investigator Award (D.T.).

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