Comparison of descending volleys evoked by transcranial magnetic and electric stimulation in conscious humans

Abstract

Objectives: The present experiments were designed to compare the understanding of the transcranial electric and magnetic stimulation of the human motorcortex.Methods: The spinal volleys evoked by single transcranial magnetic or electric stimulation over the cerebral motor cortex were recorded from a bipolar electrode inserted into the cervical epidural space of two conscious human subjects. These volleys were termed D- and I waves, according to their latency. Magnetic stimulation was performed with a figure-of-eight coil held over the right motor cortex at the optimum scalp position, in order to elicit motor responses in the contralateral FDI using two different orientations over the motor strip. The induced current flowed either in a postero-anterior or in a latero-medial direction.Results: At active motor threshold intensity, the electric anodal stimulation evoked pure D activity. At this intensity, magnetic stimulation with the induced current flowing in a posterior-anterior direction evoked pure I₁ activity. When a latero-medial induced current was used, magnetic stimulation evoked both D and I₁ activity. Using electric anodal stimulation, at a stimulus intensity of 9% of the stimulator output above the active motor threshold (corresponding approximately to 1.5 active motor threshold), a small I₁ wave appeared only in subject 1. Using magnetic stimulation with a posterior-anterior induced current, at a stimulus intensity of 21% of maximum stimulator output above the active motor threshold (corresponding approximately to 1.8 times threshold in subject 1 and to two times threshold in subject 2), a small D wave appeared in subject 1 but not in subject 2.Conclusions: Present results demonstrate that, in conscious humans at threshold intensities, electric stimulation evokes D waves and magnetic stimulation (with a posterior-anterior induced current) evokes I waves, while magnetic stimulation (with a latero-medial induced current) evokes both activities.

Introduction

Ever since its introduction, there has been considerable debate over the site at which transcranial (electric or magnetic) stimulation of the motor cortex activates the corticospinal system in man. Perhaps the most popular view at present is the `D- and I-wave' hypothesis first proposed by Day et al. (1989)on the basis of single motor unit studies in the hand. This states that transcranial anodal electrical stimulation activates corticospinal fibres directly within a few millimetres of the cell body. In contrast, transcranial magnetic stimulation tends to activate corticospinal neurones indirectly via excitatory synaptic inputs. Following Patton and Amassian (1954), these are said to produce D- and I-wave volleys in the pyramidal tract. Several studies in anaesthetised humans of direct recording of descending spinal cord volleys tended to confirm this hypothesis (Berardelli et al., 1990; Thompson et al., 1991). The `D- and I-wave' hypothesis has been further refined by several authors who have found that the probability of evoking probable D-wave changes with the direction of the current induced in the brain by the magnetic stimulus (e.g. Amassian et al., 1990; Werhahn et al., 1994). The situation may be further complicated when stimulating over the leg area of the cortex because of the changes in orientation of neuronal elements with respect to the surface of the scalp (Priori et al., 1993; Nielsen et al., 1995).

The opposite viewpoint has been championed by two groups (Edgley et al., 1990; Burke et al., 1990, Burke et al., 1993). Studying the corticospinal volleys recorded from corticospinal tract in monkeys or during surgical procedures in man, they suggested that electrical stimulation activated corticospinal fibres deep within the brain, whereas magnetic stimulation activated the same group of fibres close to the pyramidal cell body. However, it was never clear whether the smaller monkey brain or the anaesthetised human provided a valid model for the behaviour in conscious man. Indeed, some of the early conclusions of the monkey experiments have since been qualified (Edgley et al., 1997).

The situation seemed to be resolved recently by Kaneko et al. (1996)and Nakamura et al. (1996), who recorded the descending corticospinal volley from the cervical epidural space of conscious subjects. Their data was compatible with the `D- and I-wave' hypothesis. They showed that electrical stimulation evoked a D wave, that on latency considerations, was supposed to be due to stimulation of corticospinal fibres in the subcortical white matter. Magnetic stimulation with a posterior-anterior induced current across the hand area of motor cortex produced I waves, whilst if the orientation of the magnetic coil was changed to latero-medial, D waves also were generated. However, both groups used rather high intensities of stimulation, capable either of evoking a response in relaxed muscle, or producing a 1–2 mV response in active muscle. The present study is an attempt to finalise our understanding of electric and magnetic stimulation by analysing the descending volleys in conscious humans produced by stimulation over the hand area at around threshold intensities. The results give an indication of the relative thresholds for producing D- and I waves with the various types of stimulation.