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  • Journal ofPhysiology (1993), 466, pp. 521-534 521 With 5 figures Printed in Great Britain SILENT PERIOD EVOKED BY TRANSCRANIAL STIMULATION OF THE HUMAN CORTEX AND CERVICOMEDULLARY JUNCTION By M. INGHILLERJ, A. BERARDELLI, G. CRUCCU AND M. MANFREDI From the Department ofNeurological Sciences, University ofRome 'La Sapienza', Viale Universita' 30, Rome, Italy (Received 3 February 1992) SUMMARY 1. The silent period evoked in the first dorsal interosseous (FDI) muscle after electrical and magnetic transcranial stimulation (TCS), electrical stimulation of the cervicomedullary junction and ulnar nerve stimulation was studied in ten healthy subjects. 2. With maximum-intensity shocks, the average duration of the silent period was 200 ms after electrical TCS, 300 ms after magnetic TCS, 43 ms after stimulation at the cervicomedullary junction and 100 ms after peripheral nerve stimulation. 3. The duration of the silent period, the amplitude of the motor-evoked potential, and the twitch force produced in the muscle were compared at increasing intensities of magnetic TCS. When the stimulus strength was increased from 30 to 70 % of the stimulator output, the duration of the silent period lengthened as the amplitude of the motor potential and force of the muscle twitch increased. At 70 to 100 % of the output, the amplitude of the motor potential and force of the muscle twitch saturated, whereas the duration ofthe silent period continued to increase. 4. Proximal arm muscle twitches induced by direct electrical stimulation of the biceps and extensor wrist muscles produced no inhibition of voluntary activity in the contracting FDI muscle. 5. The level of background activation had no effect on the duration of the silent period recorded in the FDI muscle after magnetic TCS. 6. Corticomotoneurone excitability after TCS was studied by means of a single magnetic conditioning shock and a test stimulus consisting either of one single magnetic shock or single and double electrical shocks (interstimulus interval 1P8 ms) in the relaxed muscle. A conditioning magnetic shock completely suppressed the response evoked by a second magnetic shock, reduced the size of the response evoked by a single electrical shock but did not affect the response evoked by double electrical shocks. Inhibition of the test magnetic shock was also present during muscle contraction. 7. Our findings indicate that the first 50 ms of the silent period after TCS are produced mainly by spinal mechanisms such as after-hyperpolarization and recurrent inhibition of the spinal motoneurones. If descending inhibitory fibres MS 1085
  • M. INGHILLERI AND OTHERS contribute, their contribution is small. Changes in proprioceptive input probably have a minor influence. From 50 ms onwards the silent period is produced mainly by cortical inhibitory mechanisms. INTRODUCTION Marsden, Merton & Morton (1983) first demonstrated that electrical stimulation of the motor cortex in man produces a muscle twitch followed by a silence of EMG activity. They suggested that this silent period after cortical stimulation was different from the silent period evoked by stimulation of a peripheral nerve (Merton, 1951). Since then, other authors have recorded a silent period in the hand muscles after transcranial stimulation (TCS) and have investigated the underlying physiological mechanisms. Using surface EMG and needle recordings of single motor units from the forearm muscle, Calancie, Nordin, Wallin & Hagbarth (1987) studied the silent period after electrical TCS and suggested that the inhibitory period was determined mainly by changes in proprioceptive input induced by the muscle twitch and partly by activation of descending inhibitory influences. In a study of the silent period and H reflex conditioning in wrist flexors after magnetic TCS, Fuhr, Agostino & Hallett (1991) concluded that the silent period depended initially on spinal mechanisms and subsequently on the interruption of voluntary cortical drive. In this study we investigated the physiological mechanisms of the silent period occurring after transcranial cortical stimulation. To examine the possible role of proprioceptive inflow and spinal mechanisms, we measured the duration of the silent period, the amplitude of the motor-evoked potential (MEP) and the muscle twitch force, at various intensities of the magnetic shock and at different levels of background force. In addition, we compared the silent period evoked by electrical and magnetic TCS with that produced by electrical stimulation of the motor tracts at the cervicomedullary junction (Ugawa, Rothwell, Day, Thompson & Marsden, 1991; Berardelli, Inghilleri, Rothwell, Cruccu & Manfredi, 1991 b) and studied the excitability of muscle responses evoked by transcranial stimulation with paired transcranial shocks. METHODS Ten normal subjects aged between 25 and 41 years participated in the study. Experiments were repeated in a smaller group of five subjects including the authors. Informed consent was obtained and the study was approved by the local ethical committee. Stimulation technique Cortical stimuli were delivered by a magnetic stimulator (modified version of Novametrix Magstim 200) with a flat coil, having an outer diameter of 14 cm. The coil was centred over the vertex, with the current flowing anticlockwise when viewed from above. The cortex was also stimulated electrically with a prototype electrical stimulator that delivered single or paired shocks at short time intervals (700 V maximum output, 100 Us time constant). The anode was placed on the scalp overlying the motor areas (7 cm from the mid-line on a line joining the vertex to the external auditory meatus) and the cathode on the vertex. Stimulation varied in intensity from 50 to 100 % ofthe output ofthe stimulator. Electrical stimulation of the descending motor tracts at the level of the cervicomedullary junction was performed using the method of Ugawa et al. (1991). Briefly, surface electrodes were placed on the posterior edge of each mastoid process on both sides of the inion, with the anode on the right and the cathode on the left. Electrical stimuli were delivered with a Digitimer D180 522
  • SILENT PERIOD AFTER TRANSCRANIAL STIMULATION stimulator. Stimulus intensity varied in different subjects from 40 to 60 % of the output. Higher intensities produced spread of current to the cervical roots; this was recognized by a shortening of response latency (latencies to root stimulation were shorter than those evoked by stimulation of the descending motor tracts) and the presence ofresponses at rest (Ugawa et al. 1991). The ulnar nerve was stimulated at the wrist with supramaximal electrical stimuli (250 V, 0-2 ms duration). The biceps and wrist extensor muscles were activated directly with electrical stimuli (150 V, 0'5 ms) delivered through surface electrodes placed over the belly ofthe muscle. The rate of TCS, descending motor tracts, peripheral nerve and muscle stimulation was always longer than 0 1 Hz. Recording technique The subjects were seated comfortably on a chair with their forearm resting on a table. They were instructed to exert a 30-40 % of maximum voluntary contraction of the first dorsal interosseous (FDI) muscle and the silent period was recorded after: (1) transcranial magnetic; (2) transcranial electrical; (3) electrical stimulation of the cervicomedullary junction; (4) ulnar nerve; and (5) biceps and wrist extensor muscles stimulation. The subjects maintained the isometric contraction of the FDI muscle by abducting the index finger against a strain gauge. A strap attached to the table immobilized the fingers and wrist so as to prevent finger and hand movement assisting the first dorsal interosseous muscle. A strain gauge attached to the proximal interphalangeal joint of the index finger measured the twitch force produced by cortical and brainstem stimulation in the FDI muscle. The silent period was also studied during three levels of muscle contraction (30, 60 and 100 % of the maximum effort measured using a strain gauge). EMG activity from the FDI muscle was recorded with surface electrodes and sampled with an OTE Basis device (bandwidth 2-5000 Hz) or a Cambridge Electronic Design 1401 programmable interface. The EMG was also full-wave rectified and ten trials were averaged. From the rectified EMG activity, a screen cursor measured the duration of the silent period, from the end of the muscle potential evoked by cortical stimulation to the return of EMG activity. The latency ofthe MEPs was measured at the onset and the amplitude was measured peak to peak. The amplitude of the twitch force was measured from the onset to the peak. Conditioning experiments with paired transcranial shocks Cortical excitability was tested in five subjects at rest. A single magnetic shock was given as a conditioning stimulus. This was then followed by a test stimulus consisting of either a single magnetic shock or single or double electrical shocks given at short intervals (1P8 ms) (Inghilleri, Berardelli, Cruccu, Priori & Manfredi, 1989, 1990). The intensity of the conditioning magnetic stimulus was set to 80 % of the output of the stimulator. When the test stimulus was a magnetic shock, two Novametrix Magstim 200 stimulators were used (one for conditioning and the other for test shocks) and the two coils were positioned one above the other on the scalp. The conditioning and test shock were given at a similar intensity (80 %). Because the coil delivering the test shock was farther from the scalp, the amplitude of the unconditioned test MEP (control) was slightly smaller than the amplitude of the MEP evoked by the conditioning stimulus. The magnetic field generated by the conditioning shock had no effect on the current induced by the test shock and m