Journal of Clinical Neurophysiology
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`8(1 ):3-9, Raven Press, Ltd., New York
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`© 1991 American Electroencephalographic Society
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`History of Magnetic Stimulation of the Nervous System
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`L. A, Geddes
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`The William A. Hillenbrand Biomedical Engineering Center, Purdue University, West Lafayette, Indiana, US.A.
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`Summary: The use of a time-varying magnetic field to induce a sufficiently
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`strong current to stimulate living tissue was first reported by d'Arsonval in 1896.
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`Since then, there have been many studies in what is now called magnetic stimu­
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`lation. This paper traces the history of this field from d'Arsonval to its present
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`use in neurophysiology. Magnetic stimulation-Eddy current stim­
`Key Words:
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`ulation-Nerve stimulation.
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`Magnetic (eddy-current) stimulation is being
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`byFaradayin 1831 in a simple experiment. Formag­
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`used increasingly as a diagnostic and research tool
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`netic stimulation, Faraday's law can be restated: the
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`following the clinical demonstration of peripheral
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`induced (stimulating) current is proportional to the
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`nerve stimulation (Polson et al., 1982) and stimula­
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`rate of change of the magnetic field. The magnetic
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`tion of the human brain (Barker et al., 1985b). The
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`field is proportional to the current in the excitation
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`considerable advantage enjoyed by magnetic-pulse
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`coil; therefore, the induced (stimulating) current is
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`stimulation is the remarkable lack of sensation when
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`proportional to the first time derivative (i.e., the rate
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`compared to stimulation with skin-surface elec­
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`of change) of the current in the excitation coil.
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`trodes. With such electrodes, there is a high current
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`It is interesting to observe that magnetic stimu­
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`density under the electrode perimeter, thereby favor­
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`lation was first applied to the nervous system by
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`ing stimulation of skin receptors. With magnetic­
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`d'Arsonval (1851-1940), physicist and physician. At
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`pulse stimulation, there is no localized high current
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`the end of an 1896 paper entitled "Apparatus for
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`density at the skin surface under the excitation coil;
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`Measuring Alternating Currents of All Frequencies,"
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`therefore, the skin sensation is only slight. Because
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`the following passage appeared (author's transla­
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`of this characteristic, one manufacturer of magnetic
`tion):
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`stimulators called it "ouchless stimulation." How­
`In a verbal communication, given about a month ago to
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`ever, the equipment needed with magnetic stimula­
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`the Society, I had announced that an alternating mag­
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`tion is much larger than that required with skin­
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`netic field with an intensity ofl 10 volts, 30 amperes with
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`surface-stimulating electrodes.
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`a frequency of 42 cycles per second, gives rise to, when
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`For a magnetic field to stimulate, it must be time­
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`one places the head into the coil, phosphenes and ver­
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`varying; a static field will not stimulate. However, it
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`tigo, and in some persons, syncope.
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`is possible that a moving excitable tissue in a static
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`magnetic field could be stimulated. In practice, this
`Why d'Arsonval conducted this experiment is not
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`situation is rarely encountered.
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`known. d'Arsonval is better remembered for devel­
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`The fact that a time-varying magnetic field can
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`oping the galvanometer with Deprez in 1882. With
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`induce a voltage in a nearby conductor was discovered
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`Bernard, he used it with a thermocouple to show
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`that venous blood is hotter than arterial blood. His
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`current-measuring method used in his magnetic­
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`Address correspondence and reprint requests to Dr. L. A Geddes
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`stimulation studies consisted of passing the current
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`at The William A Hillenbrand Biomedical Engineering Center,
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`in the head-encircling coil, through a thin wire, which
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`Purdue University, West Lafayette, IN 47907, U.S.A.
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`L.A. GEDDES
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`became heated. The rise in temperature of the thin
`wire was measured with an FeNi thermocouple con(cid:173)
`nected to his galvanometer. d'Arsonval correctly
`pointed out that the galvanometer deflection was
`proportional to the square of the excitation-coil cur(cid:173)
`rent flowing through the thin wire. He also stated
`that the galvanometer reading was independent of
`the frequency of the current. The thermocouple am(cid:173)
`meter was born.
`Probably because d'Arsonval's paper was written
`in French, it was not read by many. Unaware of
`d'Arsonval's paper (1896), Beer (1902) reported a
`flickering-light sensation (phosphenes) produced by
`a magnetic field applied to the head. Soon the topic
`of magnetophosphenes became an important research
`area because alternating current was replacing direct
`current as a source of electrical energy. Sylvanus
`Thompson (1910), Dunlap (1911), and Magnusson
`and Stevens (1911, 1914) investigated magnetophos(cid:173)
`phenes because there were anecdotal accounts of
`powerhouse workers perceiving strange sensations
`when in the vicinity of transformers carrying high(cid:173)
`intensity alternating currents.
`Thompson (1910), unaware of d'Arsonval's 1896
`paper, constructed a large 32-turn coil (9 in. in diam(cid:173)
`eter and 8 in. long) and applied 800 A of power-line
`current to it. The subject placed his head in the coil
`and reported perceiving "a faint flickering illumina(cid:173)
`tion, colorless or a blush tint," being brighter in the
`peripheral field. The effect could be perceived with
`the eyes open and in the daylight. Some of the sub(cid:173)
`jects reported a strange taste sensation.
`Dunlap (1911)was not convinced that Thompson's
`experiment was valid. He thought that the loud hum
`produced by the current flowing in the transformer
`that delivered current to the coil surrounding the
`head had a psychological effect. Therefore, Dunlap
`decided to perform a cleaner experiment and con(cid:173)
`structed a 27-turn elliptical coil (8 in. long and 9 X
`10.5 in. in diameter). The coil was suspended from
`the ceiling and could be lowered over the subject's
`head. With 200 A of 60-Hz current, all subjects re(cid:173)
`ported the flickering-light sensation. The subjects
`wore earplugs. When current was not flowing in the
`head coil, it was delivered to a resistor that caused the
`transformer to produce the same sound as when cur(cid:173)
`rent flowed in the head coil. When the frequency of
`the current was 25 Hz, the subjects reported that the
`whole visual field was illuminated. A few of the sub(cid:173)
`jects reported twitching of the eyelids, even with no
`current in the coil. Dunlap concluded by stating,
`"No sensations other than the visual, which could be
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`J Clin. Neurophysiol., Vol. 8, No. 1, 1991
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`connected with the alternating field, were noticed by
`any of us. That there is no after-effect from the strong(cid:173)
`er field, I should not like to say at present. I should
`advise any experimenter to proceed cautiously. It is
`very desirable that experiments with a large range of
`amperages and frequencies be made."
`Magnusson and Stevens (1911, 1914) constructed
`two coils with elliptical cross-sections. One coil had
`205 turns with major and minor axes of8.5 in. and 12
`in.; the other coil had 203 turns with major and minor
`axes of 9.5 in. and 13.5 in. The coils could be used
`singly or arranged coaxially. Direct and alternating
`currents were passed through the coils surrounding
`the subject's head. Not surprisingly, no sensation
`was perceived when direct current was flowing. How(cid:173)
`ever, when the direct current flow was initiated and
`arrested, sensations were experienced. When the
`direct current was initiated, a luminous horizontal
`bar was perceived moving downward. When the di(cid:173)
`rect current was arrested, the luminous bar moved
`upward. With alternating current applied to the
`head-encircling coil, the flickering appeared to fol(cid:173)
`low the current frequency, being brightest with 20-30
`Hz. Above 90 Hz, the phosphenes were dimmer,
`even with a higher current in the coil. Unsuccessful
`experiments were carried out with a special coil that
`applied a 60-Hz alternating magnetic field to the ex(cid:173)
`posed sciatic nerve of the cat. Commenting on their
`results, Magnusson and Stevens stated, "It was hoped
`to determine by this (cat) experiment whether the
`locus of the excitation in the production of visual
`sensations was in the sensory elements of the retina
`itself or in the fibers of the optic nerve. The observa(cid:173)
`tions must be extended before definite conclusions
`can be made."
`More than three decades were to elapse before re(cid:173)
`search on magnetic stimulation was restarted. By
`this time, it was known that visual sensations could
`be produced by stimulation of the retina, optic nerve,
`and occipital cortex.
`Walsh (1946) reported using an iron-cored coil ( de(cid:173)
`tails given by Barlow), placed adjacent to the eye, and
`energized it with alternating current having frequen(cid:173)
`cies varying from 5 to 90 Hz. With a constant flow of
`alternating current in the coil, the visual sensation
`vanished in a few seconds, and more rapidly when
`the frequency was high and the intensity low. The
`visual sensation could be prolonged by moving the
`eyes. Recovery usually occurred in less than a min(cid:173)
`ute. Pressure applied to the eyeball abolished the
`visual response.
`The observations of Walsh were extended by Bar-
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`HISTORY OF MAGNETIC STIMULATION OF THE NERVOUS SYSTEM
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`5
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`A
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`FIG. 1. The first record of contraction of a mus(cid:173)
`cle (A) and the envelope (B) of the magnetically
`induced stimulus applied (EMF) that stimulated
`the sciatic nerve of the frog. (Redrawn from Kolin
`et al.. 1959.)
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`11
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`I I
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`low et al. ( 1947). Barlow et al. constructed a small coil
`of397 turns (10.5 cm inside diameter, 20.3 cm outside
`diameter, and 7.3 cm long) that surrounded a lami(cid:173)
`nated-iron core. The coil was placed adjacent to one
`temple but not in contact with the skin. Alternating
`current of 10-40 Hz was applied, producing colorless
`and colored flickering-light sensations. When the
`coil current was increased, the flickering light oc(cid:173)
`cupied more of the visual field. The flickering dimin(cid:173)
`ished with continued stimulation. As in Walsh's
`studies, prolongation of the effect could be achieved
`by rotating the eyeballs. Recovery also occurred with(cid:173)
`in a minute of cessation of stimulation. When the
`coil was placed over the occiput, no phosphenes were
`perceived. To demonstrate that electrical stimula(cid:173)
`tion could produce the same sensation, Barlow et al.
`placed an electrode on the side of the forehead and
`another on the back of the forearm. A 100-Hz sinu(cid:173)
`soidal current ofless than 1 mA produced the same
`flickering sensation. In commenting on their results,
`Barlow et al. stated, "As to the locus of excitation, we
`believe that this is retinal, for otherwise we cannot
`explain the effects of localized magnetic stimulus,
`pressure on the eyeball and movements of the eye(cid:173)
`ball, all of which profoundly influence the phos(cid:173)
`phenes."
`Desirous of demonstrating that an alternating
`magnetic field could stimulate nerve, Kolin et al.
`(1959) constructed an excitation coil surrounding a
`magnetically permeable bar, one end of which was
`pyramidal in shape. Using 60 and 1,000 Hz alternat(cid:173)
`ing current, they placed the pyramidal pole piece
`bver the temple and then over the occipital area. In
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`both cases, phosphenes were perceived. With 1,000
`Hz current and the pole face over the temple, all sub(cid:173)
`jects reported an intense sensation of nasal obstruc(cid:173)
`tion.
`Kolin et al. (1959) then demonstrated, for the first
`time, that an alternating magnetic field could stimu(cid:173)
`late nerve. They insulated the pole face of their elec(cid:173)
`tromagnet with plastic. Then they obtained a frog
`sciatic-nerve, gastrocnemius-muscle preparation
`and looped the sciatic nerve around the insulated
`pole face. An intense contraction of the gastrocne(cid:173)
`mius muscle was obtained with both 60 and 1,000 Hz
`current applied to the coil. They recorded the mus(cid:173)
`cle contraction and the rectified voltage picked up by
`a loop of wire around the pole face. Figure 1 presents
`the first evidence that nerve could be stimulated by
`an alternating magnetic field. To complete the in(cid:173)
`vestigation, they placed the nerve-muscle prepara(cid:173)
`tion in a Petri dish filled with saline. The dish was
`placed on the pole face, and alternating current was
`applied to the coil, resulting in a tetanic muscle con(cid:173)
`traction. This experiment offered conclusive ex(cid:173)
`perimental proof that a magnetic field could induce
`enough current in a volume conductor to stimulate a
`motor nerve.
`The modern era of magnetic stimulation was ush(cid:173)
`ered in by Bickford et al. in 1965, who were able to
`twitch skeletal muscle in intact rabbits, frogs, and
`human subjects by using a pulsed magnetic field. In
`the six human subjects, twitches were obtained in the
`muscles innervated by the ulnar, peroneal, and sciat(cid:173)
`ic nerves. The pulse duration was about 300 µs, and
`the peak field strength was 20,000-30,000 G. They
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`J Clin. Neurophysiol .. Vol. 8, No. 1. 1991
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`6
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`0
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`E -8
`a.,
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`-12
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`6·
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`CJ)
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`b
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`FIG. 2. Muscle-action potential recorded from electrodes at the
`base of the thumb of man evoked by magnetic stimulation of the
`median nerve (A) and by electrical stimulation of the same nerve
`(B). (Redrawn from Polson et al., 1982.)
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`concluded by stating, "The findings in both man and
`animals are consistent with the hypothesis that stim(cid:173)
`ulation results from eddy currents induced in the
`vicinity of motor nerves."
`Prior to Bickford's paper, sinusoidal alternating
`current was applied to the excitation coil. A high cur(cid:173)
`rent had to be used to achieve an adequately intense
`magnetic field, and the prolonged current flow caused
`the excitation coil to become hot. The stimulus in(cid:173)
`duced in the tissue was cosinusoidal with the same
`frequency as that of the source. Such a current pro(cid:173)
`duces a tetanic contraction when a motor nerve is
`stimulated by the magnetic field. However, the pulsed
`magnetic field produced by discharging a capacitor
`bank into the excitation coil typically produces a
`single, short-duration, biphasic ( or polyphasic)
`damped induced current waveform, resulting in a
`twitch when a motor nerve is stimulated. In 1975,
`Barker and co-workers at the University of Sheffield
`were studying the possibility of achieving velocity(cid:173)
`selective nerve stimulation. This led them to investi(cid:173)
`gate independently the possibility ofusing magnetic
`stimulation for clinical purposes (Barker, 1976). Sub(cid:173)
`sequently, they went on to develop a practical stimu(cid:173)
`lator, and their first report of stimulation of periph(cid:173)
`eral nerve with recording of the resultant muscle
`action potentials demonstrated the advantages of
`stimulating human motor nerves with pulsed mag(cid:173)
`netic fields (Polson et al., 1982). They first marked
`out the path of the median nerve on the surface of the
`arm. Recording electrodes were placed on the thenar
`eminence and connected to an electromyographic
`(EMG) recorder. Stimulating electrodes were placed
`on the skin over the nerve. At the same site, the edge
`of the excitation coil was placed and a pulse of cur(cid:173)
`rent was delivered, producing a peak magnetic field
`of2.2 T. The thumb muscles twitched and an EMG
`was recorded. Then the stimulus was delivered to the
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`JC/in. Neurophysiol., Vol. 8. No. 1. 1991
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`L.A. GEDDES
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`skin-surface electrode over the median nerve and the
`EMG was recorded. Figure 2 shows the first EMG of
`a magnetically stimulated motor nerve in man.
`By this time, motor-evoked potentials were becom(cid:173)
`ing of interest. The technique employs placing elec(cid:173)
`trodes on the scalp over the motor cortex and record(cid:173)
`ing ( or observing) contralateral muscle contractions.
`However, use of this method of noninvasive cortical
`stimulation requires careful electrode placement
`and is painful. Barker et al. (1985) and Jalinous et al.
`(1985) demonstrated that their magnetic stimulator
`was able to stimulate the human cortex without pain
`or discomfort. They placed an excitation coil on the
`scalp over the motor cortex of man and recorded
`twitch muscle-action potentials from the contrnlat(cid:173)
`eral abductor digitii minimi using skin-surface elec(cid:173)
`trodes. Figure 3 shows the first muscle action po(cid:173)
`tential evoked by applying a pulsed magnetic field to
`the motor cortex. This initial demonstration of mag(cid:173)
`netic stimulation of the motor cortex caused con(cid:173)
`siderable clinical interest, and the first stimulators
`designed for routine clinical use were constructed at
`the University of Sheffield for five groups in the
`United Kingdom and the United States who wished
`to evaluate the technique. The first clinical studies
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`5 ms
`,.._....
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`FIG. 3. Muscle action potentials recorded from electrodes over the
`abductor digitii minimi resulting from a magnetic pulse delivered
`by a 100-mm-diameter coil placed over the contralateral motor
`cortex (top). The lower tracing was obtained with stimuli delivered
`to the ulnar nerve at the elbow. The peak current in the coil was
`4,000 A. (Redrawn from Barker et al., 1985.)
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`HISTORY OF MAGNETIC STIMULATION OF THE NERVOUS SYSTEM
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`7
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`FIG. 4. Magnetic stimulation of the right
`phrenic nerve at the level of the diaphragm.
`Air flow velocity (pneumotachogram) and
`volume were recorded while the subject
`hyperventilated (left). Then, during the
`period ofapnea, a 100-µF capacitor. charged
`to 2,000 V. was discharged into the excita(cid:173)
`tion coil to produce an inspiration. (Ex(cid:173)
`citation coil 47 turns of 1-in. copper rib(cid:173)
`bon. 0.010 in. thick.)
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`PNEUMOTACHOGRAM
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`VOLUME
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`50L /min.
`o[
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`1000ml [
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`using magnetic stimulation were presented in 1985
`and 1986 (Barker et al.). Clinical interest in magnetic
`stimulation has continued to grow, and the Sheffield
`group introduced a number of manufacturers to the
`technique during 1985. Commercial stimulators are
`now available from four companies. The basic theo(cid:173)
`ry, advantages, and safety considerations of clinical
`magnetic stimulation have been described by Barker
`et al. (1987).
`There have been many accounts of stimulation of
`the inspiratory motor nerves with skin-surface elec(cid:173)
`trodes, the technique being known as electroventila(cid:173)
`tion (Geddes et al., 1989). To date, there has been no
`account of achieving the same goal with a pulsed
`magnetic field; Fig. 4 presents an example. The ex(cid:173)
`citation coil was placed over the right lower chest
`while air flow velocity (pneumotachogram) and its
`integral (respired volume) were recorded. On the left
`of Fig. 4, the subject hyperventilated to achieve a
`period of apnea. Then a 100-µF capacitor, charged
`to 2,000 V, was discharged into the excitation coil to
`produce an inspiration. Because the coil-capacitor
`circuit was very underdamped, several pulses of
`magnetic field were produced, resulting in a very
`short tetanic contraction of the diaphragm via phren(cid:173)
`ic-nerve stimulation.
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`SPONTANEOUS
`BREATHING
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`MAGNETIC
`STIMULATION
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`EFFICACY AND SAFETY
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`In addition to its use as a research tool, magnetic
`stimulation is employed diagnostically. In the latter
`case, two issues arise: efficacy and safety. From the
`historical literature, there is no doubt that magnetic
`stimulation is effective, i.e., motor and sensory nerves
`and the motor cortex can be stimulated consistently.
`The issue of safety is not so easily established. To this
`author, safety requires consideration of two areas:
`(1) cardiac stimulation and (2) effects on the nervous
`system.
`Several investigators have studied the possibility
`of stimulating the heart with a pulsed magnetic field.
`Rentsch (1965) estimated that it would require 1,000
`watt-seconds (joules) of energy delivered to an exci(cid:173)
`tation coil on the chest to evoke an ectopic beat.
`However, the experiment was not performed. Like(cid:173)
`wise, Irwin et al. (1970) proposed using a pulsed mag(cid:173)
`netic field for cardiac pacing, but experiments were
`not performed. Bourland et al. (1990) were the first to
`induce an ectopic heartbeat with a pulsed magnetic
`field by placing the excitation coil over the exposed
`dog heart. Figure 5 is a reproduction of their record
`in which 10,000 J were delivered to the excitation
`coil. In a subsequent study using closed-chest dogs,
`Mouchawar et al. (in press) employed two co-planar
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`J Clin. Neurophysiol., Vol. 8, No. 1, 1991
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`8
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`5
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`3
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`-3
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`L.A. GEDDES
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`r Vagal Stimulation
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`X
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`-5 .__ ____ ..__ ____ .__ ____ .__ ____ .__ ___ __,
`4
`6
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`0
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`2
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`8
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`FIG. 5. Magnetic stimulation of
`the heart of an anesthetized para(cid:173)
`lyzed dog. The top tracing is the
`EKG and the lower is blood pres(cid:173)
`sure. Vagal stimulation was used
`to arrest the heart, then a pulse of
`current was delivered to the excita(cid:173)
`tion coil to evoke an ectopic beat
`(X). (Reproduced with permission
`from Bourland et al.. 1990.)
`
`200
`
`160
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`120
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`80
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`40
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`0
`0
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`Time (sec)
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`X
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`L Magnetic Pulse Delivered
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`2
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`4
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`6
`
`8
`
`JO
`
`Time (sec)
`
`,......_
`OJ)
`::r:
`E
`E
`'---'
`il.) ,_
`;:::l
`r/J
`r/J
`il.) ,_
`0...
`]
`
`o:i
`"@
`·c
`....
`,_
`<t'.
`
`il.)
`
`coils with their edges adjacent to evoke single ectopic
`beats when the heart was arrested by vagal stimula(cid:173)
`tion. Extremely high energy (20 kJ) was required to
`achieve cardiac stimulation. The duration of the in(cid:173)
`duced current pulse was about 500 µs. Typically, it
`required discharging a 685-µF capacitor, charged to
`about 8,000 V, into the excitation coils to evoke an
`ectopic beat. This voltage is about four times that re(cid:173)
`quired to stimulate the thoracic motor nerves, and
`consequently there was a considerable body-muscle
`twitch when the pulse was delivered. That the mus(cid:173)
`cular contraction had nothing to do with producing
`the ectopic beat was proven by repeating the proce(cid:173)
`dure with the animals paralyzed with succinylcholine
`and providing artificial respiration.
`To further illustrate the point that the pulsed mag(cid:173)
`netic field strength typically used for stimulating the
`motor cortex is much less than that required to excite
`an ectopic heartbeat, one of the first Sheffield clini(cid:173)
`cal stimulators was used with the excitation coil
`
`placed over the apex beat area of the dog chest. Blood
`pressure and electrocardiogram (ECG) were moni(cid:173)
`tored. The heart was arrested by vagal stimulation
`and with the full output; the magnetic pulse only
`twitched the chest muscles.
`Silny (1985) used a dog with the chest encompassed
`by a Helmholtz coil arrangement. A single pulse of
`50 Hz sinusoidal current produced a field in excess of
`2 T. The ECG was recorded and when the current
`pulse was delivered, there occurred a period of sino(cid:173)
`atrial (SA) node arrest and a period of about 1 min in
`which there was a ventricular rhythm. At about 50 s,
`the ECG showed atrial flutter, which arrested spon(cid:173)
`taneouslywith restoration of SA nodal activity. These
`observations are consistent with stimulation of the
`vagus nerves, rather than cardiac stimulation.
`There are two reasons why the heart is so much
`more difficult to stimulate than motor nerve or the
`motor cortex. The first relates to the differences
`in excitability characteristics (strength-duration
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`J. Clin. Neurophysiol., Vol. 8, No. 1, 1991
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`HISTORY OF MAGNETIC STIMULATION OF THE NERVOUS SYSTEM
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`9
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`curves). the chronaxie for motor nerve is about 0.1
`ms; that for cardiac muscle is 1.5 ms. Typically, mag(cid:173)
`netic stimulators produce induced current stimuli
`with a pulse duration of 0.1-0.2 ms. Therefore, the
`threshold for cardiac-muscle stimulation is much
`higher than that for motor nerve. Our experimental
`studies verify this fact. The second reason relates to
`the distances from the excitation coil that these struc(cid:173)
`tures lie. The induced stimulating current produced
`by the pulsed magnetic field decreases with distance
`from the excitation coil. Typically, the heart is more
`distant from the skin surface than superficial motor
`nerves.
`The other area of safety with a time-varying mag(cid:173)
`netic field relates to (1) poststimulus effects and (2)
`the frequency of the stimuli. There are anecdotal re(cid:173)
`ports of short-lasting confusion following magnetic
`stimulation of the motor cortex. Silny ( 1985) studied
`the effects of a 50-Hz magnetic field on rats and cats.
`A field of 50 mT produced no evidence of effect; the
`animals did not attempt to escape. As yet, there are
`no data to indicate the field strength that produces a
`behavioral response when in a magnetic field.
`It is well known that electrical stimuli with a fre(cid:173)
`quency above about 10/s applied to the cortex will
`produce a convulsion. Present-day magnetic stimu(cid:173)
`lators usually have a frequency no more than 3/s (be(cid:173)
`cause of energy limitations). However, if magnetic
`stimulators become available with higher frequen(cid:173)
`cies, caution must be used when using them for cor(cid:173)
`tical stimulation.
`In conclusion, perhaps the largest gap in our
`knowledge relates to the behavioral aspects of mag(cid:173)
`netic stimulation. The transient poststimulation
`confusion may or may not be important. Awaiting
`investigation are quantitative data on the intensity
`and frequency of a magnetic field to produce be(cid:173)
`havioral changes.
`
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`Allergan EX1054
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