Electroencephalography and clinical Neurophysiology, 85 (1992) 17-21
17
© 1992 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/92/$05.00
ELMOCO 90645
Magnetic brain stimulation with a double coil: the importance of coil orientation * K . R . Mills, S.J. B o n i f a c e a n d M. S c h u b e r t * * Clinical Neurophysiology Unit, University Department of Clinical Neurology, Radcliffe Infirmary, Oxford OX2 6HE (U.K.) (Accepted for publication: 10 April 1991)
Summary The human motor cortex can be excited by currents induced by a transient magnetic field generated in a coil over the scalp. A 9 cm mean diameter circular coil centred at the vertex is optimally placed for exciting the hand area. Anticlockwise current flow in the coil preferentially excites the left hemisphere and vice versa. A double coil has been used to investigate the orientation of inducing currents at which activation of cortical neural elements is maximal. The inducing current flowed in the same direction in the central segment of the coil and followed a monophasic wave form. The coil was rotated through 360 ° over the motor area in increments of 45 o and compound muscle action potentials from the first dorsal interosseous muscle were recorded. The largest responses were obtained with the coil at about 50 o to the parasagittal plane with a backward flowing inducing current. The optimal angle did not depend on stimulus intensity or background voluntary contraction. This orientation corresponds to an maximal induced current flowing forwards approximately at right angles to the central sulcus. It is postulated that horizontal neural elements are aligned in this direction and are preferentially excited by these monophasic magnetic stimuli. The results have important implications for mapping the motor areas with magnetic stimulators.
Key words: Magnetic brain stimulation; Double coil
It is well established that the transient magnetic field produced by energising a plane circular coil placed tangentially on the human scalp can induce intracranial currents capable of exciting the motor cortex (Barker et al. 1985; Hess et al. 1987). The optimal coil position for activating intrinsic hand muscles is with the coil centred over the vertex. The direction of current flow in the coil determines which hemisphere is preferentiaUy excited: an anticloekwise monophasic pulse of inducing current activates the left hemiphere and vice versa (Hess et al. 1987; Day et al. 1990). Multiphasic pulses from a circular coil, however, evoke a response that is not influenced by coil polarity (Claus et al. 1990). Currents induced in the brain are believed to follow circular paths parallel to the plane of the coil with no current flowing radially (Branston and Tofts l990). This contrasts with electrical brain stimulation where there is thought to be a significant radial current flow. The muscle responses to magnetic and electrical
* Financial assistance from the Medical Research Council, the MS Society of America and Deutsche Forschungsgemeinschaft. ** Present address: Universitaets-Nervenklinik, Abt. Neurologie, Sigmund Freud-Str. 25, D-5300 Bonn, F.R.G.
Correspondence to: Dr. K.R. Mills, Clinical Neurophysioiogy Unit, University Department of Clinical Neurology, Radcliffe Infirmary,
OX2 6HE (U.K.). Tel.: Oxford(0865)-249891. Oxford
stimulation differ in that the former have latencies longer by up to 3 msec (Hess et al. 1986a,b). These findings have led to the suggestion that magnetic stimuli activate cortical cells trans-synaptically, whereas electrical stimuli excite cortical cell bodies or axons directly (Hess et al. 1987; Day et al. 1989). Furthermore, because induced current paths are parallel to the cortical surface, it has been suggested that horizontally oriented neural elements are activated by magnetic stimuli (Day et al. 1989). The present experiments, performed with the approval of the local Ethics Committee, have investigated intrinsic hand muscle responses to cortical stimulation with a double coil. The coil is formed of two circles wound so that current flows in the same direction in the linear contiguous segment. It is believed that separate current paths would be induced in the brain related to each limb of the coil but that current would summate under the central segment giving a focal and directed form of stimulus. By stepwise rotation of the coil relative to the brain, it has been possible to determine the orientation of the horizontal current vector which most effectively excites cortical elements.
Methods
Characteristicsof the coil The double coil (Fig. 1) consisted of 2 loops each of 5 turns and was driven by a Digitimer D190 stimulator.
18
K.R. MILLS ET AL.
CHARACTERISTICSOFDOUBLECOIL
~
~12cm---. ~ . ' " ;'
REFERENCE POSITION OF COIL
JIPPeakHagnet eacurrent k 12:000tcAfield:l6' T 15turnsin
~ 0deg ~
each loop
cm
_
Fig. 1. Characteristics of the double coil showing its dimensions and the direction of current flow (vertical arrows), the angle between the two limbs, electromagnetic specifications and ihe voltage induced in a search coil plotted against the distance from the middle of its central segment in a line that is orthogonal to the central segment and in the same plane as the limbs of the coil.
Each loop had a mean long diameter of 14 cm and the planes of the 2 loops were set at an angle of about 130 ° to facilitate placement over the scalp. The total inductance was 25 /.~H and at maximum output, a current of 12,000 A produced a peak magnetic field of 1.6 Tesla The pulse was 300/.~sec in duration and had a predominantly monophasic wave form with a small late phase. The direction of current flow through the coil was determined using an oscilloscope and a concentric search coil of the same diameter as each loop, by the first deflection of the induced wave form. When the double coil was viewed from above, the inducing current flowed in a clockwise direction through one loop and in an anticlockwise direction through the other, so that t h e direction of flow was the same in each loop through the central contiguous segment of the coil. The voltage induced in a single turn circular search coil of 2.5 cm diameter by each limb of the double coil was measured at intervals of 1 cm. The search coil was held in a plane parallel to that of one of the limbs of the stimulating coil, at a distance of 3 mm from the surface of the windings that were normally held against the scalp. Results indicated that the voltage induced was indeed maximal under the central segment of the coil (Fig. 1). The central section of the coil was extended into a straight plastic handle which was used to adjust manually the orientation of the coil with the aid of reference marks on the scalp.
Fig. 2. Diagram showing the reference position of the coil with the mid-point of the central section placed on the scalp 3 cm along the inter-aural line to the left of the vertex. Coil orientation in this parasagittal plane was designated as 0 ° when the inducing current in the central segment flowed antero-posteriorly.
Electronic Design 1401) for subsequent analysis. A total of 14 experimental runs were performed using different conditions. The mid-point of the central section of the coil was placed on the scalp to overlie the motor area, 3 cm along the inter-aural line to the left of the vertex. Coil orientation in this parasagittal plane was designated as 0 ° when the inducing current flowed backwards (Fig. 2). Orientation was changed in increo ments of 45 o clockwise relative to the parasagittal plane for the full arc of 360 °. In one subject, first the left and then the right hemispheres were stimulated and recordings were made from both hands simultaneously. At each stimulus orientation 5 CMAPs were obtained (Fig. 3) and the average latency and ampli-
0.5 mv
Stimulation and recording Compound muscle action potentials (CMAPs) were recorded with surface electrodes taped over the belly and tendon of the first dorsal interosseous (FDI) muscle of 4 healthy right handed subjects. Signals were amplified with a bandpass of 32 H z - 3 . 2 kHz (Medelec Mystro or MS6) and digitised a t 10 kHz (Cambridge
Fig. 3. Superimposition of 5 CMAPs obtained at a coil angle of 45 ° in one subject to illustrate the intertrial variability in amplitude.
MAGNETIC BRAIN STIMULATION WITH A DOUBLE COIL
t
ewe em. s re .
u, inea
e enmen a, run, a
total of 40 stimuli were delivered. In each subject, two different stimulus intensities were investigated, and a comparison was made between CMAPs obtained with FDI relaxed and with the muscle maintaining a small (about 10% maximum) voluntary contraction. One or two pauses were required during the course of the experimental session to allow the coil to cool. In order to exclude a possible temperature dependent change in the effectiveness of the stimulus, one subject received 50 stimuli at alternating orientations of 45 o and 225 o during which the coil temperature rose from a normal starting temperature to its maximum operational temperature, There was no significant change in amplitude or latency of CMAPs. Plots using polar co-ordinates were used to describe the relationship between CMAP amplitude and stimulus orientation. For each experimental condition the angle relative to the parasagittal plane (Fig. 2) of the resultant vector was calculated from: tan -] ~ V . s i n ( 0 ) / ~ ] V , cos(0)
~
180 °
~
19 A
0
270
90
B ~ /
__~
180 0 I
270-
2?0
90
180 \ 90
270
180 0
c
~90
18o
0
~ 270
D
~./~..~
0
-gf.
2/0
90
180
180
0
0
Fig. 5. Polar plots showing the amplitude of averaged CMAPs from 8 stimulus orientations at increments of 45 ° with respect to the parasagittal plane (0-180 °) in 4 subjects (A-D) with FDI relaxed (left sided plots) and activated (right sided plots). The centre of each circle corresponds to the rotation point for the double coil, 3 cm lateral to the vertex. Maximal CMAP amplitudes were obtained at angles of 0-90 °, with an increase in both the amplitude and the size of the effective stimulating arc on activation of the muscle. Calibration: radius = 2 mV.
2
where V is the CMAP amplitude obtained at each angle theta.
Results
--
-4-
/
1my| / 25m.I Fig. 4. CMAPs from 8 stimulus orientations at increments of 45 ° with respect to the parasagittal plane (0-180 ° ) in one subject (stimulus intensity 70%, FDI relaxed). Each diagram of the head is shown with the CMAP beneath it. The double coil is centred 3 cm to the left of the vertex, the direction of current flow through the central segment is indicated by the arrow on the handle in the plot at 0 °. The largest response was obtained at a stimulus orientation
of 45 o.
CMAP amplitude in right FDI was consistently highest in the 0-90 ° quadrant (Figs. 4 and 5) and markedly lower in the remaining 3 quadrants. The mean ( + / - S.D.) resultant vector for all subjects had an angle of 50 ° ( + / - 19) relative to the parasagittal plane. Where first the left and then the right hemiphere h a d b e e n stimulated, the angle of the v e c t o r was for the left hemisphere 48 o and for the right hemisphere 290 o (Fig. 6). With a stimulus intensity of 60% maxim u m , n o consistent responses were obtained in the
FDI ipsilateral to the stimulated hemisphere in this subject.
20
K.R. MILLSET AL. 0
~
'-
~ _ ~ 270
90
180
180
Stimulate: L hemisphere
Stlmu]ete:R hemisphere
Record: R FDI
Record: L FDI
Fig. 6. Two polar plots showing the amplit6edeof averaged CMAPs obtained in I subject by stimulating the left hemisphereand recording from the contracted right FDI and then vice versa. Maximum responses were obtained in the anteriorquadrant contralateralto the stimulated hemisphere,with mean vectorsof 48 o and 290 o respectively.Calibration: radius = 5 mV. Stimulusintensity60%. CMAPs with the shortest latencies were found in the 0-180 o arc, with latencies of up to 2.5-6 msec longer when obtained from other coil orientations, For all subjects, voluntary activation of FDI increased the amplitudes and widened the arc over which CMAPs could be obtained (Fig. 5). Nevertheless the angle o f maximal response was essentially the same as when the muscle was relaxed, Increasing stimulus intensity by 10%, whether FDI was relaxed or activated, also widened the arc over which responses could be obtained, but again the optimal angle relative to the parasagittal plane was similar to that in the relaxed state,
Discussion
Several workers have investigated the use of double coils for magnetic brain stimulation. Amassian et al. (1989) have used a double square coil to produce more focal stimulation of the brain than a simple plane circular coil but have not investigated the effects of coil orientation relative to the sagittal plane. R/Ssler et al. (1989) used a twin circular coil, each limb having about half the diameter of the coil used here, and showed that maximal responses in abductor digiti minimi were obtained with the inducing current flowing in an antero-posterior plane. The precise relationship of coil angle relative to the parasagittal plane to response amplitude was not, however, systematically explored, The present results indicate that the orientation, relative to the brain, of inducing currents set up by a monophasic current pulse in a double coil is critical in causing excitation of the underlying neural elements, Furthermore, the direction of current flow at a given angle is also important. The actual current paths induced in the brain are unknown, but it is believed that they would follow roughly circular paths, parallel to the skull contour, with virtually no current flowing radially,
With the limbs of the double coil set at an angle as here, there may have been a small radial current component, but this would have remained constant when the coil was rotated and is therefore unlikely to account for the present results. If currents induced in the brain by this coil excite horizontal neural elements, then the results suggest that these elements are aligned with their major axes at about 50 o to the sagittal plane, whether stimulating the right or left hemisphere (Fig. 6). This would correspond to horizontal fibres aligned approximately at right angles to the main axis of the motor strip. There is abundant anatomical evidence of horizontal fibre systems in motor cortex; some of these horizontal fibres are aligned with their long axes in a direction at right angles to the main axis of the central sulcus. Jones and Wise (1978) found that the axon branches and dendritic fields of type 1 cells are orientated precisely antero-posteriorly, i.e., at right angles to the long axis of the pre- and post-central gyri in monkey cortex. Gatter and Powell (1978)found an asymmetry in the degeneration of horizontal fibres after microelectrode lesions of the cortex; degeneration was greater in the antero-posterior direction than in the medio-lateral direction. Anatomical studies on human motor cortex (Marin-Padilla 1970) have also demonstrated horizontal fibres mainly oriented in the anteroposterior direction in layers IV and V. Physiological studies using unipolar anodal stimulation and recording from single pyramidal ceils showed that the distance over which cells could be excited was greater in the medio-lateral direction than antero-posteriorly (Landgren et al. 1962). It is possible that magnetic stimuli may be activating such a horizontal fibre system and that activation is maximal when the direction of the induced current falls parallel to the principal orientation of the fibres. The present results also indicate that the direction of current flow is critical, with inducing currents flowing backwards along the optimal vector being far more effective than those flowing in the opposite direction. Response latencies were always shortest in the 0-180 o arc. This may reflect either the capacity of the stimulus to produce a D wave in the optimal orientation but not in others, or the difference in the I wave latency of responses that occur when the direction of the current in a circular coil is reversed (Day et al. 1989). The stimulus orientation producing the largest CMAP amplitude could be accounted for by an arrangement of neural elements in the motor area such that cell bodies tend to be posterior with their processes extending forwards across the motor strip. This would include some of the dendrites of pyramidal tract neurones (PTNs) and their pre-synaptic interneurones, collateral connections between PTNs and also PTNs located in the anterior bank of the central sulcus. Alternatively, a
MAGNETIC BRAIN STIMULATION WITH A DOUBLE COIL
group of fibres from a posteriorly placed cortical area, such as the primary sensory cortex, may enter the motor cortex as a bundle oriented at about 50 o to the sagittal plane, The results have major implications if the m o t o r cortex is to be m a p p e d using magnetic stimuli. Clearly, not only is the position of the coil important, but also is its orientation relative to the brain and the direction of current flow within it.
References Amassian, V.E., Cracco, R.Q. and Maccabee, P.J. (1989) Focal stimulation of human cerebral cortex with the magnetic coil: a comparison with electrical stimulation. Electroenceph. olin. Neurophysiol., 74: 401-416. Barker, A.T., Freeston, I.L., Jalinous, R., Merton, P.A. and Morton, H.B. (1985) Magnetic stimulation of the human brain. J. Physiol. (Lond.), 369: 3P. Branston, N.M. and Torts, P.S. (1990) Magnetic stimulation of a volume conductor produces a negligible component of induced current perpendicular to the surface. J. Physiol. (Lond.), 423: 67P. Claus, D., Murray, N.M.F., Spitzer, A. and Flugel, D. (1990) The influence of stimulus type on the magnetic excitation of nerve structures. Electroenceph. clin. Neurophysiol., 75: 342-349. Day, B.L., Thompson, P.D., Dick, J.P.R., Nakashima, K. and Marsden, C.D. (1987) Different sites of action of electrical and magnetic stimulation of the human brain. Neurosci. Lett., 75: 101-106. Day, B.L., Dressier, D., Maertens de Noordhout, A., Marsden, C.D., Nakashima, K., Rothweil, J.C. and Thompson, P.D. (1989) Electric and magnetic stimulation of human motor cortex: surface EMG and single motor unit responses. J. Physiol. (Lond.), 412: 449-473.
21 Day, B.L., Dressier, D., Claus, D., Hess, C.W., Maertens de Noordhout, A., Marsden, C.D., Mills, K.R., Murray, N.M.F., Nakashima, K., RothweU, J.C. and Thompson, P.D. (1990) Erratum: Direction of current in magnetic stimulatimng coil used for percutaneous activation of brain, spinal cord and peripheral nerve. J. Physiol. (Lond.), in press. Gatter, K.C. and Powell, T.P.S. (1978) The intrinsic connections of the cortex of area 4 of the monkey. Brain, 101: 513-541. Hess, C.W., Mills, K.R. and Murray, N.M.F. (1986a) Magnetic stimulation of the human brain: the effects of voluntary muscle activity. J. Physiol. (Lond.), 378: 37P. Hess, C.W., Mills, K.R. and Murray, N.M.F. (1986b) Percutaneous stimulation of the human brain: a comparison of electrical and magnetic stimuli. J. Physiol. (Lond.), 378: 35P. Hess, C.W., Mills, FLR. and Murray, N.M.F. (1987) Responses in small hand muscles from magnetic stimulation of the human brain. J. Physiol. (Lond.), 388: 397-419. Jones, E.G. and Wise, S.P (1978) Size, laminar and columnar distribution of efferent cells in the sensory-motor cortex of monkeys. J. Comp. Neurol., 175: 391-438. Landgren, S., Phillips, C.G. and Porter, R. (1962) Cortical fields of origin of the monosynaptic pyramidal pathways to some alpha motoneurones of the baboon's hand and forearm. J. Physiol. (Lond.), 161: 112-125. Marin-PadiUa, M. (1970) Prenatal and early postnatal ontogenesis of the human motor cortex: a Golgi study. I. The sequential development of the cortical layers. Brain Res., 23: 167-183. Phillips, C.G. (1987) Epicortical electrical mapping of motor areas in primates. In: G. Brock, M. O'Connor and J. Marsh (Eds.), Motor Areas of the Cerebral Cortex. Wiley, London, pp. 5-20. Phillips, C.G. and Porter, R. (1962) Unifocal and bifocal stimulation of the motor cortex. J. Physiol. (Lond.), 162: 532-538. R6sler, K.M., Hess, C.W., Heckmann, R. and Ludin, H.P. (1989) Significance of shape and size of the stimulating coil in magnetic stimulation of the human motor cortex. Neurosci Lett., 100: 347-352.
17
© 1992 Elsevier Scientific Publishers Ireland, Ltd. 0924-980X/92/$05.00
ELMOCO 90645
Magnetic brain stimulation with a double coil: the importance of coil orientation * K . R . Mills, S.J. B o n i f a c e a n d M. S c h u b e r t * * Clinical Neurophysiology Unit, University Department of Clinical Neurology, Radcliffe Infirmary, Oxford OX2 6HE (U.K.) (Accepted for publication: 10 April 1991)
Summary The human motor cortex can be excited by currents induced by a transient magnetic field generated in a coil over the scalp. A 9 cm mean diameter circular coil centred at the vertex is optimally placed for exciting the hand area. Anticlockwise current flow in the coil preferentially excites the left hemisphere and vice versa. A double coil has been used to investigate the orientation of inducing currents at which activation of cortical neural elements is maximal. The inducing current flowed in the same direction in the central segment of the coil and followed a monophasic wave form. The coil was rotated through 360 ° over the motor area in increments of 45 o and compound muscle action potentials from the first dorsal interosseous muscle were recorded. The largest responses were obtained with the coil at about 50 o to the parasagittal plane with a backward flowing inducing current. The optimal angle did not depend on stimulus intensity or background voluntary contraction. This orientation corresponds to an maximal induced current flowing forwards approximately at right angles to the central sulcus. It is postulated that horizontal neural elements are aligned in this direction and are preferentially excited by these monophasic magnetic stimuli. The results have important implications for mapping the motor areas with magnetic stimulators.
Key words: Magnetic brain stimulation; Double coil
It is well established that the transient magnetic field produced by energising a plane circular coil placed tangentially on the human scalp can induce intracranial currents capable of exciting the motor cortex (Barker et al. 1985; Hess et al. 1987). The optimal coil position for activating intrinsic hand muscles is with the coil centred over the vertex. The direction of current flow in the coil determines which hemisphere is preferentiaUy excited: an anticloekwise monophasic pulse of inducing current activates the left hemiphere and vice versa (Hess et al. 1987; Day et al. 1990). Multiphasic pulses from a circular coil, however, evoke a response that is not influenced by coil polarity (Claus et al. 1990). Currents induced in the brain are believed to follow circular paths parallel to the plane of the coil with no current flowing radially (Branston and Tofts l990). This contrasts with electrical brain stimulation where there is thought to be a significant radial current flow. The muscle responses to magnetic and electrical
* Financial assistance from the Medical Research Council, the MS Society of America and Deutsche Forschungsgemeinschaft. ** Present address: Universitaets-Nervenklinik, Abt. Neurologie, Sigmund Freud-Str. 25, D-5300 Bonn, F.R.G.
Correspondence to: Dr. K.R. Mills, Clinical Neurophysioiogy Unit, University Department of Clinical Neurology, Radcliffe Infirmary,
OX2 6HE (U.K.). Tel.: Oxford(0865)-249891. Oxford
stimulation differ in that the former have latencies longer by up to 3 msec (Hess et al. 1986a,b). These findings have led to the suggestion that magnetic stimuli activate cortical cells trans-synaptically, whereas electrical stimuli excite cortical cell bodies or axons directly (Hess et al. 1987; Day et al. 1989). Furthermore, because induced current paths are parallel to the cortical surface, it has been suggested that horizontally oriented neural elements are activated by magnetic stimuli (Day et al. 1989). The present experiments, performed with the approval of the local Ethics Committee, have investigated intrinsic hand muscle responses to cortical stimulation with a double coil. The coil is formed of two circles wound so that current flows in the same direction in the linear contiguous segment. It is believed that separate current paths would be induced in the brain related to each limb of the coil but that current would summate under the central segment giving a focal and directed form of stimulus. By stepwise rotation of the coil relative to the brain, it has been possible to determine the orientation of the horizontal current vector which most effectively excites cortical elements.
Methods
Characteristicsof the coil The double coil (Fig. 1) consisted of 2 loops each of 5 turns and was driven by a Digitimer D190 stimulator.
18
K.R. MILLS ET AL.
CHARACTERISTICSOFDOUBLECOIL
~
~12cm---. ~ . ' " ;'
REFERENCE POSITION OF COIL
JIPPeakHagnet eacurrent k 12:000tcAfield:l6' T 15turnsin
~ 0deg ~
each loop
cm
_
Fig. 1. Characteristics of the double coil showing its dimensions and the direction of current flow (vertical arrows), the angle between the two limbs, electromagnetic specifications and ihe voltage induced in a search coil plotted against the distance from the middle of its central segment in a line that is orthogonal to the central segment and in the same plane as the limbs of the coil.
Each loop had a mean long diameter of 14 cm and the planes of the 2 loops were set at an angle of about 130 ° to facilitate placement over the scalp. The total inductance was 25 /.~H and at maximum output, a current of 12,000 A produced a peak magnetic field of 1.6 Tesla The pulse was 300/.~sec in duration and had a predominantly monophasic wave form with a small late phase. The direction of current flow through the coil was determined using an oscilloscope and a concentric search coil of the same diameter as each loop, by the first deflection of the induced wave form. When the double coil was viewed from above, the inducing current flowed in a clockwise direction through one loop and in an anticlockwise direction through the other, so that t h e direction of flow was the same in each loop through the central contiguous segment of the coil. The voltage induced in a single turn circular search coil of 2.5 cm diameter by each limb of the double coil was measured at intervals of 1 cm. The search coil was held in a plane parallel to that of one of the limbs of the stimulating coil, at a distance of 3 mm from the surface of the windings that were normally held against the scalp. Results indicated that the voltage induced was indeed maximal under the central segment of the coil (Fig. 1). The central section of the coil was extended into a straight plastic handle which was used to adjust manually the orientation of the coil with the aid of reference marks on the scalp.
Fig. 2. Diagram showing the reference position of the coil with the mid-point of the central section placed on the scalp 3 cm along the inter-aural line to the left of the vertex. Coil orientation in this parasagittal plane was designated as 0 ° when the inducing current in the central segment flowed antero-posteriorly.
Electronic Design 1401) for subsequent analysis. A total of 14 experimental runs were performed using different conditions. The mid-point of the central section of the coil was placed on the scalp to overlie the motor area, 3 cm along the inter-aural line to the left of the vertex. Coil orientation in this parasagittal plane was designated as 0 ° when the inducing current flowed backwards (Fig. 2). Orientation was changed in increo ments of 45 o clockwise relative to the parasagittal plane for the full arc of 360 °. In one subject, first the left and then the right hemispheres were stimulated and recordings were made from both hands simultaneously. At each stimulus orientation 5 CMAPs were obtained (Fig. 3) and the average latency and ampli-
0.5 mv
Stimulation and recording Compound muscle action potentials (CMAPs) were recorded with surface electrodes taped over the belly and tendon of the first dorsal interosseous (FDI) muscle of 4 healthy right handed subjects. Signals were amplified with a bandpass of 32 H z - 3 . 2 kHz (Medelec Mystro or MS6) and digitised a t 10 kHz (Cambridge
Fig. 3. Superimposition of 5 CMAPs obtained at a coil angle of 45 ° in one subject to illustrate the intertrial variability in amplitude.
MAGNETIC BRAIN STIMULATION WITH A DOUBLE COIL
t
ewe em. s re .
u, inea
e enmen a, run, a
total of 40 stimuli were delivered. In each subject, two different stimulus intensities were investigated, and a comparison was made between CMAPs obtained with FDI relaxed and with the muscle maintaining a small (about 10% maximum) voluntary contraction. One or two pauses were required during the course of the experimental session to allow the coil to cool. In order to exclude a possible temperature dependent change in the effectiveness of the stimulus, one subject received 50 stimuli at alternating orientations of 45 o and 225 o during which the coil temperature rose from a normal starting temperature to its maximum operational temperature, There was no significant change in amplitude or latency of CMAPs. Plots using polar co-ordinates were used to describe the relationship between CMAP amplitude and stimulus orientation. For each experimental condition the angle relative to the parasagittal plane (Fig. 2) of the resultant vector was calculated from: tan -] ~ V . s i n ( 0 ) / ~ ] V , cos(0)
~
180 °
~
19 A
0
270
90
B ~ /
__~
180 0 I
270-
2?0
90
180 \ 90
270
180 0
c
~90
18o
0
~ 270
D
~./~..~
0
-gf.
2/0
90
180
180
0
0
Fig. 5. Polar plots showing the amplitude of averaged CMAPs from 8 stimulus orientations at increments of 45 ° with respect to the parasagittal plane (0-180 °) in 4 subjects (A-D) with FDI relaxed (left sided plots) and activated (right sided plots). The centre of each circle corresponds to the rotation point for the double coil, 3 cm lateral to the vertex. Maximal CMAP amplitudes were obtained at angles of 0-90 °, with an increase in both the amplitude and the size of the effective stimulating arc on activation of the muscle. Calibration: radius = 2 mV.
2
where V is the CMAP amplitude obtained at each angle theta.
Results
--
-4-
/
1my| / 25m.I Fig. 4. CMAPs from 8 stimulus orientations at increments of 45 ° with respect to the parasagittal plane (0-180 ° ) in one subject (stimulus intensity 70%, FDI relaxed). Each diagram of the head is shown with the CMAP beneath it. The double coil is centred 3 cm to the left of the vertex, the direction of current flow through the central segment is indicated by the arrow on the handle in the plot at 0 °. The largest response was obtained at a stimulus orientation
of 45 o.
CMAP amplitude in right FDI was consistently highest in the 0-90 ° quadrant (Figs. 4 and 5) and markedly lower in the remaining 3 quadrants. The mean ( + / - S.D.) resultant vector for all subjects had an angle of 50 ° ( + / - 19) relative to the parasagittal plane. Where first the left and then the right hemiphere h a d b e e n stimulated, the angle of the v e c t o r was for the left hemisphere 48 o and for the right hemisphere 290 o (Fig. 6). With a stimulus intensity of 60% maxim u m , n o consistent responses were obtained in the
FDI ipsilateral to the stimulated hemisphere in this subject.
20
K.R. MILLSET AL. 0
~
'-
~ _ ~ 270
90
180
180
Stimulate: L hemisphere
Stlmu]ete:R hemisphere
Record: R FDI
Record: L FDI
Fig. 6. Two polar plots showing the amplit6edeof averaged CMAPs obtained in I subject by stimulating the left hemisphereand recording from the contracted right FDI and then vice versa. Maximum responses were obtained in the anteriorquadrant contralateralto the stimulated hemisphere,with mean vectorsof 48 o and 290 o respectively.Calibration: radius = 5 mV. Stimulusintensity60%. CMAPs with the shortest latencies were found in the 0-180 o arc, with latencies of up to 2.5-6 msec longer when obtained from other coil orientations, For all subjects, voluntary activation of FDI increased the amplitudes and widened the arc over which CMAPs could be obtained (Fig. 5). Nevertheless the angle o f maximal response was essentially the same as when the muscle was relaxed, Increasing stimulus intensity by 10%, whether FDI was relaxed or activated, also widened the arc over which responses could be obtained, but again the optimal angle relative to the parasagittal plane was similar to that in the relaxed state,
Discussion
Several workers have investigated the use of double coils for magnetic brain stimulation. Amassian et al. (1989) have used a double square coil to produce more focal stimulation of the brain than a simple plane circular coil but have not investigated the effects of coil orientation relative to the sagittal plane. R/Ssler et al. (1989) used a twin circular coil, each limb having about half the diameter of the coil used here, and showed that maximal responses in abductor digiti minimi were obtained with the inducing current flowing in an antero-posterior plane. The precise relationship of coil angle relative to the parasagittal plane to response amplitude was not, however, systematically explored, The present results indicate that the orientation, relative to the brain, of inducing currents set up by a monophasic current pulse in a double coil is critical in causing excitation of the underlying neural elements, Furthermore, the direction of current flow at a given angle is also important. The actual current paths induced in the brain are unknown, but it is believed that they would follow roughly circular paths, parallel to the skull contour, with virtually no current flowing radially,
With the limbs of the double coil set at an angle as here, there may have been a small radial current component, but this would have remained constant when the coil was rotated and is therefore unlikely to account for the present results. If currents induced in the brain by this coil excite horizontal neural elements, then the results suggest that these elements are aligned with their major axes at about 50 o to the sagittal plane, whether stimulating the right or left hemisphere (Fig. 6). This would correspond to horizontal fibres aligned approximately at right angles to the main axis of the motor strip. There is abundant anatomical evidence of horizontal fibre systems in motor cortex; some of these horizontal fibres are aligned with their long axes in a direction at right angles to the main axis of the central sulcus. Jones and Wise (1978) found that the axon branches and dendritic fields of type 1 cells are orientated precisely antero-posteriorly, i.e., at right angles to the long axis of the pre- and post-central gyri in monkey cortex. Gatter and Powell (1978)found an asymmetry in the degeneration of horizontal fibres after microelectrode lesions of the cortex; degeneration was greater in the antero-posterior direction than in the medio-lateral direction. Anatomical studies on human motor cortex (Marin-Padilla 1970) have also demonstrated horizontal fibres mainly oriented in the anteroposterior direction in layers IV and V. Physiological studies using unipolar anodal stimulation and recording from single pyramidal ceils showed that the distance over which cells could be excited was greater in the medio-lateral direction than antero-posteriorly (Landgren et al. 1962). It is possible that magnetic stimuli may be activating such a horizontal fibre system and that activation is maximal when the direction of the induced current falls parallel to the principal orientation of the fibres. The present results also indicate that the direction of current flow is critical, with inducing currents flowing backwards along the optimal vector being far more effective than those flowing in the opposite direction. Response latencies were always shortest in the 0-180 o arc. This may reflect either the capacity of the stimulus to produce a D wave in the optimal orientation but not in others, or the difference in the I wave latency of responses that occur when the direction of the current in a circular coil is reversed (Day et al. 1989). The stimulus orientation producing the largest CMAP amplitude could be accounted for by an arrangement of neural elements in the motor area such that cell bodies tend to be posterior with their processes extending forwards across the motor strip. This would include some of the dendrites of pyramidal tract neurones (PTNs) and their pre-synaptic interneurones, collateral connections between PTNs and also PTNs located in the anterior bank of the central sulcus. Alternatively, a
MAGNETIC BRAIN STIMULATION WITH A DOUBLE COIL
group of fibres from a posteriorly placed cortical area, such as the primary sensory cortex, may enter the motor cortex as a bundle oriented at about 50 o to the sagittal plane, The results have major implications if the m o t o r cortex is to be m a p p e d using magnetic stimuli. Clearly, not only is the position of the coil important, but also is its orientation relative to the brain and the direction of current flow within it.
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