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Effect of coil position and stimulus intensity in transcranial magnetic stimulation on human brain
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OF THE
NEUROLOGICAL SCIENCES
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Journal of Neurological Sciences 147 (1997) 155-159
Effect of coil position and stimulus intensity in transcranial magnetic stimulation on human brain Kazuo Kaneko”, Yasunori Fuchigami, Hideki Morita, Akira Ofuji, Shinya Kawai Department of Orthopedic Surgery, Yamguchi
University Hospital,
1144 Kogushi, Ube City, Yamaguchi, 755, Japan
Received 1 July 1996; revised 30 September 1996; accepted 21 October 1996
Abstract Evoked spinal cord potentials (ESCPs) from the cervical and high thoracic epidural space following transcranial magnetic stimulation were recorded from eight subjects in awake and anesthetized condition. Motor evoked potentials (MEPs) from the right abductor digiti minimi (ADM) and rectus femoris (RF) muscles were simultaneously recorded during voluntary contraction. The stimulus intensity was at 30% above the MEPs threshold of the ADM when the coil center was fixed on lo-20 international Cz position. In awake condition, multiple ESCP components (greater than 3) were recorded from the cervical epidural space but no or minimal components were recorded from the upper thoracic epidural space. When the coil was moved anteriorly so that the posterior edge of the coil was positioned on Cz, the amplitude of the first ESCP component was significantly increased (PcO.02) and shortened (not significant) at cervical levels. In addition, several ESCP components were more evident at high thoracic levels. Although the amplitude of the ADM was not enhanced, that of the RF was enhanced. During general anesthesia with volatile anesthetics (sevoflurane), only the first component of the ESCPs (D-wave) was elicited. Its amplitude was enhanced (P
1. Introduction Single transcranial magnetic or electrical stimulus produces multiple descending potentials in the human pyramidal tracts (Day et al., 1987; Berardelli et al., 1990; Burke et al., 1992, Burke et al., 1993). These potentials are composed of D-waves (due to direct activation of the corticospinal tract neurons) and I-waves (due to indirect or transsynaptic activation of the same neurons) (Patton and Amassian, 1954). In the peripheral nerve-skull model, Amassian et al. (1992) demonstrated that direct activation *Corresponding author. Tel.: t81 836 222268; fax.: 181 836 222267. 0022-510X/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved PII SOO22-510X(96)05324-5
of corticospinal neuron (producing D-wave) occurred when the coil was positioned in a tilted lateral sagittal position. Several papers have been published on evoked spinal cord potentials (ESCPs) following magnetic stimulation of the human motor cortex (Day et al., 1987; Berardelli et al., 1990; Burke et al., 1992; Hicks et al., 1992; Burke et al., 1993) but none about the effect of varying magnetic coil position on corticospinal excitability in human brain. We previously reported on the effect of varying stimulus intensity and voluntary contraction on corticospinal potentials by observing epidurally recorded corticospinal potentials following transcranial magnetic stimulation (Kaneko et al., 1996). In this study we investigated the
K. Kaneko et al. I Journal of Neurological
156
effect of magnetic coil position on the ESCPs following transcranial magnetic stimulation.
2. Materials
and methods
The study was conducted on eight patients (3 female, 5 males, aged 25-68 years old) with thoracic myelopathy (3 patients due to intradural extramedullary schwannoma, 3 patients due to metastatic spinal tumors, 2 patients due to ossification of the yellow ligament). Patients had incomplete paraparesis except for the two patients with intradural extramedullary schwannoma who complained only of unilateral intercostal neuralgia without motor deficit. The experimental procedure was explained to the patients in detail and informed consent for the procedure was obtained. Recording of the ESCPs following transcranial magnetic stimulation was performed before and after induction of general anesthesia. Epidural electrodes were used to record evoked muscle responses following spinal cord stimulation during intraoperative monitoring of spinal cord function (Mochida et al., 1995). They were inserted at the high thoracic level rostra1 to the lesions and advanced cranially to position the highest electrode at mid-cervical level. Epidural catheter electrodes with five recording tips at interelectrode distances of 1.5 cm (Unique Medical Co., Japan, UKG-IOO-5PM) were used in this study. In this investigation, bipolar recordings of ESCPs following transcranial magnetic stimulation were taken from the cervical epidural space in all subjects. The active electrode, with interelectrode distance was 1.5 cm, was placed in a cephalad position. In five subjects, the ESCPs from the high thoracic epidural space (Tl/2 or T2/3) were simultaneously recorded. In awake condition, motor evoked potentials (MEPs) from the right abductor digiti minimi muscle (ADM) were recorded simultaneously with the belly-tendon electrode position. In two patients who complained only of intercostal neuralgia without any long tract signs, the MEPs from the right rectus femoris muscle (RF) were also recorded. In the other six cases, reproducible MEPs were not obtained from RF. The ESCPs and MEPs were amplified, filtered by 20-3 KHz, averaged (n=5-lo), and stored with a standard electromyograph. (Dantec, Denmark, Counterpoint). At least two waves were recorded and superimposed. Multiple ESCP components following transcranial magnetic stimulation were named in their order of increasing latencies and polarities. The negative peak latencies and the peak-topeak amplitudes of each ESCP at the mid-cervical epidural space (C4/5 or C5/6) were measured and the results were expressed as mean2S.D. The conduction velocity of the ESCPs was calculated by measuring the inter-electrode distance and the negative peak latency of the first ESCP component. Transcranial magnetic stimulation was delivered by a
Sciences 147 (1997) 155-159
Novametrix Magstim Model 200 magnetic stimulator using a round 14-cm diameter coil (Magstim, Whitland, UK, Model 200). The center of the coil was fixed on Cz position based on the IO-20 international system. A counterclockwise current in the coil, as viewed from above, was delivered to stimulate the left hemisphere (Rossini et al., 1994). The stimulus intensity was set at 30% above the MEP threshold of the ADM (70-80% of output) with the coil centered on Cz position during voluntary contraction (recording sensitivity of 0.5 mV/D). The ESCPs and MEPs were also recorded when the magnetic coil was moved anteriorly so that posterior coil edge was positioned on Cz using the same stimulus output as previously defined. Recordings of ESCPs following transcranial magnetic stimulation were also taken under general anesthesia with volatile anesthetics (50: 50 nitrous oxide/oxygen mixture and end-tidal sevoflurane concentration >1.5%) at the same stimulus output utilized in the awake condition. Statistical analysis was performed by the Wilcoxon signed-rank tests using the StatView program (Abacus Concepts, Berkeley, CA, USA).
3. Result 3.1. ESCPs and MEPs elicited by two d#‘erent coil position in the awake condition Several ESCP components (greater than 3) were recorded from the cervical epidural space. With the coil center fixed on Cz, the negative peak latency of the first component (Nl) was 3.0t0.2 ms. That of the later components were 4.320.3 ms (N2), 5.920.4 ms (N3), and 7.2-t0.3 ms (N4). The conduction velocity of the first component was 58.Ok9.0 m/s. The amplitudes of each ESCP components were 13.825.9 pY (PI-N]), 13.356.3 ~.LV(P2-N2), 11.924.8 pV (P3-N3), and 14.1?10.0 pV (P4-N4). When the coil edge was positioned on Cz, the Nl latency and amplitude was 2.820.2 ms and 32.5% 15.9 p.V, respectively. The later components were distorted and their amplitudes were 10.527.4 FV (P2-N2), 9.1 k6.8 p.V (P3N3), and 6.8e7.5 pV (P4-N4), respectively. The amplitude of the first component was significantly increased compared to that recorded with the coil center fixed on Cz (PcO.02). In contrast, amplitudes of later components were slightly decreased at the cervical level (Fig. 1). In patients who had ESCPs recorded from both the cervical and high thoracic epidural spaces, several ESCP components at the high thoracic level were more evident when the coil edge was positioned on Cz in the awake condition. The onset latency and amplitude of the MEPs from the ADM were 19.52 1.4 ms and 4.9k2.5 mV, respectively, when the coil center was fixed on Cz. They were 19.02 1.3 ms and 4.422.3 mV, respectively when the coil edge was
K. Kaneko et al. I Journal of Neurological
Sciences 147 (1997) 155-159
157
Magnetic Stimulation 70% 9 Center on c.?
8 7 6
C S/6
5 4 3 2 1 0 Nl
N2
II N3
T l/2 T2l3
N4
Amplitude
1
I I
I
P, NT
P* N?
P3 N3
P4 N4
* P
Fig. I. Comparison of ESCP latency and amplitude in two different magnetic coil position. Negative peak latency and peak-to-peak amplitude of each potential is shown,
fixed on Cz. In the two patients with the MEPs recorded from the RF, although the amplitude of the first ESCP component and the MEP amplitude from the RF was increased, the MEP amplitude from the ADM remained unchanged when the coil edge was fixed on Cz (Fig. 2). 3.2. ESCPs recorded during anesthesia with volatile anesthetics In all subjects, only the first component was routinely evoked with almost similar amplitudes (12.6k5.8 pV) as that in the awake condition. Negative peak latency of the first ESCP component under general anesthesia (3.050.7 ms) was equivalent to that in the awake condition. When the coil edge was positioned on Cz, the amplitude of this first component (28.12 12.4 PV) was significantly larger (PcO.02) than that recorded when the coil center was fixed on Cz. In five patients with ESCPs recorded from the high thoracic epidural space, the amplitude of the first component was also enhanced when the coil edge was fixed on Cz. (Fig. 3). In addition, ESCPs were recorded at 100% stimulus output in two different coil positions in four subjects. The amplitude of the first ESCP component was similar in the
Fig. 2. ESCPs and MEPs following transcranial magnetic stimulation in different coil positions during voluntary contraction of the muscle. When the coil edge was fixed on Cz, several components were recorded at the high thoracic level. Amplitude of the first ESCP component was enhanced (right traces) compared to that recorded when the coil center was fixed on Cz (left traces). Amplitude of MEPs from ADM was similar in both coil position, but that from RF was enhanced when the coil edge was held on CZ.
two different coil positions. Its onset latency was however shortened at 100% stimulus intensity as compared to that recorded at previously determined intensity (Fig. 4).
00 vV’D i :.~: c siti e L
Coil Position
x
18 l&D : 3
dh
w
*
! : :
ID rvu
i/.
.
T 112
1In6 1 Sevafluranc
1.5 f
Fig. 3. ESCPs during general anesthesia with sevoflurane (same patient as the first ESCP component was recordable during anesthesia. When the coil edge was fixed on Cz, the ESCP amplitude was increased at both cervical and high thoracic levels (right traces).
in Fig. 2). Only
158
K. Kaneko et al. I Journal of Neurological
Magnetic stimulation
.
.
Fig. 4. ESCPs during general anesthesia with sevoflurane. At 70% of stimulus output, the ESCP amplitude was increased when the coil edge was fixed on Cz. The ESCP amplitude was the same in both coil position at 100% of stimulus output.
4. Discussion We recorded ESCPs following transcranial magnetic stimulation from the cervical and high thoracic epidural space in both the awake and anesthetized condition. Peak latency of the first component from the mid cervical epidural space was 3.OkO.2 ms at high stimulus intensity and its conduction velocity was about 60 m/s: consistent with that of the descending volley in the corticospinal tract. At high stimulus intensity, the first ESCP component was stable during anesthesia, but later components were easily attenuated. The effect of volatile anesthetics on these responses were consistent with those from prior studies (Hicks et al., 1992; Burke et al., 1993). Although we did not compare the ESCPs following transcranial magnetic stimulation to those following transcranial electrical stimulation, we previously reported that the amplitude of this first ESCP component after test stimulation recovered within 2 ms of interstimulus interval in paired transcranial magnetic stimulation (Kaneko et al., 1996). This implied that the first potential was generated nonsynaptically. From these results, we concluded that the first component was a D-wave (generated by direct activation of cortical motor neuron) and later components were I-waves (attenuated with volatile anesthetics) at the stimulus intensity defined in this study. Burke et al. (1993) demonstrated that transcranial magnetic stimulation produced a D-wave similar to electrical stimulation, although its amplitude was smaller than that following electrical stimulation. We had demonstrated that in awake condition, transcranial magnetic stimulation at threshold stimulus intensity of MEPs from ADM preferentially generated I-waves when the round coil was centered on Cz. Furthermore, amplitude of the D-wave was relatively smaller compared to that of I-waves when the
Sciences 147 (1997) 155-159
coil center was positioned on Cz, even if the stimulus intensity was 20-30% above the threshold of MEPs during voluntary contraction (Kaneko et al., 1996). Hence coil centered on Cz is not optimal in producing D-waves effectively. Amassian et al. (1992) suggested that coil position was a crucial determinant of whether the corticospinal tract was activated directly or indirectly in the experimental peripheral nerve skull model. Rank (1975) showed that an electrical anodal stimulation to cortical motor neuron excited them directly when it flowed nearly parallel to the trajectory of the pyramidal neurons. Magnetic stimulation using a monophasic stimulus pulse with the coil edge on Cz produces an induced current, whose direction is nearly parallel to the trajectory of the pyramidal neurons. This induced current direction is optimal in activating the cortical motor neurons or axons directly. Our study showed that the amplitude of the first ESCP components (D-wave) at cervical level was significantly increased when the coil edge was fixed on Cz in both the awake as well as the anesthetized condition. The MEP amplitude from the RF was increased but this was not so from the ADM when the coil edge was fixed on Cz. This discrepancy was because the cortical motor neurons to the trunk or lower limb muscles were also activated when the coil edge was fixed on Cz. This was consistent with a prior report that the most stable responses obtained from the tibialis anterior muscles were with the round coil centered slightly anterior to the vertex (Terao et al., 1994). When the coil edge was fixed on Cz, multiple ESCPs with enhanced first ESCP components were easily recordable from the high thoracic epidural space. Thus enhancement of D-waves was due to activation of pyramidal cells or tracts projecting not only to the upper limb but also to the trunk and lower limb muscles. We thus hypothesize that corticospinal tracts projecting to the trunk and lower limb muscles can be activated directly when the edge of the round coil is fixed on Cz. In this study we fixed the magnetic stimulus at 30% above the MEP threshold of the ADM (70-80% of output) when the coil was centered on Cz during voluntary contraction. However if the stimulus intensity was strong enough (100% of output), the amplitude of the first ESCP component (D-wave) was not enhanced even when the coil edge was on Cz. The onset latency of the first ESCP component was also shortened at 100% stimulus intensity. This means that high intensity magnetic stimulation can elicit most of the cortical motor neurons or axons directly even those deep inside the brain and the position of the coil is no longer crucial in determining whether the corticospinal tract is activated directly or indirectly. In this study we used the round coil for transcranial magnetic stimulation. The induced current from this coil can spread widely in the motor area and it may stimulate bilateral motor areas. To investigate the effect of induced current direction on corticospinal excitability following transcranial magnetic stimulation, similar study using more
K. Kaneko et al. I Journal of Neurological Sciences 147 (1997) 1.55-159
localized stimulators such as a figure-of-eight coil should be performed. In conclusion, the present study supports the importance of coil position in recording ESCPs following transcranial magnetic stimulation in the human corticospinal system. To obtain large D-waves, the edge of the magnetic coil must be fixed on Cz when using the round coil as the induced current flows parallel to the trajectory of the motor neurons. This position is also optimal for recording Dwaves distributing to truncal and lower limb muscles. However, the coil position is no longer crucial when the magnetic stimulus intensity was strong enough. Clinically, magnetic coil position is a crucial factor when recording corticospinal D-waves in monitoring of spinal cord function during neurosurgery.
References Amassian, V.E., Eberle, L., Maccabee, P.J. and Cracco, R.Q. (1992) Modeling magnetic coil excitation of human cerebral cortex with a peripheral nerve immersed in a brain-shape volume conductor: the significance of fiber bending in excitation. Electroencephalogr. Clin. Neurophysiol., 85: 291-301. Berardelli, A., Inghilleri, M., Cruccu, G. and Manfredi, M. (1990) Descending volley after electrical and magnetic transcranial stimulation in man. Neurosci. Lett., 112: 54-58. Burke, D., Hicks, R., Stephen, J., Woodforth, I. and Crawford, M. (1992) Assessment of corticospinal and somatosensory conduction simultaneously during scoliosis surgery. Electroencephalogr. Clin. Neurophysiol., 83: 388-396.
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Burke, D., Hicks, R., Gandevia, S.C., Stephen, J., Woodforth, I. and Crawford, M. (1993) Direct comparison of cortico-spinal volleys in human subjects to transcranial magnetic and electrical stimulation. J. Physiol., 470: 383-393. Day. B.L., Rothwell, J.C., Thompson, P.D., Dick, J.P.R., Cowman, J.M.A., Berardelli, A. and Marsden, C.D. (1987) Motor cortex stimulation in intact man. II. Multiple descending volleys. Brain, 110: 1191-1209. Hicks, R., Burke. D., Stephen, J., Woodforth, I. and Crawford, M. (1992) Corticospinal volleys evoked by electrical stimulation of human motor cortex after withdrawal of volatile anesthetics. J. Physiol., 456: 393404. Kaneko, K., Kawai S., Fuchigami, Y., Shiraishi, G. and Ito, T., (1996) Effect of stimulus intensity and voluntary contraction on corticospinal potentials following transcranial magnetic stimulation. J. Neurol. Sci., 139: 131-136 Mochida, K., Shinomiya, K., Komori, H. and Furuya, K. (1995) A new method of multisegment motor pathway monitoring using muscle potentials after train spinal stimulation. Spine, 20: 2240-2246. Patton, H.D. and Amassian, V.E. (1954) Single and multiple unit analysis of cortical stage of pyramidal tract activation. J. Neurophysiol., 17: 345-363. Rank, J.B., (1975) Which elements are excited in electrical stimulation of mammalian central nervous system: a review. Brain Res., 98:417-440. Rossini, P.M., Baker, A.T., Berardelli, A., Caramia, M.D., Caruso, G., Cracco, R.Q., Dimitrijevic, M.R., Hallet, M., Katayama, Y., Lucking, C.H., Maertens de Noordhout, A.L., Marsden, C.D., Murray. N.M.F, Rothwell, J.C., Swash, M. and Tomberg, C. (1994) Non-invasive electrical and magnetic stimulation of the brain, spinal cord and roots: basic principles and procedures for routine clinical application. Report of an IFCN committee. Electroenceph. Clin. Neurophysiol., 91: 7992. Terao, Y., Ugawa, Y., Sakai K., Uesaka, Y., Kohara, N. and Kanazawa, I., (1994) Transcranial stimulation of the leg area of the motor cortex in human. Acta Neurol. Stand., 89: 378-383.
OF THE
NEUROLOGICAL SCIENCES
ELSEVIER
Journal of Neurological Sciences 147 (1997) 155-159
Effect of coil position and stimulus intensity in transcranial magnetic stimulation on human brain Kazuo Kaneko”, Yasunori Fuchigami, Hideki Morita, Akira Ofuji, Shinya Kawai Department of Orthopedic Surgery, Yamguchi
University Hospital,
1144 Kogushi, Ube City, Yamaguchi, 755, Japan
Received 1 July 1996; revised 30 September 1996; accepted 21 October 1996
Abstract Evoked spinal cord potentials (ESCPs) from the cervical and high thoracic epidural space following transcranial magnetic stimulation were recorded from eight subjects in awake and anesthetized condition. Motor evoked potentials (MEPs) from the right abductor digiti minimi (ADM) and rectus femoris (RF) muscles were simultaneously recorded during voluntary contraction. The stimulus intensity was at 30% above the MEPs threshold of the ADM when the coil center was fixed on lo-20 international Cz position. In awake condition, multiple ESCP components (greater than 3) were recorded from the cervical epidural space but no or minimal components were recorded from the upper thoracic epidural space. When the coil was moved anteriorly so that the posterior edge of the coil was positioned on Cz, the amplitude of the first ESCP component was significantly increased (PcO.02) and shortened (not significant) at cervical levels. In addition, several ESCP components were more evident at high thoracic levels. Although the amplitude of the ADM was not enhanced, that of the RF was enhanced. During general anesthesia with volatile anesthetics (sevoflurane), only the first component of the ESCPs (D-wave) was elicited. Its amplitude was enhanced (P
1. Introduction Single transcranial magnetic or electrical stimulus produces multiple descending potentials in the human pyramidal tracts (Day et al., 1987; Berardelli et al., 1990; Burke et al., 1992, Burke et al., 1993). These potentials are composed of D-waves (due to direct activation of the corticospinal tract neurons) and I-waves (due to indirect or transsynaptic activation of the same neurons) (Patton and Amassian, 1954). In the peripheral nerve-skull model, Amassian et al. (1992) demonstrated that direct activation *Corresponding author. Tel.: t81 836 222268; fax.: 181 836 222267. 0022-510X/97/$17.00 0 1997 Elsevier Science B.V. All rights reserved PII SOO22-510X(96)05324-5
of corticospinal neuron (producing D-wave) occurred when the coil was positioned in a tilted lateral sagittal position. Several papers have been published on evoked spinal cord potentials (ESCPs) following magnetic stimulation of the human motor cortex (Day et al., 1987; Berardelli et al., 1990; Burke et al., 1992; Hicks et al., 1992; Burke et al., 1993) but none about the effect of varying magnetic coil position on corticospinal excitability in human brain. We previously reported on the effect of varying stimulus intensity and voluntary contraction on corticospinal potentials by observing epidurally recorded corticospinal potentials following transcranial magnetic stimulation (Kaneko et al., 1996). In this study we investigated the
K. Kaneko et al. I Journal of Neurological
156
effect of magnetic coil position on the ESCPs following transcranial magnetic stimulation.
2. Materials
and methods
The study was conducted on eight patients (3 female, 5 males, aged 25-68 years old) with thoracic myelopathy (3 patients due to intradural extramedullary schwannoma, 3 patients due to metastatic spinal tumors, 2 patients due to ossification of the yellow ligament). Patients had incomplete paraparesis except for the two patients with intradural extramedullary schwannoma who complained only of unilateral intercostal neuralgia without motor deficit. The experimental procedure was explained to the patients in detail and informed consent for the procedure was obtained. Recording of the ESCPs following transcranial magnetic stimulation was performed before and after induction of general anesthesia. Epidural electrodes were used to record evoked muscle responses following spinal cord stimulation during intraoperative monitoring of spinal cord function (Mochida et al., 1995). They were inserted at the high thoracic level rostra1 to the lesions and advanced cranially to position the highest electrode at mid-cervical level. Epidural catheter electrodes with five recording tips at interelectrode distances of 1.5 cm (Unique Medical Co., Japan, UKG-IOO-5PM) were used in this study. In this investigation, bipolar recordings of ESCPs following transcranial magnetic stimulation were taken from the cervical epidural space in all subjects. The active electrode, with interelectrode distance was 1.5 cm, was placed in a cephalad position. In five subjects, the ESCPs from the high thoracic epidural space (Tl/2 or T2/3) were simultaneously recorded. In awake condition, motor evoked potentials (MEPs) from the right abductor digiti minimi muscle (ADM) were recorded simultaneously with the belly-tendon electrode position. In two patients who complained only of intercostal neuralgia without any long tract signs, the MEPs from the right rectus femoris muscle (RF) were also recorded. In the other six cases, reproducible MEPs were not obtained from RF. The ESCPs and MEPs were amplified, filtered by 20-3 KHz, averaged (n=5-lo), and stored with a standard electromyograph. (Dantec, Denmark, Counterpoint). At least two waves were recorded and superimposed. Multiple ESCP components following transcranial magnetic stimulation were named in their order of increasing latencies and polarities. The negative peak latencies and the peak-topeak amplitudes of each ESCP at the mid-cervical epidural space (C4/5 or C5/6) were measured and the results were expressed as mean2S.D. The conduction velocity of the ESCPs was calculated by measuring the inter-electrode distance and the negative peak latency of the first ESCP component. Transcranial magnetic stimulation was delivered by a
Sciences 147 (1997) 155-159
Novametrix Magstim Model 200 magnetic stimulator using a round 14-cm diameter coil (Magstim, Whitland, UK, Model 200). The center of the coil was fixed on Cz position based on the IO-20 international system. A counterclockwise current in the coil, as viewed from above, was delivered to stimulate the left hemisphere (Rossini et al., 1994). The stimulus intensity was set at 30% above the MEP threshold of the ADM (70-80% of output) with the coil centered on Cz position during voluntary contraction (recording sensitivity of 0.5 mV/D). The ESCPs and MEPs were also recorded when the magnetic coil was moved anteriorly so that posterior coil edge was positioned on Cz using the same stimulus output as previously defined. Recordings of ESCPs following transcranial magnetic stimulation were also taken under general anesthesia with volatile anesthetics (50: 50 nitrous oxide/oxygen mixture and end-tidal sevoflurane concentration >1.5%) at the same stimulus output utilized in the awake condition. Statistical analysis was performed by the Wilcoxon signed-rank tests using the StatView program (Abacus Concepts, Berkeley, CA, USA).
3. Result 3.1. ESCPs and MEPs elicited by two d#‘erent coil position in the awake condition Several ESCP components (greater than 3) were recorded from the cervical epidural space. With the coil center fixed on Cz, the negative peak latency of the first component (Nl) was 3.0t0.2 ms. That of the later components were 4.320.3 ms (N2), 5.920.4 ms (N3), and 7.2-t0.3 ms (N4). The conduction velocity of the first component was 58.Ok9.0 m/s. The amplitudes of each ESCP components were 13.825.9 pY (PI-N]), 13.356.3 ~.LV(P2-N2), 11.924.8 pV (P3-N3), and 14.1?10.0 pV (P4-N4). When the coil edge was positioned on Cz, the Nl latency and amplitude was 2.820.2 ms and 32.5% 15.9 p.V, respectively. The later components were distorted and their amplitudes were 10.527.4 FV (P2-N2), 9.1 k6.8 p.V (P3N3), and 6.8e7.5 pV (P4-N4), respectively. The amplitude of the first component was significantly increased compared to that recorded with the coil center fixed on Cz (PcO.02). In contrast, amplitudes of later components were slightly decreased at the cervical level (Fig. 1). In patients who had ESCPs recorded from both the cervical and high thoracic epidural spaces, several ESCP components at the high thoracic level were more evident when the coil edge was positioned on Cz in the awake condition. The onset latency and amplitude of the MEPs from the ADM were 19.52 1.4 ms and 4.9k2.5 mV, respectively, when the coil center was fixed on Cz. They were 19.02 1.3 ms and 4.422.3 mV, respectively when the coil edge was
K. Kaneko et al. I Journal of Neurological
Sciences 147 (1997) 155-159
157
Magnetic Stimulation 70% 9 Center on c.?
8 7 6
C S/6
5 4 3 2 1 0 Nl
N2
II N3
T l/2 T2l3
N4
Amplitude
1
I I
I
P, NT
P* N?
P3 N3
P4 N4
* P
Fig. I. Comparison of ESCP latency and amplitude in two different magnetic coil position. Negative peak latency and peak-to-peak amplitude of each potential is shown,
fixed on Cz. In the two patients with the MEPs recorded from the RF, although the amplitude of the first ESCP component and the MEP amplitude from the RF was increased, the MEP amplitude from the ADM remained unchanged when the coil edge was fixed on Cz (Fig. 2). 3.2. ESCPs recorded during anesthesia with volatile anesthetics In all subjects, only the first component was routinely evoked with almost similar amplitudes (12.6k5.8 pV) as that in the awake condition. Negative peak latency of the first ESCP component under general anesthesia (3.050.7 ms) was equivalent to that in the awake condition. When the coil edge was positioned on Cz, the amplitude of this first component (28.12 12.4 PV) was significantly larger (PcO.02) than that recorded when the coil center was fixed on Cz. In five patients with ESCPs recorded from the high thoracic epidural space, the amplitude of the first component was also enhanced when the coil edge was fixed on Cz. (Fig. 3). In addition, ESCPs were recorded at 100% stimulus output in two different coil positions in four subjects. The amplitude of the first ESCP component was similar in the
Fig. 2. ESCPs and MEPs following transcranial magnetic stimulation in different coil positions during voluntary contraction of the muscle. When the coil edge was fixed on Cz, several components were recorded at the high thoracic level. Amplitude of the first ESCP component was enhanced (right traces) compared to that recorded when the coil center was fixed on Cz (left traces). Amplitude of MEPs from ADM was similar in both coil position, but that from RF was enhanced when the coil edge was held on CZ.
two different coil positions. Its onset latency was however shortened at 100% stimulus intensity as compared to that recorded at previously determined intensity (Fig. 4).
00 vV’D i :.~: c siti e L
Coil Position
x
18 l&D : 3
dh
w
*
! : :
ID rvu
i/.
.
T 112
1In6 1 Sevafluranc
1.5 f
Fig. 3. ESCPs during general anesthesia with sevoflurane (same patient as the first ESCP component was recordable during anesthesia. When the coil edge was fixed on Cz, the ESCP amplitude was increased at both cervical and high thoracic levels (right traces).
in Fig. 2). Only
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Magnetic stimulation
.
.
Fig. 4. ESCPs during general anesthesia with sevoflurane. At 70% of stimulus output, the ESCP amplitude was increased when the coil edge was fixed on Cz. The ESCP amplitude was the same in both coil position at 100% of stimulus output.
4. Discussion We recorded ESCPs following transcranial magnetic stimulation from the cervical and high thoracic epidural space in both the awake and anesthetized condition. Peak latency of the first component from the mid cervical epidural space was 3.OkO.2 ms at high stimulus intensity and its conduction velocity was about 60 m/s: consistent with that of the descending volley in the corticospinal tract. At high stimulus intensity, the first ESCP component was stable during anesthesia, but later components were easily attenuated. The effect of volatile anesthetics on these responses were consistent with those from prior studies (Hicks et al., 1992; Burke et al., 1993). Although we did not compare the ESCPs following transcranial magnetic stimulation to those following transcranial electrical stimulation, we previously reported that the amplitude of this first ESCP component after test stimulation recovered within 2 ms of interstimulus interval in paired transcranial magnetic stimulation (Kaneko et al., 1996). This implied that the first potential was generated nonsynaptically. From these results, we concluded that the first component was a D-wave (generated by direct activation of cortical motor neuron) and later components were I-waves (attenuated with volatile anesthetics) at the stimulus intensity defined in this study. Burke et al. (1993) demonstrated that transcranial magnetic stimulation produced a D-wave similar to electrical stimulation, although its amplitude was smaller than that following electrical stimulation. We had demonstrated that in awake condition, transcranial magnetic stimulation at threshold stimulus intensity of MEPs from ADM preferentially generated I-waves when the round coil was centered on Cz. Furthermore, amplitude of the D-wave was relatively smaller compared to that of I-waves when the
Sciences 147 (1997) 155-159
coil center was positioned on Cz, even if the stimulus intensity was 20-30% above the threshold of MEPs during voluntary contraction (Kaneko et al., 1996). Hence coil centered on Cz is not optimal in producing D-waves effectively. Amassian et al. (1992) suggested that coil position was a crucial determinant of whether the corticospinal tract was activated directly or indirectly in the experimental peripheral nerve skull model. Rank (1975) showed that an electrical anodal stimulation to cortical motor neuron excited them directly when it flowed nearly parallel to the trajectory of the pyramidal neurons. Magnetic stimulation using a monophasic stimulus pulse with the coil edge on Cz produces an induced current, whose direction is nearly parallel to the trajectory of the pyramidal neurons. This induced current direction is optimal in activating the cortical motor neurons or axons directly. Our study showed that the amplitude of the first ESCP components (D-wave) at cervical level was significantly increased when the coil edge was fixed on Cz in both the awake as well as the anesthetized condition. The MEP amplitude from the RF was increased but this was not so from the ADM when the coil edge was fixed on Cz. This discrepancy was because the cortical motor neurons to the trunk or lower limb muscles were also activated when the coil edge was fixed on Cz. This was consistent with a prior report that the most stable responses obtained from the tibialis anterior muscles were with the round coil centered slightly anterior to the vertex (Terao et al., 1994). When the coil edge was fixed on Cz, multiple ESCPs with enhanced first ESCP components were easily recordable from the high thoracic epidural space. Thus enhancement of D-waves was due to activation of pyramidal cells or tracts projecting not only to the upper limb but also to the trunk and lower limb muscles. We thus hypothesize that corticospinal tracts projecting to the trunk and lower limb muscles can be activated directly when the edge of the round coil is fixed on Cz. In this study we fixed the magnetic stimulus at 30% above the MEP threshold of the ADM (70-80% of output) when the coil was centered on Cz during voluntary contraction. However if the stimulus intensity was strong enough (100% of output), the amplitude of the first ESCP component (D-wave) was not enhanced even when the coil edge was on Cz. The onset latency of the first ESCP component was also shortened at 100% stimulus intensity. This means that high intensity magnetic stimulation can elicit most of the cortical motor neurons or axons directly even those deep inside the brain and the position of the coil is no longer crucial in determining whether the corticospinal tract is activated directly or indirectly. In this study we used the round coil for transcranial magnetic stimulation. The induced current from this coil can spread widely in the motor area and it may stimulate bilateral motor areas. To investigate the effect of induced current direction on corticospinal excitability following transcranial magnetic stimulation, similar study using more
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localized stimulators such as a figure-of-eight coil should be performed. In conclusion, the present study supports the importance of coil position in recording ESCPs following transcranial magnetic stimulation in the human corticospinal system. To obtain large D-waves, the edge of the magnetic coil must be fixed on Cz when using the round coil as the induced current flows parallel to the trajectory of the motor neurons. This position is also optimal for recording Dwaves distributing to truncal and lower limb muscles. However, the coil position is no longer crucial when the magnetic stimulus intensity was strong enough. Clinically, magnetic coil position is a crucial factor when recording corticospinal D-waves in monitoring of spinal cord function during neurosurgery.
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