Clinical Neurophysiology 133 (2022) 39–47

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Clinical Neurophysiology
journal homepage: www.elsevier.com/locate/clinph

Assessment of thoracic spinal cord electrophysiological activity throughmagnetoneurography
Jun Hashimoto a, Shigenori Kawabata a,b,⇑, Toru Sasaki a, Yuko Hoshino b, Kensuke Sekihara b,
Yoshiaki Adachi c, Taishi Watanabe d, Yuki Miyano d, Yuki Mitani d, Shinji Sato d, Sukchan Kim d,
Toshitaka Yoshii a, Atsushi Okawa aaDepartment of Orthopaedic Surgery, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, Japan
Department of Advanced Technology in Medicine, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku,
Tokyo 113-8510, Japanc
Applied Electronics Laboratory, Kanazawa Institute of Technology, 3 Amaike-cho, Kanazawa City, Ishikawa 920-1331, Japand
RICOH Company, Ltd., 1-3-6 Nakamagome, Ohta-ku, Tokyo 143-8555, Japanba r t i c l e

i n f oArticle history:
Accepted 30 September 2021
Available online 5 November 2021
Keywords:
Magnetoneurography
Magnetospinography
Thoracic myelopathy
Spinal cord
Electrophysiological activity
Sciatic nerve stimulation

h i g h l i g h t s
 The biomagnetic field around the current flowing in the thoracic spinal cord was measured by a mag-netoneurograph system.
 Our novel method for synchronized bilateral sciatic nerve stimulation obtained an adequate magnetic

signal for assessment.
 This is the first report to achieve noninvasive and detailed visualization of thoracic electrophysiolog-

ical activity.

a b s t r a c t
Objective: Noninvasive and detailed visualization of electrophysiological activity in the thoracic spinal
cord through magnetoneurography.
Methods: In five healthy volunteers, magnetic fields around current flowing in the thoracic spinal cord
after alternating unilateral and synchronized bilateral sciatic nerve stimulation were measured using amagnetoneurograph system with superconductive quantum interference device biomagnetometers.
The current distribution was obtained from the magnetic data by spatial filtering and visualized by superimposing it on the X-ray image. Conduction velocity was calculated using the peak latency of the current
waveforms.
Results: A sufficiently high magnetic signal intensity and signal-to-noise ratio were obtained in all participants after synchronized bilateral sciatic nerve stimulation. Leading and trailing components along
the spinal canal and inward components flowing into the depolarization site ascended to the upper thoracic spine. Conduction velocity of the inward current in the whole thoracic spine was 42.4 m/s.
Conclusions: Visualization of electrophysiological activity in the thoracic spinal cord was achieved throughmagnetoneurography and a new method for synchronized bilateral sciatic nerve stimulation.
Magnetoneurography is expected to be a useful modality in functional assessment of thoracic myelopathy.
Significance: This is the first report to use magnetoneurography to noninvasively visualize electrophysiological activity in the thoracic spinal cord in detail.
Ó 2021 International Federation of Clinical Neurophysiology. Published by Elsevier B.V. This is an open
access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

Abbreviations: MNG, magnetoneurography; MRI, magnetic resonance imaging; OPLL, ossification of the posterior longitudinal ligament; SCEP, spinal cord evoked
potential; SEP, somatosensory evoked potential; SNR, signal-to-noise ratio; SQUID, superconductive quantum interference device.
⇑ Corresponding author at: Department of Advanced Technology in Medicine, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45
Yushima, Bunkyo-ku, Tokyo 113-8510, Japan.
E-mail addresses: hash.orth@tmd.ac.jp (J. Hashimoto), kawabata.orth@tmd.ac.jp (S. Kawabata), t-sasaki.orth@tmd.ac.jp (T. Sasaki), hoshino.atm@tmd.ac.jp (Y. Hoshino), ksekihara@nifty.com (K. Sekihara), adachi@ael.kanazawa-it.ac.jp (Y. Adachi), taishi.watanabe@jp.ricoh.com (T. Watanabe), yuki.yh.hasegawa@jp.ricoh.com (Y. Miyano), yuuki.
ym.mitani@jp.ricoh.com (Y. Mitani), shinji.s1.satoh@jp.ricoh.com (S. Sato), sukchan.kim@jp.ricoh.com (S. Kim), yoshii.orth@tmd.ac.jp (T. Yoshii), okawa.orth@tmd.ac.jp (A.
Okawa).
https://doi.org/10.1016/j.clinph.2021.09.023
1388-2457/Ó 2021 International Federation of Clinical Neurophysiology. Published by Elsevier B.V.
This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

J. Hashimoto, S. Kawabata, T. Sasaki et al.

Clinical Neurophysiology 133 (2022) 39–47

1. Introduction

2. Materials and methods

Thoracic myelopathy causes severe symptoms, such as backpain, numbness of the lower extremity, gait disturbance, andbowel and bladder dysfunction. Although its surgical treatment iseffective (Aizawa et al., 2007, Matsuyama et al., 2005), reported
risk factors for a poor surgical outcome include a longer preoperative duration of symptoms, worse preoperative symptoms, andossification of the posterior longitudinal ligament (OPLL) (Aizawa
et al., 2007, Onishi et al., 2016). Early and precise diagnosis of thoracic myelopathy is essential, but difficult. For instance, thoracic
myelopathy often occurs simultaneously with cervical myelopathy
and lumbar spinal canal stenosis and can be overlooked (Hsieh
et al., 2014, Shields et al., 2019). Furthermore, OPLL develops at
multiple spinal levels, complicating identification of the responsible lesion.
Diagnosis of thoracic myelopathy requires both morphologicaland functional assessment. Magnetic resonance imaging (MRI) is
useful and widely used for obtaining morphological information,such as cord compression and intracord signal changes. However,
not all cases of thoracic myelopathy have clinical symptoms(Kato et al., 2012, Matsumoto et al., 1998). Physical and neurological examinations as basic functional assessment methods areunable to identify a detailed responsible lesion because there are
no deep tendon reflex and manual muscle tests specific to eachlevel in the thoracic spine, unlike in the cervical and lumbar spine.
Furthermore, comorbid lumbar spinal stenosis often interfereswith the functional assessment due to the similarity of their symptoms (Hsieh et al., 2014). Although electrophysiological testing
including somatosensory evoked potentials (SEPs) is additionallyperformed, the signal is weaker in the spinal cord than in the
peripheral nerves because of its depth from the body surface(Kakigi et al., 1982, Yamada et al., 1982). Detailed measurementof spinal cord evoked potentials (SCEPs) requires epidural electrodes, which are useful but invasive (Shinomiya et al., 1988,
Tani et al., 2000). Therefore, noninvasive and detailed electrophysiological testing is necessary.
We have developed a magnetoneurography (MNG) system thatcan noninvasively assess the neurophysiological activity of the
spinal cord and the peripheral nerves by measuring the magnetic
fields around the neural current. It is based on the principle thatmagnetic fields are barely influenced by the surrounding tissue,
which includes bone, muscle, and cerebrospinal fluid (Trahms
et al., 1989). Highly sensitive magnetic sensors (Adachi et al.,2017) enable us to measure the biomagnetic signals around thespinal cord, which are just 10 9 of those of the geomagnetic field(Wijesinghe, 2010). Moreover, the current distribution is obtained
from the magnetic signals, and the currents, including intra-axonal
currents and inward currents flowing into the depolarization site
(Noble, 1966), are observed with high spatial resolution.
In our previous studies, MNG was used to visualize electrophysiological activity in the spinal cord of animals (Fukuoka et al., 2004,
Fukuoka et al., 2002, Hoshino et al., 2005, Kawabata et al., 2002,
Ohkubo et al., 2003, Sakaki et al., 2020, Tomizawa et al., 2008,
Tomori et al., 2010). Furthermore, the electrophysiological activity
in the cervical spinal cord of healthy volunteers was measured
after peripheral nerve stimulation (Sumiya et al., 2017), whereasthat in the cauda equina was measured after tibial nerve and peroneal nerve stimulation (Ishii et al., 2012, Ushio et al., 2019). However, visualization of thoracic electrophysiological activity was notachieved because the signal obtained by percutaneous stimulationof the peroneal or tibial nerve was too weak. The aim of this study
was thus to noninvasively visualize thoracic electrophysiologicalactivity through MNG by using a novel method, synchronizedbilateral sciatic nerve stimulation.

2.1. Participants
The study protocol was approved by the institutional review
board of Tokyo Medical and Dental University Medical Hospital.
Written informed consent was obtained from all participants. This
study included five healthy volunteers without neurological symptoms or abnormal findings on thoracic and lumbar spinal MRI.
They were all men aged 28–45 years (mean, 34.6 years) with amean body mass index of 20.9 kg/m2.
2.2. MNG system
In a magnetically shielded room, biomagnetic fields were measured with a 132-channel superconductive quantum interference
device (SQUID) biomagnetometer developed with Kanazawa Institute of Technology and RICOH Company, Ltd. (Fig. 1) (Adachi et al.,2017). The biomagnetometer contains 44 cylindrically shaped
SQUID sensors in an area of 130  180 mm (Fig. 2a). Each sensor
measures magnetic fields in three orthogonal directions to obtain
three-dimensional biomagnetic information. The X, Y, and Z directions were set from the left to right, from the caudal to cranial, andfrom the ventral to dorsal of the body in the positive direction,
respectively (Fig. 2b).
2.3. Measurement
Participants were placed in a relaxed supine position with theirthoracic or lumbar back on the sensors (Fig. 3). Frontal and lateral
X-rays obtained the positional information between the body andsensors through marker coils set at the four corners. The bilateral
sciatic nerves were electrically stimulated at the proximal popliteal
fossa (square wave pulse; 5 Hz in frequency; 0.3 ms in duration) by
an MEE system (Nihon Kohden Company, Tokyo, Japan). The cathode and anode of the sealed surface electrodes were placed overthe proximal popliteal fossa and the patellar tendon, respectively.
Supramaximal stimulation (1.2 times as strong as the maximal
compound motor action potentials) was performed while the system monitored the compound muscle action potentials of both theabductor hallucis muscle and extensor digitorum brevis muscle.
Evoked magnetic fields from the lumbar to upper thoracic spine
in response to alternating unilateral and simultaneous bilateral sciatic nerve stimulation were measured by shifting the measurement areas several times under the following conditions:sampling rate, 40 kHz; band-pass filter, 100–5000 Hz; averaging
2000 times in the lumbar area, 4000 times in the lower thoracic
area, and 8000 times in the middle to upper thoracic areas. The
dual signal subspace projection method reduced artifact noise
related to electrical stimulation (Sekihara et al., 2016). The intensity of the signal was defined as the maximum baseline-to-peakamplitude, whereas that of the noise was defined as the root meansquare of the values 0–5 ms before the stimulation. The signal-tonoise ratio (SNR) value was calculated by dividing the maximum
baseline-to-peak amplitude by the noise. The measurement wasconsidered reliable if the SNR value was 3 or more. The magnetic
signal intensity and SNR value were statistically compared after
unilateral (average of left and right) and bilateral sciatic nerve
stimulation by paired t-test after normality was examined by the
Shapiro-Wilk normality test. A P value less than 0.05 was considered statistically significant.
Unit gain constraint recursively applied null-steering spatial filtering obtained the current temporal distribution from the magnetic data (Kumihashi and Sekihara, 2010, Sekihara andNagarajan, 2015). The current distribution at the depth of the40

Clinical Neurophysiology 133 (2022) 39–47

J. Hashimoto, S. Kawabata, T. Sasaki et al.

Fig. 1. Appearance of the magnetoneurography system in a magnetically shielded room. A customized bed was placed in the center of the room, and a smaller box withSQUID sensors (a) was set on the same plane as that of the bed. The dotted square indicates the sensor area. The box with sensors protruded from a cryostat box (b), which
refrigerated the sensors with liquefied helium to maintain superconducting conditions. Two irradiating devices were set to check the positional relationship between thesensors and the participant’s measurement area from the frontal (c) and lateral (d) views. SQUID, superconductive quantum interference device.

(a)

(b)

25

23

22

180
20 22

(mm)
23

25

22

68 mm

r = 200

15.5 mm

22

X coil
Y coilZ coil

22 130
22
22
y
z

x

Side viewy

Top viewzx

SQUID sensors

Fig. 2. An array of SQUID sensors. A total of 44 SQUID sensors are arranged in a 180 mm  130 mm area along a rounded surface (a) in the box shown in Fig. 1(a). Each sensor(b) measured three orthogonal directional magnetic fields via X, Y, and Z coils. SQUID, superconductive quantum interference device.

alternating bilateral sciatic nerve stimulation. Second, we calculated each peak latency of the inward currents reaching the centerof the L3 vertebra, where the caudal equina, including the sciatic
nerve component, is found in the spinal canal. Third, the timingof the stimulation was shifted by the difference in peak latency
so that the bilateral current reached the L3 vertebra at the sametime.

spinal canal was visualized by its superimposition on the frontal Xray. Moreover, the current waveforms flowing in the spinal canalwere obtained using a ‘‘virtual electrode”, which can be placed
anywhere to obtain the current waveform. The conduction velocities were calculated from the peak latencies and the distanceobtained by the X-rays.

2.4. Novel stimulation method
3. Results
We developed a method for synchronized bilateral sciatic nerve
stimulation to obtain much stronger currents (Fig. 4). First, the current distribution of the lumbar spinal area was measured after

We measured the evoked magnetic fields of the lumbar andthoracic spinal area in response to alternating unilateral and syn41

J. Hashimoto, S. Kawabata, T. Sasaki et al.

Clinical Neurophysiology 133 (2022) 39–47

Fig. 3. Lateral view of the sensors and subject. The subject lay on the bed in a relaxed supine position and placed his back on the sensors. The bilateral sciatic nerves were
stimulated at the proximal popliteal fossa.

Left sciatic nerve stimulation

Synchronized bilateral sciatic nerve stimulation

Right sciatic nerve stimulation

L2

L2

L2

11.250 ms
11.250 ms

11.450 ms
L3

L3

L3

5 nAm
L4

3 ms

L4

11.450 ms

0.200 ms

Right

11.250 ms

shift the timing of stimulation

L4

Stimulation

Right
Left

5 nAm

L3

3 ms

Stimulation

L3

Left
Stimulation

L3

Fig. 4. Synchronized bilateral sciatic nerve stimulation. The peak latencies of the inward currents at the center of the L3 vertebra were 11.250 and 11.450 ms after left andright sciatic nerve stimulation, respectively. The inward currents were adjusted so that they reached the L3 vertebra at the same time by shifting the timing of the stimulationby the difference in the peak latency (0.200 ms).

bilateral sciatic nerve stimulation, the left and right stimulation
timing was shifted by 0.1 or 0.2 ms for each participant. The datafrom cases 2 and 3 were not considered reliable because the SNRvalues were less than 3 in the measurement of the upper thoracic
spinal area after unilateral sciatic nerve stimulation.
The magnetic waveforms at the mid-thoracic spinal area after
bilateral sciatic nerve stimulation in a representative 35-year-old
man are shown in Fig. 5. The X-directional waveforms increasedin peak latency at more cranial areas. In other words, they traveledto the cranial area along the thoracic spine. The Y- and Zdirectional waveforms had opposite polarities on the bilateral sides
to the spinal column and traveled to the cranial area bilaterally 30–
60 mm away from the spine.
The evoked current distribution in the lumbar and thoracic
spinal areas after bilateral sciatic nerve stimulation was visualized
as a pseudo-color map including the intensity and vector of thechronized bilateral sciatic nerve stimulation in all participants.
Table 1 shows the magnetic signal intensity and SNR value in thecaudal direction at the L2, T10, T6, and T2 vertebra levels along
the spinal column for the X-coils after left, right, and bilateral stimulation, reflecting the magnetic field intensity around the trailingcomponent of intra-axonal current. Both the magnetic signal intensity and SNR value in each participant decreased at more cranialareas due to temporal dispersion after unilateral and bilateral sciatic nerve stimulation. Synchronized bilateral sciatic nerve stimulation resulted in a significantly higher magnetic signal intensity
and SNR value in the lumbar, lower thoracic, and middle thoracic
spinal area than unilateral stimulation (paired t-test, all P values < 0.05). In most measurements, the magnetic signal intensity
after bilateral sciatic nerve stimulation was almost the same as
the sum of those after left and right sciatic nerve stimulation, butdiffered in some measurements at cranial region. In synchronized42

Clinical Neurophysiology 133 (2022) 39–47

T1

T1

T1

T1

T1

13.0 (5.4)

14.0 (5.3)

13.1 (5.7)

14.8 (5.1)

11.0 (5.2)

Bil. Stim.
Uni. Stim.

T5
T5
T5
T8
T6
T6
T5
T7
T5
T7
12.2 (5.7)

21.9 (8.3)

18.5 (7.7)

23.0 (7.8)

28.5 (9.4)

4.9 (1.9)
5.9 (3.8)––––
7.5 (3.0)
4.5 (1.6)
8.5 (4.0)
7.1 (3.4)
6.4 (2.5)
18.9 (8.9)

Uni. Stim.
Bil. Stim.

20.6 (7.7)

T2

Bil. Stim.

current and was superimposed on the frontal X-ray (Fig. 6). Threekinds of current components propagated as a group from the lumbar region to the upper thoracic spine. First, the leading current
components with a cranial vector flowed along the spine. Second,
the inward current components directing orthogonally to thespinal canal flowed bilaterally 30–60 mm lateral to the spine.
Finally, the trailing current components with a caudal vector followed them along the spine. The inward currents reached the L3level 10.5 ms after bilateral sciatic nerve stimulation, and theirgrouped currents traveled to the cranial direction over time. The
currents could be seen in the upper thoracic spinal area, although
the current intensity decreased at the more cranial area due totemporal dispersion. A movie detailing the current distribution isshown in Video 1. A group of currents propagated to the lower thoracic spine and seemed to disappear at 11 ms and reappear. Then,the currents flowed to the upper thoracic spine.Video 1.

These current components were also presented as the current
waveforms obtained by ‘‘virtual electrodes”. The leading and trailing intra-axonal components were confirmed as the upward anddownward traveling currents, respectively in Fig. 7a-c, and theinward components were confirmed as the upward traveling currents in Fig. 7d-f. Their current waveforms gradually increased inpeak latency and decreased in amplitude at more cranial areas.
The waveforms after synchronized bilateral sciatic nerve stimulation were close to the combined waveforms after right and left
stimulation, except in the thoracolumbar region where the waveforms were complicated. Consequently, the currents conductedto more cranial areas after bilateral sciatic nerve stimulation thanthose after unilateral stimulation. Table 1 shows how far the
inward currents conducted to the cranial area with a SNR exceeding 3 in each participant. Although the inward currents after unilateral sciatic nerve stimulation conducted only to the middle
thoracic area, those after bilateral stimulation conducted to T1 in
all participants.
Table 2 shows the peak latency and the conduction velocity of
the inward currents in the lumbar and thoracic spinal area after
bilateral sciatic nerve stimulation in each participant. The conduction velocity of the inward current in the whole thoracic spine after
bilateral sciatic nerve stimulation was 42.4 ± 3.5 m/s, which was
calculated by dividing the distance from the T12 to T1 vertebrae
on X-ray by the peak latency difference of the inward current.
Inversely, the conduction velocity in the lumbar spine was 82.7 ±6.1 m/s.

Uni. Stim.

35.9 (13.2)
172 (24.9)

191 (27.8)

166 (21.1)

155 (26.8)

82.3 (16.0)
62.3 (18.1)
87.4 (13.7)
98.5 (12.5)
88.0 (19.6)
88.6 (19.1)
78.4 (11.3)
94.1 (16.3)
82.8 (10.6)
106 (12.0)
86.8 (14.9)
20.9
61
171

20.7
55
163
33

34.6

5

mean

male

23.3
78
183
32
4

male

22.6
60
163
45
3

male

28
2

male

176

57

18.4

Left
Right
Left
Right
Left
Right
Left
Right
Left
Right
19.6
56
169
male
35
1

BMI, body mass index; Uni. Stim., Unilateral sciatic nerve stimulation; Bil. Stim., Bilateral sciatic nerve stimulation.

38.4 (15.4)

34.5 (10.7)

37.3 (12.4)

31.3 (11.5)

8.2 (4.4)
9.0 (5.0)
7.0 (3.2)
7.4 (3.2)
16.4 (6.5)
12.7 (4.8)
8.8 (4.0)
9.0 (5.1)
10.3 (4.2)
7.9 (3.8)
9.7 (4.4)
198 (23.5)

Bil. Stim.

38.1 (16.1)

24.3 (9.2)
14.8 (5.5)
20.2 (8.0)
15.0 (4.4)
18.3 (6.2)
21.4 (7.1)
16.5 (6.0)
17.1 (5.7)
17.8 (5.7)
19.3 (7.0)
18.5 (6.5)

Uni. Stim.
Bil. Stim.

148 (25.1)

Uni. Stim.

T6
T10

Magnetic signal, fT (Signal-to-noise ratio)

L2
BMI,
kg/m2
Body
weight, kg
Body
height, cm
Sex
Age,
years
Case

Table 1
Participants’ demographic characteristics, magnetic signal intensity, signal-to-noise ratio, and how far the current conducted after unilateral and bilateral sciatic nerve stimulation by magnetoneurography.

How far the current
conducted

J. Hashimoto, S. Kawabata, T. Sasaki et al.

4. Discussion
Here, we successfully visualized the electrophysiological activity of the thoracic spinal cord with MNG. SEPs from the body surface cannot be evaluated in detail and need a high skill level tominimize noise (Cracco, 1973, Kakigi et al., 1982, Yamada et al.,1982). On the other hand, epidural SCEPs obtain detailed information but are invasive and difficult to perform (Jones et al., 1982,
Macon and Poletti, 1982). As a result, these methods are not widespread. To the best of our knowledge, we are the first to conduct
noninvasive and detailed functional assessment of the thoracic
spinal cord. This was possible because our novel method for synchronized bilateral sciatic nerve stimulation obtained a sufficiently
high magnetic signal intensity and SNR value. In our previous
study, the magnetic signal intensity of the lumbar spinal area after
unilateral peroneal nerve stimulation had a peak-to-peak amplitude of 60 fT (Ushio et al., 2019). In the present study, however,
the magnetic signal intensity after synchronized bilateral sciatic43

J. Hashimoto, S. Kawabata, T. Sasaki et al.

Clinical Neurophysiology 133 (2022) 39–47

y

T5

x

z

T10

Rt

Fig. 5. Magnetic fields on each sensor and X-ray image. The magnetic fields measured using 44 sensors are represented as time on the horizontal axis and magnetic signal
intensity on the vertical axis and are superimposed on the frontal X-ray of the mid-thoracic spinal area. Moreover, three directional magnetic fields (X, Y and Z axes) aresuperimposed on each sensor. The X, Y, and Z directions are set positive from the left to right, from the caudal to cranial, and from the dorsal to ventral of the body,respectively.

T1

T7

T12
10 nAm

2 nAm

1.2 nAm

0.6 nAm

0

0

0

0

L4

Fig. 6. Current distribution after synchronized bilateral sciatic nerve stimulation in a representative case of a 35-year-old male. The current distribution is superimposed on
the frontal X-ray image and arranged from the lumbar to upper thoracic spinal area along the time course. White arrows indicate the direction of the current at each point,
and the color indicates the intensity: red is strong and blue is weak. The leading component flowed into the L1, T10, T5, and C7 levels at 10.500, 12.600, 15.225, and 17.175 ms
after stimulation, respectively. Similarly, the inward components, which are bilaterally perpendicular to the spinal canal, and the trailing components with a caudal vector
follow the leading component. The leading, inward, and trailing components flow to the upper thoracic spine as one group. In this figure, the current intensity becomes
smaller at more cranial areas due to temporal dispersion, and the color scale is changed to improve its visualization.

than the peroneal head during peroneal nerve stimulation. The
stimulus point was shifted proximally, reducing temporal dispersion, in which currents gradually decay with conduction. Finally,
and most importantly, our novel approach to synchronized bilateral sciatic nerve stimulation succeeded in obtaining a muchhigher signal intensity. Inward currents with sufficient SNR value
conducted only to the middle thoracic spinal area after unilateral
sciatic nerve stimulation but through the whole thoracic spinal

nerve stimulation was much higher, 172 fT, even though it was
expressed as baseline-to-peak amplitude which is approximately
half of peak-to-peak amplitude.
There are three possible reasons why a much higher signal
intensity and SNR value were obtained. First, stimulation of the sciatic nerve including not only the peroneal, but also the tibial nerve
branch, involved more nerve fibers. Second, we stimulated the sciatic nerve at the proximal popliteal fossa where it is more proximal
44

Clinical Neurophysiology 133 (2022) 39–47

J. Hashimoto, S. Kawabata, T. Sasaki et al.
(a) Intra-axonal currents (right sciatic nerve stimulation)(b) Intra-axonal currents (left sciatic nerve stimulation)(c) Intra-axonal currents (synchronized bilateral sciatic nerve stimulation)

T1

T1

T1

T2

T2

T2

T3

T3

T3

T4

T4

T4

T5

T5

T5

T6

T6

T6

T7

T7

T7

T8

T8

T8

T9

T9

T9

T10

T10

T10

T11

T11

T11

T12

T12

T12

L1

L1
10 nAm

L2

3 ms

L3

L1
10 nAm

L2

3 ms

L3

10 nAm

L2

3 ms

L3

(d) Left inward currents (right sciatic nerve stimulation)(e) Left inward currents (left sciatic nerve stimulation)(f) Left inward currents (synchronized bilateral sciatic nerve stimulation)

T1

T1

T1

T2

T2

T2

T3

T3

T3

T4

T4

T4

T5

T5

T5

T6

T6

T6

T7

T7

T7

T8

T8

T8

T9

T9

T9

T10

T10

T10

T11

T11

T11

T12

T12

T12

L1

L1

L1
4 nAm

4 nAm

4 nAm

L2

L2
3 ms

L3

L2
3 ms

L3

3 ms

L3

Fig. 7. Current waveforms in the thoracic and lumbar spine after unilateral and bilateral sciatic nerve stimulation. The current waveforms in (a), (b), and (c) are obtained fromthe virtual electrodes set on the center of each vertebra from L3 to T1 after right, left, and bilateral sciatic nerve stimulation, respectively. The upward direction of the
waveform is the cranial direction. The leading and trailing intra-axonal components are confirmed as the positive peak at 10 ms and the negative peak at 11.5 ms at the L3level, respectively. Their current waveforms gradually increase in peak latency in more cranial areas and travel from the lumbar to thoracic spinal area. In (d), (e), and (f), thecurrent waveforms for the inward components are obtained from virtual electrodes set 35 mm left from the center of each vertebra after right, left, and bilateral sciatic nerve
stimulation, respectively. The upward direction of the waveforms is the direction perpendicular to the spinal canal. The inward components are observed as the positive peakat 10.5 ms at the L3 level. Waves traveling from the lumbar to thoracic spine are observed.

Table 2
Participants’ functional characteristics measured by magnetoneurography.
Case

1
2
3
4
5
Mean

Peak latency, ms

Conduction velocity, m/s

L3

T12

T7

T1

L3-L1

T12-T10

T7-T3

T12-T1

10.43
11.25
10.35
11.39
10.13
10.71

12.46
12.83
12.33
12.99
11.68
12.46

14.93
16.94
14.85
15.91
14.63
15.45

18.30
18.90
18.34
18.94
17.76
18.45

83.9
80.0
75.2
82.5
91.9
82.7

40.0
30.0
33.5
37.0
34.1
34.9

44.9
49.7
48.1
50.3
41.7
46.9

44.9
38.0
41.6
46.9
40.7
42.4

cord because the points used to stimulate both the peroneal andtibial branches with supramaximal intensity often differ between
the left and right sides. Consequently, the magnetic signal intensi-

area after synchronized bilateral sciatic nerve stimulation. The
stimulation timing was shifted by 0.1 or 0.2 ms in every participant
to match the timing of the bilateral current entries into the spinal45

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Clinical Neurophysiology 133 (2022) 39–47

the T10-12 spinal area (Table 2). In addition, detailed visualizationof the current distribution by MNG showed that the ascending currents seemed to disappear and appear again at the lower thoracic
spine (Video 1). One possible reason is that ascending currents
may cancel each other out due to complex branching and synapsing when they enter the spinal cord. In addition, MNG calculated
evoked currents from the magnetic signals, not actual currents,and magnetic signals with opposite vectors cancel each other out
and make it seem that there is no current. Another possible reason
is that MNG may be unable to detect the magnetic fields risingfrom the current flowing from the dorsal to the ventral direction
because MNG measures from the dorsal direction. Our next stepis to investigate the electrophysiological activity of the lower thoracic spine.
This study has several limitations. First, a small number of participants were analyzed. Second, relatively young volunteers wereenrolled, and further study of elderly individuals, who are more
likely to have thoracic myelopathy and similar conditions, isneeded. Measurement in a more diverse and larger population willallow us to determine the normal range of the conduction velocity
according to age and permit accurate assessment of spinal cord
function. Third, the electrophysiological activity in the conus
medullaris is not yet understood. This will be our next research
topic.
In conclusion, MNG permitted visualization of the electrophysiological activity in the thoracic spinal cord via a novel method forsynchronized bilateral sciatic nerve stimulation. MNG is expected
to be a useful modality for the functional assessment of thoracic
myelopathy.

ties after synchronized bilateral sciatic nerve stimulation obtained
almost the same as the sum of those after left and right stimulationin the lumbar and lower thoracic region. However, some measurements in the middle thoracic region did not show similar results
because the interactive effect of the facilitation or inhibition
between the currents after left and right stimulation could not be
eliminated due to the increased variability by temporal dispersion.
In addition, the inward currents in the thoracolumbar region after
bilateral stimulation were different from the combined current
after left and right stimulation because the neural activity may
be complicated where the caudal nerve enters the spinal cord.
Traveling current waveforms in the lumbar and thoracic spine
were observed after synchronized bilateral sciatic nerve stimulation and, interestingly, the conduction velocities in the thoracic
and lumbar spine were very different at 42.4 and 82.7 m/s, respectively. This result is similar to that of a previous SEP study (Cracco,1973) and indicates that the mainly observed components weredifferent between the lumbar and thoracic spine. The faster wave
in the lumbar spine may be due to retrograde conduction in the
motor nerve or conduction through group Ia muscle afferent fibers
because more motor nerves were stimulated by supramaximal
stimulation in compound motor action potentials. Moreover,because the faster wave stopped propagating at the lower thoracic
spine, a component represented as F wave or H wave may beobserved.
An epidural SCEP study during scoliosis surgery revealed thatseveral currents with different speeds propagated in the thoracic
spine (Jones et al., 1982); the faster current ascends in the
spinocerebellar tract from the peripheral nerves through group Ia
afferent muscle fibers while the slower current ascends in the dorsal column. On the other hand, SEPs from the body surface arereported to be unable to clearly separate their two components(Cracco, 1973). The slower wave propagating in the thoracic spinein this study is probably derived from components ascending in
the dorsal column, although we cannot exclude the possibility thatseveral components were mixed. Regarding conduction velocity,spinal SEPs measured from the body surface after peripheral nerve
stimulation showed that the ascending current propagated atabout 50–70 m/s in the thoracic spine (Cracco, 1973, Desmedt
and Cheron, 1983, el-Negamy and Sedgwick, 1978, Jones et al.,
1982, Kakigi et al., 1982, Schiff et al., 1984, Yamada et al., 1982),
which is faster than in the present study. This dissociation may
arise from how distances and latencies are measured. The distanceof the spinal cord was measured on the body surface in previous
studies, and it was possibly overestimated because of the spinal
curvature (thoracic kyphosis) (Desmedt and Cheron, 1983). In
other words, the actual conduction velocity may be slower. However, in this study, a more accurate distance was obtained throughfrontal and lateral X-rays that included spinal curvature information. Moreover, we adopted peak latency, related to the mostnumerous components, not onset latency, used by most previous
studies and related to the fastest components. Therefore, the conduction velocity in this study may be slower.
Conduction velocity was clearly altered in the lower thoracic
spine. The possible reason is that complex branching and synaptictransfer occurs at the entry zone of the spinal cord. In previous
studies of SEPs from the body surface, the amplitude was highest
there because pre- and postsynaptic fibers concentrate at theconus medullaris (Cracco, 1973, Desmedt and Cheron, 1983,
Kakigi et al., 1982, Maccabee et al., 1983), with epidural SEPs
revealing that the conduction velocity decreased to about 30 m/s
due to synapsing (Jones et al., 1982, Lloyd and McIntyre, 1950,
Macon and Poletti, 1982). In the present study, the current waveforms, presented as a representative case in Fig. 7c, f, also showedthat the current amplitude was the highest in the upper lumbar
region and that the mean conduction velocity was 34.9 m/s inFunding
This research was supported by RICOH Company. The funding
body played no role in study design, data collection and analysis,
preparation of the manuscript, or the decision to publish.
Declaration of Competing Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared
to influence the work reported in this paper.
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