Clinical Neurophysiology 131 (2020) 2460–2468

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

Visualization of electrical activity in the cervical spinal cord and nerveroots after ulnar nerve stimulation using magnetospinography
Yuki Miyano a, Shigenori Kawabata b,⇑, Miho Akaza c, Kensuke Sekihara b, Yuko Hoshino b, Toru Sasaki d,
Taishi Watanabe a,d, SukChan Kim a, Shinji Sato a, Yuki Mitani a, Yoshiaki Adachi e, Atsushi Okawa daHealthcare Business Group, RICOH Company, Ltd., 2-3-10 Kandasurugadai Chiyoda-ku, Tokyo 101-0062, Japan
Department of Advanced Technology in Medicine, Graduate School of Tokyo Medical and Dental University, 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, Japan
Respiratory and Nervous System Science, Biomedical Laboratory Science, Graduate School of Medical and Dental Sciences, Tokyo Medical and Dental University, 1-5-45 Yushima,
Bunkyo-ku, Tokyo 113-8510, Japand
Department of Orthopaedic Surgery, Tokyo Medical and Dental University,1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8510, Japane
Applied Electronics Laboratory, Kanazawa Institute of Technology, Kanazawa-shi, Ishikawa 920-1331, Japanbca r t i c l e

i n f oArticle history:
Accepted 14 July 2020
Available online 05 August 2020
Keywords:
Magnetoneurography
Magnetospinography
Evoked magnetic field
Somatosensory evoked potential
Ulnar nerve

h i g h l i g h t s
 We successfully obtained magnetospinography (MSG) measurements in spinal cord after ulnar nerve

stimulation.
 Neural currents flow into the intervertebral foramina between C6/7 and T1/2.
 MSG with ulnar nerve stimulation at elbow is effective for lower cervical spinal cord activation.

a b s t r a c t
Objective: To establish a method for magnetospinography (MSG) measurement after ulnar nerve stimulation and to clarify its characteristics.
Methods: Using a 132-channel magnetoneurography system with a superconducting quantum interference device, cervical MSG measurements were obtained for 10 healthy volunteers after stimulation of
the ulnar nerve at the elbow and the wrist, and neural current distribution was calculated and superimposed on the cervical X-ray images.
Results: Neuromagnetic signals were obtained in all participants after applying the stimulus artifact
removal algorithm. The measured magnetic field intensity after elbow stimulation was about twice thatafter wrist stimulation. Calculated neural currents flowed into the intervertebral foramina at C6/7 to T1/2
and propagated cranially along the spinal canal. The conduction velocity from the peak latency of inward
currents at C5-C7 was 73.4 ± 19.6 m/s.
Conclusions: We successfully obtained MSG measurements after ulnar nerve stimulation. The neural currents flowed into the spinal canal from more caudal segments after ulnar nerve stimulation comparedwith median nerve stimulation, and these MSG measurements were effective in examining the spinal
tracts at C5/6/7.
Significance: This is the first report on the use of MSG to visualize electrical activity in the cervical spinal
cord and nerve root after ulnar nerve stimulation.
Ó 2020 International Federation of Clinical Neurophysiology. Published by Elsevier B.V. This is an open
access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Abbreviations: CSP, common-mode subspace projection; DSSP, dual signal
subspace projection; MSG, magnetospinography; SEP, somatosensory evoked
potentials; SQUID, superconducting quantum interference device; UGRENS, unit
gain constraint recursively applied null-steering spatial filtering.
⇑ Corresponding author.
E-mail addresses: yuki.yh.hasegawa@jp.ricoh.com (Y. Miyano), kawabata.
orth@tmd.ac.jp (S. Kawabata), mihonuro@tmd.ac.jp (M. Akaza), k-sekihara@nifty.
com (K. Sekihara), hoshino.atm@tmd.ac.jp (Y. Hoshino), t-sasaki.orth@tmd.ac.jp(T. Sasaki), taishi.watanabe@jp.ricoh.com (T. Watanabe), sukchan.kim@jp.ricoh.com(S. Kim), shinji.s1.satoh@jp.ricoh.com (S. Sato), yuuki.ym.mitani@jp.ricoh.com(Y. Mitani), okawa.orth@tmd.ac.jp (A. Okawa).

1. Introduction
Advances in diagnostic imaging modalities, such as magnetic
resonance imaging (MRI), have led to progress in the morphological diagnosis of cervical cord compression lesions. In the elderly,
due to the possibility of asymptomatic spinal cord compression(Matsumoto et al., 1998; Bednarik et al., 2008; Nagata et al.,https://doi.org/10.1016/j.clinph.2020.07.009
1388-2457/Ó 2020 International Federation of Clinical Neurophysiology. Published by Elsevier B.V.
This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

Y. Miyano et al. / Clinical Neurophysiology 131 (2020) 2460–2468

2014; Nakashima et al., 2015), not only morphological but also
neurofunctional information must be effectively obtained for the
diagnosis of cervical cord disorders.
Conventional electrophysiological studies, such as somatosensory evoked potentials (SEP), are effective for detecting any conduction deficits in the cervical spinal cord, but not for detecting
local conduction blocks. Similarly, needle electromyography can
detect motor neuron anterior horn lesions, but is not suitable for
examining the spinal tracts (white matter). Spinal cord evoked
potentials are useful for detailed functional evaluation of spinal
tracts, but may not be suitable as a preoperative test procedure
due to the need to place recording electrodes in the epidural spaceor other sites close to the spinal cord (Shinomiya et al., 1988; Tani
et al., 2000; Tamaki et al., 2007).
Neuromagnetic recording, which is hardly affected by the conductivity of surrounding tissue, provides higher spatial resolution
compared with conventional electrical potential measurement
and can be used to measure neural activity in the spinal cord andcauda equina, which are located deep from the body surface andsurrounded by the spinal bone tissue (Ishii et al., 2012; Sumiya
et al., 2017; Ushio et al., 2018). Sumiya et al. measured the spinal
cord evoked magnetic field of the cervical spinal cord after median
nerve stimulation and successfully visualized neural activities
flowing through the intervertebral foramina at C4/5-Th1/2 into
the spinal canal and ascending in the spinal canal. However, since
the uppermost nerve roots forming the median nerve are located at

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C5 or C6, it is difficult to diagnose spinal tract disorders at C5/6 orlower levels using magnetospinography (MSG) with median nerve
stimulation. The ulnar nerve, which originates from nerve roots atlower levels, would be theoretically more advantageous in the
diagnosis of spinal cord disorders, but produces only a weak neuralsignal (Mackert et al., 2001). This has made it difficult to evaluateneural activity in the spinal canal with high spatial accuracy afterulnar nerve stimulation.
The aim of this study was to establish a method for MSG measurement using ulnar nerve stimulation and to clarify its characteristics in order to facilitate the diagnosis of spinal cord disorder at
the C5/6 level and below.

2. Methods
2.1. Subjects
This study involved 10 healthy volunteers with no abnormal
neurological findings (10 men; mean [± SD] age, 31.9 ± 6.0 years;
height, 172.6 ± 5.6 cm; weight, 66.8 ± 13.0 kg; and BMI, 22.3 ± 3.4).
This study was approved by the ethics committee of Tokyo
Medical and Dental University (approval No.: M2000-1229) andconducted in accordance with the Declaration of Helsinki. Written
informed consent was obtained from all participants.

Fig. 1. Magnetoneurography system. (a) Measurement procedure. The participant was placed in the supine position with the back of the neck on the sensor area.
Anteroposterior and lateral cervical plain X-rays were taken in the measurement position. (b) Superconducting quantum interference device (SQUID) sensor array. A total of
44 vector-type SQUID sensors are arranged in a 180 mm  130 mm area. (c) Anteroposterior plain X-ray image taken in the measurement position with the vector sensor
positions superimposed on a front-view photograph taken during measurement. (d) Lateral plain X-ray image taken in the measurement position with the sensor array thensuperimposed on a lateral-view photograph taken during measurement. The sensor array is curved to fit the lordosis of the cervical spine.

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2.2. Measurement of evoked magnetic fields and somatosensory
evoked potentials
All measurements were performed in a magnetically shieldedroom using the 132-channel superconducting quantum interference device (SQUID) magnetoneurography system co-developed

by RICOH Company, Ltd., Kanazawa Institute of Technology, andTokyo Medical and Dental University (Adachi et al., 2017). This system is equipped with 44 vector-type SQUID sensors that measuremagnetic fields in three orthogonal directions in an array with anarea of 180 mm  130 mm. The sensor array surface is curved to
fit to the lordosis of the cervical spine (Fig. 1).
Participants were placed in the supine position in a relaxedstate and the C4 to Th2 vertebrae were located on the sensor array.
Anteroposterior and lateral plain X-ray images were taken in themeasurement position to determine the positional relationshipbetween the cervical spine and the sensors.
The right and left ulnar nerves were electrically stimulated
alternatively at the wrist with a stimulation frequency of 3–5 Hz
and duration of 0.3 ms. Stimulus intensity was set to a supramaximal level by measuring SEP (EPi-EPc) at Erb’s point, and SEP was
simultaneously recorded during magnetic field measurement toconfirm that the maximum SEP amplitude was maintained using
an MEB-2312 system (Nihon Kohden Corporation, Japan).
The induced magnetic field was measured over the skin in theback of the neck with a bandpass filter of 100–5000 Hz and sampling rate of 40,000 Hz, and the measurements were averaged until
the signal-to-noise (S/N) ratio was about 5 or higher (4000–8000
times).
The ulnar nerve was stimulated under the same conditions as
those used for magnetic field measurement, and SEP was recorded
from the C5 posterior-anterior surface electrode (C5S-AN) using
the MEB-2312 system with a 10,000-Hz sampling rate and 20–
3000-Hz bandpass filter and taking the average of 1000 responses.
SEP recording was performed twice to confirm reproducibility.
The ulnar nerve was then stimulated at a supramaximal stimulus intensity at the elbow, and the induced magnetic field and SEP
were measured at the neck using the same procedure.
2.3. Signal processing and electrical source estimation

Fig. 2. Stimulation artifact removal by Dual signal subspace projection (DSSP)
processing. (a) Original neuromagnetic fields after elbow stimulation. All waveforms of each sensor are superimposed. Since the stimulation artifacts overlap until
approximately 10 ms after stimulation, the early latency neuromagnetic signals
could not be evaluated. (b) Artifact removed from neuromagnetic fields after elbow
stimulation. Stimulation artifacts were reduced and the neuromagnetic field could
be evaluated from early latency.

Dual signal subspace projection (DSSP) was applied to measured magnetic field data to reduce artifacts due to electrical stimulation (Sekihara et al., 2016). Unit gain constraint recursively
applied null-steering spatial filtering (UGRENS) was then applied
to the magnetic field data after artifact removal in order to calculate the distribution of the neural currents in the neckFig. 3. Waveforms of the magnetic signal after artifact removal from each vector sensor. (a) Positions of the vector sensors superimposed on an X-ray image of the cervicalspine. (b) Three-directional magnetic fields recorded by each vector sensor in response to left ulnar nerve stimulation at the wrist. Black traces are magnetic fields in theventral–dorsal direction (Z axis; dorsal is upward in the graphs). Red traces are magnetic fields in the left–right direction (X axis; right is upward). Green traces are magnetic
fields in the cranio–caudal direction (Y axis, cranial is upward). The lower panel shows the magnetic field waveform in the Y-axis direction of the vector sensor surrounded by
the green dashed square. (c) Three-directional magnetic fields recorded by each vector sensor in response to left ulnar nerve stimulation at the elbow. The lower panel shows
the waveform of the same Y-axis sensor as the one for wrist stimulation. Elbow stimulation produced a neuromagnetic field with an amplitude approximately twice that
produced by wrist stimulation.

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Fig. 4. Time course of neural current distribution in response to left ulnar nerve stimulation. (a) Wrist stimulation. (b) Elbow stimulation. Color indicates current density andwhite arrows show the direction and strength of currents on the XY plane. At first, leading components of the intra-axonal current appeared from the stimulated side andflowed into the intervertebral foramen and ascended along the spinal canal to the cranium ((a) 9.0–9.7 ms (b) 5.5–6.2 ms after stimulation, black asterisk). Subsequently,
trailing intra-axonal currents appeared and propagated along the neural pathway ((a) 10.05–11.8 ms (b) 6.55–8.3 ms, light blue asterisk). Between the leading currents andthe trailing currents, an inward current flowed perpendicular to the spinal canal and propagated cranially along the side of the spinal canal ((a) 10.05–11.1 ms (b) 6.55–
7.95 ms, black star).

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Y. Miyano et al. / Clinical Neurophysiology 131 (2020) 2460–2468(Kumihashi et al., 2010; Sekihara et al., 2015). The region of interest was defined as the plane at the same depth as the vertebral
canal obtained from a cervical lateral X-ray image taken in themeasurement position (the distance in the Z-axis direction fromthe sensor is the same as that of the vertebral canal).
The calculated current distribution was superimposed on the Xray images taken in the measurement position. Virtual electrodes
were set at each vertebral and intervertebral level between C4/5
and Th1/2 to calculate current waveforms at each point. At a signal
level equal to or less than the noise level (S/N ratio  1) was
assigned a value of 0 to currents flowing into the intervertebral
foramina.
To compare the distribution of the current flowing into theintervertebral foramina at C4/5-Th1/2 in the median and ulnar
nerves, we used a dataset for the median nerve from a previous
study (Sumiya et al., 2017). The relative intensity of currents tothe largest current that flowed through the intervertebral level at
the stimulated sides were calculated for each participant, andthose after median nerve stimulation (n = 20) were compared withthose after ulnar nerve stimulation (n = 20) using a t-test with
post-hoc test.
3. Results

64 ± 12.0 fT and 7.5 ± 0.4 ms with elbow stimulation, respectively(Fig. 3).
3.2. Current distribution map
Current distribution maps revealed three current components
with either wrist or elbow stimulation (Fig. 4). The first component
was the leading component of the intra-axonal current, which flowed mainly into the C6/7-Th1/Th2 intervertebral foramina at 10.
2 ± 0.9 ms after wrist stimulation and 6.4 ± 0.4 ms after elbow
stimulation on average, and then ascended in the spinal canal(Fig. 4; black asterisks). The second component was the trailingcomponent of the intra-axonal current, which flowed after theleading component into the intervertebral foramina at 11.6 ± 0.9
ms after wrist stimulation and 7.4 ± 0.5 ms after elbow stimulation
on average, and propagated along the course of nerves (Fig. 4; light
blue asterisks). The third component was inward currents flowing
perpendicularly to the course of nerves between the leading andthe trailing components and propagated cranially on the convex
side of the nerves and outside the spinal canal (Fig. 4; black stars).
The mean latency for the inward currents propagating through the
C5 level was 12.0 ± 0.9 ms after wrist stimulation and 8.0 ± 0.4 ms
after elbow stimulation. The current intensity after elbow stimulation was about twice that after wrist stimulation.

3.1. Magnetic field signals
3.3. Calculated current waveforms at the virtual electrode
Before removal of stimulation artifacts, neuromagnetic fields inearlier latent phases were not observed in 6 of 20 nerves after wrist
stimulation and were not observed in all 20 nerves after elbow
stimulation because electrical stimulation-induced artifacts overlapped with signals until about 10 ms after stimulation (Fig. 2a).
After artifact removal, cervical nerve evoked magnetic fields could
be observed from early latent phases in all cases (20 nerves in 10
participants) (Fig. 2b).
The magnetic field signals showed 2–4 phasic waveforms, similar to those of evoked magnetic fields after median nerve stimulation reported previously (Sumiya et al., 2017). The mean amplitude
and latency of the maximum peak of the Y-axis sensor, which areconsidered to represent the depolarization of spinal nerve fibers,
were 30 ± 7.8 fT and 11.5 ± 0.8 ms with wrist stimulation andIn our previous study using MSG, we noted that the waveforms
from virtual electrodes on the stimulation side (Fig. 5; white asterisks) represented intra-axonal currents of the nerve roots flowing
into the intervertebral foramina while those from the contralateralside (Fig. 5; black asterisks) represented inward currents at the
depolarization site ascending in the spinal canal (Sumiya et al.,2017).
With wrist stimulation, the waveforms of inward currents atthe depolarization site ascending in the spinal canal were obtainedwith good S/N ratios (3 or higher) from Th1/2 up to C5/6 in 18 of 20
nerves (90%), with only 8 of the 20 nerves (40%) providing good S/Nratios up to C4/5. With elbow stimulation, the corresponding
waveforms were obtained with good S/N ratios from Th1/2 up to

Fig. 5. Calculated current waveforms at virtual electrodes. Virtual electrodes were set 20 mm lateral from the midline of the spinal canal. Black waveforms are calculated
currents in response to stimulation of the ulnar nerve at the elbow and gray waveforms are those from stimulation at the wrist. The upward waveform shows the current
flowing toward the midline from the virtual electrode. Waveforms of virtual electrodes (white asterisk) on the ipsilateral side of the stimulation indicate the current flowing
into the intervertebral foramina. Waveforms of virtual electrodes (black asterisk) on the contralateral side of the stimulation indicate the ascending inward currents at the
depolarization site. Neural currents in response to the elbow stimulation (black waveforms) have faster latency, larger amplitude, and a higher S/N ratio than those in
response to wrist stimulation.

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C5/6 in all nerves (100%) and up to C4/5 in 17 of 20 nerves (85%)(Fig. 5). The conduction velocity between the C5 and C7 levels
was 73.4 ± 19.6 m/s, as determined from the peak latency of
inward currents at the depolarization site after elbow stimulation.

The peak latency of SEP corresponding to N11 was largely consistent with that of inward currents calculated from MSG at the C5level (Fig. 6a). Linear single regression analysis showed a high correlation (r = 0.92) (Fig. 6b).

3.4. Comparison with somatosensory evoked potentials

3.5. Individual variations in peak currents flowing into theintervertebral foramina

The peak latency of SEP recorded as the C5 posterior-anteriormontage after ulnar nerve stimulation at the elbow, which corresponds to N11 after median nerve stimulation at the wrist, could
be determined in 17 nerves.

The peak intensity of the trailing intra-axonal current flowing
into the intervertebral foramina at C4/5-Th1/2 was calculated
and plotted for 20 nerves of all 10 healthy volunteers (Fig. 7). After

Fig. 6. Correlation between magnetospinography (MSG) and somatosensory evoked potentials (SEP). (a) Waveforms of calculated currents from MSG and SEP. Lower
waveforms are the calculated inward currents from MSG at the C4-Th1 vertebral level in response to ulnar nerve stimulation at the elbow. The upper wave is SEP recorded by
C5 posterior-anterior montage. Peak latency of SEP (corresponding to N11 in SEP after median nerve stimulation at the wrist) coincided with peak latency (.) of inward
current calculated from MSG at the C5 level. (b) Correlation between peak latency of inward current from MSG and SEP at the C5 level. The peak latency of the calculated
inward current at the C5 level and SEP recorded with C5 posterior-anterior montage matched well across 17 participants (r = 0.92).

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Fig. 7. Spatial distribution of the peak intensity of the trailing intra-axonal current following wrist and elbow stimulation of right and left ulnar nerves in 10 participants. The
intra-axonal current after ulnar nerve stimulation mainly flowed into the C6/7-T1/2 level, and the C7/T1 current was the largest in most participants. The current
distributions after elbow stimulation and wrist stimulation were similar, but the current intensity after elbow stimulation was about twice that after wrist stimulation.

ulnar nerve stimulation, electrical currents flowed mostly into
C6/7-T1/2, with the peak intensity recorded at C7/T1. The meancurrent intensity after wrist stimulation was 0.72 ± 0.31 nAm,
1.70 ± 0.45 nAm, and 0.94 ± 0.34 nAm at C6/7, C7/T1, and T1/2,
respectively, while that after elbow stimulation was 1.25 ± 0.51
nAm, 3.81 ± 0.96 nAm, and 2.18 ± 0.75 nAm, respectively. Foraminal current at C5/6 was present in only 1 of 20 nerves after wrist
stimulation, whereas foraminal current at C4/5 was not observedin any nerve.
The correlation coefficient between the current intensity flowing into the intervertebral foramina after wrist stimulation andthat after elbow stimulation was 0.91 ([Current after elbow stim.
] = 2.03 * [Current after wrist stim.] + 0.076, p < 0.01), indicatinga high level of correlation and a similar pattern of current
distribution.
When comparing the distribution of currents flowing into theintervertebral foramina after ulnar nerve stimulation at the elbow
with that after median nerve stimulation, relative intensity of thecurrent flowing into the C5/6 and C6/7 foramina was significantly
lower after ulnar nerve stimulation (p < 0.001) (Fig. 8).

4. Discussion
4.1. Efficacy of artifact removal method
Before artifact removal, stimulation artifacts overlapped withearly neuromagnetic field signals in 30% of cases after wrist stimulation and in all cases after elbow stimulation, where the site ofstimulation was closer to the recording site, making it difficult toestimate the source of signals. These stimulation artifacts wereadequately removed in all cases using the DSSP method(Sekihara et al., 2016). In a previous study on MSG after median
nerve stimulation reported by Sumiya et al., artifacts were
removed using the common-mode subspace projection (CSP)
method (Sekihara et al., 2017), which requires not only evokedneuromagnetic field data after median nerve stimulation, but also
data for stimulation artifacts alone (Sumiya et al., 2017). The DSSP
method used in the present study does not require data for stimulation artifacts alone, and thus requires a shorter total measurement time and provides a greater advantage for clinicalapplication compared with the CSP method.

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SEP corresponding to N11 recorded as C5 posterior-anterior montage was largely consistent with the peak latency of inward currents calculated from MSG at the C5 level, suggesting that neuralactivity in the posterior column of spinal cord can be measured
with high spatial resolution based on inward currents recorded
by MSG.
4.3. Comparison of wrist stimulation and elbow stimulation

Fig. 8. Comparison of the distribution of the currents flowing into the intervertebral foramina after ulnar nerve stimulation at the elbow and after median nerve
stimulation (Sumiya et al., 2017). The relative intensity of the current flowing into
the C5/6 and C6/7 foramina was significantly lower after ulnar nerve stimulation.

4.2. Characteristic of MSG in response to ulnar nerve stimulation
Current distribution maps revealed three current components,
namely, the leading and trailing components of the intra-axonal
current and inward currents between them, which propagated cranially by flowing through the intervertebral foramina into thespinal canal, after either wrist or elbow stimulation. The conduction velocity between the C5 and C7 levels was 73.4 ± 19.6 m/s,
which was physiologically relevant. This result was consistent withthe value obtained by MSG after median nerve stimulation (73.0 ±15.8 m/s) (Sumiya et al., 2017).
After ulnar nerve stimulation, intra-axonal currents flowed
mainly into the C6/7-T1/2 intervertebral foramina, which is consistent with the anatomical finding that the ulnar nerve contributes
to the C7-T1 nerve roots (Sinha et al., 2016). Anatomically, only
C8/T1 root innervation is thought to contribute to ulnar nerve
stimulation at the wrist, with additional contribution from C7 root
innervation of the flexor carpi ulnaris to elbow stimulation(Standring et al., 2008). Although foraminal current at C6/7 (C7root innervation) was observed in 19 nerves and C5/6 (C6 root
innervation) was observed in 1 nerve after wrist stimulation(Fig. 7), further studies, including animal experiments, are needed
to confirm this finding because the accuracy of signal source estimation by the spatial filtering method may not be sufficient. The
absence of movement in the hand muscles innervated by the median nerve was confirmed with the unaided eye, but the possibilityof co-stimulation of the median nerve during stimulation at thewrist cannot be eliminated.
In sum, the present measurement and signal processing methods enabled visualization of neural activities in the nerve roots
and spinal cord after ulnar nerve stimulation. The peak latency ofMackert et al. (2001) reported conductive magnetic fields in thecervical nerve roots after ulnar nerve stimulation at the wrist, but
the evoked signals were small (10 fT). Elbow stimulation is theoretically advantageous because it involves stimulation of morenerve fibers and is less affected by dispersion due to the shorter
interval from stimulation to recording compared with wrist stimulation. At the same time, because the neuromagnetic fields in
response to stimulation at the elbow have greater overlap withstimulation artifacts, clinical application has been difficult. In thisstudy, the introduction of the artifact removal method could
enable practical use of MSG with elbow stimulation.
The signal intensity of the measured magnetic field with elbow
stimulation was approximately twice that with wrist stimulation,
making it possible to estimate the signal source from data with agood S/N ratio. Current waveforms were acquired with good S/Nratios up to the C4/5 level in 40% with wrist stimulation and 85%
with elbow stimulation, demonstrating the superiority of elbow
stimulation. While electrical currents flowing into the intervertebral foramina also showed a similar distribution pattern between
wrist and elbow stimulation, a 2-fold higher current intensity
was recorded with the latter, suggesting that elbow stimulation
is more suitable for clinical application.
4.4. Comparison with median nerve stimulation: Advantages anddisadvantages
This study showed that the relative intensity of the current
flowing into the C5/6 and C6/7 foramina was significantly higher
after median nerve stimulation than after ulnar nerve stimulation(Fig. 8). This does not contradict previous findings that the roots
contributing to the median nerve are located in more cranial segments (Sinha et al., 2016).
Since the uppermost nerve roots forming the median nerve areat the C5 (C4/5) level, electrical currents ascending along the posterior column of spinal cord and those in the nerve roots are mixed
at C5/6 and lower levels making it difficult to detect abnormalities
in the posterior column of the spinal cord. By comparison, the C7
nerve roots (at C6/7) are the uppermost roots forming the ulnar
nerve, making ulnar nerve stimulation more advantageous for
detecting abnormalities in the posterior column at C5/6/7 or lower
levels.
Taken together, MSG with median nerve stimulation should be
used for the diagnosis of C5 or C6 radiculopathy or abnormalities in
the posterior column at C4/5 or higher levels while MSG with ulnar
nerve stimulation should be used for examining the posterior column at the C5/6/7 levels.
5. Conclusion
Using cervical MSG with ulnar nerve stimulation, we successfully visualized neural activities flowing into the intervertebral
foramina at the C6/7-T1/2 levels and ascending in the spinal canal.
Our data suggest that ulnar nerve stimulation is more effective
than median nerve stimulation for the diagnosis of spinal cord disorders at C5/6/7, because ulnar nerve stimulation results in neuralactivity flowing into lower cervical vertebral levels. Moreover, in2468

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MSG measurements, elbow stimulation produces more intense signals than wrist stimulation and thus is more advantageous for clinical application.
Funding
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Author contributions
Y. Miyano, S. Kawabata, M.A., and A.O. took part in the conception and design of the project; Y. Miyano, S. Kawabata, T.S., T.W., S.
Kim, S.S., Y. Mitani, and Y.A. were involved in its execution; and Y.
Miyano. S. Kawabata., M.A., T.W., K.S. and Y.A. performed analysis
and interpretation of data. All authors have approved the submission of this manuscript.
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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