Clinical Neurophysiology 123 (2012) 1656–1661

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

Conductive neuromagnetic ﬁelds in the lumbar spinal canal
Senichi Ishii a, Shigenori Kawabata a,⇑, Shoji Tomizawa a, Masaki Tomori a, Kyohei Sakaki a,
Kenichi Shinomiya a, Kensuke Sekihara b, Tomoya Sato b, Yoshiaki Adachi c, Atsushi Okawa aaDepartment of Frontier Surgical Therapeutics, Section of Orthopedic and Spinal Surgery, Division of Advanced Therapeutical Sciences,
Graduate School of Tokyo Medical and Dental University, Tokyo, Japanb
Department of Systems Design and Engineering, Tokyo Metropolitan University, Hino, Tokyo, Japanc
Applied Electronics Laboratory, Kanazawa Institute of Technology, Kanazawa, Shikawa, Japana r t i c l e

i n f oArticle history:
Accepted 23 December 2011
Available online 27 January 2012
Keywords:
Neuromagnetic ﬁeld
Lumbar spine
Cauda equina

h i g h l i g h t s
 We used a superconducting quantum interference device ﬂuxmeter developed for use with the spine tomeasure propagating neuromagnetic ﬁelds at the surface of the lower back after stimulation of tibial
nerves at the ankle.
 We simultaneously measured cauda equina action potentials with an epidural catheter-type electrodeto validate the accuracy of the neuromagnetic ﬁeld measurements.
 This method provides a noninvasive functional examination tool for lumbar spine disease.

a b s t r a c t
Objective: To measure neuromagnetic evoked ﬁelds in the lumbar spinal canal.
Methods: Using a newly developed superconducting quantum interference device (SQUID) ﬂuxmeter,
neuromagnetic ﬁelds of 5 healthy male volunteers were measured at the surface of the lower back after
stimulation of the tibial nerves at the ankles. For validation, we inserted a catheter-type electrode percutaneously in the lumbar epidural space in 2 of the subjects and measured cauda equina action potentials
after tibial nerve stimulation.
Results: Neuromagnetic ﬁelds propagating from the intervertebral foramina into the spinal canal were
measured, and the latencies of the magnetic ﬁelds corresponded largely with those of the cauda equinaaction potentials.
Conclusions: We successfully measured ascending neuromagnetic ﬁelds originating at the nerve root andthe cauda equina with high spatial resolution. Future studies will determine whether neuromagnetic ﬁeld
measurement of the lumbar spine can be a useful diagnostic method for the identiﬁcation of the disordered site in spinal nerves.
Signiﬁcance: We successfully measured neuromagnetic ﬁelds in the lumbar spinal canal, which have previously been difﬁcult to verify. Future studies will determine whether neuromagnetic ﬁeld measurementof the lumbar spine can be a useful diagnostic method for identifying disorders of spinal nerves.
Ó 2011 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights
reserved.

1. Introduction
Among patients with lumbar spine disease, such as lumbar
spinal canal stenosis, many show compression of the cauda equina
at multiple levels in morphologic images. In addition, the nerve
root often appears to be compressed not only inside the spinal canal but also in the intervertebral foramen or extraforaminally. It isdifﬁcult to diagnose nerve lesions in such patients with the use of⇑ Corresponding author. Address: 1-5-45 Yushima, Bunkyo-ku, Tokyo 113-8519,
Japan. Tel.: +81 3 5803 5279; fax: +81 3 5803 5281.
E-mail address: kawabata.orth@tmd.ac.jp (S. Kawabata).

imaging methods alone. Therefore, a method for the evaluation of
nerve function with high spatial resolution would be helpful. Taniguchi and colleagues measured cauda equina action potentials(CEAPs) after stimulation of the tibial or peroneal nerve with a needle electrode inserted into yellow ligament and reported that diagnosis of lesions is possible (Taniguchi et al., 2005). However, thisinvasive procedure can only be performed under general anesthesia. Therefore, the development of a noninvasive method isdesirable.
There are reports evaluating action potentials of the cauda equina and spinal cord from outside of the body (Cracco, 1973; Smalland Matthews, 1984; Eisen, 1986), but detailed diagnosis of spinal

1388-2457/$36.00 Ó 2011 International Federation of Clinical Neurophysiology. Published by Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.clinph.2011.12.014

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lesions remains difﬁcult. It is thought that this is because spinal
nerves are situated deep from the body surface and are surroundedby the osseous tissue of the spine. Magnetic ﬁelds resulting fromelectrical nerve activity are not affected by surrounding tissues.
Neuromagnetic recording has theoretically greater spatial resolution than electrical recording (Trahms et al., 1989; Hashimoto
et al., 1991, 1994; Fukuoka et al., 2002, 2004; Kawabata et al.,2002). Tomori et al. (2010) used neuromagnetic recording at the
body surface in animals to diagnose spinal cord lesions. In addition,
conduction delay and conduction block have been visualized in human cervical spine (Adachi et al., 2008; Sato et al., 2009); therefore,
progress is being made in the diagnosis of cervical spinal lesions.
In the lumbar spine, recording of conductive evoked magnetic
ﬁelds at the body surface after stimulation of the tibial nerve has
been reported (Curio et al., 1995; Mackert et al., 1997, 2001a,b).
Mackert et al. (1998) also reported that the propagating ﬁeld signal
disappears around the intervertebral foramen in patients with S1
radiculopathy, thereby showing the potential clinical applicationof magnetic ﬁeld measurement in the lumbar spine. However, clear
magnetic ﬁeld waveforms were observed only up to the intervertebral foramen in these studies. Klein et al. (2006) reported that they
could detect a propagating signal along the sciatic nerve andplexus lumbosacralis up to around the intervertebral foramen of
L5, and they could also detect a stationary signal in the upper partof the lumbar region. However, the signals ascending along the
spinal canal could not be observed clearly, that is, activity of thecauda equina could not be detected. Therefore, further improvements are necessary for the clinical application of nerve magnetic
ﬁeld measurement in the lumbar spine.
The aim of the present study was to measure neuromagnetic
ﬁelds at the surface of the lower back after peripheral nerve stimulation of the lower extremity in healthy subjects with the use of asupine position-type superconducting quantum interference device (SQUID) ﬂuxmeter developed for use with the spine. We also
aimed to show that cauda equina action magnetic ﬁelds (CEAFs)
can be recorded in detail at the body surface and that detailed analysis at the level of clinical application is possible in the lumbar
spine.

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500 Hz–5 kHz was applied to the SQUID signals. A total of 4000–
6000 responses were recorded at a sampling rate of 40 kHz andaveraged separately for left and right nerve stimulation.
We used a unit gain normalized minimum-norm (UGMN) ﬁlter
method to estimate the current source. This is a spatial ﬁltering
technique used to reconstruct the current source (Sekihara et al.,2005; Sekihara and Nagarajan, 2008). With this method, we extracted data for the depth of the nerve pathway from the lateral
X-ray image and set reconstruction points on the pathway. Withthe use of the magnetic ﬁeld data from all measurement points,
we can reconstruct the direction and intensity of the current
source on each reconstruction point and can visualize the conductive direction, distribution, and temporal change of the current
source. This method is suitable for the reconstruction of the signal
source with length and extension. This is in comparison to the conventional equivalent dipole method, which reconstructs the signal
to just 1–2 points. The propagation pathway of the estimated electrical currents was superimposed on lumbar spine X-rays.
2.2. Measurement of SEPs
For comparison, somatosensory evoked potentials (SEPs) in response to tibial nerve stimulation were recorded simultaneouslywith the use of surface electrodes placed over the T12, L3, and L5
spinous processes, ischial tuberocity, and popliteal fossa. A reference electrode was placed on the contralateral anterior superior
iliac spine. A band-pass ﬁlter of 100 or 500 Hz–5 kHz was applied
to the signals, and 2000 responses were recorded and averaged.
2.3. Measurement of CEAPs
Cauda equina action potentials were also recorded after tibial
nerve stimulation in 2 subjects (subjects 4 and 5) with the use ofa catheter electrode (Unique Medical Co., Tokyo, Japan) placed in
the epidural space at the lumbar level. The distance between eachrecording point was 15 mm. A reference electrode was placed on
the contralateral anterior superior iliac spine. Signals were ﬁlteredwith a 100 Hz or 500 Hz–5 kHz band-pass ﬁlter, and 2000 responses were recorded and averaged.

2. Materials and methods
3. Results
2.1. Measurement of CEAFs
3.1. Measurement of CEAFs after stimulation of the tibial nerve
The study protocol was approved by the Ethics Committee ofTokyo Medical and Dental University. Inside a magneticallyshielded room, 5 volunteer male subjects, 21–32 years of age (mean25.4 years), 163–189 cm in height (mean 171 cm), 54–76 kg in
weight (mean 63.4 kg), without any neurologic deﬁcit, were placedin a relaxed supine position (Fig. 1C). The right and left tibial nerves
were electrostimulated transcutaneously at each ankle, alternately(4–17 Hz; monophasic square-wave pulses; 0.2–3 ms width; constant current of 5–17 mA, clearly above the motor threshold foreach subject).
Magnetic signals were recorded at 35 or 40 points (Fig. 2) with a105- or 120-channel SQUID biomagnetometer system (Kanazawa
Institute of Technology, Kanazawa, Japan) (Fig. 1A and B). A vector-type SQUID sensor was assigned to each measurement point.
Each sensor was equipped with 3 gradiometric pickup coils orthogonal to each other to enable simultaneous detection of 3 independent magnetic ﬁeld components. The diameter and baseline lengthof the pickup coils were 16 and 68 mm, respectively (Adachi et al.,2008). The typical noise ﬂoor at 500 Hz was around 3 fT/Hz0.5. The
measurement area was centered at the spinous process of L4 andplaced coplanar to the lower back (no distance between the bodysurface and the dewar surface). A band-pass ﬁlter of 100 or

For all subjects, CEAFs could be recorded after tibial nerve stimulation (Fig. 3). The spike waves of the obtained magnetic ﬁelds
showed biphasic conﬁgurations; the ﬁrst deﬂection of magnetic
signals on the left side of the assumed L5 and S1 nerves (dotted line
in Fig. 3) was directed outward (amplitudes up to 30 fT), and thatof the right side was directed inward (amplitudes up to 30 fT).
The polarity reversed for the second deﬂection. The peak of the ﬁrst
magnetic signals emerged at 13.7–18.6 ms (average 15.3 ms), andthe peak of the second magnetic signals emerged at 15.6–21.1
ms (average 17.6 ms). The peak-to-peak amplitude was 21–57 fT(mean 32.6 fT). These waves propagated in a caudal to cranial
direction at a conduction velocity of 43.2–69.6 m/s, as calculated
from the peak latency; these velocities were consistent with physiologic nerve conduction velocities.
The isomagnetic ﬁeld maps of CEAFs showed a quadrupolar pattern (Fig. 4A). The intra-axonal currents ﬂowed from the axon depolarization site in the opposite direction along the nerve. The leading
and trailing intra-axonal currents generated the magnetic ﬁelds(Fig. 4B). The ﬁeld generated by the leading intra-axonal currents
directed outward from ventral to dorsal on the left side of the nerve
and inward from dorsal to ventral on the right side of the nerve.

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Fig. 1. (A) Vertical, cylinder-shaped cryostat with a sensor area protruding from the side. (B) An array of SQUID vector gradiometers with a 5  8 matrix-like arrangement. (C)The sensor surface is curved to ﬁt to the lordosis of the subject’s lumbar spine.

These quadrupolar ﬁelds emerged from the caudal area of the stimulated side, propagated to the center of the lumbar spine diagonally, and subsequently propagated cranially along the lumbar
spinal canal at the L3–L5 level, according to the neural pathway.
3.2. Estimated current sources

Fig. 2. CEAFs were recorded at 35 or 40 points over the skin surface after
stimulation of the tibial nerve. Measurement points were arranged in a 5  7 or
5  8 matrix, and the distance between each point was 20 mm in both thelongitudinal and lateral directions.

The current sources of measured CEAFs were estimated by the
UGMN ﬁlter method and visualized and superimposed onto Xray images (Fig. 5). A conducting forward and backward current
ﬂow, according to the pathway from the nerve roots to the cauda
equina, was recognized. In addition, volume currents surrounding
intra-axonal currents were also observed. The forward current ﬂow(leading axonal current ﬂow) emerged at 13.5–17.5 ms (average
15.4 ms), and the backward current ﬂow (trailing axonal currentﬂow) emerged at 15.8–20.7 ms (average 18.3 ms). The conduction
velocity of the current source waveform was 56.1–66.7 m/s, as calculated from the peak latency.
3.3. SEPs and CEAPs

Depolarization was located between the cranial leading magnetic
ﬁelds and the caudal trailing magnetic ﬁelds. This quadrupolar pattern is characteristic of the magnetic ﬁelds of nerve axonal activity.

Waveforms of SEPs recorded from the electrode placed on the
L5 spinous process showed negative peaks in latency between

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epidural CEAPs were recorded were superimposed onto the CEAPs(Fig. 7). These waveforms corresponded almost exactly in bothsubjects in whom CEAPs were recorded.
4. Discussion

Fig. 3. Waveform arrangement of CEAFs after left tibial nerve stimulation based on
measurement points. The waveforms are superimposed onto a schematic representation of the lumbar spine taken from the anterior–posterior view of an X-ray
image. Signals above the baseline indicate outﬂux magnetic ﬂow from ventral todorsal, and signals below the baseline indicate inﬂux magnetic ﬂow from dorsal toventral. The dotted line indicates the left L5 and S1 nerve roots and cauda equina
ascending along the left side of the spinal canal, which we assumed.

14.9 and 19.1 ms, and the waveform recorded from the electrodeplaced on the L3 spinous process showed negative peaks in latency
between 17.4 and 21.0 ms (Fig. 6A). Nerve conduction velocity between the L3 and L5 spinous processes was 32.4–357.6 m/s (mean152.2 m/s), as calculated from the onset latency of the signal, andvaried widely among subjects.
Waveforms of CEAPs recorded from the epidural electrodes
showed propagation in the caudal to cranial direction (Fig. 6B).
Nerve conduction velocity between L3 and L5 was 52.6–70.6 m/s(mean 64.5 m/s), as calculated from the onset latency.
The volume current components perpendicular to the nerve
pathway were reconstructed from measured CEAFs by the UGMN
ﬁlter method, and those waveforms estimated at 5 points in which

The magnetic ﬁelds identiﬁed in the present study showed aquadrupolar pattern characteristic of the magnetic ﬁelds of nerve
axonal activity. In addition, the ﬁelds propagated along the spinal
canal in a caudal to cranial direction, and the latencies of the magnetic ﬁelds corresponded with those of the epidural action potentials. These results indicate that the magnetic ﬁelds originated in
the cauda equina inside the spinal canal and nerve roots.
Neuromagnetic recording has been reported for the purpose offunctional diagnosis of nerve disorders such as cervical spondylotic
myelopathy and lumbar spinal stenosis. With respect to cervicalspine disease, we previously reported on the utility of neuromagnetic recording of spinal cord evoked ﬁelds after stimulation of
the thoracic spinal cord, and a device for the identiﬁcation of thedisordered site has been developed (Adachi et al., 2006, 2007,2008; Sato et al., 2009). In the lumbar spine, studies of neuromagnetic ﬁelds measured over the surface of the lower back after tibial
nerve stimulation in humans have visualized the conduction ofcompound action potentials (Curio et al., 1995; Mackert et.al.,
1997, 1998, 2001a,b). However, reports of propagation of the signal
inside the spinal canal were not detailed.
Patients with lumbar spinal canal stenosis (LSCS) often havesymptoms originating from central stenosis. For the accurate identiﬁcation of the disordered site in patients with multiple stenoses
in the lumbar spine, measurement of CEAFs inside the spinal canalis required. Clinically, L3/4 and L4/5 are often disordered (Hallet al., 1985). These disordered sites could be identiﬁed by observing signals originating in the cauda equina after tibial nerve stimulation. However, measurements of neuromagnetic ﬁelds in the
lumbar spine have been difﬁcult to obtain. The reason is considered to be that the cauda equina in the lumbar spine is thin and situated deep in comparison to the cervical spinal cord. In addition,
the thoracic spinal cord can be stimulated by epidural electrodes
when measuring spinal cord evoked ﬁelds (SCEFs) on the cervicalspine, but in the lumbar spine, we can stimulate only a thin
peripheral nerve. In fact, spinal cord evoked potentials (SCEPs) in
response to stimulation of the thoracic spinal cord are approximately 10 lV (Tani et al., 1999), whereas CEAPs are approximately

Fig. 4. (A) Isomagnetic ﬁeld maps of CEAFs. Red indicates outﬂux magnetic ﬂow from ventral to dorsal, and blue indicates inﬂux magnetic ﬂow from dorsal to ventral. The
quadrupolar magnetic ﬁeld propagated according to the neural pathway. (B) Characteristic quadrupolar pattern of axonal neuromagnetic ﬁelds.

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Fig. 5. Estimated current sources for CEAFs after tibial nerve stimulation. Small arrows indicate the current direction and intensity, and the color density indicates the current
intensity. Propagating intra-axonal currents and volume currents were identiﬁed.

Fig. 6. (A) Waveforms of SEPs after left tibial nerve stimulation recorded on the
T12, L3, and L5 spinous processes, and on the ischial tuberosity and popliteal fossa.
The waveforms indicated propagation, though the conduction velocity varied
widely among subjects. (B) Waveforms of CEAPs after left tibial nerve stimulation
recorded from an epidural electrode placed at the level of L3–L5. Waveforms
showed propagation in the caudal to cranial direction.

2 lV, suggesting that evoked magnetic ﬁelds in the lumbar spine
are also small.
In the present study, we detected signals ascending along the
spinal canal and clearly visualized the signals in detail. Possible
reasons why we were able to detect CEAFs include the following.
First, the subjects remained in a comfortable and stable supine
position. Therefore, body movements and noise caused by muscle
activity in response to stimulation were minimized. Second, ﬁttingof the curved surface of the sensor to the lumbar lordosis

Fig. 7. Volume current components of current sources calculated from CEAFs (darkwaveforms) were superimposed onto epidural CEAPs (light waveforms). (A) Left
tibial nerve stimulation. (B) Right tibial nerve stimulation. The waveforms
corresponded almost exactly.

minimized the distance between the sensors and nerves. In previous reports, the contact surface of the sensor was plane or concaveand did not ﬁt along the spine.
Furthermore, we were able to reconstruct the signal source
originating in the cauda equina by analysis of the obtained signals
with the UGMN ﬁlter method. This spatial ﬁlter method allowed us
to reconstruct the current at any point. We found that CEAPs corresponded exactly with currents of components perpendicular to
the nerve pathway reconstructed from magnetic data. Reconstructed currents perpendicular to the nerve pathway are considered to represent axonal depolarization (Tomori et al., 2010). We
were able to demonstrate the high accuracy of measurement ofneuromagnetic ﬁelds. This method may be useful for the accurate
identiﬁcation of the disordered site in spinal diseases. In addition,

S. Ishii et al. / Clinical Neurophysiology 123 (2012) 1656–1661

given that we were able to measure neural activity around theintervertebral foramen, this method may be useful in the diagnosis
of foraminal stenosis, which can be difﬁcult.
Financial interests
The authors declare no ﬁnancial interests.
Acknowledgements
The authors thank Mr. S. Fujii, Mr. R. Nakamura, and Mr. Y. Kawada of Tokyo Metropolitan University for their generous help andtechnical assistance.
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