IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-28, NO.
7, JULY 1981
Characteristics of Somatosensory Evoked Potentials
Recorded over the Spinal Cord and Brain of Man
ARTHUR M. SHERWOOD, MEMBER, IEEE
Abstract-Evoked potentials were recorded from the skin over the
lumbar and cervical portions of the spinal cord, and the scalp over the
sensory cortex of the brain, using averaging techniques. Responses
could be identified over the cauda equina and root entry zone in the
lumbar spine to stimulation of the tibial nerve at the popliteal fossa.
These responses had characteristics of nerve root and spinal cord events
in their thresholds, timing, duration, and refractoriness. Stimulation
of the median nerve at the wrist likewise resulted in recognizable re-
sponses over root entry portions of the cervical spinal cord. These
later waves had a morphology suggestive of components arising from
nerve plexus, nerve roots, and spinal cord. Responses recorded over
the spinal cord were in the 1-10 ,uV amplitude range. Tibial, peroneal
and median nerve stimulation were used to elicit 1-20 jV responses
recorded over the cortex, which were found to be sensitive to the site,
amplitude, and rate of stimulation.
INTRODUCTION
FOLLOWING early efforts at recording evoked potentials
over the brain more than 30 years ago [1], the applica-
tion of evoked potential recording has spread widely, to the
point that it is currently used in virtually every medical center
in this country. The availability of modern instrumentation,
including high quality amplifiers and inexpensive digital signal
processing equipment, makes it possible to meet the need for
noninvasive monitoring of activity in the nervous system.
Various applications of the technique for recording averaged
evoked potentials have become useful in diagnosis, in longi-
tudinal studies to detect regression or recovery of function,
and to provide a means of monitoring the efficacy of the
central nervous system during surgery on the spine or the
spinal cord.
Due to the small signals involved, recording of evoked neural
activity has been more dependent on developments in elec-
tronics than was, for example, recording of cardiac electrical
activity, which contains sufficient energy for directly driving
a recording device. Thus, progress from Berger's initial record-
ing of spontaneous brain electrical activity [21, or electro-
encephalography, to Dawson's work on averaging evoked po-
tentials from the brain [1] was based, in part, on more than
two decades of rapid progress in electronics. The earliest re-
cordings from the human spinal cord by Magladery et al. [31
were made using invasive techniques, and depended on good
amplifiers, not averaging. Modern computer technology has
greatly facilitated the large amount of work being done today.
Advances in the use of cortically recorded somatosensory
Manuscript received January 13, 1981; revised March 4, 1981. This
work was supported by the Bob and Vivian Smith Foundation, Hous-
ton, TX, the Rehabilitation Research and Training Center No. 4 under
Rehabilitation Services Administration Grant 16-P-56813-6, and the
Rehabilitation Services Administration under Grant 13-P-59275-6.
The author is with the Department of Clinical Neurophysiology,
The Institute for Rehabilitation and Research, Houston, TX 77030.
0018-9294/81/0700-0481$00.75 C 1981 IEEE
481
evoked potentials (SEP's) has been reviewed by Desmedt and
Noel [4]. In the last two decades, noninvasive techniques for
recording lumbar spinal cord evoked potentials (LSEP's)
based upon signal enhancement through synchronous averag-
ing have been developed by Liberson et al. [5 ], by Cracco [6],
and others. More recently, Jones [7] and El-Negamy and
Sedgwick [8] reported successful efforts to record and charac-
terize cervical spinal cord evoked potentials (CSEP's) as well.
The work reported in this paper has been done in the De-
partment of Clinical Neurophysiology of The Institute for Re-
habilitation and Research, a specialized rehabilitation hospital
affiliated with the Baylor College of Medicine. Located within
this hospital is a regional spinal cord injury center, as well as
a center for treatment of patients with a variety of neuro-
muscular and brain disorders. Within this setting, we are
faced with the practical problems of restoring function to
paralyzed individuals. In order to accomplish this goal, our
own research is focused on the study of sensory and motor
function, and particularly functions of the spinal cord in
chronic patients with central nervous system lesions, varied
in both site and extent.
In this context, we use evoked potentials as one tool for
exploring the site and degree of such lesions, along with a
battery of other tests [9], [10]. We have focused upon re-
cording from the lumbosacral portion of the spinal cord,
from the cervical portion of the spinal cord, and from the
sensory cortex of the brain, with stimulation of the peroneal
and tibial nerves in the lower extremity, and the median
nerve in the upper extremity. In this paper, we present tech-
niques for recording these potentials and describe the charac-
teristics of their waveforms.
METHODS
Data presented were collected from twelve male and five
female normal healthy adults, ranging in age from 21 to 65
years, and from one T8 female spinal cord injury patient,
27 years old.
Potentials were recorded using TECA AA6 Mk III amplifiers
with a gain of 25 000, bandwidth of 16 Hz-8 kHz, and an in-
put impedance of more than 100 MQ2. Amplifier noise re-
ferred to the input was less than 2 ,V peak-to-peak. Samples
were digitized with a Preston analog-to-digital converter
which has a maximum digitization speed of 500 kHz and a
+- 2 V full-scale range with a 12 bit plus sign digital output,
for a resolution of 500 ,uV/bit. With a 16 channel multi-
plexer, this allows a sampling rate of 31 kHz per channel, or
up to 500 kHz for one channel. Data from the ADC are passed
from a Hewlett-Packard 1000 data processing system with an
HP 2111 F minicomputer and disk and magnetic tape storage.
482 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-28, NO. 7, JULY 1981
Using this system, 128 responses were averaged to produce
each output waveform. The raw evoked responses, together
with timing and stimulus control signals, were recorded on
a Honeywell 7600 14 channel FM tape recorder for subse-
quent reanalysis.
Stimulus timing was provided by a custom programmable
stimulus control unit [11], which provided trigger pulses to
a dual channel Grass Model S-8 stimulator which was used
with Grass constant voltage stimulus isolation units. Stimulus
pulses were arranged for a pulsewidth of 500 ,s duration
using an amplitude range from 10 to 150 V. The stimulus
control unit delivered trigger pulses at any desired rate or,
if necessary, at a variable delay after a QRS complex of the
electrocardiogram triggered an oscilloscope [20]. The delay Fig. 1. Lumbar spinal evoked potentials (LSEP's). Bilateral tibial
was chosen so as to cause the stimulus response window to
occur in a quiescent portion of the EKG cycle. Stimulating bilateral H waves in the triceps surae muscles, resulted in these char-
and recording electrodes were placed appropriately for each
of the three recording situations described below.
Lumbosacral Recordings
For recording from the lumbar portions of the spinal cord,
electrodes in the form of 4 by 2 cm chlorided silver (fine)
strips were placed transversely over the spinous processes at
the T6, T12, L2, L4, and S1 vertebral levels, and taped se-
curely to the skin. The T6 electrode served as the reference,
and was connected to the positive input of each of the differ-
ential preamplifiers. Impedance between each pair of elec-
trodes was kept below 5000 Q by proper preparation of the
skin in all studies for all leads. Stimulating electrodes were
placed over the tibial nerves bilaterally at the popliteal fossae.
For optimum depolarization of the nerve with minimum dis-
comfort, we used a 2 cm lead disk as the cathode, placed in
close proximity to the nerve trunk, and a 8 by 8 cm lead
plate placed on the opposite side of the leg as the anode.
Stimulus intensity was adjusted to induce reflex or direct
activation of the triceps surae muscles. The wide spacing of
the recording electrodes provided a monofocal arrangement
for recording activity over the lumbar spine (the T6 refer-
ence site has been previously shown to be relatively inactive
following such a stimulus [13], [14]). Thus, there was a
large EKG representation in these leads, which was eliminated
from the averaged records by use of the EKG trigger scheme
described above.
Cervical Spinal Cord Recording
Responses from the cervical spinal cord have been recorded
over the seventh cervical vertebra referenced to a Beckman
recessed electrode, placed over the suprasternal notch to
record activity across the spinal cord. In a separate channel,
the seventh cervical lead was referenced to a chlorided silver
disk electrode placed at the Fz position (10-20 International
EEG Standard placement [15]). To monitor the afferent
volley, a Beckman recessed electrode was placed on the skin
of the supraclavicular fossa over the brachial plexus at Erb's
point; the reference electrode was placed 3 cm above it on the
neck. The stin6ulus site was the median nerve at the wrist,
using 1 cnv aiinless steel disks held 3 cm apart in a plastic
housing. 'trapped to the skin surface. Stimulus strengths
iafnged from sensory threshold to 4 times sensory threshold.
since '.these leads had relatively large EKG representations
0.00 5.00 10.00 15.00 20.00 25.00
MILLISECONDS
nerve stimulation with 128, 0.5 ms, 45 V pulses, adjusted to induce
acteristic double-peaked nerve root responses in the L 4 and S 1 leads,
and the single, negative peak in the T12 lead. No digital filtering or
smoothing (other than averaging) was used in any of these figures.
also, it was desirable to use the EKG trigger scheme as de-
scribed above.
Cervical Somatosensory Evoked Potential Recordings
For recording cortical responses, silver-silver chloride cup
electrodes attached by Grass EC 52 paste were placed over
the vertex at a point 2 cm behind the Cz position (10-20
system), and bilaterally on a line from the vertex electrode
to the external ear canal, 7 cm from the vertex, behind the
standard C3 and C4 positions. For upper extremity evalua-
tion, the median nerve was stimulated at the wrist as de-
scribed above. Lower extremities were stimulated through
the tibial and peroneal nerves at the popliteal fossae, as de-
scribed above. Stimulus strengths were normally adjusted
to a level of twitch motor threshold.
RESULTS
Lumbosacral Responses
Fig. 1 shows an example of the evoked electrical potentials
recorded over the spine at lower thoracic, lumbar, and sacral
segments, obtained by bilateral stimulation of the tibial nerves
at a strength sufficient to elicit an H (Hoffman) reflex. As
can be seen in the figure, there were two kinds of responses.
At the T12 level, there was a smooth, predominately negative
wave which we have labeled the S (spinal cord) response, using
Magladery's terminology [3], [14]. In the lower leads, L4
and S 1, the responses were double-peaked, with a predomi-
nantly early negative wave. The first negative peak has been
labeled the R (dorsal root) response, and the second the A
(anterior root) response. These responses were reproducible
within the same subject and from subject to subject, with
minor variations in the location of the transition from the
double peak to the single peak response, presumably corre-
sponding to intrasubject anatomical variability. The S wave
has been shown to arise in the spinal cord itself, while the R
and A waves arise in the nerve roots [3], [14]. Examination
of the changes in amplitude resulting from increasing stimulus
strength showed that the R wave was first to appear, and that
the A wave increased, then stabilized or decreased as the
stimulus intensity increased. Changes in the A wave amplitude
corresponded to changes in the H-reflex response recorded
SHERWOOD: EVOKED POTENTIALS OVER SPINAL CORD AND BRAIN
0.00 8.00 16.00 24.00 32.00 40.00
MILLISECONDS
Fig. 2. Cervical spinal evoked potentials (CSEP's). Unilateral stimula-
tion of the median nerve with 0.5 ms, 33 V pulses, at 1.5 times the
sensory threshold, was used to excite the electroneurogram response
over Erb's point, and the spinal nerve root and cord responses are
recorded from the Cv7 electrode referenced to the suprasternal
notch and to the Fz scalp lead. The far field potential can be seen
in the mastoid lead referenced to the Fz scalp lead.
in the triceps surae muscle. Evaluation of the response to
stimulus pulse pairs revealed that the R wave recovered in
about 1 ms, and the S wave in less than 5 ms.
The average onset latency of the S wave recorded at the T12
level was 10.8 ms, while the average onset of the R wave at
the S I level was 12.7 ms. The amplitude of the S wave ranges
from 1 to 15 uV in adult subjects. The duration of the S wave
was approximately 7 ms, and that of the R and A waves ap-
proximately 4 ms.
We are currently recording such lumbosacral spinal cord
evoked potentials on a routine clinical basis for the evalua-
tion of lesions of the lumbar plexus and spinal cord, where
subjective reports of sensation from the patient are frequently
inadequate to define the nature and extent of any lesions pres-
ent. This is particularly true when the patient has multiple
lesions of the spinal cord. Asymmetries in the responses from
the two -legs, as well as losses in ascending signals, can be seen
in this manner.
Cervical Spinal Cord Evoked Potentials
Evoked potentials can also be recorded over the cervical
spinal cord. An example of such a recording is shown in Fig.
2, together with an electroneurogram recorded above Erb's
point, showing the brachial plexus response. The CSEP had a
relatively smooth, slow positive peak at approximately 10 ms
and a more complex negative peak at 12-13 ms, with a charac-
teristic notch at about 12.5 ms. These negative waves were
followed by a longer slight positivity. In the later response,
which used the scalp reference, the earliest positivity is not
as evident, although the later negative peak or multiple peaks
are well in evidence, and the longer latency, positive peak was
more pronounced and of longer duration and complexity, as
can also be seen in the mastoid lead.
When tested with increasing stimulus strength, the negative
complex at 13 ms was the first waveform to appear, and it
appeared at approximately 1.3 times the sensory threshold.
At 1.5 times the sensory threshold, the earlier positive wave
began to appear. The amplitude of the response recorded in
483
the Cv7-Fz lead ranged from approximately 1 ,V to as much
as 10 ,uV when using a stimulus intensity sufficient to elicit a
supramaximal, direct muscle (M wave) response. When this
response was examined by delivering double pulses at varying
intervals, the amplitude of the second response in the response
pair returned to the control amplitude after a 4 ms interval in
the Erb's point recording (peripheral nerve response). In the
Cv7-SS lead, partial recovery of the response complex begins
as early as 2 ms, but the full morphology of the wave was not
seen until the pulse separation was 10 ms, and the amplitude
of the overall complex remained suppressed for more than
20 ms.
Examination of records obtained from patients with injury
of spinal cord segments above Cv6 revealed essentially nor-
mal morphology of the electroneurogram recorded over Erb's
point, and of the responses from Cv7-SS electrodes. However,
the latter portions of the response recorded from electrodes
at Cv7-Fz, found in normal subjects, was absent in the patient's
recording [161. This suggests the spinal cord origin of the
earlier portions of these waveforms, and the brainstem or brain
origin of the later components.
When the normal records -are compared with responses ob-
tained from electrodes placed epidurally, within the spinal
canal and over the posterior midline of the spinal cord, the
surface recordings are of much less complexity and of lower
frequency content than are the recordings made just outside
the dura, as would be anticipated. This can be seen in Fig. 3,
showing simultaneous records from electrodes both inside
the spinal canal and on the surface of the skin over the neck,
clearly showing the effects of the relative electrode position
on both complexity and amplitude of the responses.
In several instances, it has even been possible to record cervical
activity in response to tibial nerve stimulation. Differential
recordings from cervically located epidural electrodes showed
typical responses of about 16-18 ms latency, 1-2 ,V ampli-
tude, and fairly high frequency content, compared to signals
recorded on the surface. No clear representation of these
responses was recordable at the overlying skin surface in
these subjects. Evoked responses were successfully recorded
from the skin primarily in locations close to the nerve root
entry zones, or over other relatively large generator structures.
Cortical Somatosensory Evoked Potentials
Somatosensory evoked potentials recorded over the sensory
cortex are more widely used, and more easily obtained, than
are the spinal cord responses. Fig. 4 illustrates the character-
istic responses obtained while stimulating the left median
nerve at the wrist in a normal subject. This recording illus-
trates the predominantly contralateral nature of the response.
Averaging is begun 40 ms prior to the stimulus to provide a
background level for comparison with the evoked response.
The earliest wave in this complex is the initial negative peak,
which has a latency of 19 ms, followed by a positive peak at
24 ms. These early components of the waveform are the
most stable and, hence, are the most widely used for detecting
the presence or absence of a response. If recording simulta-
neously from electrodes over the spinal cord and overjtl-e
brain, the cortical response can be identified at a lower stim-
ulus intensity than that which is necessary to produce a m6a-
484 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-28, NO. 7, JULY 1981
o:.oo s:.oo ib.oo 15. oo 2b. oo 25. oo
MILLISECONDS
Fig. 3. CSEP recording from surface and epidural electrodes. Stimulat-
ing the left median nerve at 80 V induced the waveforms shown in
a head injury patient. The epidural electrodes, placed for therapeutic
stimulation, were radiologically found to be over the midline at the
second and third cervical vertebral levels. Differential recording from
the epidural electrode pair (second trace) was arranged so that nega-
tive activity in the Cv3 electrode resulted in an upward trace deflec-
tion. The top trace shows activity between the lower epidural elec-
trode and the reference electrode at the suprasternal notch.
-j.~~~~~~~~~~4F
o
o CZ-F
3.00 40.00o 8b.00o 120. 00 I1 0. 00 200.00
M I LL I SECONDS
Fig. 4. Somatosensory evoked potentials recorded from cortical struc-
tures. Stimulation of the left median nerve at the twitch threshold
for the thenar muscle (68 V, 0.5 ms) resulted in the predominantly
contralateral activity in the C4-Fz (right) lead. Averaging began
40 ms prior to the stimulus in this and remaining filgures.
surable response from the skin over the spinal cord. The
amplitude of response -to median nerve stimulation on the
contralateral side rgesfrom about 1 to 20 ,V, while the
ipsilateral respont is approximately one-fourth as large.
The responsSJs to stimulation of the lower extremity are
lower in am$itude and increased in latency (Fig. 5). The
cortical re .onse to tibial or peroneal nerve stimulation is
charactertied by a positive peak at 43 ms, with later peaks
occurring with increasing variability in latency and amplitude.
Consistent with the somatotopic organization of the sensory
Cortex, these reponses are best seen in the electrode over the
central 'ulcus, i.e., the Cz-Fz lead.
o.00 40. 00 80. 00 120. 00 160.00 200.00
MILLISECONDS
Fig. 5. Lower extremity (peroneal nerve) SEP. Stimulation of the
right peroneal nerve at the popliteal fossa with 0.5 ms, 54 V pulses,
at the twitch threshold in the anterior tibialis muscle, resulted in
the activity shown. Characteristic of tibial and peroneal nerve re-
sponses, the larger response in the Cz-Fz lead presumably arises from
the somatoptic localization of the leg sensory response.
The cortical evoked response to stimulation of the lower
extremities in patients with lesions of the spinal tracts demon-
strates a variety of response possibilities. The response can be
present in toto, absent, or may be modified in shape through
a prolongation of latency, temporal dispersion, or reduction
in amplitude of one or more components. For example, in
spinal cord injury patients with so-called clinically complete
lesions, i.e., those with no sensation and with no voluntary
motor activity, a variety of SEP results may be found, from
a completely flat trace to a relatively normal waveform [17] .
We have also found that the response produced depends
not only on the amplitude and pulsewidth of the stimula-
tion and on the site of stimulation, but also on the rate of
stimulation. In both normal subjects and spinal cord injury
patients, larger amplitudes are obtained with lower rates of
stimulation, as illustrated in Fig. 6 with data collected in a
normal individual. Not only are the late components lost
at the higher rates of stimulation, but the early components
are modified at rates as slow as 1 Hz. Note that the earliest
positivity tends to disappear as the rate is increased above
0.5 Hz. In many other normal studies, the loss of features of
the waveforms above 0.5 Hz is much more pronounced. Re-
cordings from patients with impairment of spinal columns
show even more loss of fidelity in response as the rate is
increased from 0.5 Hz.
DISCUSSION
Common Problems in Recording Evoked Potentials
There are a number of problems common to the recording
of evoked potentials in response to peripheral nerve stimula-
tion, whether arising from the brain or the spinal cord. Most
of these problems revolve around the fact that the generator
activity occurs over a small cross-sectional area relative to the
distance to the recording electrodes on the skin surface. As a
consequence of the distance and the size, potentials recorded
on the skin surface are typically 1-10 ,uV in amplitude. These
SHERWOOD: EVOKED POTENTIALS OVER SPINAL CORD AND BRAIN
0.00 40.00 80.00 120.00 160.00 2b0. 00
MILLISECONDS
Fig. 6. Effects of variable rate on the SEP. Displaying only the Cz-Fz
responses, recorded in the same fashion as were the data in Fig. 5,
the effects of different stimulus rates can be noted. At the 12.5 Hz
rate, the averaging window of 200 ms exceeds the 80 ms stimulus
period, resulting in the display of two stimulus artifacts, and portions
of three responses.
very small signals are present in combination with undesired
electrical signals arising from activity of cardiac, smooth, or
skeletal muscles. In addition, such small signals require the
use of high-gain electronic amplifiers, which add electronic
noise to the signal path. Thus, great care must be taken in the
acquisition and processing of these signals to adequately pre-
serve the fidelity of the recorded response for proper analysis.
Another consequence of the distance from the generator site
to the recording site is the reduction in the rate of change of
the angle of observation measured from the recording elec-
trode to the leading edge of the depolarization wave in the
neural structure. This reduction in the angular frequency of
the wavefront at the observation point as a result of its dis-
tance from the recording electrode produces a loss of high fre-
quency content in the waveform and results in an effective
smoothing of the observed potentials [18]. This process is
sometimes called the "spatial filtering" effect, and can be seen
in Fig. 3, comparing the second and fourth traces. The end
result of this filtering effect is highly dependent on the type,
number, and orientation of the generator structures.
Electronic Design: Using good electronic design principles,
it is possible to obtain amplifiers with gains in the range of
20 000-100 000 and bandwidths in the range of 1-10 kHz,
while maintaining a noise level of less than 3 ,uV peak-to-peak,
and even less if more restricted bandwidths are used. Precau-
tions must be taken to insure that any residual electronic
noise is not synchronous with the stimulus. To date, ampli-
fiers which combine these characteristics with the capability
to reject distortion and baseline shifts due to the imposition
of large overloads from, for example, stimulus artifacts, have
not become commercially available. Thus, special precautions
must be taken to minimize the direct coupling of signals
from the stimulating electrodes to the recording electrodes.
This can be accomplished in some situations through orthog-
onal orientation of the stimulating and recording vectors,
485
and through good grounding at a point equidistant from
the two electrodes in each differential pair.
Although not generally available, one promising approach
has been successful in dealing with the problem of return to
baseline. Walker and Kimura [19] have described a modifica-
tion of the basic ac-coupled amplifier design which permitted
them to achieve a return to baseline of approximately 1 ms.
It is necessary to use a bandpass recording scheme (ac cou-
pled) in recording low-level biological signals, due to the in-
evitable offset dc potential existing between the inputs to the
differential amplifier and the high gains required. Walker
used a dc-coupled amplifier with a switchable low-pass feed-
back loop to achieve the necessary baseline stabilization.
Cortical SEP's are frequently recorded using a low-pass filter
of 500 Hz or even 100 Hz. Obviously, the diffuse source and
its distance from the recording electrodes and the postsynaptic
nature of the cortical potentials suggest that little high fre-
quency information is present on the scalp. However, record-
ings made over the spinal cord, particularly those with responses
characteristic of nerve roots, have much higher frequency con-
tent, and require as much as 10 kHz bandwidth. Latency
shifts in the response peaks are apparent when changing from
10 to 1 kHz [20].
While 16 Hz is the typical setting for the high-pass filter in
these studies, it is sometimes useful to lower the cutoff to 1
or 2 Hz in cases when the stimulus artifact is troublesome
[21]. This has the effect of stabilizing the baseline at a new
equilibrium level rather than allowing a recovery to zero
during the averaging window with the resultant sloping base-
line during that time.
The biological noise is not easily reduced. Due to the fact
that the recording electrodes are relatively distant from the
signal generators, and that large muscle signal generators are
as close or closer to the recording electrodes than are the
neural generators, great care must be exercised in reducing
the amount of muscle activity, particularly in those muscles
closest to the recording electrodes. This means that much
attention must be given to the subject relaxation, without
which it becomes virtually impossible to record. Attention
must also be given to the fact that the stimulus itself may be
uncomfortable and cause a loss of relaxation and subsequent
degradation of the recording conditions. Although these are
obvious comments, their importance cannot be overempha-
sized, due to the nature of the recording process.
Attention must also be given to the nature of the biological
noise, to insure that it is not synchronous with the stimulus
also. For instance, it is necessary to distinguish between
evoked neural activity and evoked muscular activity recorded
by volume conduction from a (possibly) more distant site.
Because of the size of the latter, there is a large chance that
such crosstalk can occur, making it necessary to carefully ob-
serve the characteristics of the two. The use of stimulus pulse
pairs, timed so that the second pulse falls in the refractory
period for excitation of the muscle but not the neural ele-
ments, provides one possible way of making such a distinction.
Similarly, the stimulus rate must be selected carefully to
avoid distortion of the signal through intrastimulus interac-
tions, which might result in partial or complete refractoriness
of the neural generators.
486 IEEE TRANSACTIONS ON BIOMEDICAL ENGINEERING, VOL. BME-28, NO. 7, JULY 1981
Problems ofMonitoring Evoked Spinal Cord Responses
Bifocal Versus Monofocal Recording: In addition to the
problems described above, noninvasive recording of potentials
from the spinal cord is particularly challenging, due to the
fact that the signal source is not only small, but also is sep-
arated from the recording site by many layers of interposed
muscle tissue. Because of the distance, pairs of electrodes on
the skin over the spinal cord and connected for bifocal record-
ing will detect only very small short-duration signals. We
therefore made use of a monofocal recording scheme, in
which a reference electrode is placed at some distance away,
over an electrically quiet structure. This increased the amount
of electrical activity detected in the lead arising from the EKG.
As described in the methods, timing of the stimulation can be
done in such a way as to avoid coincidence of the major ac-
tivity of the EKG with the averaging window. This greatly
decreases the number of responses needed to be averaged for
adequate representation of the waveform [20]. Alternately,
there are a number of schemes for detecting an out-of-range
signal in the averaging window and rejecting the sample so
contaminated. However, such methods depend on correct
selection of the range of interest.
Generator Site: Examination of our results and of the
results of others such as Cracco et al. [22], who made such
recordings in children, shows that the first recognizable re-
sponses to electrical stimulation of a peripheral nerve occur
over the relatively large neural structures of the sensory cor-
tex, which serves as a sort of "biological amplifier." The
second place the response can be seen is over the spinal cord,
with its synaptic interactions, appearing virtually simulta-
neously with electroneurograms recorded over peripheral
nerves. Finally, it appears over the cauda equina, arising
from volleys in the nerve roots. It is extremely difficult to
recognize the response to stimulation of the lower extremities
when recording from the skin over the spinal cord of adults
at vertebral levels much above the tenth thoracic vertebra.
Presumably, this difficulty is due to the relatively small cross
section of ascending fibers which are excited in this region.
When properly positioned epidural electrodes are used for
recording, however, small responses can be detected in the
cervical portion of the spinal cord in response to stimulation
of nerves in the legs. Thus, surface recordings are of only
limited utility in following the progress of induced volleys
of nerve impulses as they travel up the spinal cord, but sur-
face electrodes are quite useful for monitoring activity in
the root entry portions of the spinal cord.
Problems in Recording Cortical SEP's
Many of the problems and questions regarding the recording
of evoked cortical somatosensory responses with surface elec-
trodes have been resolved [4]. However, no consensus has
been reached on the exact site(s) of the generator(s) of all
components of the waveform, nor even of their precise charac-
teristics. The aspect of- SEP's addressed in this paper is the
relevance of the stimulus rate to the morphology of such
waves, particularly when stimulating nerves of the lower
extremities. Desmedt suggests a 0.2 or at most 0.5 Hz rate
of stimulation [23]. Others have suggested the use of 5 Hz
[21] or even more [24]. In our experience, the rate of stimu-
lation significantly affects the shape of the responses recorded,
particularly in data acquired from patients with injury- or
disease-induced lesions of the spinal tracts [25]. A word of
caution-the use of modern digital control techniques in
achieving the various rates of stimulation can, through their
precision in timing, inadvertently result in synchronization
of the stimuli with line frequency subharmonics, with con-
sequent enhancement of the line frequency components
along with the desired neural responses.
Clinical Applications ofSomatosensory Evoked Potentials
Somatosensory evoked potentials have been widely used as
a clinical tool, both for diagnosing a variety of different
neurological disorders [26], and for research on the integrated
sensory system. Evoked potentials recorded over the spinal
cord, however, are not commonly used. Indeed, questions have
been raised as to the origin of waves recorded over the cervical
spinal cord. Now it is becoming increasingly clear that these
early waves arise in spinal cord structures [27] - [29], and such
spinal cord recordings are beginning to be applied in a variety
of situations, for diagnosing the level and degree of spinal cord
injury [30], for studying lesions accompanying such diseases
as multiple sclerosis [31], and in monitoring the integrity of
the spinal cord during surgical procedures on the spine [32].
CONCLUSIONS
The use of high-quality amplifiers and analog-to-digital con-
verters, coupled with modern computer technology, have
made it possible to adapt what were previously techniques
reserved only for experiments in a research laboratory setting
to routine use in clinical measurements, thereby providing a
valuable, noninvasive diagnostic tool to the clinical neurophys-
iologist. Such technology is a necessary but not sufficient
element in any meaningful application of SEP's, and does not
obviate the need to maximally control the measurement
setting. Factors such as good subject relaxation, elimination
of EKG artifacts, control of stimulus rate, choice and prepara-
tion of stimulating and recording sites, and avoidance of
synchronous electronic and biological noise must be con-
sidered. Proper consideration of these factors can lead to
useful, clinical cortical and spinal cord evoked potential
recordings.
Future developments, other than obvious improvements in
amplifier quality, minor improvements in computer elements,
etc., will depend on a detailed understanding of the underlying
physiological mechanisms which produce such potentials.
The current state of the art was built upon numerous efforts
in experimental neurophysiology to define the nature of the
reflex and sensory functions which we now measure clinically.
The testing functions, however, are far from those naturally
occurring in the organism, and new methods need to be de-
vised. The biomedical engineer needs to utilize his knowledge
of instrumentation and signal analysis, together with current
understanding of physiology, to provide more natural test
stimuli. Normal movement is controlled by the flow of nerve
impulses. Biomedical engineers can contribute to the develop-
ment of systems and algorithms adequate for the measurement
SHERWOOD: EVOKED POTENTIALS OVER SPINAL CORD AND BRAIN
of responses to such events. Such developments will be neces-
sary to increase our understanding of the underlying principles
of operation of the nervous system.
ACKNOWLEDGMENT
The author gratefully acknowledges the helpful discussions
with Dr. M. R. Dimitrijevic in formulating many of the ideas
presented in this paper. Review and critique by Dr. T. Prevec
and Dr. D. Lehmkuhl were also quite useful. Technical sup-
port in recording was provided by B. McKay, Reg. EEG Tech.,
J. VanZandt, EEG Tech., and J. Halter, M.S.E.E.
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A Arthur M. Sherwood (S'69-M'70) was born in
Johnson City, TN, in 1942. He received the
B.E.E. and M.S.E.E. degrees in electrical engi-
neering from the Georgia Institute of Tech-
nology, Atlanta, in 1966, and the Ph.D. degree
<va t'in biomedical engineering from Duke Univer-
V
: .P. _ =g g sity, Durhamn, NC, in 1970.
From 1970 to 1976, he was on the Bioengi-
neering faculty at Texas A&M University. He
has worked with The Institute for Rehabilita-
tion and Research, Houston, TX, since 1972,
and in his present capacity as full-time Director of Research for the
Department of Clinical Neurophysiology starting in 1976. He is also an
Adjunct Associate Professor at Baylor College of Medicine, Waco, TX.
Dr. Sherwood is a member of the IEEE Engineering in Medicine and
Biology Society and the Society for Neuroscience. He is a Registered
Professional Engineer.