Intraoperative Monitoring of Neural Function
Handbook of Clinical Neurophysiology, Vol. 8
M.R. Nuwer (Ed.)
# 2008 Elsevier B.V. All rights reserved
CHAPTER 16
Corticospinal tract monitoring with D- and I-waves from
the spinal cord and muscle MEPs from limb muscles
Vedran Deletisa,* and Francesco Salab
a
Center for Endovascular Surgery and Intraoperative Neurophysiology, Institute for Neurology and Neurosurgery,
Roosevelt Hospital, New York, NY 10019, USA
b
Department of Neurological and Visual Sciences, Section of Neurosurgery, University Hospital, 37100 Verona, Italy
16.1. Introduction
16.1.1. Intraoperative neurophysiology of the
corticospinal tract
Intraoperative monitoring (IOM) of the functional
integrity of the corticospinal tract (CT) has specific
requirements due to the pharmacologic influence of
applied anesthetics and the limitations inherent in sur-
gery on an unconscious patient. These factors present
advantages and disadvantages for both IOM and the
continued physiological exploration of the CT. With
this in mind, several IOM methodologies have been
developed, which give us an unique opportunity to
explore the physiology of the CT, especially within
the spinal cord. The application of these methodolo-
gies expands on what is currently possible during
IOM of the functional integrity of the motor system.
The experience in intraoperative neurophysiology
of the CT comes from different sources.

When we are facing an existing neurological deficit
in a patient coming to surgery, IOM teaches us the
essential elements of maintaining the functional
status of the motor system

When an acute injury to the motor system occurs
during surgery, we can identify the pathophysiol-
ogy of such event through IOM and learn how to
prevent this from happening in the future. A special
value has transient, that is, reversible, injury

The knowledge we gained from experimental work
done in animals, especially that done in primates
*
Correspondence to: Vedran Deletis, M.D., Ph.D., Institute
for Neurology and Neurosurgery, St. Luke’s Roosevelt
Hospital, 1000 Tenth Avenue, Suite 11G-78, New York,
NY 10019, USA.
Tel.: þ1-212-636-3281; fax: þ1-212-636-3159.
E-mail: vdeletis@chpnet.org (V. Deletis).
235

Neurophysiological data collected intraoperatively
from neurologically intact patients.
16.2. Methodology of electrical stimulation of the
brain with recording activity of the CT
16.2.1. Methodologies for intraoperative
electrical stimulation of the CT
The strong pulse(s) of electrical current applied on the
scalp can overcome the impedance barrier of bone and
soft tissue and stimulate the brain. In Fig. 1, we present
schematics of the basic methodology to intraoperatively
monitor motor evoked potentials (MEPs) from the spinal
cord’s epi- or subdural space, or limb muscles by using
single and multipulse stimulating techniques applied
transcranially or over the exposed motor cortex respec-
tively. The single pulse stimulating technique is used
to elicit D- and I-waves, while the multipulse stimulating
technique is used to elicite muscle MEPs. This schema
will help readers to better understand the methodology
of intraoperatively eliciting and recording of MEPs.
In Fig. 2, details of the positioning of stimulating
electrodes over the scalp use to elicite MEPs are
shown. The electrode placement on the skull is based
on the International 10/20 EEG system. Note that
instead of Cz, the Cz electrode is placed 1 cm
behind the typical Cz point because it corresponds
better to the primary motor cortex of lower extremi-
ties. We prefer to place a full set of stimulating elec-
trodes for transcranial electrical stimulation (TES)
because sometimes which montage will provide bet-
ter muscle MEPs without unnecessary muscle twitch-
ing is unpredictable. For eliciting D-wave muscle
twitching — which can be disturbing to the surgeon
— is not an issue because a single stimulus applied
transcranially over the exposed brain does not elicit
236
Fig. 1. Intraoperative methodology for eliciting and
recording motor evoked potentials (MEPs) from the spinal
cord and limb muscles. Top: illustration of electrode posi-
tions for transcranial (A) and direct (B) electrical stimula-
tion of the motor cortex according to the International
10–20 EEG system. Middle: schematic diagram of the
positions of the catheter electrodes (each with three record-
ing surfaces) places cranial to the tumor (control electrode)
and caudal to the tumor to monitor the incoming signal
passing through the site of surgery. In the middle are D-
and I-wave records rostral and caudal to the pathology.
Please note the peak latency difference between cranial
and caudal recordings of the D- and I-waves which are
marked with vertical lines. Bottom: recording of muscle
MEPs from the thenar, tibialis anterior, and abductor hallu-
cis muscles after eliciting them with a short train of electri-
cal pulses applied transcranially. (Modified from Deletis
et al., 2001b with permission from the International Feder-
ation of Clinical Neurophysiology.)
significant muscle twitching, and in most patients
twitching might be completely absent.
For transcranial stimulation, cork screw-like elec-
trodes (CS electrodes; Viasis, Neurocare, Madison,
WI) are preferable due to their secure placement
V. DELETIS AND F. SALA
Fig. 2. Top: actual position of electrode inserted in the
scalp for TES (front row: C3, C1, Cz, C2, and C4, and
6 cm ¼ (Cz þ 6 cm). Electrodes positioned posteriorly
are for recordings of the somatosensory evoked potentials.
The most used stimulation montage is C1/C2. Bottom:
insert, cork screw electrode, enlarged with a scale in mm.
and low impedance below 1 kO (Journee et al.,
2004). Alternatively, EEG needle electrodes may be
used. We do not recommend the use of EEG cup
electrodes fixed with collodium because they are
impractical and their placement is time consuming.
The only exception is for young children in whom
the fontanel still exists. Since the CS electrodes can
penetrate the fontanel during placement, the use of
EEG cup electrodes is preferable.
The brain depth where electrical current activates
CT depends on a few factors: (a) the type of stimu-
lation, whether TES or direct cortical stimulation
(DCS), (b) the intensity of the applied current, and
(c) the position of stimulating electrodes. A very
strong current applied transcranially can penetrate
deep into the brain to the brainstem (Rothwell
et al., 1994). This is not the case after direct stimula-
tion of the brain because less current is required
to activate CT (usually not more than 25 mA).
In Fig. 3, graphic presentations of different ways of
MOTOR EVOKED POTENTIALS 237

Fig. 3. Top left: current flow during TES and direct brain stimulation via grid electrode are presented schematically. During
strong TES, current penetrates deep in the brain, activating both CTs. During direct brain stimulation, using a grid electrode
current flow is restricted to a single corticospinal tract if one uses low current intensity and activates only restricted moto-
neuron pools from selective cortical areas (upper or lower extremities depending on the position of the stimulating elec-
trode). Top right: difference in amplitude and latencies of the D-waves record epidurally over the upper thoracic spinal
cord in a patient undergoing surgery for a spinal cord tumor. Note the 1.9 ms difference between latencies of the
D-waves when elicited with low intensity of current and stimulating montage C1/C2 versus high intensity of current and
montage C3/C4. Note the higher amplitude of the D-wave when more axons of the CT are recruited and current penetrates
deep in the brain (C3/C4 montage and 240 mA stimulating current). Bottom: D- and I-waves recorded after single electrical
stimulus delivered transcranially (Cz anode/6 cm anterior cathode) in a 14-year-old patient with idiopathic scoliosis. As a
result of increasing the intensity of the stimulus, the electrical current activates the CT deeper within the brain and the
latency of the D-wave becomes shorter. As current becomes stronger, more I-waves are induced (100% corresponds to
750 V of stimulator output). Note that at the bottom, the three traces of D-waves have a double peak as a result of CT acti-
vation at different depths within the brain. (Modified from Deletis, 2002 with permission from Elsevier.)

stimulating CT at the different depths of the brain are

shown.
16.2.2. Methodologies for recording MEPs
There are essentially two intraoperative methods that
give us fast feedback (practically “online”) on the
functional integrity of the CT’s fast neurons: (1) elicit-
ing D- and I-waves using a single pulse stimulation,
either transcranially (TES) or over the exposed motor
cortex, while recording them from the epi(sub)dural
space of the spinal cord, and (2) eliciting muscle MEPs
after TES or direct multipulse electrical stimulation
of the motor cortex and recording them from limb
muscles.
16.2.3. Recording of the D- and I-waves from
epi- or subdural space of the spinal cord
This method is a direct clinical application of Patton
and Amassian’s discovery in the 1950s, in which the
electrically stimulated motor cortex in monkeys
generated a series of well-synchronized descending
volleys in the pyramidal tract (Patton and Amassian,
1954). The first conducted volley through fast neu-
rons of CT (FNCT), following transsynaptic (indirect
or I-wave) volley, represents asynaptic activation of
the CT (direct or D-wave). This knowledge of CT
neurophysiology, collected in primates, can in most
cases be applied to humans. Boyd et al. (1986)
238
obtained the first recordings of the D-wave in
humans. This particular method of IOM of the CT
began to be employed during spine, spinal cord, and
brain surgery. We must be aware that even small
methodological details of recording D-waves are of
the utmost importance and should be followed in
order to achieve reliable results.
The recording catheter electrode we used was a
JX-330 (Arrow International, Reading, PA) because
of its optimal distance of 18 mm between each of
its three recording cylinders and optimal recording
surface of 12.3 mm2 (Fig. 4). For practical purposes,
any recording electrode designed for this purpose
would be appropriate and good recording can be
obtained. In our design, we optimized features of
recording electrodes, including a semirigid feature
for easy penetration in epi(sub)dural space. This elec-
trode also has a double lumen with the ability to
inject saline in order to improve contact of electrodes
and surrounding tissue when the electrode is placed
percutaneously. Most epidural electrodes are dispos-
able. If one uses a nondisposable type, extreme care
should be taken to insure the electrode is clean before
sterilization to improve its electrical properties. To
clean the electrode, we recommend one of the follow-
ing procedures: immerse the electrode contacts in
saline and pass a 9 V DC current (regardless of polar-
ity) through it until a bubble of gas cleans the contact
Fig. 4. Semirigid catheter electrode for recording MEPs
(D-wave) from the spinal cord, either epi- or subdurally;
the electrode passed through a 14-gauge Touhy needle
for percutaneous placement in the epidural space. To the
left (enlarged) are two openings marked with asterisks for
flushing the three cylindrical recording contacts (1, 2, and
3) through the injection site (top, right). The same electrode
can be placed in open surgical field, after laminectomy,
without the need for a Touhy needle. (Modified from
Deletis, 2002 with permission from Elsevier.)
V. DELETIS AND F. SALA
surface for a period of a few minutes, or use an ultra-
sound cleaner (Branson 1210, Branson Ultrasonics
Corporation, Danbury, CT) and submerse the elec-
trode in the cleaner for 5 min. Both techniques will
remove any film or biological material remaining on
the contact surfaces, and decrease their impedance.
This maneuver will diminish the stimulus artifact,
which usually appears when contact surfaces have
high impedance. Because of the short latency of the
D-wave, a large stimulus artifact in an uncleaned elec-
trode can pose an insurmountable obstacle for D-wave
recording. As it was presented in Fig. 1, during moni-
toring of the D-wave in patients with spinal cord
pathology, two catheter electrodes should be placed
at the caudal and rostral edge of laminectomy. The ros-
tral electrode is the controlled electrode for nonsurgi-
cally induced changes in the D-wave, while the
caudal electrode monitors surgically induced changes
to the CT. The amplitude of the D-wave recorded over
the cervical spinal cord can be 60 mV or more, while
over the thoracic segments it may only be 10 mV. With
a stimulating rate of 2 Hz, it takes 2–4 averaged
responses to get a reliable D-wave. This results in an
update every second. Unfortunately, the maximal
stimulating rate in most of the commercially available
TES stimulators is 1 Hz.
The strong electric stimulus applied over C1/C2
points activates both CTs; therefore, the D-wave
represents activity from both of them. If C3 or C4
versus Cz-1 cm montage is used, the D-wave repre-
sents activity from predominantly one CT. D-wave
monitoring can be achieved in patients as young as
21 months old (Szelenyi et al., 2003).
16.2.3.1. Disadvantages of D-wave monitoring
Though there are enormous advantages in using
D-wave monitoring intraoperatively (see Section
16.5), there are also some disadvantages that must
be considered.

In about 20% of patients with intramedullary spinal
cord tumors (IMSCT), or postradiation myelopa-
thy, the D-wave was not present at the beginning
of surgery even if the muscle MEP was. These find-
ings are consistent with previous reports suggesting
that radiation therapy seriously damages conductiv-
ity in the spinal cord’s long tracts (Scisciolo et al.,
1991). This phenomenon is probably due to the
desynchronization of the D-wave (descending
activity through the CT) (Deletis and Kothbauer,
1998). Therefore, this activity cannot be recorded
MOTOR EVOKED POTENTIALS 239

Fig. 5. A: Recording of a D-wave cranially (upper trace) and caudally (lower trace) to an intramedullary spinal cord tumor
(IMSCT). Note the well synchronized D-wave cranial in contrast to the desynchronized D-wave caudal to the tumor.
B: Very small epidurally recorded MEPs caudal to a high cervical intramedullary tumor (due to extreme desynchroniza-
tion), despite large muscle MEPs recorded from a small hand muscle elicited after a short train of six stimuli were present
(to the right). (Modified from Deletis, 2002 with permission from Elsevier.)

caudally at the lesion site (tumor, myelopathy)
(Fig. 5). In this situation, when the D-wave is absent
at the beginning of surgery, the disappearance of
muscle MEPs during surgery cannot be used to
predict either permanent or transient lesions to the
motor system, primarily because in those patients,
specific information about CT is not obtainable.

Another disadvantage of the D-wave monitoring
method is that it cannot be applied caudally to the
Th 10–11 spinal cord segments during surgery.
There is a lack of fast-conducting neurons of the
CTs used to generate D-waves of amplitudes suffi-
cient for monitoring.

An article by Ulkatan et al. (2006) challenged the
use of D-wave methodology during scoliosis sur-
gery because of a high percentage of false positive
and negative data (Fig. 6). Their explanation is
that the data of the D-wave amplitude increment
(in 4 patients out of 93) or decrement (21 out of 93)
comes from a new spatial relationship between the
epidural recording catheter and spinal cord after
surgical correction of the scoliosis, without parallel
changes of muscle MEPs. Therefore, the authors
expressed concern about using the D-wave as a
method to judge the functional integrity of the
CTs during monitoring of this specific pathology
(Ulkatan et al., 2006).

According to the report by MacDonald and Janusz
(2002), simultaneous monitoring during thoracoab-
dominal aneurysm surgery of D-wave, muscle MEPs,
and somatosensory evoked potentials (SEPs)
revealed that SEPs can better detect spinal cord seg-
mental ischemia of the gray matter than D-wave can
in one patient. In other patients, however, muscle
MEPs were more sensitive to the ventral gray matter
ischemia than SEPs (MacDonald and Janusz, 2002).
240 V. DELETIS AND F. SALA

Fig. 6. Upper: proposed mechanism of the D-wave amplitude changes (schematic drawings) in relation to the spinal cord
and epidural recording catheter A: before correction of spine deformity, B: after correction of spine deformity (the spinal
cord is now in closer proximity to the ERC than before it was corrected), and C: after correction of the spine deformity
(the spinal cord is now further from the ERC than before it was corrected). Bottom: the recordings from the patient’s epi-
dural space (D-wave) and lower extremities muscles (muscle MEPs) during surgery for idiopathic scoliosis. Left bottom:
D-wave amplitude showed significant increment during correction of the scoliosis and it did not improve till the end of
the surgery. Muscle MEPs during and after correction of scoliosis showed no changes and patient did not have any motor
deficit postoperatively. (Note: muscle MEPs during correction has not been shown). Right bottom: the recordings from
another scoliotic patient. D-wave amplitude showed significant decrement during and at the end of the correction of the sco-
liosis. Muscle MEPs during and after correction of scoliosis showed no changes. CT ¼ corticospinal tract; ERC ¼ epidural
recording catheter; mMEP ¼ muscle MEP. (Modified from Ulkatan et al., 2006 with permission from the International
Federation of Clinical Neurophysiology.)

In the same report, MacDonald described false pos-
itive results of D-wave monitoring due to scalp
edema. It remains a question of interpretation
whether these results belong to the category of
real false positive data when the scalp edema can
be rectified by an increased intensity of stimulation
or the use of more lateral stimulating montage
(C3/C4) where scalp edema is less prominent.
Scalp edema can produce false positive results dur-
ing muscle MEP monitoring as well.

Another relative disadvantage of D-wave monitoring
is the percutaneous placement of the epidural elec-
trode when the epidural space is not surgically open,
which might be a burden for the anesthesiological
MOTOR EVOKED POTENTIALS
or surgical team. Some authors placed a long small-
diameter catheter subdurally a day before surgery.
According to their report, they did not have serious
complications such as bleeding, infection, etc.
(Tamaki et al., 1985, 1986).

Pronounced dural adhesion during reoperation, or
following with therapeutic irradiation of the spinal
cord, may prevent placement of epidural electrodes.
16.2.4. Recording muscle MEPs from limb muscles
Recordings of muscle MEPs could be done either
with a disposable EEG needle electrode or with sur-
face electrodes. Both give decent amplitudes of mus-
cle MEPs. The prefered muscles for monitoring the
MEPs of the upper extremities are: abductor digiti
minimi, first dorsal interosseus, abductor pollicis bre-
vis as well as flexors and extensors of the forearm.
For the lower extremities, the tibialis anterior and
abductor hallucis brevis are appropriate muscles
because of the reach of CT innervations to the spinal
a-motoneurons (Jankowska et al., 1975).
16.3. Relationship between D- and I-waves,
recorded from the spinal cord and MEPs
recorded from the limb muscles
In order to understand the mechanism of muscle
MEP generation and its behavior during different
types of surgery, it is critical to understand the gener-
ation of D- and I-waves as elements in the chain of
events preceding the generation of muscle MEPs.
The electrical stimulation of the motor cortex or sub-
cortical motor pathways activates the FNCT whose
activity can be easily recorded from an electrode
placed near the spinal cord as a synchronized activity
named D-wave (direct activation of CT) (Patton and
Amassian, 1954). If the CT fast conducting neurons
are activated indirectly through vertically oriented
neurons — which end synaptically on CT neurons
— this activation is called an I-wave (indirect activa-
tion of the CT). The synaptic connections involved in
I-wave generation, which are sensitive to anesthetics
and not very well synchronized, makes them unsuit-
able for intraoperative use.
The opposite is true for the D-wave. This is an
asynaptic activity of the CT (“neurogram of the
CT”). Stimulation of the CT occurs intracranially dis-
tal to the cortical motoneuron body. Recording is
done caudal to the surgical site, but above the synapses
241
of the CT with the a-motoneuron. Since no synapses
are involved between the stimulating site and the
recording site, the D-wave is very stable and reliable.
Therefore, we consider it the “gold standard” for mea-
suring the functional integrity of the CT.
Generation of muscle MEPs during anesthesia
depends on the excitability of the a-motoneurons in
the anterior horns. Muscle MEPs can be generated
only if the resting potential of a-motoneurons reaches
the firing threshold, and thus, transmits this activity
via motor axons of the peripheral nerves and neuro-
muscular junctions to the muscle.
A very critical element in the chains of events
after stimulation of the CT is the constantly changing
excitability of a-motoneurons, which is influenced by
the depth of anesthesia. A critical depolarization
of the a-motoneurons can be achieved by D-
and I-waves, by multiple D-waves (in the case of
multipulse stimulating technique, where multiple
D-waves are generated), or a combination of the
two. I-waves have an amplitude three times higher
than what is actually recorded via epidural elec-
trodes. Their actual amplitude can be confirmed in
“killed end recordings” (Amassian and Deletis,
1999). Furthermore, even relatively light changes in
the anesthetic regimen might influence the genera-
tion of muscle MEPs by changing the amount of
I-waves in the descending drive impinging a-moto-
neurons. Multiple D-waves, generated by multipulse
stimulation techniques, represent a very efficient
solution for successfully eliciting muscle MEPs
because the firing threshold of a-motoneurons can
be reached either by a combination of the D- and
I-waves or by multiple D-waves.
16.3.1. Facilitation of the D-wave
Our previous work (Rodi et al., 1996) described
another neurophysiological phenomenon related to
the train stimulation technique. When three or more
electrical stimuli were applied to the motor cortex
during relatively light anesthesia, they not only elic-
ited a matching number of D-waves, but also addi-
tional I-waves (Fig. 7A). We believe that these
additional I-waves are generated by facilitating the
effect of multiple stimuli on the corticomotoneuronal
synapses within the motor cortex. We termed this
phenomenon “facilitation of I-waves.” These epidu-
rally recorded I-waves do not disappear after a mus-
cle relaxant is administered, the facilitation of
I-waves is an important contributing factor in the
242 V. DELETIS AND F. SALA

Fig. 7. The relationship between the number of transcranial electrical stimuli, ISI and the generation of D- and I-waves and
tibialis anterior (TA) muscle MEPs. A: Single and double stimuli applied transcranially elicit one and two D-waves only,
respectively. Three and four stimuli elicit three and four D-waves, respectively at a reduced amplitude with additional
I-waves and no muscle MEPs until a fifth stimulus is added. B: Increasing the ISI to 4 ms markedly increases the efficacy
of the stimuli in eliciting a TA response associated with the complete recovery of the D-wave amplitude at an ISI of 4 ms.
Train of five stimuli are needed with an ISI of 2 ms in order to elicit muscle MEPs in the tibial anterior muscle (A,5), while
with an ISI of 4 ms only three stimuli are needed to elicit muscle MEPs in the tibial anterior muscle (B,3). D ¼ D-wave;
I ¼ I-wave; PM ¼ paraspinal muscle artifact. (Reprinted from Deletis et al., 2001b with permission from the International
Federation of Clinical Neurophysiology.)

generation of additional descending volleys that end
on the spinal a-motoneuron. It is the number of
volleys arriving to the a-motoneuron, regardless of
identity as D- or I-waves that is essential for bringing
it above the firing threshold (Deletis et al., 2001b).
16.3.2. Recovery time of the D-wave
There is a frequency limit for the transmission of
descending volleys through the CT axons to the
a-motoneurons. This limitation can be easily tested
by applying two identical electrical stimuli transcra-
nially with different interstimulus intervals (ISIs).
This test can show the recovery time of the second
D-wave response. Using this paradigm (conditioning
and test stimuli), a D-wave recovery curve can be
plotted relative to the amplitude and latency of the
second D-wave. We show that the optimal ISI for
the complete recovery of the second D-wave ampli-
tude and latency is around 4 ms using stimulus dura-
tion of 500 ms of moderate intensity (Deletis et al.,
2001a). While with high stimulus intensity, complete
recovery happened even with ISI of 2 ms (Novak
et al., 2004). Because the a-motoneurons are opti-
mally bombarded, when the train of equal stimuli
elicits D-waves of equal amplitudes, the optimal ISI
for muscle activation is expected to be 4 ms. Fig. 7
indicates that with an ISI of 4 ms, three stimuli are
sufficient to elicit muscle MEPs due to the complete
recovery of each consecutive D-wave. Comparatively,
using the identical stimulus intensity but decreasing
the ISI to 2 ms, five stimuli are needed to elicit muscle
MEPs which are of even smaller amplitude. This is due
to the incomplete recovery of the amplitude of each
MOTOR EVOKED POTENTIALS 243

consecutive D-wave. This rule applies only if a single
stimulus elicits a single D-wave.
16.3.3. Number of D- and I-waves
As previously stated, to allow for complete recovery
of the D-wave, the ISI in the multipulse train should
be 4 ms when using moderate intensity stimuli.
In situations where a single stimulus generates more
than a single D-wave, the optimal ISI should be set
long enough to allow the entire set of D- and
I-waves to recover. In turn, this will allow the next
set of D- and I-waves to fully develop. Therefore,
the second stimulus can generate the same pattern
of D- and I-waves (Fig. 8). Otherwise, the second
set of D- and I-waves could fall into the CT axon
refractory period resulting from the first set. This is
the case in Fig. 8A where a single stimulus generates
a single D- and multiple I-waves. In this case, only
two stimuli 8 ms apart are necessary to generate mus-
cle MEPs (8D). If the ISI is shorter (e.g., 4.1 ms,
Fig. 8B), partial cancellation of D- and I-waves elic-
ited by a second stimulus will occur. Consequently,
the total number of D- and I-waves will be insuffi-
cient to bring a-motoneurons to firing level and mus-
cle MEPs will not be generated. This mechanism
could be important in a lightly anesthetized patient
as well as in patients with idiopathic scoliosis where
a single stimulus generates multiple I-waves.
16.3.4. “Build up” phenomenon
If the multipulse technique (in a nondeeply anesthetized
patient) with a repetition rate of 1 or 2 trains/s is per-
formed, each consecutive muscle MEPs will have an
increased amplitude. In cases where the intensity of sti-
muli is just slightly above the threshold, the first few
trains will not generate muscle MEPs at all. At the same
time, the D-wave amplitudes will remain the same. This
phenomenon is called “build up” and is due most likely
to the activation of another system in generating of mus-
cle MEPs than the FNCT.

Fig. 8. A: In this patient, a single stimulus delivered over the exposed motor hand area elicits a single D-wave and multiple
I-waves. The ISI should be long enough to prevent the second set of D and I, elicited by a second stimulus, from falling into
the CT axon refractory period resulting from the previous waves (as is the case in trace (B). When the ISI is 5.9 ms (C) and
8 ms (D), this will not occur, resulting in a sufficient numbers of D- and I-waves to elicit MEPs. The stimulus is marked by
arrow and D-wave by asterisk. (Reprinted from Deletis et al., 2001b with permission from the International Federation of
Clinical Neurophysiology.)
244 V. DELETIS AND F. SALA

Fig. 9. Shows mapping of the CT by D-wave collision technique (see text for explanation). S1 ¼ transcranial electrical
stimulation (TES); S2 ¼ spinal cord electrical stimulation; D1 ¼ control D-wave (TES only); D2 ¼ D-wave after combined
stimulation of the brain and spinal cord; R ¼ the cranial and caudal electrodes for recording the D-wave in the spinal epi-
dural space. Below left: negative mapping results (D1 ¼ D2). Below right: positive mapping results (D2 wave amplitude
significantly diminished after collision). Insert: hand held stimulating probe over the exposed spinal cord. (Modified from
Deletis and De Camargo, 2001.)

16.4. The D-wave collision technique
This is a novel technique that involves simultaneous
TES of the motor cortex with concurrent stimulation
of the CT from the surgically exposed spinal cord
caudal to a lesion site (Fig. 9)
This newly developed technique has allowed us to:
(a) intraoperatively map the anatomical position of the
CT within the surgically exposed spinal cord and (b)
semiquantitatively determine the number of unaffected,
desynchronized, and blocked (nonconducting) FNCT.
16.4.1. Mapping of CT intraoperatively
The application of the D-wave collision technique
has allowed us to find the anatomical position of
the CT within the surgically exposed spinal cord.
In 18 patients undergoing surgery for thoracic
IMSCTs, we elicited D-waves by TES and recorded
them cranially and caudally in relation to the spinal
cord tumor. Simultaneous with TES, we stimulated
the surgically exposed spinal cord (caudal to the tumor
site) with a miniature bipolar hand held probe
(#5522.010 INOMED, GmbH, Germany). The tips of
the probe were 1 mm apart and delivered constant cur-
rent stimuli up to 2.5 mA in intensity, 0.5 ms in dura-
tion, and 1 Hz as the repetition rate. Whenever the
stimulating probe was in a close proximity to the
CT, the D-wave elicited by TES collided with the
“anti-D-wave” elicited by the spinal cord stimulation.
This collision resulted in the diminished amplitude
of the D-wave recorded cranially to the lesion (see
Fig. 9) (Deletis and De Camargo, 2001).
Preliminary experience with this method indicates
an impressive ability to selectively map the spinal
cord for the CT. Using this method, the CT can be
localized within 1 mm. This is in concordance with
the other CT mapping techniques, which show the
same degree of selectivity and can be used to stimu-
late cranial nerves and motor nuclei within the brain-
stem (Deletis et al., 2000).
16.4.2. Calculations on the number of fast
neurons in the CT
Using the D-wave collision technique one can semi-
quantitatively determine the number of unaffected,
desynchronized, and blocked (nonconducting) FNCT,
Fig. 10.
Pathology of the spinal cord may affect FNCT in
different ways: some of the fibers passing through
the lesion site may not be affected at all while some
of them may become desynchronized. Therefore, each
fiber may conduct D- and I-waves with a different
MOTOR EVOKED POTENTIALS 245

Fig. 10. Schematic of semiquantitative calculation of unaffected, desynchronized, and blocked fast CTs neurons (see text
for explanations). S1 ¼ transcranial electrical stimulation; S2 ¼ stimulation of the spinal cord caudal to the lesion site;
R1 ¼ recording of the D-wave cranial to the spinal cord lesion; R2 ¼ recording of the D-wave caudal to the spinal cord
lesion. (Modified from Deletis, 2006 with permission from the International Federation of Clinical Neurophysiology.)

conduction velocity. The third group of FNCT
becomes blocked by the lesion and is nonfunctional
and nonconducting (Fig. 10A). D-waves from unaf-
fected FNCT can be easily recorded caudally to the spi-
nal cord lesion while other waves from desynchronized
or blocked FNCT cannot be recorded. However, even
desynchronized FNCT can elicit muscle MEPs
(Fig. 5) indicating that these fibers remain functional.
Before collision takes place (TES alone) (Fig. 10B)
the amplitude of the D-wave recorded cranially to the
lesion semiquantitatively represents the total amount
of FNCT approaching the lesion. The amplitude of
the D-wave recorded caudally to the lesion represents
the amount of unaffected axons of the FNCT trans-
verse lesion. The amplitude difference between the
cranial (R1) and caudal (R2) D-waves represents the
total amount of blocked þ desynchronized FNCT
which does not contribute to the D-wave amplitude
caudal to the lesion and thus is not recorded.
After collision takes place (TES together with spi-
nal cord stimulation) (Fig. 10C), the amplitude of the
cranially recorded D-wave (R1) represents the
amount of blocked (nonconducting) FNCT since
stimulation of the spinal cord caudal to the lesion
activates both unaffected and desynchronized FNCT,
but not blocked fibers since they can not conduct
through the lesion. Activation of desynchronized
and unaffected fibers by caudal stimulation of the
spinal cord produces a volley that travels as an
“anti-D-wave” moving antidromically. This wave
collides with the descending D-wave elicited by
TES and diminishes its amplitude.
By subtracting the D-wave amplitude difference
in Fig. 10B (R1–R2) from the D-wave amplitude in
Fig. 10C (R1) one can semiquantitatively determine
the amount of desynchronized but still function-
ing FNCT: [(nonconducting þ desynchronized)] –
nonconducting ¼ desynchronized.
246 V. DELETIS AND F. SALA

Furthermore, the D-wave collision technique can
be successfully employed to intraoperatively evalu-
ate the exact levels and extension of the spinal cord
lesion, while determining the upper level of the last
nonaffected segment of the spinal cord (see Fig. 11).
A collision with diminution of the D-wave, recorded
cranially, but not caudally, can be obtained only with
the stimulation of spinal cord CTs up to the lesion
level. The technique can be judged against “killed
end potential” recordings of the D-wave as it
was performed in the same paraplegic patient
(Fig. 11).
16.5. Importance of simultaneous intraoperative
recordings of the D- and I-waves and muscle
MEPs for the preservation of the functional
integrity of the motor tracts
The importance of using combined methodologies to
intraoperatively monitor the functional integrity of
the motor system is

to prevent intraoperatively induced neurological
injury to the motor system

to predict transient paraplegia and differentiate it
from permanent paraplegia

Fig. 11. Upper: 12-year-old boy undergoing surgery for intramedullary anaplastic astrocytoma after having been paraplegic
for 4 days prior to surgery. D-wave collision technique has been used to depict the exact level of nonfunctioning CTs. Note
the decrement of the D-wave at the nonaffected left and right CT (marked with an asterisk). The collision could not be
obtained caudally to the level of injury (market with a dot). Lower: the identical level of injured CTs corresponds with
the appearance of “injury potential” (marked with an asterisk).
MOTOR EVOKED POTENTIALS

to better understand the mechanism of injury

to document the exact moment of injury

to use monitoring records as a significant educa-
tional tool
Combining muscle MEPs and D-wave monitor-
ing is extremely important in IMSCT surgeries
because of the risk of selectively injuring the CT
and consequently inducing a permanent motor def-
icit. Monitoring muscle MEPs only may suffice for
spine surgery because injury to the cord is expected
to be diffused and not selectively limited to the CT
or other descending motor systems. Therefore, in
spine surgery, mMEP monitoring would likely
reflect an injury to the CT. Nevertheless, we very
much encourage monitoring the functional integ-
rity of the motor system using both methods when-
ever possible except for IMSCT surgeries when we
consider necessary.
Figure 12 illustrates an example of intraoperative
neurophysiological criterion for transient paraplegia
(disappearance of muscle MEPs from the lower
extremities, with preserved 50% amplitude of the
D-wave at the end of surgery). Surgeons respecting
this criterion will continue with the surgery despite
the disappearance of muscle MEPs, thus achieving
the surgical goal of gross total IMSCT resection. This
is a critical during resection of spinal cord epen-
dymomas because complete resections result in com-
plete recoveries.
Table 1 was based on the combined techniques
of the D-wave and muscle MEPs monitoring, and
on the postoperative motor outcome of 93 patients
who underwent surgery for IMSCTs (Kothbauer
et al., 1998). During this type of surgery, muscle
MEPs usually disappear before any significant
change is recorded in the D-wave. The loss of mus-
cle MEPs alerts the surgeon to use caution, but also
offers a window of opportunity to proceed with the
surgery until the D-wave declines to 50% of its
baseline, at which time, the decision must be made
to aggressively remove the tumor or not. Using a
50% drop in the D-wave as the criterion to halt
the surgery, not one single patient of the 93 had a
permanent motor deficit 38% had transient motor
deficits that were predicted by the loss of muscle
MEPs.
When injury to the nervous system happens
intraoperatively, it is very important to document
the exact time of injury along with all the circum-
stances surrounding this event. We have introduced
247
Fig. 12. Muscle MEPs recorded from right and left TA
muscle (left) and D-wave recorded epidurally over the lower
cervical spinal cord (right). During surgery for a Th4–Th6
ependymoma, we observed the progressive loss of the left
(time 14:55) and right (time 15:38) tibialis anterior muscles
(left panel). Meanwhile, the D-wave amplitude decreased
by 30% of its initial value and surgery was not stopped.
However, at 16:00, when the attempt was made to remove
the last piece of tumor adherent to the left anterolateral cor-
ticospinal tract, we observed a dramatic drop of D-wave
amplitude and surgery was transiently stopped. Corrective
measures were taken and total tumor removal was finally
achieved 20 min later more or less when the D-wave ampli-
tude recovered to 7.90 mV. At finishing, D-wave amplitude
had recovered and it was 11.32 mV (86% of its opening
baseline amplitude). This neurophysiological data indicates
postoperative transient paraplegia. The patient completely
recovered within a week. (Reprinted from Sala et al., 2004
with permission from Springer, New York.)
a method of simultaneously recording the video
stream from the operating microscope together with
the neurophysiological data. The postfact analysis
using frame by frame as presented in Fig. 13, shows
the usefulness of this method. Today’s modern
Table 1
Principles of motor evoked potential (MEP) interpreta-
tion (from Deletis, 1999)
D-wave Muscle MEP a Motor status
Unchanged or Preserved Unchanged
30–50% decrease
Unchanged or Lost uni- or Transient
30–50% decrease bilaterally motor deficit
>50% decrease Lost bilaterally Long-term
motor deficit
a
In the tibialis anterior muscle(s).
248
Fig. 13. Three consecutive frames from the composite video
taken during surgery for intramedullary spinal cord tumor are
shown (starting from the top to the bottom). Each frame con-
sists of an upper part with an image from the operative micro-
scope and a lower part with continuous recordings of MEPs
from the right and left tibialis anterior muscles (R.TA, L.
TA), as well as the right and left abductor hallucis muscles
(R.AHB, L.AHB). In the first frame, the surgeon had just
started to take the part of the tumor adherent to the lateral (left)
side of the tumor cavity using an ultrasonic aspirator. In the
second and third frames, the exact moment is shown when
the surgeon’s actions damages the spinal cord resulting in
the loss of the left tibialis anterior muscle MEPs. Fortunately,
the D-wave, which had been simultaneously recorded,
remained stable (not shown). Disappearance of MEPs in one
leg with preserved D-wave postoperatively resulted in tran-
sient left leg monoplegia. The patient recovered completely
in two weeks (see also Table 1). Arrow in each frame indicates
tip of ultrasonic aspirator probe.
V. DELETIS AND F. SALA
technology enables us to simultaneously record on
DVD or similar electronic media a composite video
consisting of a video stream from the operating
microscope, neurophysiological traces, and anesthe-
siological data. These comprehensive recordings are
very useful for solving previously unresolved events
occurring during (neuro) surgical procedures. The
use of frame by frame off-line analysis via composite
video recordings, used in the detection of the exact
moment of surgically induced injury to the spinal
cord, is presented in Fig. 13.
16.6. Transient paraplegia and its clinical
significance
The disappearance of D-wave during surgery of IMSCT
is a neurophysiological marker for plegia. The illustra-
tion in Fig. 14 shows the importance of the D-wave
monitoring and its predictor value. Fortunately, the
D-wave usually does not suddenly disappear but
gradually, giving the surgeon the opportunity to
modify his strategy before the injury becomes irrevers-
ible. The only exception (sudden and irreversible disap-
pearance of the D-wave) is likely related to a vascular
insult that can occur between the spinal cord and the
tumor in the vascular territory of the anterior spinal
artery if bipolar coagulation is used on the ventral cleav-
age plane.
A clinical phenomenon that we observe more
commonly is the so-called “transient paraplegia.”
The definition of “transient paraplegia” came into
our practice with consistent observation of patients
operated on for IMSCT acquiring severe motor defi-
cits (not always necessarily a “plegia”) and then
invariably recovering a few days or weeks after sur-
gery. These patients peculiarity presented the loss
of one or more mMEPs from the involved limbs intra-
operatively but preservated a D-wave above the 50%
of its baseline amplitude.
These patients are likely those in whom IOM
prevented an irreversible injury to the spinal cord.
One possible explanation (Deletis and Kothbauer,
1998) is that, unlike from the D-wave, muscle
MEPs are generated by the combined action of
CT neurons as well as those of the propriospinal
and other descending tracts within the spinal cord.
Lesioning this non-CT supportive motor system
can result in early postoperative transient motor
deficits, but, in the long term, will be functionally
compensated for by the CTs. This group of patients
with reversible motor deficit is likely the one that
MOTOR EVOKED POTENTIALS 249

Fig. 14. Left: stable D-wave through an intramedulary spinal cord tumor removal. The presence of epidural MEPs at the end
of the procedure predicts a long-term preserved motor function postoperatively. Right: rapid loss of D-wave during intrame-
dullary spinal cord tumor removal. In this instance, the patient became permanently quadriplegic after surgery. (Modified from
Morota et al., 1997 with permission from Lippincott Williams and Wilkins.)

may account for the benefits of IOM in IMSCT
surgery. As suggested by our recent clinical experi-
ences (Sala et al., 2006), it seems that the benefit of
IOM becomes evident only a few months after surgery
for IMSCT, while early neurological outcomes
are similar in monitored and nonmonitored patients.
These clinical data likely reflect the “transient para-
plegia” phenomenon. Monitored patients, where the
D-wave has been preserved at the end of the procedure,
retain the potentiality for clinical recovery. Accord-
ingly, we have learned that the preservation of the
D-wave represents a very strong prognostic indicator
of a good long-term motor outcome and we are not
aware, so far, of a single exception to this rule.
16.7. Conclusion
Intraoperative neurophysiology of the spinal cord
motor pathways has dramatically evolved over the past
decade, offering unique opportunities in applying basic
neurophysiological principles of the spinal cord to clin-
ical practice. Through IOM, we have learned some of
the neurophysiological mechanisms behind the changes
in the postoperative neurological outcome of patients
operated on the spine or with spinal cord pathologies.
Similarly, clinical importance of the “transient para-
plegia” phenomenon has provided new insights into
the basic pathophysiology of the spinal cord.
Future goals should include the possibility to
quantify D-waves and gather semiquantitative infor-
mation about fast conducting neurons in each CTs.
Furthermore, we should critically evaluate the roles
of more quantitative muscle MEP criteria (based
on threshold, amplitude, and waveform) for spinal
procedures other than IMSCT surgery.
Neurophysiological criteria to warn the surgeon
to take corrective measures, prevent neurological defi-
cits, and predict the prognosis have been well established
for spine and spinal cord surgery. In contrast, such
criteria are far less standardized for MEP monitoring
during brain surgery involving motor areas (Neuloh
et al., 2004). One of the limitations in this field is the
existence of only one anecdotal report of D-wave record-
ings during these procedures (Yamamoto et al., 2004),
which mean that data on specific CT recording is very
scarce. Reaching the same level of reliability for MEPs
for brain surgery as we have already achieved for spinal
cord surgery will be a challenge for future research.
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