You are on page 1of 8

INVITED REVIEW

Montages for Invasive Monitoring


Allyson A. Pickard and Christopher T. Skidmore
Department of Neurology, Jefferson Comprehensive Epilepsy Center at Thomas Jefferson University, Philadelphia, Pennsylvania, U.S.A.

Summary: Invasive EEG monitoring using subdural strip and strategies for organizing, displaying, and interpreting
Downloaded from https://journals.lww.com/clinicalneurophys by B1Ie3HEQKAu4++vUm0n3PPzFMFn++jJfAokdNkSyraMOE7ERYDQ5z2nCP6475DtV3gjwXlZw1OeRoLrqDsuE/DpTYrhYAW6YcVjnsGMp+H7v5+7SJoJ7JFkbVVa+gG6LgV75QOaIj3Y= on 06/18/2020

grid electrodes or stereo electrodes is a valuable tool in intracranial EEG.


the evaluation of some patients before epilepsy surgery. Key Words: Intracranial EEG, Invasive EEG, Stereo EEG, Subdural
Although each patient will receive a custom montage for grid, Subdural strip, Montage.
data interpretation, an organized and consistent approach
within an institution is necessary. This article will discuss (J Clin Neurophysiol 2019;36: 337–344)

S ubdural strip and grid electrodes were the predominant


intracranial EEG implantation technique performed in the
United States until recently, whereas stereo EEG (sEEG) was
posterior grid may be named RBG, for example. Should two
electrodes be present in the same anatomic structure, an additional
designator is used and named from most anterior to most posterior.
more commonly used in Europe. Over the last 10 years, the For example, if two electrodes are located in the left subtemporal
number of epilepsy centers in the United States performing sEEG region, the more anterior electrode would be named LSTA and the
has grown. Regardless of the technique used, intracranial EEG more posterior would be named LSTB, as in Fig. 1.
implantation is tailored to the individual patient, and while there In the case of sEEG, the location of the terminal deep
are standard areas implanted for study, there is no standard contact is used for anatomic naming of the electrode with the
montage. Each patient has a custom montage made to reflect the understanding that the remaining contacts typically traverse other
relevant areas of investigation that have been implanted based on grey and white matter structures. A detailed understanding of the
clinical and radiographic data. It must be considered whether to anatomic structures through which these electrodes traverse is
use a bipolar or reference montage, whether to include critical for proper EEG interpretation, described further below. In
extracranial electrodes, and how to arrange the many channels our institution, we use the sEEG labels that were developed by
for review. our European colleagues, as shown in Table 2.
Subdural strip and grid electrodes have contacts that are
arranged in a bed of silicone in one or several rows with an
interelectrode distance of 1 cm.1 Individual contacts are numer-
ELECTRODE AND CONTACT NAMING ically labeled by the electrode manufacturer and may vary
Naming of the electrodes should be consistent within an between manufacturers beyond a 1 · 8 strip. Contact number
institution to allow for clarity in interpretation and should always one is typically in the column furthest from the electrode wires
be included in the final video EEG monitoring report to permit though its orientation with respect to the outgoing wires may
other institutions to review the data if needed. Subdural strip, vary. The contacts are numbered along the row approaching the
subdural grid, and sEEG electrodes are named based on their side of the wire tail. When moving to the next row, the
anatomic localization. For subdural strip and grid electrodes, three- numbering begins again at the contact furthest from the wire,
to four-letter labels are suggested, with the first letter reserved for see Fig. 1 for an example. These numerical labels, however, are
hemisphere (L for left or R for right) and the second two to three not radiopaque and care to properly reorient the contacts in
for the anatomic structure (AT for anterior temporal, ST for relation to the wire tail must be taken when reviewing head
subtemporal, IH for interhemispheric, SMA for supplementary imaging such as a postoperative skull x-ray or computed
motor area, and so forth). An example of subdural grid locations tomography scan (Fig. 2) to ensure a proper orientation.
and names that we use at our institution is provided in Table 1 and Stereo-EEG electrodes typically have 4 to 18 electrodes
Fig. 1. Subdural grid electrodes that cover a much larger area of arranged 2 to 10 mm apart.1 By convention, the contact furthest
cortex and typically multiple lobes are given a single-letter from the wire tail, which is also the most distal from the insertion
designation (A, B, C, etc) based on their anterior to posterior point, is numbered first. See Table 3 for an example of a bilateral
location with respect to one another, with “A” being the most temporal and orbitofrontal implant. Individual electrode contact
anterior. Occasionally, a hemispheric designator is placed in front numbers are then added to the electrode label with a hyphen and
of the grid name and/or a “G” is added at the end to designate the combined on the final montage. For example, a left amygdalar
electrode as a grid, both used as is clinically relevant. A large right electrode would have its individual contacts named LA-1, LA-2,
LA-3, and so forth.
The authors have no funding or conflicts of interest to disclose.
Address correspondence and reprint requests to Christopher T. Skidmore, MD,
Department of Neurology, Thomas Jefferson University, 901 Walnut St, 4th
Floor, Philadelphia, PA 19107, U.S.A.; e-mail: christopher.skidmore@
jefferson.edu. ADDITIONAL ELECTRODES
Copyright  2019 by the American Clinical Neurophysiology Society
ISSN: 0736-0258/19/3605-0337 The use of simultaneous scalp and intracranial EEG record-
DOI 10.1097/WNP.0000000000000619 ings is not routinely performed at all epilepsy centers; however, it

clinicalneurophys.com Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 337

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
A. A. Pickard and C. T. Skidmore Montages for Invasive Monitoring

TABLE 1. Common Electrode Labels (Fig. 1) TABLE 2. Common sEEG Electrode Labels
LFG: left frontal grid Category Label Description
LTG: left temporal grid
Mesial temporal A Amygdala
LOFA: left orbitofrontal anterior strip
B Hippocampal head
LOFB: left orbitofrontal posterior strip
C Anterior hippocampal body
LAT: left anterior temporal
D Posterior hippocampal body
LSTA: left subtemporal anterior
E Enthorinal cortex
LSTB: left subtemporal mid
Posterior temporal P Anterior basal temporal/pole
LSTC: left subtemporal posterior
Q Posterior basal temporal
Insula I Inferior insula
may have some advantages.2,3 Intracranial EEG, in particular J Superior insula
K Anterior insula
sEEG, has an inherent sampling bias because of the choice of
L Insular apex
implantation sites. The use of scalp EEG complements the Cingulate V Anterior cingulate
precise yet limited coverage of intracranial EEG by providing full U Mid-cingulate
cranio-spatial coverage. This, however, comes at a much lower T Mid-posterior cingulate
sensitivity as scalp EEG spikes are only observable with cortical S Posterior cingulate
activation of at least 10 cm2 of gyral cortex.4 Because of this, Orbitofronal OF Orbitofrontal
intracranial EEG onset should always precede scalp EEG onset. Broca’s BA Pars orbitalis
If it does not, the EEG reader should be concerned that the true BB Pars triangularis
ictal onset is not covered by the intracranial electrodes. BC Pars opercularis
Combined scalp and intracranial EEG can also help confirm Wernicke’s WA Posterior superior temporal
WB Angular gyrus
a falsely lateralized or localized scalp onset. For instance, an
WC Supramarginal gyrus
orbitofrontal seizure confirmed on intracranial EEG may appear Motor ML Leg motor
as a “temporal lobe” seizure on scalp EEG. MA Arm motor
Sensory SL Leg sensory
SA Arm sensory
SMA PA Premotor cortex
PB Posterior superior frontal gyrus
Above outlines nomenclature used throughout many European centers as well as at
our institution.
sEEG, stereo EEG.

Patients often undergo an initial presurgical workup using


scalp EEG recordings to capture seizures. It may be helpful to
add scalp recording during intracranial EEG monitoring to
confirm the seizures currently being recorded match those
captured during the presurgical workup. When scalp electrodes
are used, the conventional 10-20 or 10-10 system should be used.
However, scalp electrode locations will often need to be altered
because of the presence of the surgical incisions used for
intracranial electrode placement.
Defining clinical onset is helpful in determining that the
ictal EEG onset recorded truly represents the ictal onset zone.
For intracranial EEG, clinical onset should always be pre-
ceded by (or rarely simultaneously with) ictal onset. Clinical
onset occurring before ictal onset would suggest that an
electrode is not residing in the true ictal onset zone. Video
recording, electromyography, and electrocardiography may
FIG. 1. Lateral and inferior view of typical subdural strip and grid be used to help determine clinical onset. Subtle changes in
electrode configuration. See Table 1 for electrode label descriptions. motor behavior (detected with electromyography electrodes)
The filled black rectangles associated with each grid or strip represent
or a rapid onset of tachycardia (seen on electrocardiography)
the wire tail. This can be visualized on x-ray imaging, which permits
confirmation of the orientation of the electrodes in the brain. LAT, may precede changes in behavior that are observable clini-
left anterior temporal; LFG, left frontal grid; LOFA, left orbitofrontal cally or on video review. Video recording, like scalp EEG
anterior strip; LOFB, left orbitofrontal posterior strip; LSTA, left recordings, can also help confirm that the seizures captured on
subtemporal anterior; LSTB, left subtemporal mid; LSTC, left intracranial EEG are similar to those previously recorded or
subtemporal posterior; LTG, left temporal grid. observed clinically.

338 Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 clinicalneurophys.com

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
Montages for Invasive Monitoring A. A. Pickard and C. T. Skidmore

FIG. 2. Lateral and anteroposterior skull x-ray


demonstrating the electrodes depicted in Figure 1.

This can be used to an advantage when choosing a reference


REFERENTIAL VERSUS BIPOLAR when it is compared with the much higher amplitude cortical
A referential montage is only as useful as the quality of the electrode recordings. Stereo-EEG electrodes often have contacts
reference. The choice of an adequate, electrically silent reference that pass through white matter that had previously been thought
is therefore essential. There exist a number of options. An to be electrically neutral and therefore a good referential
earlobe or similar extracranial ground electrode may be used but, candidate. However, there is now evidence that white matter
as in scalp recordings, is subject to the same contamination by signals may be contaminated with distant gray matter signals,
electromyographic activity. Unique to sEEG are choices of possibly because of white matter fiber tracts.5 This creates an
reference in the bone or white matter.2 Stereo EEG electrodes unreliable area of reference and therefore white matter contacts
typically have contacts that reside in the white matter or within must be carefully chosen. Regardless of the reference electrode
the burr hole space of the skull (“in the bone”), or both. Both chosen, the same principles that apply to scalp electrodes apply
locations may be chosen by review of the individual contacts to intracranial electrodes, a topic covered by Dr. Kalamangalam’s
passing through these structures, usually with postoperative article in this issue.
imaging discussed later in this article. Bone has low electrical The use of a bipolar montage circumvents concern regarding
conductance and is responsible for the lower amplitude of scalp the contamination of an external reference. The potential between
recordings as it is able to resist fluctuations in electrical activity. two nearby contacts cancels contamination and electrical fluctu-
ation from a remote source that is presumed to affect each contact
equally, called common mode rejection.6 This also allows
smaller, more local activity to be highlighted. At the intracranial
TABLE 3. Example of Implanted sEEG Electrodes
level, this allows the measurement of electrical potentials across
1 LOF Left orbitofrontal 180319-093 D08-15AM areas of 1 cm2 or less, helping to increase spatial resolution and
2 LP Left temporal pole 181002-072 D08-10AM precisely define ictal onset where focal high-frequency activity is
3 LA Left amygdala 180961-033 D08-12AM seen. It is perhaps reassuring then that epileptiform activity at
4 LB Left hippocampus head 180961-040 D08-12AM ictal onset may be observed at one intracranial electrode and not
5 LC Left hippocampus body 200004-003 D08-15AM
in its contiguous contacts, at least initially.7,8 However, more
6 LQ Left temp postbasal 180961-046 D08-12AM
7 ROF Right orbitofrontal 200004-077 D08-15AM
diffuse cerebral activity, such as theta activity in the hippocam-
8 RP Right temporal pole 200001-068 D08-10AM pus, may be minimized or even lost because of common mode
9 RA Right amygdala 180961-045 D08-12AM rejection.7 This can be visualized as diffuse attenuation of the
10 RB Right hippocampus head 180972-006 D08-15AM background EEG across multiple electrical contacts. Remontag-
11 RC Right hippocampus body 180372-038 D08-15AM ing into a referential montage will confirm a diffuse clinical onset
12 RQ Right temp postbasal 180961-042 D08-12AM and highlight the actual ictal activity in these cases.
The table above names the sEEG electrodes which were implanted and the terminal
target that was selected for each. The unique serial number for each inserted electrode is
included in the second to last column. This can be seen on the extracranial portion of the
electrode and permits the EEG technician to properly identify the electrodes when
connecting the patient to an EEG machine. The last column identifies the type of CREATING THE MONTAGE
electrode implanted, with lettering and numbering determined by the manufacturer. In
this example, DIXI Medical electrodes were used. For the left orbitofrontal electrode, the When many electrodes are implanted, there are naturally
“D08” listed in D08-15AM designates that each electrode has a diameter of 0.8 mm, the many channels (128–256 or more) to be placed into the final
“15” designates 15 contacts in the electrode, and the “AM” designates constant spacing patient montage. Subdural strip and grid electrodes can often
of the contacts along the length of the electrode.
sEEG, stereo EEG. cover a large anatomic area of cortex. As such, a montage of
channels involving contiguous contacts across each row is often

clinicalneurophys.com Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 339

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
A. A. Pickard and C. T. Skidmore Montages for Invasive Monitoring

FIG. 3. A, EEG showing half of the electrodes included in the full montage. This spacing of channels permits more accurate interpretation
of the involved electrodes, but requires scrolling of the screen up and down. Note how the LTG grid is only partially displayed. B, The second
half of electrodes including the completion of grid LTG. Alternately, the computer monitor may be rotated 908 into a portrait orientation to
allow for display of more channels. Please note additional depth electrodes LA, LB, and LC are included in the full montage that are not
included in Figure 1. LTG, left temporal grid.

340 Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 clinicalneurophys.com

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
Montages for Invasive Monitoring A. A. Pickard and C. T. Skidmore

FIG. 4. A, EEG showing only the LTG. This montage is created based on the numerical order of the contacts. The black arrows represent
focal spikes. B, Now the LTG grid has been remontaged to group the temporal contacts together in the lower part of the montage. The
epileptiform discharges (black arrows) are now more obviously temporal in origin with a negative phase reversal at contact LTG-49. C, The
same epileptiform discharge is remontaged into a referential montage with the LTG contacts listed in numerical order. Contact LA-4 is
chosen for reference as it is located in white matter and found to be electrically silent. Note the epileptiform discharges (black arrows) are
again seen best at contact LTG-49. D, The same epileptiform discharges are remontaged into a referential montage with the LTG contacts
listed in anatomic order (temporal electrodes near the bottom). LTG, left temporal grid.

used. Typically, the montage will begin with the most anterior Figure 3 demonstrates the EEG montage that was initially created
electrodes and then subsequent posterior electrodes are included. for the intracranial implant depicted in Fig. 1. As you can see,

clinicalneurophys.com Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 341

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
A. A. Pickard and C. T. Skidmore Montages for Invasive Monitoring

FIG. 5. A, Bitemporal, cingulate, and orbtiofrontal sEEG implant. In this montage, the mesial temporal electrodes from the right and left
(separated by an ECG channel) were selected with removal of the other electrodes from the montage once the mesial onset pattern was
identified. This permits a more focused review of the critical electrodes. Ictal onset (black arrow) was localized to contacts LB-4 and LC-2,
which were located in the head and body of the hippocampus, respectively. B, The next EEG page demonstrates ictal spread to the
amygdala, most prominent in contact LA-1. sEEG, stereo EEG.

342 Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 clinicalneurophys.com

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
Montages for Invasive Monitoring A. A. Pickard and C. T. Skidmore

a decision was made to list the orbitofrontal electrodes first (left brain MRI using one of the many software tools available.9,10
orbitofrontal) followed by the 4 · 6 frontal lobe grid and then the This will give a visual representation of the implanted electrodes
8 · 8 grid that is covering the frontal and parietal peri-rolandic and often allows individual contacts to be selected for localiza-
cortex and the superior aspect of the left temporal grid. Often the tion. Contiguous contacts within an electrode that exist in an area
individually numbered rows of the grid are connected in a bipolar favorable for study are grouped within the montage. Then all
fashion in a linear numbered sequence, as in the montage electrodes within that same area of brain are grouped together in
channels for left frontal grid and left temporal grid in Fig. 3. the final array.
Care must be taken to avoid connecting the end contact of one
row with the first contact of the next row because this will lead to
confusing findings on the bipolar montage. Larger grids, such as
8 · 8 grids, often cover multiple lobes, and a decision needs to be VISUAL DISPLAY
made as to whether the individual contacts should be connected Once a montage has been created, there are several ways to
in a linearly numbered method as shown in Fig. 4A or instead use improve its display for high-yield interpretation. The computer
an anatomic method that groups contacts based on the lobe monitor may be rotated 908 into a portrait orientation. This allows
or region they cover. In Fig. 4B, the same 8 · 8 grid depicted in for more channels to be seen on the screen at one time with
Fig. 4A was remontaged to group the contacts over the temporal reasonable spacing between channels to permit proper visualiza-
lobe separately from the frontal and parietal groups. On initial tion and interpretation. It may also be helpful to insert a one-
review of the EEG sample displayed in Fig. 4A, there seems to channel gap between electrodes to improve visual analysis. Filter
be a spike that is widely distributed over the grid; however, in the settings are often not recommended during EEG acquisition.2 On
remontaged view in Fig. 4B, the spike is maximal in the contacts EEG review, however, the typical 60-Hz filter may be applied if
over the temporal neocortex. Creating a montage based on the a malfunctioning electrode is identified. A low-frequency filter of
anatomic location of the electrodes permits the EEG reader to 0.01 Hz may also be helpful to detect infraslow activity and
quickly differentiate the involved lobe of the cortex and aids in negative baseline shifts that may occur 1 to 10 seconds before
localization of the ictal onset zone. initial ictal EEG discharges.11,12 Choice of sampling rate
The decision to read the intracranial EEG using a bipolar or becomes important to ensure high-frequency activity such as
referential montage is a personal decision, and each method has ripples ranging from 80 to 250 Hz,13 and fast ripples greater than
its strengths and weaknesses as outlined above. In our center, we 250 Hz14 are observed. The sampling of these signals must be
review the EEG using a bipolar montage but create a referential twice the highest frequency of interest according to Shannon
montage when needed if we suspect a large generator or if we theorem.15 Therefore, a sampling rate greater than 500 Hz is ideal
need to confirm the findings noted on the bipolar montage. to capture the majority of ripples. To capture fast ripples,
Figures 4C and 4D demonstrate the same interictal spike seen in a sampling rate greater than 1,000 Hz is needed. At our
Figs. 4A and 4B but now in a referential montage to an institution, we routinely record all intracranial data at a sampling
uninvolved electrode. Figures 4C and 4D demonstrate the rate of 2,000 Hz.
numerical montage and the anatomic montage approaches,
respectively, which were previously highlighted.
Stereo-EEG electrodes reach many areas of the brain in
addition to cortex, so it must be considered whether to take an
electrode-based approach as with the subdural contacts of smaller REFERENCES
grids or to prioritize their anatomic location as with larger grids. 1. Kovac S, Vakharia VN, Scott C, Diehl B. Invasive epilepsy surgery
The anatomic model has the advantage of grouping channels in evaluation. Seizure 2017;44:125–136.
close structural proximity together for review. This lends itself to 2. Landre E, Chipaux M, Maillard M, Szurhaj W, Trebuchon A. Electro-
physiologic technical procedures. Neurophysiol Clin 2018;48:47–52.
sEEG interpretation, where a more three-dimensional map can be 3. Ramantani G, Maillard J, Koessler L. Correlation of invasive EEG and
obtained. In Figures 5A and 5B (consecutive EEG pages), there scalp EEG. Seizure 2016;41:196–200.
is a focal onset in the left hippocampus that eventually spreads to 4. Tao JX, Baldwin M, Ray A, Hawes-Ebersole S, Ebersole JS. The impact
of cerebral source area and synchrony on recording scalp electroenceph-
the left amygdala but does not involve the right side. The alography ictal patterns. Epilepsia 2007;48:2167–2176.
proximal contacts sitting in the temporal neocortex are also not 5. Mercier M, Bickel S, Megevand P, et al. Evaluation of cortical local
involved. The patient had orbitofrontal and cingulate electrodes field potential diffusion in stereotactic electro-encephalography record-
as well, but this review montage was created to highlight the ings: a glimpse on white matter signal. Neuroimage 2017;147:219–
232.
mesial temporal region. This permits the reviewer to quickly 6. Lachaux JP, Rudrauf D, Kahane P. Intracranial EEG and human brain
determine spread within the mesial temporal structures and mapping. J Physiol Paris 2003;97:613–628.
spread, if any, to the contralateral regions. 7. Zaveri HP, Duckrow RB, Spencer SS. On the use of bipolar montages
Naturally, accurate localization of electrode contacts is key for time-series analysis of intracranial electroencephalograms. Clin
Neurophysiol 2006;117:2102–2108.
to designing an anatomic-based montage. Electrode locations 8. Alarcon G, Guy CN, Binnie CD, Walker SR, Elwes RD, Polkey CE.
must first be confirmed to allow identification of cortical and Intracerebral propagation of interictal activity in partial epilepsy:
subcortical contacts and an appropriate reference to be chosen if implications for source localization. J Neurol Neurosurg Psychiatry
1994;57:435–449.
desired. There are several methods used that often include co- 9. Dalal SS, Edwards E, Kirsch HE, Barbaro NM, Knight RT, Nagarajan
registration of a preoperative brain MRI with intraoperative SS. Localization of neurosurgically implanted electrodes via photograph-
photos, skull x-ray, postoperative head CT, or postoperative MRI-radiograph coregistration. J Neurosci Methods 2008;174:106–115.

clinicalneurophys.com Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 343

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.
A. A. Pickard and C. T. Skidmore Montages for Invasive Monitoring

10. Yang AI, Wang X, Doyle WK, et al. Localization of dense intracranial 13. Worrell GA, Gardner AB, Stead SM, et al. High-frequency oscillations
electrode arrays using magnetic resonance imaging. Neuroimage in human temporal lobe: simultaneous microwire and clinical macro-
2012;63:157–165. electrode recordings. Brain 2008;131:928–937.
11. Ikeda A, Terada K, Mikunk N, et al. Subdural recording of ictal DC 14. Jacobs J, Levan P, Chatillon C, Olivier A, Dubeau F, Gotman J. High
shifts in neocortical seizures in humans. Epilepsia 1996;37:662– frequency oscillations in intracranial EEGs mark epileptogenicity rather
674. than lesion type. Brain 2009;132:1022–1037.
12. Rodin E, Modur P. Ictal intracranial infraslow EEG activity. Clin 15. Shannon C. Communication in the presence of noise. Proc Inst Radio
Neurophysiol 2008;119:2188–2200. Eng 1949;37:10–21.

344 Journal of Clinical Neurophysiology Volume 36, Number 5, September 2019 clinicalneurophys.com

Copyright © by the American Clinical Neurophysiology Society. Unauthorized reproduction of this article is prohibited.

You might also like