clinical article

Detection of third and sixth cranial nerve palsies with

a novel method for eye tracking while watching a short
film clip
Uzma Samadani, MD, PhD,1,2 Sameer Farooq,2 Robert Ritlop, MEng,2 Floyd Warren, MD,1,3
Marleen Reyes, BA,1,2 Elizabeth Lamm, BA,2,4 Anastasia Alex, BS,3 Elena Nehrbass, BS,1,2
Radek Kolecki, MS,2 Michael Jureller, BS,2 Julia Schneider,2 Agnes Chen, BA,2 Chen Shi, BS,1,2
Neil Mendhiratta, BA,1,2 Jason H. Huang, MD,5 Meng Qian, PhD,6 Roy Kwak, MD,1
Artem Mikheev, MS,7 Henry Rusinek, PhD,7 Ajax George, MD,7 Robert Fergus, PhD,4
Douglas Kondziolka, MD,2 Paul P. Huang, MD,2 and R. Theodore Smith, MD, PhD3
1
New York Harbor Health Care System, Manhattan Veteran’s Administration; Departments of 2Neurosurgery, 3Ophthalmology,
6
Psychiatry, and 7Radiology, New York University School of Medicine; 4Department of Computer Science, Courant Institute, New
York University, New York, New York; and 5Department of Neurosurgery, Scott and White Health Care, Temple, Texas

Object  Automated eye movement tracking may provide clues to nervous system function at many levels. Spatial
calibration of the eye tracking device requires the subject to have relatively intact ocular motility that implies function of
cranial nerves (CNs) III (oculomotor), IV (trochlear), and VI (abducent) and their associated nuclei, along with the multiple
regions of the brain imparting cognition and volition. The authors have developed a technique for eye tracking that uses
temporal rather than spatial calibration, enabling detection of impaired ability to move the pupil relative to normal (neuro-
logically healthy) control volunteers. This work was performed to demonstrate that this technique may detect CN palsies
related to brain compression and to provide insight into how the technique may be of value for evaluating neuropathologi-
cal conditions associated with CN palsy, such as hydrocephalus or acute mass effect.
Methods  The authors recorded subjects’ eye movements by using an Eyelink 1000 eye tracker sampling at 500 Hz over
200 seconds while the subject viewed a music video playing inside an aperture on a computer monitor. The aperture moved
in a rectangular pattern over a fixed time period. This technique was used to assess ocular motility in 157 neurologically
healthy control subjects and 12 patients with either clinical CN III or VI palsy confirmed by neuro-ophthalmological examina-
tion, or surgically treatable pathological conditions potentially impacting these nerves. The authors compared the ratio of
vertical to horizontal eye movement (height/width defined as aspect ratio) in normal and test subjects.
Results  In 157 normal controls, the aspect ratio (height/width) for the left eye had a mean value ± SD of 1.0117 ±
0.0706. For the right eye, the aspect ratio had a mean of 1.0077 ± 0.0679 in these 157 subjects. There was no difference
between sexes or ages. A patient with known CN VI palsy had a significantly increased aspect ratio (1.39), whereas 2 pa-
tients with known CN III palsy had significantly decreased ratios of 0.19 and 0.06, respectively. Three patients with surgically
treatable pathological conditions impacting CN VI, such as infratentorial mass effect or hydrocephalus, had significantly
increased ratios (1.84, 1.44, and 1.34, respectively) relative to normal controls, and 6 patients with supratentorial mass effect
had significantly decreased ratios (0.27, 0.53, 0.62, 0.45, 0.49, and 0.41, respectively). These alterations in eye tracking all
reverted to normal ranges after surgical treatment of underlying pathological conditions in these 9 neurosurgical cases.
Conclusions  This proof of concept series of cases suggests that the use of eye tracking to detect CN palsy while
the patient watches television or its equivalent represents a new capacity for this technology. It may provide a new tool
for the assessment of multiple CNS functions that can potentially be useful in the assessment of awake patients with
elevated intracranial pressure from hydrocephalus or trauma.
http://thejns.org/doi/abs/10.3171/2014.10.JNS14762
Key Words  abducent nerve; diplopia; eye movement tracking; hydrocephalus; oculomotor nerve; prepontine cistern;
diagnostic and operative techniques

Abbreviations  CN = cranial nerve; EDH = epidural hematoma; ICP = intracranial pressure; pds = prism diopters; SDH = subdural hematoma; TBI = traumatic brain
injury.
submitted  April 4, 2014.  accepted  October 27, 2014.
include when citing  Published online December 12, 2014; DOI: 10.3171/2014.10.JNS14762.
Disclosure  Dr. Samadani has intellectual property and equity in Oculogica, Inc., and Mr. Ritlop has equity in Oculogica, Inc. The aforementioned company did not con-
tribute any funding to this study and had no influence over its design or this paper’s content.

©AANS, 2014 J Neurosurg  December 12, 2014 1

U. Samadani et al.

T
he cranial nerves (CNs) are known to be suscep- Methods
tible to changes in intracranial pressure (ICP) due Subject Selection
to mass effect or hydrocephalus. Early detection of
subclinical CN palsy in awake patients thus might prove Subjects were recruited in accordance with institu-
useful for assessment of patients with hydrocephalus, pos- tional review board policy. Written informed consent was
sible shunt malfunction, or traumatic brain injury (TBI). obtained from all subjects prior to participation.
We developed a novel algorithm for eye tracking per- Control subjects were employees, volunteers, visitors,
formed while subjects watch a music video playing inside and patients at the investigating institutions. Inclusion
an aperture on a computer monitor. The aperture moves criteria for normal control subjects were as follows: age
around the monitor periphery at a known rate so that the 7–100 years; vision correctable to within 20/50 bilaterally;
position of the pupil can be analyzed at any given time intact ocular motility; and ability to provide a complete
based on the time elapsed since the start of the video. By ophthalmological, medical, and neurological history as
using elapsed time analysis, our method should be able well as medications/drugs/alcohol consumed within the
to detect impaired ability to move the pupil relative to 24 hours prior to tracking. Parents were asked to corrobo-
normal controls. Our algorithm sets the amount of time rate details of the above for children 7–17 years old. Exclu-
that the eye should be moving in any given direction es- sion criteria were history of strabismus, diplopia, palsy of
sentially constant and then quantitates the distance that it CN III, IV, or VI, papilledema, optic neuropathy, dementia
travels. Because the method does not entail spatial cali- or cognitive impairment, hydrocephalus, sarcoidosis, my-
bration, it does not compensate for impaired motility and asthenia gravis, multiple sclerosis or other demyelinating
can be used in patients who do not follow commands, disease, active or acute epilepsy, stroke/hemorrhage, or
such as those with aphasia, patients in a persistent vegeta- brain injury sufficiently significant to result in hospitaliza-
tive state, and small children. tion. Control subjects reporting any brain injury within the
The CN III is classically impacted by supratentorial week prior to recruitment for eye-tracking tests were also
mass effect, which may lead to transtentorial herniation.1 excluded.
A clinical indicator of transtentorial herniation is palsy of Patients were recruited for participation specifically be-
the oculomotor nerve due to compression by the uncus as cause they were known to have palsy of CN III or VI, or
the nerve courses along the tentorial notch after its exit mass lesions or pathological entities impacting CN III or
from the pontomesencephalic junction and prior to its en- VI. Mass lesion inclusion criteria were as follows: lesion
try into the cavernous sinus. Among other functions, the apparent on radiographic imaging, clinical necessity for
oculomotor nerve innervates the superior and inferior rec- resection, and patient able to consent to and engage in eye
ti muscles of the orbit, rotating the eyeball up and down. tracking. Exclusion criteria were the same as for normal
A CN III palsy in the context of trauma or stroke and evi- subjects, plus bilateral compression of optic nerves result-
dence of radiographic transtentorial herniation may poten- ing in decreased visual acuity, visual field deficit, sellar
tially be an indication for neurosurgical intervention.29 lesion, and cavernous sinus invasion. Subjects who under-
The abducent nerve exits the ventral pontomedullary went neurosurgery were tracked pre- and postoperatively
junction, courses through the prepontine cistern, and trav- at their convenience, as described in the case descriptions.
els through the Dorello canal into the cavernous sinus Ophthalmological examinations of neurosurgical patients
before innervating the lateral rectus muscle of the orbit, were performed as described in the individual case de-
lateralizing the pupil.26 It is known to be susceptible to scriptions. All of the surgically treated patients were ex-
myriad disorders, including ischemia, diabetes mellitus, amined by a board-certified, experienced attending neuro-
trauma, and hydrocephalus.19 surgeon familiar with standard techniques for neurological
We hypothesized that our eye-tracking algorithm would examination.
detect clinical and subclinical palsies of the abducent and Subjects who wore glasses were tracked without refrac-
oculomotor nerves. To test this hypothesis we tracked eye tion correction, whereas those who wore contact lenses
movements in 157 normal control subjects to establish a were tracked with the lenses in place. Subjects with toric
range for normal eye movement ratios with our algorithm. contact lenses were asked to remove lenses for the track-
We then compared the ratio of vertical versus horizontal ing procedure. The eyes of each of the test subjects were
eye movement for normal subjects to subjects with known tracked serially and separately; however, the visual stimu-
pathological conditions of these nerves who were recruited lus was presented binocularly.
from the ophthalmology and neurosurgery clinics. Patients
with supratentorial lesions resulting in uncal mass effect Visual Stimulus
who are assessed with this novel eye-tracking algorithm Subjects’ eye movements were recorded with an Eye-
would be expected to demonstrate decreased vertical/hori- link 1000 eye tracker (SR Research) at a distance of 55
zontal eye movement relative to normal controls. Patients cm from a computer monitor over a fixed time period
with infratentorial lesions or other pathological entities of 220 seconds. The visual stimuli were music videos
impacting CN VI would be expected to have increased including Shakira’s “Waka-Waka” (World Cup soccer
vertical/horizontal eye movement ratios. We performed tribute); K’Naan’s “Wavin’ Flag (When I Grow Older I
prospective measurement of that ratio in patients with con- will be Stronger);” Michael Jackson’s “Man in the Mir-
firmed CN III and VI palsies (positive controls) and in sta- ror;” “Hakuna Matata” (from the Lion King); and Shankar
ble, awake neurosurgical patients undergoing procedures Ehsan Loy’s “Bhumbroo.” The videos played continuous-
for supratentorial and infratentorial mass lesions. ly in a square aperture with an area 1/8 the screen size of

2 J Neurosurg  December 12, 2014

 Detection of cranial nerve palsies with eye tracking

the monitor. The aperture remained stationary at the upper the distribution of male aspect ratio and female aspect ra-
left corner of the monitor screen for the first 10 seconds, tio was statistically significantly different from 0.
then moved clockwise along the outer edges of a 17-inch–
diameter monitor for 5 complete cycles of 40 seconds each Perimesencephalic Cistern Volume
plus an extra 10 seconds at the end of the last cycle. The The actual space around CN III as it travels from the
first 10 and last 10 seconds of the full data set were dis- interpeduncular cistern at the pontomesencephalic junc-
carded to yield 200 seconds of data. Sound volume was tion to the cavernous sinus is difficult to quantify with
adjusted to the subject’s preference. great accuracy. To overcome this limitation, we assessed
preoperative CT scans for reduction in perimesencephalic
Data Analysis cistern volume relative to the maximal-volume postop-
The eye tracker sampled pupil position at 500 Hz, yield- erative scan by using established segmentation methodol-
ing 100,000 samples over 200 seconds. We created scat- ogy36 originally adapted from MRI analysis.25 To correct
terplots of the entire time series by plotting the 100,000 (x, for variable angulation of the skull on axial CT images
y) pairs representing the 2 orthogonal components of the that could be introduced by misalignment of the head be-
instantaneous angle of pupil reflection over time to cre- tween scans, we realigned and resampled each CT volume
ate “box trajectories” that reflected the cartesian location to a standard (template) coordinate system. This was done
of the pupil over time. In control subjects, these figures by marking in 3D space the left eye lens (LE), the right eye
look like boxes, reflecting the location of the aperture as lens (RE), and the junction of the superior colliculi (C). In
it moved around the screen over time (Fig. 1, left column), the template space these 3 corresponding structures—LE′
with each cycle shown in a different color (red, green, RE′ C′—were positioned symmetrically such that the prin-
cyan, magenta, blue). cipal axis of the brainstem was in the z direction (across
plane). We then computed the rigid body (volume-preserv-
Aspect Ratio ing) transformation (T) that best mapped the triangle <LE
Elapsed time quantitation enables localization of the RE C> onto the triangle <LE′ RE′ C′>. The transforma-
video aperture during measurement of eye positions. The tion T was used to resample the CT volume to the template
panels on the left side of Fig. 1 demonstrate pupil position space. The cistern was then segmented by placing a 4-cm-
as the video traverses all 4 sides of the rectangular viewing diameter cylinder centered on the center of the brainstem
monitor, with each cycle of the video shown in a different and extending vertically (head-foot direction) from pineal
color (red, green, cyan, magenta, blue). The panels on the gland to tuberculum sellae. For each voxel within the cyl-
right side show only the mean coordinates of 5 cycles as inder we computed the voxel’s partial volume (Pv) of CSF
the video traverses the top (red) or bottom (cyan) of the according to its attenuation (A) measured in Hounsfield
units (HU): Pv = (Abrain - A)/(Abrain - Awater). Here Abrain
rectangular monitor. In each particular case (e.g., normal
= 48 HU, and Awater = 0 HU. The Pv was constrained to
subject, CN VI palsy, epidural hematoma [EDH]), as the
[0–1]. The cistern volume was computed as the sum of
video traverses the top of the monitor over 10 seconds, the
Pv values within the cylinder multiplied by voxel volume,
patients’ pupils have a median value where the red dots
excluding the suprasellar cistern.
are. As the video traverses the bottom of the monitor, the
pupils have a median value where the cyan dots are. Thus,
the height of the box is calculated as the median y cartesian Radiology Analysis
coordinate during the first 10 seconds minus the median y Two experienced board-certified radiologists who were
coordinate during the third 10 seconds. The box height (h) blinded to the eye-tracking findings evaluated the preop-
was defined as the difference y2 - y1, where y2 is the me- erative CT images to assess mass effect on CN III.
dian of y cartesian coordinate values as the video traversed
the top and y1 is the median of y cartesian coordinate val- Results
ues as the video traversed the bottom of the monitor (Fig. The 157 control subjects were 52% male and had a
1, left column). The box width (w) was similarly defined mean age of 36.73 ± 16.90 years (mean ± SD) and a range
as x2 - x1, with x2 = median x coordinate as the aperture of 7–87 years. The mean aspect ratio for the left eye was
traversed the right side, and x1 = the median x for the left 1.0117 ± 0.0706. For the right eye it was 1.0077 ± 0.0679.
side. The aspect ratio was defined as h/w. Thus, eye-track- A sample result in a normal patient is shown in Fig. 1A
ing recordings for a person with decreased vertical relative (left). Below it, Fig. 1B is from a patient with diabetes who
to horizontal eye movement would yield a decreased aspect had a CN VI palsy demonstrating an aspect ratio of 1.39
ratio. We defined an outlier as 2 SDs away from the mean, (p < 0.001), showing that the height of the box is greater
which was calculated using the mean function on Excel. than its width. The bottom row, Fig. 1C, demonstrates cal-
culation of aspect ratio in an awake patient with an acute
Statistics Comparing Age and Sex Among Control EDH. In this particular case the aspect ratio is actually
Subjects negative, because over all 5 cycles as the video traverses
A linear regression between aspect ratio and age was the top of the rectangle the pupils are where the red dots
calculated and a regression t-test was used to determine are clustered, whereas as it traverses the bottom they are
whether the slope of the regression line was statistically where the cyan dots are clustered.
significantly different from 0. A Mann-Whitney-Wilcoxon Just as a patient with a CN VI palsy due to diabetes had
test was used to determine if the true difference between an increased aspect ratio (Fig. 1B), 2 patients with CN III

J Neurosurg  December 12, 2014 3

U. Samadani et al.

FIG. 1. Tracking eye movements to detect ocular dysmotility. The scatterplots show the eye position of 1 eye as the video travels
around the computer monitor. On the left, the first cycle is plotted in red, the next in green, then cyan, magenta, and blue. A normal
control eye movement trajectory follows the video aperture as it moves in a box shape. Aspect ratio is defined as height/width. The
right side of the figure depicts how the height of the box is measured by obtaining the median values over 5 cycles as the video
traverses the monitor during the 1st and 3rd 10 seconds of each cycle (plotted in red and cyan, respectively). The width would be
obtained by calculating median values over 5 cycles during the 2nd and 4th 10 seconds of each cycle. The aspect ratio of an ideal-
ized control subject by definition should be 1.0 since the time spent traversing the top and bottom of the boxes (providing height)
is equal to the time spent traversing the sides of the boxes (providing width). The mean aspect ratio for the eye tracked in panel
A was 1.01. Panel B represents a diabetic patient with a CN VI palsy. This 56-year-old man with hemoglobin A1C values ranging
from 8.7% to 9.4% (reference range 4.6%–6.5%) presented with horizontal diplopia worse at distance and improved by covering or
closing 1 eye. Visual acuity was 20/30 and he had full motility on examination. He had esotropia of 20 prism diopters (pds), with 30
pds on left gaze and 12 pds on right gaze, consistent with a mild right CN VI palsy. Right eye tracking revealed an abnormal trajec-
tory relative to a normal control with an aspect ratio equal to 1.39 (p < 0.001), suggesting decreased lateral pupil movement as the
video traversed the top and bottom of the screen. Panel C depicts the box height analysis of a patient for whom the aspect ratio is
negative, due to CN III compression from an acute EDH. Figure is available in color online only.

palsies, due to either tumor involvement or diabetes, had Illustrative CN III Cases
decreased aspect ratios (Fig. 2 left and right, respectively).
These resulted in aspect ratios of 0.1870 (Fig. 2 left) and Chronic Subdural Hematoma
0.05637 (Fig. 2 right), demonstrating decreased vertical The patient was an 86-year-old right-handed man with
relative to horizontal pupil movement. a medical history of hypertension, hyperlipidemia, and
In normal control subjects, regression analysis of as- mild chronic renal insufficiency, and an ophthalmological
pect ratio by age revealed no association. Sex also did not history of bilateral cataract surgery (2 years and 8 years
impact aspect ratio on the Mann-Whitney-Wilcoxon test. prior), pseudophakia, and scleral buckling. He had a base-

4 J Neurosurg  December 12, 2014

 Detection of cranial nerve palsies with eye tracking

Perimesencephalic cistern compression (on immediate

preoperative CT scan): right cistern 80% of baseline, left
cistern 61% of baseline.
Radiologist 1: “The brainstem is shifted right, there is
medialization of the left uncus, and it may barely touch
cisternal CN III. Separately there is mass effect on the left
cavernous sinus by the uncus (loss of CSF cleft).”
Radiologist 2: “The patient has a full uncus with medial
displacement. There is mass effect on the cistern, but no
overt compression of CN III.”

FIG. 2. Left: Eye tracking of a subject whose right CN III was surgically Acute EDH
severed prior to its entrance into the cavernous sinus during resection The patient was a 62-year-old, right-handed man with
of a tumor involving the nerve. A 76-year-old man with a medical history a medical history of goiter/iatrogenic hypothyroidism, hy-
of glaucoma and myopia, and current presbyopia, had right upper eyelid pertension, and hyperlipidemia, and an ophthalmological
ptosis and a pupil that was fixed and nonreactive to light or accom- history of glaucoma controlled with latonoprost drops.
modation. He had a large-angle (50-pd) right exotropia and 14-pd right
hypotropia in primary gaze. He was not able to adduct to the midline He had 20/20 vision bilaterally. He presented with syn-
in the right eye, nor was there any significant vertical duction capacity copal fall and loss of consciousness persisting a few min-
in the right eye. Steristrips were applied to elevate the right upper lid utes. At presentation he was awake, alert, and had fluent
and the patient underwent eye tracking which revealed an aspect ratio speech. His pupils were equal and extraocular movements
(height/width of box trajectory) equal to 1.0206 in the left eye and 0.1870 remained intact. His head CT showed a small right fron-
in the right eye (p < 0.001 for right eye).  Right: Eye tracking of a subject toparietal EDH underlying a stellate skull fracture. Eye
with a right CN III palsy secondary to diabetes mellitus. A 79-year-old movement tracking was performed (Fig. 4). Five hours
man with a history of hypertension and diabetes mellitus with hemoglo-
bin A1C values ranging from 8.2% to 11.4% over the past year (normal later his examination findings deteriorated and he devel-
range 4.6%–6.5%) presented to the emergency room complaining of oped drowsiness, dysarthria, left-sided neglect, and a left
3 days of painful double vision. On examination he demonstrated right pronator drift. His pupils remained equal and extraocular
eyelid ptosis. His motility was intact in the left eye. In the right eye he movements remained intact by examination. He under-
had exotropia of 8 pds. The patient was then seen in follow-up 11 days went craniotomy, evacuation of EDH, and cranial plating
later in clinic. At that time his examination remained unchanged except of the skull fracture. Postoperatively his left-sided neglect
for decreased motility of the right eye at -4 adduction, -4 elevation, and and pronator drift resolved over the subsequent 48 hours.
-4 depression. Steristrips were applied to elevate the right upper lid
and the patient underwent eye tracking, which revealed an aspect ratio He scored 13/50 on the Executive Interview 25 Assess-
(height/width of box trajectory) equal to 0.05637 in the right eye, sug- ment Test (EXIT) on postoperative Day 7. Eye tracking
gesting that the right eye is an outlier from normal. Figure is available in was repeated on postoperative Days 7, 11, and 35. He was
color online only. discharged home after 1 week of inpatient rehabilitation
and returned to work 2 months after surgery.
line visual acuity of 20/25 (right eye) and 20/30 (left eye). Perimesencephalic cistern compression (on preopera-
The patient took 81 mg of aspirin per day prophylactically. tive CT scan): right cistern 27% of baseline, left cistern
The patient fell without losing consciousness and presented 35% of baseline.
several weeks later with headache, but was otherwise neu- Radiologist 1: “There is contact with CN III on the
rologically well. A head CT was performed and demon- right side.”
strated a small left-sided subdural hematoma (SDH) (Fig. Radiologist 2: “There is no evidence of overt CN III
3A). Aspirin was discontinued and platelets were trans- compression.”
fused. Eye tracking was performed and demonstrated 2
of 5 cycles with reduced vertical amplitude. The headache Right Frontal Metastasis
resolved spontaneously and the patient elected to undergo A 63-year-old man, a 100-pack-year smoker who had
observation of this lesion. Eight days later the headache be- declined to see a physician for his entire adult life and
came exacerbated and a repeat CT scan demonstrated en- thus reported no relevant medical or ophthalmological
largement of the hematoma (Fig. 3B). The patient remained history, presented to the emergency room with a cough,
intact on neurological examination, exhibiting neither ne- requesting treatment for a flulike illness. On examina-
glect nor pronator drift. His pupils remained symmetrical. tion he was noted to be disoriented and to have a mild left
Eye tracking was again performed and demonstrated de- hemiparesis. Pupils were equal and reactive, and extraocu-
creased vertical amplitude on 5 of 5 cycles, with an aspect lar movements appeared intact. Head CT demonstrated a
ratio of 0.27. The patient underwent SDH drainage, during right frontal mass, and chest radiograph showed a large
which 100 ml of fluid was extracted using a closed twist- left upper lobe chest mass. The patient was administered
drill drainage system. Head CT and eye tracking was re- Decadron (10 mg orally every 6 hours), and a CT scan
peated after removal of the twist drainage apparatus (Fig. of the chest/abdomen/pelvis (not shown) and brain MRI
3C). Despite persistence of residual SDH, the eye tracking studies (Fig. 5A) were obtained. Eye movement tracking
vertical amplitude was normal. His headaches resolved was performed 48 hours after admission, immediately be-
and he became asymptomatic. The patient was discharged fore right frontal craniotomy for resection of a moderately
home after participating in physical therapy. well-differentiated squamous cell carcinoma metastasis.

J Neurosurg  December 12, 2014 5

U. Samadani et al.

FIG. 3. Exacerbation and reversibility of pupillary vertical amplitude in a patient with SDH. An 86-year-old man with a history of
cataracts presented with headache several weeks after a fall. Initial axial CT scans showed a small SDH (A, left) with an open
perimesencephalic cistern (arrow). Eight days later his headache became exacerbated, and repeat imaging demonstrated that the
SDH had expanded, creating mass effect on the brain and pushing the medial aspect of the temporal lobe into the perimesence-
phalic cistern (B, arrow). A twist-drill drain was placed and 100 ml of subdural fluid was evacuated, resulting in resolution of the
mass effect on the perimesencephalic cistern (C, arrow). Figure is available in color online only.

A radiographic gross-total resection was performed. The with left leg weakness resulting in a fall. On examination
patient went home 1 week after his craniotomy and under- he had mild left hemiparesis without neglect. Platelets
went repeat eye tracking at a follow-up visit 1 month later. were transfused, eye tracking was performed, and a twist-
He subsequently underwent radiation therapy to his whole drill drainage procedure was performed. More than 200
brain. He declined treatment for the lung mass and died 7 ml subdural fluid was removed. The patient’s left hemi-
months after his initial diagnosis. paresis resolved and he was discharged to rehabilitation.
Perimesencephalic cistern compression (on immediate Sixteen days after the procedure, repeat eye tracking was
preoperative CT scan): right cistern 77% of baseline, left performed.
cistern 73% of baseline. Perimesencephalic cistern compression (on immediate
Radiologist 1: “There is subtle shift of the uncus to- preoperative CT scan [Fig. 5B]): right cistern 61% of base-
wards the midline. It likely does not contact cisternal CN line, left cistern 73% of baseline.
III, but may press on the ipsilateral cavernous sinus, since Radiologist 1: “Cisterns are effaced but there is no di-
the CSF cleft adjacent to the sinus is gone.” rect mass effect on CN III.”
Radiologist 2: “The uncus is medially deviated; there is Radiologist 2: “There is mass effect, but no overt com-
no overt compression on CN III.” pression of CN III.”

Right SDH Left Glioblastoma Multiforme

The patient was an 87-year-old man with a medical his- The patient was a 67-year-old man with a medical his-
tory of hypertension, hyperlipidemia, diabetes, chronic tory of prostate cancer, hypertension, hyperlipidemia,
renal insufficiency, prostate cancer treated with radia- alcoholism in remission, and gunshot wound to the left
tion, and cerebrovascular disease treated with left carotid shoulder with retained missile fragment. His ophthalmic
endartectomy. His ophthalmic history was significant for baseline was 20/40 vision in the right eye and 20/50 in
pseudophakia, glaucoma, left eye cataract, and allergic the left eye. He presented with 2 months of stuttering and
conjunctivitis. His visual acuity was 20/20 and 20/25. He right arm and hand weakness. He had a witnessed sei-
took aspirin (81 mg) sporadically. The patient presented zure on the day of presentation that began with shaking
6 J Neurosurg  December 12, 2014
 Detection of cranial nerve palsies with eye tracking

FIG. 4. A 62-year-old patient with an acute EDH and bilateral perimesencephalic compression after a fall. The patient presented
with a neurologically nonfocal examination and CT scans showing a small right frontoparietal EDH and nondisplaced skull fracture.
On presentation he was verbally appropriate without focal neurological deficit. Pupil size was equal by gross examination and
extraocular movements appeared intact when eye tracking was performed. Four hours later the patient developed a left prona-
tor drift and intermittent dysarthria. We performed EDH evacuation and fracture repair. He underwent repeat eye tracking on
postoperative Days 7, 11, and 35. Aspect ratio on the day of presentation was negative for the left eye. Ratios are listed on the
figure for the day of presentation and postoperative Day 35. Conventional scatterplots are shown in panel A. Panel B depicts the
eye tracking as a plot of the cartesian coordinate of the pupil on the y axis and time on the x axis, with each 40-second cycle in a
different color. Such a plot reveals that the position of the pupil is altered at roughly the same points during each cycle as the video
circumnavigates the monitor 5 times. This suggests that the patient is awake during tracking because the pupils are not lost and
that the alterations are not coincidental but driven by a common intrinsic pathological entity, because they repeatedly occur at the
same place in 5 consecutive cycles. Figure is available in color online only.

of the right upper extremity and progressed to general- junction metastasis was performed by a surgeon at anoth-
ized tonic-clonic activity. On examination he had intact er institution, with worsening right hand coordination and
pupils and extraocular movements. His speech was slow ataxia. On examination the patient had right pronator drift
with paraphasic errors and difficulty with repetition and and hemineglect. A CT scan revealed edema at the surgi-
naming. Head CT scans obtained with contrast revealed a cal site and MRI studies (Fig. 5D) revealed a peripherally
left frontotemporal cystic mass (Fig. 5C). The patient un- enhancing collection in the previous tumor cavity. Eye
derwent eye tracking and subsequently underwent awake tracking was performed and then the patient was taken
stereotactic drainage of the cyst, which revealed necrotic to the operating room for reexploration craniotomy and
cells and was nondiagnostic for malignancy, followed by evacuation of an abscess deep to the dura mater. He was
awake stereotactic craniotomy with speech mapping for treated with antibiotics for 12 weeks postoperatively. Eye
resection of a glioblastoma multiforme. Gross-total resec- tracking was then repeated.
tion was achieved radiographically. The patient had pre- Perimesencephalic cistern compression (on immediate
served speech but mild hemiparesis postoperatively and preoperative CT scan): right cistern 79% of baseline, left
participated in rehabilitation prior to discharge home. He cistern 84% of baseline.
underwent repeat eye tracking at 1 month postoperatively. Radiologist 1: “Cisterns patent. No uncal shift. No con-
He received Temodar and radiation therapies as an outpa- tact with CN III.”
tient and remained independent in activities of daily liv- Radiologist 2: “No evidence of CN III compression.”
ing, with no tumor recurrence at 7 months postoperatively. None of the patients with supratentorial lesions who
Perimesencephalic cistern compression (on immediate were found to have restricted vertical amplitude on eye
preoperative CT scan): right cistern 42% of baseline, left tracking reported diplopia or other symptoms of discon-
cistern 39% of baseline. jugate gaze. All of the patients were reported to have nor-
Radiologist 1: “Cisterns patent. No uncal shift. No con- mal ocular motility on examination by a neurosurgeon or
tact with CN III.” ophthalmologist, which suggests that the palsies are sub-
Radiologist 2: “No evidence of CN III compression.” clinical.

Intracranial Abscess Illustrative CN VI Cases

A 65-year-old man with a medical history of hyper- Calvarial Mass With Cerebellar Compression
tension, hyperlipidemia, coronary artery disease, and A 54-year-old man presented with a medical history of
posttraumatic stress disorder, with no known ophthalmic poorly differentiated papillary thyroid carcinoma resected
disorders and visual acuity of 20/20 bilaterally presented 5 and 3 years prior and then treated with radioactive iodine
2 weeks after left parietal craniotomy for an esophageal and whole-beam radiation therapy. He reported a tender
J Neurosurg  December 12, 2014 7
U. Samadani et al.

FIG. 5. Preoperative imaging and pre- and postoperative eye tracking of 4 subjects with supratentorial mass lesions. Aspect ratios
are provided within the figure.  A: Axial MRI sequences obtained in a 63-year-old man with a right frontal brain mass.  B: Head CT
scans obtained in an 87-year-old man with an SDH.  C: Head CT scans obtained in a 67-year-old man with a glioblastoma multi-
forme.  D: Axial MRI studies obtained in a 65-year-old man with an intracranial abscess. The single arrows designate the lesions
in all images (and the second, large arrow in B right indicates uncal mass effect). Figure is available in color online only.

mass on the back of his head and a progressive occipital contralateral to the peripontine cistern narrowing on MRI
headache that was improved by supine positioning. The scan that resolved after lesion resection.
patient denied nausea, vomiting, dizziness, diplopia, or vi-
sion difficulty. Physical examination by a neuro-ophthal- A Cerebellar Mass
mologist demonstrated normal extraocular motility and no A 56-year-old man with a medical history significant
evidence of papilledema. Dilated funduscopic examina- for 35 years of cigarette smoking, daily marijuana use, and
tion revealed sharp, pink, and flat optic discs with a cup/ hypertension presented with dull occipital headaches that
disc ratio of 0.3 in both eyes. Imaging revealed a calvarial- improved with ibuprofen, as well as blurred vision and an
based mass (Fig. 6A and B). There was narrowing of the unsteady gait. Detailed ophthalmological examination re-
right prepontine cistern on MRI (Fig. 6C, arrow), but no vealed 20/25 visual acuity, normal ocular motility, and no
transependymal flow to suggest hydrocephalus (Fig. 6D). evidence of papilledema, with sharp, pink, and flat optic
Eye tracking was performed (Fig. 6, right panel, upper discs and a cup/disc ratio 0.35 in both eyes. Chest radio-
row). His aspect ratio of 1.84 in the left eye was highly graph revealed a mass in the right upper lobe. Brain imag-
significantly greater than normal controls. The patient un- ing revealed a right cerebellar mass pushing the brainstem
derwent craniectomy for resection of the mass, and cra- to the left and resulting in narrowing of the left prepontine
nioplasty reconstruction. Eye tracking was repeated on cistern (Fig. 7A, arrow). There was no evidence of transep-
postoperative Day 1 (Fig. 6, right panel, lower row) and endymal flow on T2-weighted MRI (Fig. 7B). Eye tracking
demonstrated return to the normal range in both eyes. He was performed (Fig. 7, right panel, upper row) and revealed
did well and was discharged home, neurologically well, a highly significantly elevated aspect ratio of 1.44 in the
on postoperative Day 3. This patient’s preoperative eye right eye. Retrosigmoid suboccipital craniotomy was per-
tracking demonstrated an increased aspect ratio in the eye formed for resection of the brain tumor. Eye tracking was
8 J Neurosurg  December 12, 2014
 Detection of cranial nerve palsies with eye tracking

FIG. 6. Resection of a calvarial mass causing right prepontine cistern narrowing normalizes the aspect ratio. The imaging (A–D)
demonstrates a large calvarial mass compressing the cerebellum and causing asymmetrical mass effect on the prepontine cistern.
(The arrow in C indicates mass effect on CN VI.) Preoperative eye tracking is shown in the right panel, upper row, and demon-
strates a highly significantly increased aspect ratio in the left eye as well as mildly abnormal tracking in the right eye. Eye tracking
obtained on postoperative Day 1 is shown in the right panel, lower row, and demonstrates the return to normal aspect ratio in both
eyes. Figure is available in color online only.

repeated on postoperative Day 1 (Fig. 7, right panel, lower scheduled to undergo biopsy of her lung mass for evalua-
row) and was normal in both eyes. The patient remained tion of sarcoidosis.
neurologically well and was discharged home on postop-
erative Day 4. In this patient, eye tracking demonstrated an Discussion
increased aspect ratio in the eye contralateral to the peri-
pontine cistern narrowing on the MRI study that resolved Many methodologies exist for assessment of CNS func-
after lesion resection. tion, ranging from physical examination to radiographic
imaging and electrical activity assessment. Nonetheless,
some pathological conditions, such as elevated ICP, con-
Neurosarcoidosis cussion, and shunt malfunction remain difficult to diag-
A 59-year-old woman presented with a 1-year history of nose, even with invasive means.
progressive intermittent vertigo, biparietal headache, and We present the eye-tracking results in 157 subjects
imbalance. She reported intermittent horizontal diplopia. without known significant neurological or ophthalmo-
Ophthalmological examination revealed full ocular motil- logical pathological conditions. These subjects watched a
ity, and no evidence of papilledema or neurosarcoidosis. video that traveled the perimeter of a rectangular viewing
Admission MRI of the brain revealed hydrocephalus with- monitor at a speed of 10 seconds per edge. The test was
out evidence of a discrete mass (Fig. 8 left). Eye tracking very easily tolerated and no subjects had to be excluded
was performed preoperatively (Fig. 8, right panel, upper due to inattention. In an idealized model, the ratio of ver-
row) revealing a highly significantly decreased aspect ratio tical to horizontal eye movement would be equal to 1.00
in the left eye (0.81) and a highly significantly increased because the time spent traveling vertically versus horizon-
aspect ratio in the right eye (1.34) relative to normal con- tally should be the same. We noted that normal subjects
trols. A ventriculoperitoneal shunt was placed, relieving had mean ratios of 1.01 for both the left and right eyes,
the headaches. Eye tracking was repeated on postopera- with a relatively low standard deviation of approximately
tive Day 2 (Fig. 8, right panel, lower row) and revealed 7%. There was no significant difference between the eyes
return to the range of normal in both eyes. The angioten- in these controls.
sin-converting enzyme I level in CSF was elevated, at 4.8 We then demonstrated that subjects with CN III pal-
U/L (reference range 0–2.5 U/L). Subsequent evaluation sies or supratentorial mass effect had decreased vertical/
revealed increased gallium uptake on lung scan and me- horizontal eye movement ratios and that subjects with CN
diastinal lymphadenopathy on chest CT. The patient was VI palsies, infratentorial mass effect, or hydrocephalus
J Neurosurg  December 12, 2014 9
U. Samadani et al.

FIG. 7. Resection of a right cerebellar mass causing left prepontine cistern narrowing normalizes the aspect ratio. The imaging (A
and B) demonstrates a large cerebellar mass compressing the left prepontine cistern, which is designated by an arrow. Preopera-
tive eye tracking is shown in the right panel, upper row, and demonstrates a highly significantly increased aspect ratio in the right
eye. Eye tracking obtained on postoperative Day 1 is shown in the right panel, lower row, and demonstrates the return to normal
aspect ratio. Figure is available in color online only.

had increased ratios, consistent with the activities of the monocularly or binocularly. It is possible that CN III itself
affected nerves. is the locus, perhaps by ischemia from pressure exerted
in the interpeduncular fossa. When the lesion is only af-
Cranial Nerve III fecting 1 eye, as in many of the cases, it is less likely to
Our data suggest that we have developed an eye-track- be supranuclear.16,17,28 To impact only 1 eye, a subtentorial
ing algorithm that captures the decreased vertical ocu- supranuclear lesion would have to invoke skew deviation,
lar motility associated with CN III palsy while a subject which does not arise in the course of midbrain compres-
watches a brief video of their choice that moves within sion from the mass effect of supratentorial lesions.7 Mon-
an aperture on a viewing monitor (Figs. 2 and 3). Patients ocular paresis of ocular elevation can occur in patients
with supratentorial mass lesions demonstrated low outly- with lesions near the posterior commissure, but this is very
ing value aspect ratios preoperatively, which reverted to rare and does not supervene in cases of midbrain compres-
normal postoperatively (Figs. 4 and 5). Because a low as- sion from the mass effect of supratentorial lesions.2,14,28
pect ratio suggests decreased vertical relative to horizontal Perhaps the case best illustrating a patient with both su-
movement of the eye, such a finding may be mediated via pranuclear and probable CN III deficit is depicted in Fig.
CN III. Our algorithm was sensitive enough to detect su- 5C. This patient had a large left cystic mass and was mod-
pratentorial mass effect confirmed by an algorithm quan- erately aphasic at presentation due to postictal state and
titating perimesencephalic cistern volume, regardless of Todd paralysis. The tracking in both eyes was abnormal
whether uncal mass effect was noted by a radiologist. but the aspect ratio was lower on the side contralateral to
Our algorithm may potentially be clinically useful for the lesion, as is seen in the other patients with supratento-
the early detection of supratentorial mass effect and trans- rial mass effect. If the lesion were purely supranuclear one
tentorial herniation. Determining the exact mechanism might expect the aspect ratios to be relatively equal. Un-
underlying the phenomenon we are observing will be the equal ratios suggest an infranuclear mechanism.
subject of future studies. In every patient with a supra- Figure 5A and B depicts patients who clearly have more
tentorial pathological entity in whom we performed eye substantive mass effect than the others, and in both cas-
tracking, the abnormal findings occurred while tracking of es decreased vertical eye movement seems to be almost
the eye contralateral to the entity. This has occurred con- matched by decreased horizontal eye movement. These
sistently in our entire database of patients and regardless patients may also have decreased horizontal eye move-
of whether the afferent stimulus to the eyes is presented ment, reflecting CN VI palsy from either increased ICP or
10 J Neurosurg  December 12, 2014
 Detection of cranial nerve palsies with eye tracking

FIG. 8. Shunting of CSF in a patient with hydrocephalus presumably caused by sarcoidosis normalizes the aspect ratio. The MR
image (left) was obtained in a patient with neurosarcoidosis resulting in hydrocephalus. Her eye tracking is abnormal in both eyes
preoperatively (right, upper row), with an increased aspect ratio. This ratio returns to normal postoperatively (right, lower row).
Figure is available in color online only.

direct mass effect on the nerve. Additionally, because both logical conditions such as congenital progressive external
eyes are affected, there may be a supranuclear component ophthalmoplegia22,31 are also going to produce abnormali-
to the altered tracking. ties in vertical movements. In addition, disorders causing
The patient with the greatest quantitative difference in a restrictive problem impacting the orbit (thyroid orbi-
perimesencephalic volume between his pre- and postop- topathy,13,34 previous trauma, extraocular muscle infiltra-
erative CT scan had bilateral decreases in pupillary verti- tion, and inflammation) will also cause problems with eye
cal amplitude on eye tracking. This patient presented after movements that may involve more of the vertical (most
a fall resulting in a right frontoparietal skull fracture and frequently in the case of trauma) than the horizontal move-
small EDH causing almost no subfalcine herniation (Fig. ments. None of the patients in our study had any history
4A, upper CT image) but reduction in perimesencephalic of these conditions, and in all of them their eye tracking
cistern volume to 27% of the postoperative value on the improved to normal after surgery was performed to ad-
right side and 35% of postoperative volume on the left dress their supratentorial mass lesions, suggesting that the
(lower CT image). Postoperatively, CT and MRI studies lesion’s mass effect may indeed be the cause of their motil-
(Fig. 4A, right column) revealed no evidence of residual ity dysfunction.
structural injury; however, the patient’s eye box trajectory
persisted in having increased variability, raising the pos- Cranial Nerve VI
sibility that the eye tracking is reflecting the impact of ra- We present a series of cases in which patients had in-
diographically silent brain injury. The impairment of his creased vertical relative to horizontal movement of the eye
cognitive capabilities after surgery is consistent with the when we used the same algorithm. Two patients had clini-
association between mild brain injury and eye-tracking cally apparent CN VI deficits confirmed by the neuro-oph-
variability. Impaired reading ability in patients sustaining thalmologist’s examination. The other two did not have CN
supratentorial brain injury or stroke has been attributed in VI palsies on neuro-ophthalmological examination, and
part to deficits in fixation, saccade, and pursuit.10 Smooth only 1 of these 2 had intermittent complaints of diplopia.
pursuit during target blanking has been hypothesized to The 2 with cerebellar mass effect had radiographic com-
reflect shearing of cerebellar–cortical tracts, resulting pression of CN VI. The patient with neurosarcoidosis had
from mild brain injury.33 Diffusion tensor imaging dem- radiographic evidence of hydrocephalus, which can lead to
onstrating disruption of white matter tracts also correlates stretching of CN VI. Because CN VI innervates the lateral
with impaired visuomotor task completion.8 rectus, and we note decreased horizontal relative to verti-
A potential limitation of the study could be that con- cal movement in these patients relative to normal control
ditions other than supratentorial mass lesions can cause subjects and similar to the first 2 subjects with confirmed
changes in vertical ocular motility. Myasthenia gravis,35 CN VI palsy, our results are consistent with detection of
supranuclear palsies,5,6,11 and primary eye muscle patho- subclinical CN VI palsy in these patients. The abducent
J Neurosurg  December 12, 2014 11
U. Samadani et al.

nerve moves the pupil laterally, and these subjects dem- from midposition, or approximately 30° total from top to
onstrated decreased lateral movement on eye tracking. In bottom or side to side. Thus, the algorithm does not re-
the 3 patients in whom the pathology could be surgically quire or assess the full range of ocular motility, nor the en-
treated, these trajectories resembled normal controls after tire visual field. Use of a larger monitor, or one positioned
treatment. closer to the subject, would enable assessment of these.
One potential utility of this technology is detection of A second limitation is that our technique has not been
symptoms caused by hydrocephalus. Here we described rigorously compared with gold-standard physical exami-
1 patient with hydrocephalus due to sarcoidosis. Her eye nation or scleral coil techniques. Another potential limita-
tracking was abnormal in both eyes preoperatively and tion of this study is lack of formal visual acuity testing in
returned to normal postoperatively. However, given the controls as well as test subjects. Because subjects removed
diverse baseline ocular pathological conditions in hydro- glasses and toric lenses for viewing to optimize the abil-
cephalic patients,3,15,37 it is likely that tracking results will ity of the eye-tracking camera to find the pupil, some may
need to be compared with each patient’s own normative have experienced impaired vision. Future studies will be
data to be useful in that particular context. A second po- needed to clarify the acuity necessary for optimal track-
tential utility is the monitoring of awake patients with ing. Patients with mass lesions were tracked under the
suspected elevated ICP, because CN VI is known to be same conditions (no glasses) each time they underwent
susceptible to elevated ICP.19 tracking, so it is unlikely that visual acuity accounts for
In the 2 patients with tumors causing mass effect their alterations in eye tracking.
with compression of CN VI as it exits the pontomedul- One might wonder if the eye-tracking deficits we are
lary junction through the prepontine cistern, the abnormal seeing in patients with mass lesions are due to inatten-
eye-tracking pattern must be due at least in part to either tion, psychomotor disturbance, or other spurious events.
nuclear or nerve compression. If it were due to a supranu- Arguing strongly against this is the fact that abnormali-
clear mechanism, it would most likely affect both eyes the ties were demonstrated not in 1 cycle, as the eyes followed
same way.16 In the third illustrative CN III case, which was the video aperture circumnavigating the monitor, but in 5
diagnosed in a 63-year-old man with right frontal metasta- serial cycles. If a person were inattentive, the probability
sis, the patient had a highly significantly increased aspect that they would be inattentive in exactly the same pattern
ratio in the left eye and only a marginally increased one for 5 consecutive times is low. This is further illustrated in
in the right eye. His calvarial lesion was sufficiently large Fig. 4B, in which the same patient’s data are tracked over
that it may have been compressing both nerves, in unequal 35 days and plotted as a cartesian coordinate on the y axis
quantities. In the fourth illustrative CN III case, which was versus time on the x axis. Not only are the eyes moving
diagnosed in an 87-year-old man with right SDH, the pa- in similar patterns over cycles within the same tracking
tient had only 1 eye with an increased aspect ratio pre- session, but also between tracking sessions as the tracking
operatively that returned to normal postoperatively. That disorder steadily improves over 35 days. In all cycles the
these patients both improved by postoperative Day 1 after disruption is in the same regions. Such a finding would be
tumor resection suggests that their pathological condition consistent with an intrinsic pathological entity causing the
was altered by the surgeries to remove these tumors. eye-tracking problem, as opposed to a volitional act by the
subject being tracked.
Implications and Limitations Our methodology assesses physiological functioning of
Ocular motility is commonly assessed in 9 cardinal the CNS, and thus is different from imaging technologies
positions as well as with cross-cover testing. Other tests enabling visualization of brain anatomy, or monitors that
include the Titmus housefly test, the Lang stereo test, assess pressure rather than the impact of elevated pres-
the Hess screen test, red-filter test, Maddox rod evalua- sure. Our methodology is also different from technologies
tion, and Lancaster red-green test.12,30 In young children, such as the electroencephalogram that measures electri-
who may be less cooperative with an examiner, binocular cal activity. Eye tracking most closely resembles physical
gaze conjugacy may only be assessable with simpler algo- examination of a subject, which also yields information
rithms, such as following an object moving in a set trajec- regarding physiological functioning. Unlike a physical ex-
tory.9 When such tests are performed in conjunction with amination, however, eye tracking does not necessarily re-
the remainder of the neuro-ophthalmic and physical evalu- quire a trained examiner and could be performed remotely
ation, one can localize neurological lesions and quantitate or in an automated fashion. Conceivably one could assess
ocular motility deficits, particularly those associated with a patient with hydrocephalus for a shunt malfunction by
TBI,18 with great accuracy. Despite this capability, other having them watch a video on their home computer.
than assessment of gaze in the cardinal positions, these Unlike conventional eye tracking, in which subjects
tests are not used routinely in the emergency setting due to follow instructions to be deliberately calibrated and thus
the need for a trained practitioner to administer them, the are conscious that their eye movements are being tracked,
requirement for sophisticated equipment, and the urgent nonspatially calibrated tracking could occur via a webcam
nature of many neurological disorders. while someone is reading or watching a video. It does not
Unlike these techniques, our technology does not ex- require that the subject explicitly consent to being tracked
amine the full range of ocular motility. If the subject’s eyes prior to assessment of their CNS functioning, and thus
are positioned 55 cm from the center of the 30 × 35–cm raises ethical considerations. Dementia, Parkinson dis-
viewing monitor, this algorithm elicits pupil movement in ease, progressive supranuclear palsy, schizophrenia, amy-
a maximum range of approximately 15° in any direction otrophic lateral sclerosis, autism, and fragile X syndrome
12 J Neurosurg  December 12, 2014
 Detection of cranial nerve palsies with eye tracking

are among the numerous diseases with characteristic 11. Clark D, Eggenberger E: Neuro-ophthalmology of movement
anomalies that are detectable using eye-movement track- disorders. Curr Opin Ophthalmol 23:491–496, 2012
ing technology.4,20,21,23,24,27,32 12. da Cunha Matta AP, Nunes G, Rossi L, Lawisch V, Dellato-
las G, Braga L: Outpatient evaluation of vision and ocular
motricity in 123 children with cerebral palsy. Dev Neurore-
Conclusions habil 11:159–165, 2008
13. Dagi LR, Zoumalan CI, Konrad H, Trokel SL, Kazim M:
In this paper we present proof of concept data support- Correlation between extraocular muscle size and motility
ing a method for tracking eye movements while a subject restriction in thyroid eye disease. Ophthal Plast Reconstr
watches television or a video that reveals weakness of the Surg 27:102–110, 2011
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Acknowledgments thalmol 12:104–109, 1992
18. Goodrich GL, Flyg HM, Kirby JE, Chang CY, Martinsen
Dr. Samadani’s work is supported in part by the Department GL: Mechanisms of TBI and visual consequences in military
of Veterans Affairs (VA), Veterans Health Administration, Office and veteran populations. Optom Vis Sci 90:105–112, 2013
of Research and Development, Rehabilitation Research and 19. Hanson RA, Ghosh S, Gonzalez-Gomez I, Levy ML, Gilles
Development Service, via a VA Merit Award (1I01RX000319-01), FH: Abducens length and vulnerability? Neurology 62:33–
and she was supported by a Career Development Award from the 36, 2004
American College of Surgeons/Neurosurgery Research Education 20. Hicks SL, Robert MP, Golding CV, Tabrizi SJ, Kennard C:
Foundation of the AANS. She is also supported by the Steven and Oculomotor deficits indicate the progression of Huntington’s
Alexandra Cohen Center for Veteran Post-Traumatic Stress and disease. Prog Brain Res 171:555–558, 2008
Trau­matic Brain Injury; by the Thrasher Research Fund; and by 21. Kennedy DP, Adolphs R: Impaired fixation to eyes following
Re­search to Prevent Blindness. amygdala damage arises from abnormal bottom-up attention.
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an indicator of mild traumatic brain injury. Neurosci Lett Mendhiratta, Mikheev, Rusinek, George, Kondziolka. Drafting
410:203–207, 2006 the article: Samadani, Alex, Nehrbass, Schneider, Chen, Shi.
34. Tamhankar MA, Kim JH, Ying GS, Volpe NJ: Adult hyper- Critically revising the article: Samadani, Warren, Schneider,
tropia: a guide to diagnostic evaluation based on review of Chen, Kwak, Kondziolka, Huang. Reviewed submitted version
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35. Vaphiades MS, Bhatti MT, Lesser RL: Ocular myasthenia Alex, Nehrbass, Kolecki, Schneider, Chen, Shi, Mendhiratta,
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36. Yang AI, Balser DS, Mikheev A, Offen S, Huang JH, Babb Huang, Smith. Approved the final version of the manuscript
J, et al: Cerebral atrophy is associated with development of on behalf of all authors: Samadani. Statistical analysis: Lamm,
chronic subdural haematoma. Brain Inj 26:1731–1736, 2012 Jureller, Shi, Qian, Fergus, Huang. Administrative/technical/
37. Zeiner HK, Prigatano GP, Pollay M, Biscoe CB, Smith RV: material support: Samadani, Ritlop, Reyes, Nehrbass, Kolecki.
Ocular motility, visual acuity and dysfunction of neuropsy- Study supervision: Samadani, Warren, Fergus, Smith.
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cated hydrocephalus. Childs Nerv Syst 1:115–122, 1985 Supplemental Information
Previous Presentation
Portions of this work were presented in abstract form (poster) at
Author Contributions the Association for Research in Vision and Ophthalmology, May
5, 2014, in Orlando, Florida.
Conception and design: Samadani, Farooq, Ritlop, Huang.
Acquisition of data: Samadani, Farooq, Warren, Reyes, Lamm,
Alex, Nehrbass, Kolecki, Jureller, Schneider, Chen, Shi, Correspondence
Mendhiratta, Kwak, Mikheev, Rusinek, George, Smith. Analysis Uzma Samadani, 423 E. 23rd St., MC 112, New York, NY
and interpretation of data: Samadani, Farooq, Alex, Jureller, Shi, 10010. email: [email protected].

14 J Neurosurg  December 12, 2014