Detection of third and sixth cranial nerve palsies with a novel method for eye tracking while watching a short film clip

Abstract

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 (neurologically 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 neuropathological 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 examination, 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 patients 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.

Keywords: CN = cranial nerve; EDH = epidural hematoma; ICP = intracranial pressure; SDH = subdural hematoma; TBI = traumatic brain injury; abducent nerve; diagnostic and operative techniques; diplopia; eye movement tracking; hydrocephalus; oculomotor nerve; pds = prism diopters; prepontine cistern.

Figures

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 idealized 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 trajectory 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.

FIG. 2

Left: Eye tracking of a subject whose right CN III was surgically severed prior to its entrance into the cavernous sinus during resection of a tumor involving the nerve. A 76-year-old man with a medical history of glaucoma and myopia, and current presbyopia, had right upper eyelid ptosis and a pupil that was fixed and nonreactive to light or accommodation. 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 in the right eye, nor was there any significant vertical duction capacity in the right eye. Steristrips were applied to elevate the right upper lid and the patient underwent eye tracking which revealed an aspect ratio (height/width of box trajectory) equal to 1.0206 in the left eye and 0.1870 in the right eye (p < 0.001 for right eye). Right: Eye tracking of a subject with a right CN III palsy secondary to diabetes mellitus. A 79-year-old man with a history of hypertension and diabetes mellitus with hemoglobin A1C values ranging from 8.2% to 11.4% over the past year (normal range 4.6%–6.5%) presented to the emergency room complaining of 3 days of painful double vision. On examination he demonstrated right eyelid ptosis. His motility was intact in the left eye. In the right eye he had exotropia of 8 pds. The patient was then seen in follow-up 11 days later in clinic. At that time his examination remained unchanged except for decreased motility of the right eye at −4 adduction, −4 elevation, and −4 depression. Steristrips were applied to elevate the right upper lid and the patient underwent eye tracking, which revealed an aspect ratio (height/width of box trajectory) equal to 0.05637 in the right eye, suggesting that the right eye is an outlier from normal. Figure is available in color online only.

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 perimesencephalic 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.

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 pronator 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×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.

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 multiforme. 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.

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 demonstrates 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.

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. Preoperative 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.

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.