Laryngoscope 93: September 1983. EYE TRACKING ABNORMALITIES IN PATIENTS WITH CEREBROVASCULAR DISEASE.*+ Horst R. KONRAD, M.D., LEONARD P. RYBAK, M.D., Ph.D., DON E. RAMSEY, M.D., DARREL R. ANDERSON, M.D., Springfield, IL. ABSTRACT. Ten patients with disequilibrium, ataxia, and cerebrovascular abnormalities were studied using computer aided eye tracking and vestibular function tests, The patients had severe abnormalities in smooth pursuit (decreased gain) and saccade tests (increased delay, decreased accuracy). Optokinetic responses were less affected. The gain of the vestibulo-oculomotor reflex was sometimes affected. Patients with eye track- ing abnormalities frequently had symptoms of difficulty reading and watching television, When the lesion was asymmetrical, abnormal eye tracking tests usually pointed to the side of the lesion. Computer aided eye tracking tests are a useful adjunct to the evaluation of the patient with suspected vascular disease. They help to locate areas of central nervous system dysfunction, and produce an objective measurement of the severity of impairment. Conversely, when impairment of the smooth pursuit or saccade system is detected in patients being evaluated for disequilibrium, an assessment of the patients’ cerebrovascular system should be considered. Patients may complain of disequilibrium, visual disturbances, and ataxia due to cerebrovascular dis- ease. In order to better quantify the relationship be- tween cerebrovascular disease and impairment of visual and vestibular reflexes, we performed com- puter aided measurements of eye tracking and ves- tibulo-oculomotor reflexes on a series of patients undergoing an investigation of their cerebrovascu- lar system, *Presented at the Meeting of the Middle Section of the American Laryngological, Rhinologica!, and Otological Society, Inc., St. Louis, MO, January 22, 1983. 4From Southern INinois University School of Medicine, Springfield, IL. Send Reprint Requests to Horst R. Konrad, M.D., Department of Surgery, SIU School of Medicine, P. O, Box 3926, Springfield, IL 62708, » z, 1 Fig. 1. This is an intravenous digital subtraction arteriogram (DSA) with the patient in RPO projection, This shows a high grade (80%) stenosis of the origin of the right internal carotid artery and an even more severe stenosis of the origin of the left internal carotid artery. 1171 MATERIALS AND METHODS. Patients who were scheduled for arteriography, digital sub- traction arteriography, or ultrasound imaging of cerebral ves- sels, who complained of disequilibrium, visual disturbances, or were alaxic, were selecLed for this study. Their eye movements were recorded with electro-oculography and analyzed on a digital computer.’? Tests included evaluation of smooth pursuit, sac- cade and optokinetic reflexes as well as rotational and caloric testing of the vestibulo-oculomotor reflexes. All patients subse- quently underwent digital subtraction or conventional arteriog- raphy of the cerebral vessels. Most of these patients also under- went CT scan of the head. Fig. 2. Post contrast enhanced CT scan through the high supraventricular area. This shows an area of contrast enhance- ment in the medial left parietal lobe. Adjacent cuts showed ser- piginous structures extending to and from this area of enhance- ment consistent with feeding arteries and draining veins of an arteriovenous malformation, 1172 KONRAD, ET AL.: EYE TRACKING ABNORMALITIES. Se, Fig. 3. Lateral view left internal carotid intra-arterial digital subtraction angiogram. This shows large arteriovenous malfor- mation left parietal region supplied by branches of the anterior cerebral and middle cerebral arteries. An injection into the vertebral artery showed supply from branches of the posterior cerebral artery, also. CASE REPORTS, Case 1. A 70-year-old female had symptoms of ataxia and disequili- brium with intermittent difficulties reading and watching tele- vision. Digital subtraction arteriogram showed 80% right inter- nal carotid artery occlusion and almost complete occlusion of the left internal carotid artery (Fig. 1). She had decreased gain on smooth pursuit to left at both .2 and .4 Hz. She had increased saccade delays for right going saccades. She had normal op- tokinetic responses. Her vestibulo-oculomotor reflexes were re- duced both to rotational and caloric stimulation. Optokinetic re- sponses were normal. Case 2. A 40-year-old male had symptoms of disequilibrium, difficulty reading, and left sided headache of 7 months duration. CT scan Fig. 5, A lateral view from left common carotid arteriogram shows a high grade (85%) stenosis of the origin of left internal carotid artery. Fig. 4. CT, Two cuts from posterior post enhancement CT scan showing a peripheral low density area in the left parietal region consistent with an old infarct. showed a left parietal lesion which enhanced with contrast (Fig. 2), Arteriogram showed this to be an arteriovenous malforma- tion in the superficial parts of the left occipitoparietal area (Fig. 3). Saccade tests showed abnormally long saccade delays for right going saccades. He had borderline low caloric responses on the left. Smooth pursuit and OKN tests were normal. Case 3. A 69-year-old male developed episodes of loss of left sided vi- sion and ataxia. He also developed inability to read. CT scan sug- gested an old infarct of the left parietal region (Fig. 4). An arteriogram showed almost complete left internal carotid occlu- sion (Fig. 5). Smooth pursuit was normal at .2 Hz, but was abnor- mal in both directions at .4 Hz. Saccade velocities were de- creased bilaterally with right going saccades most affected. Sac- cade accuracy was diminished bilaterally, but saccade delay was Fig. 6. A lateral view of left common carotid arteriogram shows an extremely high grade (90%) stenosis of the proximal in- ternal carotid artery just distal to its origin. Right carotid arteriography showed predominant filling of the left anterior cerebral and middle cerebral vessels from the right internal carotid artery. Fig. 7. These are two views from intravenous digital subtrac- tion arteriogram. The top view is an RPO view of the aortic arch. This shows very high grade stenosis of the left subclavian artery just distal to its origin and proximal to the origin of the left vertebral artery. The RPO view of the carotid bifurcations shows a moderate (50 to 60%) stenosis of the origin of the left internal carotid artery with a relatively normal appearing right carotid bifurcation. Note the delayed flow in the left vertebral artery compared to the right vertebral artery due to the subclavian stenosis. normal, Optokinetic gain (OKN) was diminished in both direc- tions. The patient underwent a left carotid endarterectomy. Three months later, repeat tests showed return to normal values in all tests except smooth pursuit at .4 Hz which had improved but was still slightly outside the normal range. Case 4. A 65-year-old male developed disequilibrium, intermittent loss of vision, and ataxia. Arteriography showed almost complete ob- struction of the left internal carotid artery (Fig. 6), with the left cerebral circulation filling from the right side through the circle of Willis. The patient had decreased gain for smooth pursuit at .4 Hz in both directions and had severe increase in saccade delay bilaterally, but accuracy and velocity were not affected, KONRAD, ET AL.: EYE TRACKING ABNORMALITIES. 1173 Fig. 8. This is an intravenous digital subtraction arteriogram. The RPO view of the aortic arch (top bottom) shows a high grade stenosis of the subclavian artery proximal to the origin of the vertebral artery and faint filling of a hypoplastic right vertebral artery. The RPO view of the carotid bifurcations (top, bottom) shows a moderate (50 to 60%) stenosis of the left internal carotid artery with relatively normal appearing right carotid bifurca- tion. Case 5. An 87-year-old female complained of episodes of dise- quilibrium and difficulty reading, lasting 2 weeks, for the last 2 years, Arteriogram showed a severe stenosis of the left subcla- vian artery proximal to the vertebral artery origin (Fig. 7) and moderate stenosis of the left internal carotid artery. Smooth pur- suit tests showed decreased gain at .4 Hz with left going pursuit severely limited. Saccade showed severe increase in saccade de- lay and marked scatter in saccade accuracy. She also had a de- creased caloric response on the right. Case 6. A 76-year-old male presented with episodes of disequilibrium, ataxia and difficulty reading. Digital subtraction arteriogram showed stenosis of the left subclavian artery proximal to the origin of the vertebral artery and a hypoplastic right vertebral artery and stenosis of the left internal carotid artery (Fig. 8). 1174 4s mainte ati Fig. 9-A. Lateral view of a left common carotid arteriogram shows relatively high grade stenosis of the origin of the internal carotid artery and external carotid artery. There is a relatively high grade stenosis of the carotid siphon. Smooth pursuit had decreased gain to the left. Saccade had de- creased accuracy bilaterally and increased delays to the left. VOR had decreased gain and caloric tests had bilateral de- creased responses. Optokinetic responses were normal, Case 7. A 75-year-old female experienced progressive disequilibrium and difficulty reading. Arteriogram shows high grade stenosis of left internal carotid artery and fairly extensive atherosclerosis of both carotid siphons and of the left middle cerebral artery (Figs. 9-A and B). Both anterior cerebral arteries filled from the right sided injection via a large anterior communicating artery (Figs. 9-A and B). Smooth pursuit showed decreased gain bilaterally particularly at .4 Hz. Saccade showed increased delays, de- creased accuracy, and decreased velocity in both directions, Op- tokinetic tests showed decreased gain in both directions and caloric tests showed a barely significant left caloric weakness, Case 8, A 78-year-old female with severe hypertension was admitted to the hospital with severe disequilibrium, ataxia, and difficulty moving her eyes. Neurological evaluation suggested an acute brain stem stroke, The patient gradually improved. When she was ambulatory with help, eye tracking and vestibular tests, and digital subtraction angiography were performed. The carotid bi- furcation showed bilateral atherosclerosis but no significant ste- nosis. Smooth pursuit showed severe decrease in gain both at .2 and .4 Hz in both directions, Saccade test showed both increased delays and decreased accuracy bilaterally. Optokinetic re- sponses were reduced to the right and normal to the left. VOR was normal, After her hypertension was controlled, her symp- toms improved. Case 9. A 64-year-old female had an 11-year history of severe hyper- tension, Approximately 2', years ago she developed a severe gait KONRAD, ET AL.: EYE TRACKING ABNORMALITIES. 9b Fig. 9-B, This slightly oblique AP view of the left. common ca- rotid injection shows the stenosis in the carotid siphon and also a moderate stenosis in the horizontal portion of the left middle cerebral artery. The horizontal segment of the anterior cerebral artery in hypoplastic. impairment and was unable to walk. She had intermittent epi- sodes of dysarthria which cleared spontaneously. She gradually improved over a 6 month period then again became worse 2 weeks prior to testing, She developed severe worsening of her gait impairment and difficulty reading, She also has postural vertigo with the left side down. Her blood pressure was 219/130. On examination she appeared to have limitation of horizontal as well as upward gaze. CT scan revealed cerebral atrophy with multiple focal low density areas in both frontal and parietal regions (Fig. 10}, This was compatible with multiple small in- farcts. A previous angiogram showed arteriosclerotic changes without significant stenosis. Smooth pursuit had marked de- crease in gain on .2 and .4 Hz bilaterally. She had severe decrease in saccade velocity accuracy and increase in saccade delay bilaterally, VOR was only slightly decreased and calorics were normal. The patient gradually improved with control of her hy- pertension and ambulatory rehabilitation. Case 10. A 66-year-old male had episodes of vertigo with nausea and vomiting and right sided tinnitus. Between episodes he had no disequilibrium, ataxia, or visual symptoms. Because of a right carotid bruit the patient had an ultrasonic arteriogram which showed over 80% stenosis of the right carotid artery. This was confirmed on contrast arteriography. Smooth pursuit, saccade and OKN were normal. VOR showed decreased gain to left and caloric tests showed a 45% right caloric weakness. Symptoms and findings are summarized in Table I, DISCUSSION. Patients are generally referred for cerebrovascular evaluations because of transient ischemic attacks, carotid bruits or neurological changes suggestive of impending cerebrovascular accident. Some of these KONRAD, ET AL,: EYE TRACKING ABNORMALITIES. Fig. 10. This is a non-contrast enhanced CT scan in the high ventricular region. There is considerable enlargement of the lateral ventricles and there are focal peripheral low density areas over the convexities consistent with old bilateral infarcts. patients also have symptoms of disequilibrium or on careful questioning have noted visual symptoms associated with abnormalities of their eye tracking system, These are usually described as difficulty reading, watching television, driving or sewing. Many of these patients see an ophthalmologist or optometrist because they are concerned about vi- sual impairment. On examination these patients may have broad based gait, difficulty with Rhom- berg and tandem walking, and many have gaze impairment. Frequently, the eye tracking abnormal- 1175 ity can be determined only by oculographic record- ings or by computed aided measurements of eye movement reflexes. In the patients we studied, we found decreased gain on smooth pursuit in 8 of 10 patients. In patients who had primarily carotid dis- ease the major pursuit impairment was in the direc- tion of the carotid lesion (ipsilateral). Nine of 10 pa- tients had abnormal saccade tests. In 5 of 7 with pri- mary carotid disease, saccade delay was abnormally increased, primarily contralaterally. One patient with ipsilateral saccade delay also had bilateral vertebral artery disease and one patient had normal saccade interval but contralateral decreased saccade velocity and bilateral decreased saccade accuracy. A patient with multiple small cerebral infarcts had se- vere impairment of smooth pursuit and saccade in both directions. Optokinetic tests were usually nor- mal, The optokinetic test stimulates both foveal and peripheral visual field. This is a much broader stim- ulus than pursuit, which is triggered primarily by foveal vision. The peripheal visual field stimulus in OKN may be a stronger input to the central eye movement system and may require more central damage before impairment can be detected. The ves- tibulo-oculomotor reflex was only severely impaired in two patients. Patient 1 had almost complete oc- clusion of both internal carotid arteries and Patient 6 had carotid as well as vertebral artery disease. Unilateral carotid artery disease on the other hand does not necessarily produce impairment of eye tracking reflexes as illustrated by Patient 10. This patient had episodic vertigo but not disequilibrium, ataxia, or visual eye movement symptoms. Despite significant carotid artery occlusion, the patient had normal eye tracking tests. His caloric abnormality may be due to a peripheral labyrinthine disorder TABLE I. Symptoms and Findings. X-ray CT Scan sp Saccade Carotid Vertebral .2 4 Del Vel ACC OKN VOR Caloric A _D_ Read _R L L L RLERL RE RL RL Re RL RL 1 x x x x x x x xX XX xx Parietal 2 x x x x x x 3.x x x xX xx x xXx XX 4 x x xX x XX XX 5 x x x x XXX xXx x 6 x x x x x Xx x x Xx xx xXx xx 7 x x x XX XX XX XX XX x Brainstem 8 x infarct XX XX XX xXx x Artherosclerotic Multiple plaques no stenosis infarcts 9 x x XX XX XX _ XX_ XX 10 x a 1176 KONRAD, ET AL.: EYE TRACKING ABNORMALITIES. unrelated to his cerebrovascular disease or related to end artery disease in the labyrinthine blood sup- ply. Adequate cross circulation at the circle of Willis can apparently perfuse both hemispheres sufficient- ly to produce normal eye tracking even in significant unilateral carotid obstruction. One patient who was tested before and after carotid endarterectomy had resolution of his saccade abnormalities and improve- ment in smooth pursuit. CONCLUSION. Patients with cerebrovascular disease may de- velop abnormalities in their eye tracking system. When they do, they have symptoms of disequili- brium and difficulty with visual tasks requiring pre- cise or rapid eye movements. Such patients have in- creased intervals between the onset of target move- ment and the onset of eye movement (saccade delay) suggesting an increase in the time required for the visual information to complete its trip through the visual oculomotor reflex pathways. The accuracy and the velocity of saccades is also affected. In most cases of saccade impairment, carotid disease was bilateral and the greatest impairment occurred in saccades away from the side of the major occlusion (contralateral). Patient 2 had a precisely located le- sion in the left parietal cortex. He had abnormal sac- cade delays for right going (contralateral) saccades, a finding similar to those of Baloh’? in man and Lynch‘ in monkeys. The smooth pursuit system was affected by a decrease in gain usually worse for pur- suit in the direction of the greater occlusion (ip- silateral). This agrees with the finding of Baloh.’ Although carotid artery occlusion does not neces- sarily mean damage to central nervous system structures, this study suggests that when patients with suspected cerebrovascular disease have symp- toms of eye tracking dysfunction, they frequently have measurable contralateral saccade abnor- malities and ipsilateral pursuit abnormalities on computer aided measurements, suggesting central nervous system impairment. The more commonly used optokinetic test, however, is usually normal. The vestibulo-oculomotor reflex is only involved in more extensive vascular occlusion or when vertebral arteries are also impaired. Postoperative resolution of saccade abnormalities and improvement in smooth pursuit suggests the need for further studies in patients with carotid occlusive disease over time, as well as pre and postoperative measure- ments. Such information would further clarify our indication for endarterectomy in patients with ca- rotid occlusive disease. BIBLIOGRAPHY, 1. Baloh, R. W., Sills, A. W., Kumley, W. E., e¢ al: Quan- titative Measurement of Saccade Amplitude, Duration, and Ve- locity. Neurology, 25:1065-1070, 1975. 2. Baloh, R. W., Kumley, W. E., Sills, A. W., e¢ al: Quan- titative Measurement of Smooth Pursuit Eye Movements, Ann. Otol. Rhinol, Laryngol, 85:111-119, 1976. 3. Baloh, R. W., Honrubia, V. and Sills, A.: Eye-Tracking and Optokinetic Nystagmus: Results of Quantitative Testing in Pa- tients with Well-Defined Nervous System Lesions. Ann. Otol, 86:108-114, 1977. 4, Lynch, J, C., Mountcastle, V. B., Talbot, W. H., et al: Parietal Lobe Mechanisms for Directed Visual Attention. J. Neu- rophysiol,, 40;:362-389, 1977. AMERICAN SOCIETY FOR HEAD AND NECK SURGERY CALL FOR PAPERS. The 26th Annual Meeting of the American Society for Head and Neck Surgery will be held May 9-10, 1984 at the Breakers in Palm Beach, Florida. Only original (unpublished and/or unpresented material) should be submitted. Manuscripts should be written in the format required by the Archives of Otolaryngology, the Society’s official journal, with the required number of copies sent to the Secretary of the Society or handled to the Secretary prior to presentation. Six (6) copies of a 250 word abstract should be submitted to the program chairman by September lst, 1983. Notifications of acceptances will be mailed November 15th, 1983. Please send six (6) copies of abstracts to: John M. Fredrickson, M.D., Program Chairman, Department of Otolaryngology, Washington University Medical School, 517 South Euclid, St. Louis, MO 63110. F265