Lightning eye movements

Journal of the Neurological Sciences, 27 (1976)71-78 © Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands

71

L I G H T N I N G EYE M O V E M E N T S

J. N. ALPERT, H. SUGA and E. PERUSQUIA Department of Neurology, St. Luke's Episcopal Hospital, Texas Medical Center, Houston, Tex. 77025 (U.S.A.)

(Received 2 June, 1975)

SUMMARY Physiologic studies were performed on a patient who demonstrated lightning eye movements, palatal myoclonus and myoclonic jerks of the left platysma and sternocleidomastoid muscles. The myoclonus and lightning eye movements were separate phenomena with no defined relationship to each other. Analysis of this ocular dyskinesia identified strictly horizontal saccadic oscillations, 2 to 5 Hz in frequency, with amplitudes varying greatly but often reaching 25 °. A brief stationary period between each saccadic oscillation was frequently observed. They were particularly induced by vertical or horizontal ocular pursuit as well as sustained upward or downward ocular deviation. Caloric nystagmus abolished the oscillations but they persisted, irregularly, during optokinetic nystagmus. Thus a faulty visual fixation mechanism is postulated to precipitate lightning eye movements. Contrast studies revealed a mass lesion arising from the right dorsolateral portion of the medulla. These results indicate that lightning eye movements occur with caudal as well as rostral brain-stem lesions. From the clinical findings cerebellar pathway involvement is likely.

INTRODUCTION Lightning eye movements (LEM) are an uncommon ocular dyskinesia. There is only one previous clinical report (Atkin and Bender 1964). Several other ocular dyskinesias have been described including ocular dysmetria, cerebellar "kippdeviationen", flutter-like oscillations, saccadic nystagmus and opsoclonus (Orzechowski

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72 1927' Cogan 1954; G o l d b e r g and Jampel 1963; D a r o f f a n d Hoyt 1971" Ellenbergcr. K e t t n e r and Stroud 1972' Alpert, Coats and Perusquia 1975). These have generztlly been a t t r i b u t e d to cerebellar disease (Cogan 1954; G o l d b e r g and Jampel 1963: Ross and Z e m a n 1967; Bray, Ziter, Lahey and Myers 1969; Ellenberger and Netsky 1970; Daroff a n d Hoyt 1971; Ellenberger et al. t972; Alpert et al. 1975). Ellenberger et al. feel that these dyskinesias are a b n o r m a l i t i e s of the o c u l o m o t o r saccadic system. Cogan has interpreted ocular dysmetria and flutterlike oscillations as due to an impaired ocular fixation m e c h a n i s m u n d e r cerebellar control. K o r n h u b e r attributed " k i p p d e v i a t i o n e n " to defective cerebellar inhibition of mesencephalic reticular f o r m a t i o n ( D a r o f f a n d Hoyt 1971). This case report and physiologic study deals with a patient who d e m o n s t r a t e d both lightning eye m o v e m e n t s and palatal myoclonus. Studies confirmed a mass lesion arising from the dorsolateral p o r t i o n of the medulla. Physiologic data revealed the lightning eye m o v e m e n t s to be saccadic oscillations but suggested that defective ocular fixation plays the m a j o r role in this particular ocular dyskinesia. Case report

A 30-year-old woman was admitted to the hospital in November, 1973 because of progressive unsteadiness and difficulty "focusing" her eyes. Present illness. The patient stated that her symptoms began in November, 1971 when she noted intermittent lightheadedness and faintness. Three months later she began to lose her balance and was admitted to a hospital for diagnostic evaluation. Her investigations included normal cerebrospinal fluid (CSF) examination, arteriography of the posterior circulation and pneumoencephalography. In January 1972 she was treated with prednisone but her symptoms became progressively worse. She felt that her eyes were moving uncontrollablyand consequently had difficulty in reading. There was progressive loss of balance. She had intermittent numbness as well as hot and cold sensations on the left side of the body. Three weeks prior to readmission the patient noted a constant "heart beat" in the left side of the neck with a similar sound in the left ear. Past history, family history and social history were noncontributory. Review of systems was unremarkable except for intermittent epigastric burning associated with nausea and vomiting. Physical examination

Vital signs and general physical examination were normal. Neurologic examination revealed "scanning" speech. There were abnormal ocular, palate and neck movements described separately below. Atrophy and fasciculations were noted on the right side of the tongue. There was bilateral finger-to-nose dysmetria. Gait was slightly wide-based and heel-toe walking was poorly performed. Reflex and sensory examinations were normal. Examination o f eye, palate and neck movements

There was persistent, intermittent spontaneous oblique nystagmus with the quick phase directed upward and to the right. This was present in all directions of gaze except for downward eye deviation. This nystagmus was frequently interrupted by rapid saccadic shifts in the horizontal plane. These latter movements appeared to be induced by a change in visual fixation and especially on upward eye deviation. They appeared grossly to be of moderate to large amplitude. During attempted smooth pursuit, a combination of spontaneous nystagmus and saccadic eye movements were seen. Ocular dysmetria was intermittently present but could not be consistently elicited, possibly because of other superimposed abnormal eye movements. Optokinetic nystagmus was elicited only in the vertical plane, upward better than downward. Continuous symmetrical oscillations of the soft palate were observed. These oscillations were of small amplitude and were rapid, and alternating between elevation and depression. The movements seemed to be of equal velocity in both directions. There was no apparent association with the rapid saccadic eye movements but the relationship with the spontaneous oblique nystagmus could not be ascertained visually. Occasional irregular myoclonic jerks were noted of the left platysma and

Fig. 1. A : pneumoencephalogram demonstrating elevation of the fourth ventricle on the right side. B" lateral view shows mass in floor of fourth ventricle (small arrow) while the diameter of the upper brain stem (long arrow) is not increased.

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Fig. 2. Electroencephalographic recordings of spontaneous eye movements during direct forward gaze. As in all records shown in this report, upward deflections correspond to eye movements upward in the vertical channel and to the right in the horizontal channel. The high amplitude spikes seen in the vertical channels are blink artifacts. The eyes-open records (top 2 traces) were obtained with the patient in the sitting, head upright position, fixating on a spot 3 ft away. Fig. 3. Pursuit test (sinusoidal tracking test) demonstrating horizontal saccadic oscillations during both horizontal (upper 2 traces) and vertical (lower 2 traces) pursuit. Fig. 4. Gaze test reveals occasional small amplitude saceades and persistent upward beating nystagmus. Fig. 5. Upward gaze (upper 2 traces) and downward gaze (lower 2 traces) elicit bursts of high amplitude horizontal saccadie oscillations.

sternocleidomastoid muscles. There were no obvious precipitating factors nor any definite relation with either eye or palate movements.

Laboratory data Complete blood count, blood urea nitrogen, fasting blood sugar, liver functions and urinalysis were normal. Serology was non-reactive. Chest and skull films, barium enema and upper gastro-

75 intestinal series were normal. Gall bladder X-rays revealed cholelithiasis. An electrocardiogram, electroencephalogram and brain scan were normal. The CSF protein was 37 mg/100 ml and immunoelectrophoretic patterns were normal. Spinal fluid serology was negative and no cells were seen. Vertebral angiography showed equivocal signs of an intramedullary mass. Pneumoencephalography clearly defined a mass lesion arising from the right dorsolateral portion of the medulla (Fig. 1). Hospital course

The patient had repeated episodes of severe vomiting with occasional hematemesis. Gastroscopy revealed a healed Mallory-Weiss tear at the gastroesophageal junction. Radiotherapy was given to the brain stem for a total of 5000 rads over 5 weeks. The neurologic status remained unchanged during this period. Methods

Recording procedure. Eye movements were recorded with a 6-channel pen-writing recorder with a rectilinear pen linkage. Frequency response (3 db down points) was 0.1 to 15.6 Hz. Gain was fixed at 100/~V per cm for all tests. Paper speed was 10 mm/sec. Electrodes were placed lateral to the outer canthi to record horizontal eye movements and above and below the right eye to record vertical eye movements. During one recording an electrode was pasted to the soft palate. The electro-oculographic examination consisted of the following tests: (1) calibration and gaze test; (2) sinusoidal tracking test, in which the patient followed a sinusoidally moving spot of light that was projected onto the wall; the spot subtended an angle of ± 20 ° from center and we tested with frequencies of 0.3 and 0.6 Hz; (3) optokinetic test; (4) position tests with examination for nystagmus in the sitting, supine, right and left lateral and head-hanging positions; and (5) caloric tests according to the Fitzgerald-Halipike procedure. The gaze, optokinetic and sinusoidal tracking tests were done in both vertical and horizontal directions. Results

Fig. 2 compares spontaneous eye movements during visual fixation and after eye closure. There is persistent upward nystagmus with a rightward beating component which is enhanced on eye closure. There are occasional spontaneous horizontal saccades which average about 5 ° in amplitude and are not evident with eye closure. Fig. 3 is a tracing of ocular pursuit in vertical and horizontal planes. Upward nystagmus is recorded in both vertical channels simultaneously with horizontal saccadic movements. The latter are seen most frequently during leftward and downward pursuit. There are up to 5 saccadic movements per sec with a brief stationary period usually noted between each movement. Amplitudes of up to 25 ° are seen and contrast sharply with small amplitude oscillations recorded during visual fixation. Horizontal ocular deviation (Fig. 4) results in persistent upward nystagmus with a rightward beating component whereas there is no clearly directed horizontal component on left lateral gaze. Occasional small amplitude saccades are seen interspersed with the nystagmus in the horizontal channels. Vertical ocular deviation (Fig. 5) elicits bursts and intermittent high amplitude saccadic oscillations. These are superimposed on the upward nystagmus present on both upward and downward gaze. Induced horizontal optokinetic nystagmus (Fig. 6) elicits saccadic oscillations when quick phases of nystagmus should be leftward directed (horizontal trace - left to right). Rare saccades are noticed with the stimulus moving from right to left. Upward nystagmus is present throughout the tracing. During induced vertical optokinetic nystagmus (Fig. 7) occasional saccades are seen when the stimulus moves downward. No downward beating nystagmus was elicited. Caloric nystagmus (Fig. 8) effectively abolishes these saccadic oscillations both with the eyes open and closed. Slow phase velocities increased with visual fixation demonstrating "failure of fixation suppression", a sign suggesting brain stem or cerebellar pathology (Alpert 1974). There was no frequency relationship between the palatal myoclonus and the saccadic oscillations (Fig. 9). The spontaneous oblique and upward beating nystagmus rarely appeared to be equal in frequency to the palate movements. The frequency of the spontaneous nystagmus was altered by numerous factors including ocular deviation, eye closure, and induced nystagmus. Saccadic oscillations were associated with a reduced frequency of the spontaneous nystagmus. Conversely palate movements remained at approximately 180/min and unaltered by factors which affected the nystagmus. These findings contrast with previous reports of synchronous ocular and palate movements (Bender, Nathanson and Gordon 1952; Cooper 1958; Yap, Mayo and Barton 1968).

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Fig. 6. Horizontal optokinetic nystagmus demonstrating quick phases only to the right with saccadic oscillations noted in lower horizontal trace. Fig. 7. Vertical optokinetic nystagmus demonstrating occasional horizontal saccades when upward beating nystagmus is elicited. Downward nystagmus is not produced. Fig. 8. Caloric nystagmus demonstrating absence of saecadic oscillations and enhancement of nystagmus slow phase velocity with eye opening (arrows). Fig. 9. Tracings of vertical nystagmus, lightning eye movements, and palatal myoclonus demonstrating no relationship between these phenomena. DISCUSSION

Atkin and Bender first characterized lightning eye movements (Atkin and Bender 1964). One o f their cases manifested conjugate horizontal saccadic eye movements in bursts o f 3 to 4 movements lasting less than 0~5 sec, generally 3-5 ° in amplitude, induced by upward gaze with a brief stationary period between successive jerks. Occasionally a monocular adducting jerk occurred. Anatomic analyses revealed

77 bilateral lesions in the region of the pretectum and paramedian zone of the pontine reticular formation (PPRF). Experimental work in the rhesus monkey by Pasik, Pasik and Bender (1969), appeared to confirm the above observations. However, the experimentally-induced lightning eye movements from pretectal lesions resulted mainly in vertical oscillations with the oculogram demonstrating what appear to be both quick and slow phases suggesting nystagmus, rather than saccadic oscillations with a stationary period between successive jerks. Cogan has described "flutter-like oscillations" in patients with cerebellar disease (Cogan 1954). His description includes to and fro pendular oscillations, often associated with a change in fixation, of small amplitude and with a frequency of about 10 Hz. He attributed this ocular dyskinesia to faulty fixation mechanisms regulated by cerebellar structures. Unfortunately no eye movement recordings were included to facilitate comparison with other reports. Goldberg and Jampel have also described flutter-like oscillations in cerebellar disease. They described the eye movements as horizontal, pendular, occurring during fixation and saccades, with a frequency of about 10 Hz and a amplitude of 5-10 °. In 1 case there was an increased frequency with blinking, eye closure and fatigue. Opsoclonus is manifested by irregular multidirectional chaotic saccades which are most often described as conjugate. It is precipitated by visual fixation, usually constant, and present during both wakefulness and sleep. Cerebellar "kippdeviationen", analyzed by Kornhuber, are horizontal conjugate oscillations suppressed by visual fixation, released by eyelid closure, with a frequency of 2.5/sec and amplitude between 10 and 30 ° (Daroff and Hoyt 1971). Saccadic nystagmus (Alpert et al. 1975) is a sustained horizontal ocular dyskinesia present only during visual fixation. The oscillations are conjugate, 2 to 3 Hz in frequency and varying between 3 and 7° in amplitude. Ellenberger et al. (1972) postulated that all ocular dyskinesias, dysmetria, flutter and opsoclonus are a manifestation of a disturbed saccadic oculomotor system. Their cases demonstrated increased dyskinesias when the saccadic system was active, during spontaneous gaze, quick phase of caloric and optokinetic nystagmus, and REM sleep. Conversely, the movements were reduced during ocular pursuit, lid closure and sleep. Our patient revealed an ocular dyskinesia corresponding to the cases of Atkin and Bender except for larger amplitude movements. The lighlning eye movements in our case were also strictly horizontal and most effectively induced by vertical and horizontal ocular pursuit and sustained upward or downward ocular deviation. Caloric nystagmus abolished the lightning eye movements. Thus, in contrast to Ellenberger's cases, the pursuit system was active when this dyskinesia was most prominent. Cogan's description and Goldberg and Jampel's recordings of flutter-like oscillations demonstrated pendular eye movements. Our recordings usually revealed a brief stationary period between the saccadic oscillations. Opsoclonus is precipitated by visual fixation but is present during sleep (Smith and Walsh 1960) and is multidirectional. "Kippdeviationen" are suppressed by visual fixation although also conjugate and horizontal. Conversely, lightning eye movements are only horizontal and present only during visual fixation.

78 F u r t h e r analysis o f o u r d a t a s u p p o r t s C o g a n ' s c o n t e n t i o n t h a t there is faulty h o r i z o n t a l o c u l a r fixation in m a n y o c u l a r dyskinesias. W h e n the fixation mechanism s h o u l d be active, d u r i n g p u r s u i t o f a moving target, lightning eye m o v e m e n t s were precipitated. This was m o s t evident d u r i n g midline vertical pursuit m o v e m e n t s when defects in h o r i z o n t a l fixation should be m o s t obvious. Eye m o v e m e n t s to the left o f the midline also elicited m o r e oscillations suggesting t h a t laterality m a y p l a y a role in visual fixation mechanisms. W i t h a t t e m p t s at visual fixation s t r a i g h t a h e a d the patient h a d r e d u c e d a m p l i t u d e o f the saccadic oscillations a l t h o u g h they were never abolished. The absence o f vertical oscillations suggests a s e p a r a t i o n o f vertical and h o r i z o n t a l c o n t r o l o f visual fixation. O p s o c l o n u s would a p p e a r to affect both systems. Several a d d i t i o n a l c l i n i c o - a n a t o m i c a l c o r r e l a t i o n s can be made. A right-sided m e d u l l a r y lesion was associated with m y o c l o n u s o f the left side o f the neck and symmetrical p a l a t a l m y o c l o n u s . This s u p p o r t s the clinical a n d e x p e r i m e n t a l observations o f Bender et al. (1952) a n d F r e e m a n (1933) who n o t e d c o n t r a l a t e r a l m y o c l o n u s following lesions in the region o f the inferior olive. O c u l a r dyskinesias m a y occur in the absence o f cerebellar disease a l t h o u g h cerebellar p a t h w a y s in b r a i n s t e m are p r o b a b l y involved in o u r patient. A p a r t i c u l a r f o r m o f o c u l a r dyskinesia, lightning eye m o v e m e n t s , occurs with m e d u l l a r y as well as pretecta 1 lesions. BIBLIOGRAPHY Alpert, J. N. (1974) Failure of fixation suppression - - A pathologic effect of vision on caloric nystagmus, Neurology (Minneap.), 24: 891-896. Alpert, J. N., A. C. Coats and E. Perusquia (1975) "Saccadic nystagmus" in cerebellar cortical at rophy, Neurology ( Minneap.) , 25: 676-680. Atkin, A. and M. B. Bender (1964) "Lightning Eye Movements" (ocular myoclonus), J. neurol. Sei., 1:2-12. Bender, M. B., M. Nathanson and G. G. Gordon (1952) Myoclonus of muscles of the eye, face and throat, Arch. Neurol. Psychiat. (Chic.), 68: 44-58. Bray, P. F., F. A. Ziter, M. E. Lahey and G. G. Myers (1969) The coincidence of neuroblastoma and acute cerebellar encephalopathy, J. Pediat., 75: 983-990. Cogan, D. (1954) Ocular dysmetria, flutter-like oscillations of the eyes and opsoclonus, Arch. Ophthal., 51 : 318-335. Cooper, J. (1958) Eye movements associated with myoclonus, Amer. J. Ophthal,. 46: 205-209. Daroff, R. B. and W. F. Hoyt (1971) Supranuclear disorders of ocular control systems in man Clinical, anatomical and physiological correlations. In: P. Bach-y-Rita, C. C. Collins and J. E. Hyde (Eds.), The ControlofEye Movements, Academic Press, New York, N.Y., pp. 191-195. Ellenberger, Jr., C., J. L. Keltner and M. H. Stroud (1972) Ocular dyskinesia in cerebellar discase, Brain, 95, 685-692. Ellenberger, Jr., C. and M. G. Netsky (1970) Anatomic basis and diagnostic value of opsoclonus, Arch. Ophthal., 83: 307-310. Freeman, W. (1933) Palatal myoclonus, Arch. Neurol. Psychiat. (Chic.), 29: 742-755. Goldberg, R. T. and R. S. Jampel (1963) Flutterlike oscillations of the eyes in cerebellar disease, Amer. J. OphthaL, 55: 1229-1233. Orzechowski, C. (1927) De l'ataxie dysmetrique des yeux, J. Psychol. Neurol., 35: 1-18. Pasik, T., P. Pasik and M. B. Bender (1969) The pretectal syndrome in monkeys, Brain, 92: 871-884. Ross, A. T. and W. Zeman, (1967) Opsoclonus, occult carcinoma and chemical pathology in dentate nuclei, Arch. Neurol (Chic.), 17: 546-551. Smith, J. L. and F. B. Walsh (1960) Opsoclonus-ataxic conjugate movements of the eyes. Arch. OphthaL, 64: 244-250. Yap, C., C. Mayo and K. Barron (1968) "Ocular bobbing" in palatal myoclonus, Arch. NeuroL (Chic.), 18: 304-310. -

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