Uniocular Nystagmus in Monocular Visual Loss

UNIOCULAR NYSTAGMUS IN MONOCULAR VISUAL LOSS ROBERT D. YEE, MD

and GLENN

W.

JELKS, MD

ROBERT

W.

BALOH, MD

VICENTE HONRUBIA, MD ALL BY INVITATION

LOS ANGELES, CALIFORNIA

Uniocular nystagmus was studied by electro-oculography in ten patients with monocular visual loss caused by ocular and optic nerve lesions. In these patients, visual loss was congenital or acquired in childhood or adult life. In all patients the oscillations were present in the primary position of gaze and were vertical, pendular, and of variable and low frequency (less than, or equal to, 1.0 Hz) and amplitude (usually less than 5°). Refixation saccades, smooth pursuit, optokinetic nystagmus, and vestibuloocular responses to rotation in the horizontal and vertical planes were within normal limits. The irregularity, low frequency, and low amplitude of this form of nystagmus cause it to often be missed during casual clinical examination, but easily differentiate it from other causes of uniocular nystagmus.

Submitted for publication Oct 25, 1978. From the Department of Ophthalmology (Drs Vee and Jelks). the Department of Neurology (Dr Baloh), and the Division of Head and Neck Surgery, Department of Surgery (Dr Honrubia). UCLA School of Medicine. Los Angeles. Presented at the 197R Annual Meeting of the American Academy of Ophthalmology. Kansas City. Mo. Oct 22-26. Reprint requests to Jules Stein Eye Institute. Department of Ophthalmology. UCLA School of Medicine. Los Angeles. CA 90024 (Dr Vee).

DISSOCIATED nystagmus in the primary position of gaze in which involuntary oscillations are present in only one eye is an unusual ocular motor sign. It had previously been described in spasmus nutans,l congenital nystagmus,2.3 and various disorders affecting the brainstem, such as multiple sclerosis,4.5 tumors,6 and syphilis. 7 The precise localization of lesions resulting in dissociated nystagmus in these disorders, however, is not known.

Uniocular nystagmus has also been described in monocular visual loss in early childhood, resulting from optic nerve glioma,8 opacities of the media, anisometropia, and strabismic amblyopia. 9 Features of the uniocular nystagmus in monocular visual loss that may differentiate it from dissociated nystagmus from other causes, however, have not been emphasized. The present study presents the spectrum of clinical features in patients with uniocular nystagmus and visual loss and characterizes the nystagmus and function of the ocular motor system in these patients quaptitatively by electro-oculography.

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METHODS Ten patients with severe monocular visual loss and uniocular nystagmus were studied. Nine of the patients were found within a sixmonth period during screening of outpatients in a general ophthalmology clinic. Monocular, vertical, and horizontal eye movement recordings were made with dc electrooculograms (EOGs).lO During recording of vertical eye movements, the upper eyelids were immobilized with cotton-tipped applicators to minimize eyelid movement artifacts. The band width of the recording system was 0 to 100 Hz. Eye movemen ts were displayed on a curvilinear chart recorder and recorded simultaneously on FM magnetic tape. Eye movement data stored on the tape were later digitized at 200 samples per second. Amplitude, velocity, and frequency of eye movements were analyzed quantitatively by a laboratory digital computer system.l1-1:l The nystagmus was recorded in the primary position of gaze, and the effects of eccentric gaze, monocular occlusion, eyelid closure, and darkness were studied. Smooth pursuit, saccadic, optokinetic, and vestibuloocular eye movements were studied in five patients. Details of the techniques for stimulating the smooth pursuit, saccadic, optokinetic, and vestibuloocular systems have been described previously.12-14 During all tests, the patient's head was immobilized, and stimuli were presented in both the horizontal and vertical planes. During stimulation of the optokinetic and vestibuloocular systems in the vertical plane, the patient's head was tilted toward the right shoulder. Smooth pursuit movements were induced

OPHTH AAO

by instructing the patient to track a luminous spot on a videoscreen that moved in sinusoidal patterns at 0.2 to 0.4 Hz and 30° amplitude. Saccadic eye movements were induced by instructing the patient to track the luminous spot moving in square-wave steps of random amplitude, direction, and frequency. Optokinetic nystagmus (OKN) was produced by placing the patient within a 125-cm diameter drum that was rotating sinusoidally at 0.05 Hz and peak amplitude of 60° /sec. The interior of the drum had 2.5-cm wide, white, vertical stripes placed every 15° on a black background so that the patient's entire visual field was stimulated. During stimulation of the vestibuloocular response (VOR), the patient was rotated sinusoidally in the dark at 0.05 Hz and a peak velocity of 60° /sec. The patient was asked to perform mental arithmetic during the test. To quantitate smooth pursuit, OKN, and VOR, the "gain" of each eye movement system (peak eye velocity/peak stimulus velocity) was calculated and compared with similar responses from normal subjects.

RESULTS

Clinical Features (Table

1)

The age of patients ranged from 15 to 56 years. Although five of the ten patients had histories of visual loss before the age of 10 years, five patients sustained uniocular visual loss after 10 years of age, three of them in adult life. The duration between loss of vision and exami-

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TABLE

513

1

CLINICAL FEATURES

PATIENT

ONSET* AGE (YR)

AGEt (YR)

VISUAL ACUITY

1

Birth

55

OD 20/25 OS Lpt

2

Birth

50

3

Birth

56

4

4

26

5

7

30

6

11

15

7

13

22

8

20

21

9

24

31

10

47

49

OD CF§ at 10 ft OS 20/20 OD 20/30 OS HMII OD 20/25 OS CF at 2 ft OD CF at 2 ft OS 20/20 OD 20/20 OS HM OD CF at 4 ft OS 20/20 OD CF at 5 ft OS 20/20 OD 20/200 OS 20/20 OD 20/100 OS LP

OCULAR LESION

OS: posterior staphyloma, posterior lenticonus, optic atrophy OD: strabismic amblyopia OS: congenital cataract, congenital glaucoma OS: corneal leukoma-keratitis OU: juvenile glaucoma OS: traumatic cataract OD: traumatic cataract OD: orbital cellulitis, optic atrophy OD: traumatic cataract, optic atrophy OD: immature, presenile cataract OS: mature, presenile cataract

• Age at which uniocular visual loss detected.

t Age at time of present study. tL.ight perception. §Counting fingers. IIHand movements.

na tion in this study ranged from one to 56 years. Interestingly, none of the patients had been diagnosed to have nystagmus until examination in this study, although all of them had had numerous ophthalmic examinations previously. Loss of vision was uniformly severe with visual acuity of 20/200 or less. Five patients had optic atrophy. Of the five patients without known damage to the optic nerve, four had opacities of the ocular media (cataract or corneal leukoma) and one had strabismic amblyopia.

Nystagmus Characteristics

(Table

2)

All patients had nystagmus only in the eye with visual loss. The nystagmus was present in the primary position of gaze in all patients and was chiefly vertical; small horizontal components were present in the nystagmus in two patients. The nystagmus waveform was pendular in all patients, with movements of approximately equal velocity in both vertical directions,

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TABLE

OP HTH AAO

2

NYSTAGMUS CHARACTERISTICS PATIENT

1 2 3 4 5 6 7 8 9 10

DIRE CTIO N

Vertical Vertical Vertica l Vertical Oblique Vertical Vertical Vertical Oblique Vertical

WAVEFORM

Pendular Pendular Pendular Pendular Pendular Pendular pendular Pendular Pendular Pendular

FREQUENCY (HZ)*

AMPLITUDE (O)t

1.5 3.8 4.0 6.5 5.2 4.0 3.5 2.0 10.0 3.5

1.0 0.8 0.7 0.9 0.8 0.7 0.4 0.5 0.3 0.6

'Mean frequency. tMean amplitude.

resembling sine waves (Fig 1). The vertical oscillations were of uniformly low velocity (less than 25° /sec), low frequency (less than 1.0 Hz), and small amplitude (maximum amplitude usually less than 5°). Characteristically, the nystagmus was extremely irregular in frequency and in amplitude and was often clinically noticeable only when exaggerated after refixation or maintained eccentric gaze. In three of eight patients tested, eccentric gaze increased the amplitude of the nystagmus, and in seven of the eight, the amplitude was increased after a horizontal or vertical refixation . In four of five patients tested, loss of fixation by the eye with normal vision because of darkness or eyelid closure did not affect the nystagmus; in the remaining patient, the . amplitude was decreased in darkness. Attempted convergence increased the amplitude in two of two patients tested.

Saccades and Smooth Pursuit

(Table

3)

Quantitative parameters of saccadic and smooth pursuit eye movements were similar in both eyes of each patient; only data from the eyes without nystagmus are presented. The latency, accuracy, and velocity-amplitude relationship of saccades in the vertical and horizontal planes in all the patients were within normal ranges established previously.12 In the visually impaired eyes, the pendular oscillations appeared to be superimposed on the normal saccadic movements (Fig 2). The mean gain (±SD) of smooth pursuit movements (eye velocity) in the horizontal plane in the normal subjects was 0.93± 0.111'\ in the vertical plane, 0.7B± 0.10. The mean gains of the horizontal and vertical smooth pursuit movements in the patients were 0.93±0.03 and 0.B7±0.06, respectively. These values were not signif-

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icantly different from those in the normal subjects (P>.lO, Student's t test). The pendular oscillations

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appeared to be superimposed on the pursuit movements in the visually impaired eyes. Optokinetic and Vestibuloocular Responses

A

The pattern of eye movements during optokinetic stimulation and rotation of the patients in the dark was similar to that in normal subjects (Fig 3). Optokinetic and vestibuloocular responses were quantitatively similar in both eyes of each patient; only data from the eyes without nystagmus are presented. The mean gain of the optokinetic response in the normal subjects was O.71±O.2214 in the horizontal plane and O.72±O.11 in the vertical plane. The horizontal and vertical gains in the patients were O.78±O.08 and O.71±O.12, respectively. There were no significant differences in these values between the normal subjects and patients (P>.lO).

15 de\lreesI

B

15 degreesI

c 15 dellreesI

Fig I.-Uniocular vertical nystagmus in primary position. Top, Right eye. Bottom, Left eye. A, Patient 4. B, Patient 5. C, Pa tient 9. Deflections up are upward ; down , downward .

In normal subjects, the mean gain of the vestibuloocular response

3

TABLE

SMOOTH PuRSUIT. OPTOKINETIC NYSTAGMUS, AND VESTIBULOOCULAR RESPONSE GAIN* SMOOTH PURSUIT

OPTOKINETIC NYSTAGMUSt

VESTIBULOOCULAR RESPONSEt

PATIENT

HORIZONTAL

VERTICAL

HORIZONTAL

VERTICAL

HORIZONTAL

VERTICAL

1 2 4 5 9

0 9. 2 0.93 0.95 0.90 0.96

0.88 0.90 0.90 0.85 0.84

0.85 0.81 0.80 0.65 0.80

0.60 0.82 0.81 0.60

0.68 0.46 0.42 0.46 0.58

0.40 0.54 0.52 0.67

"Gain: peak eye velocity/ peak stimulus velocity. tGain of slow cGmponent of nystagmus.

i

...

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A

15 degreesI

B

15 degreesI

15 degreesI

2 sec

I--i

Fig 2. -Vertical saccades in patient 4. A, T arget movement. B, Right eye. C, Left eye. Velocity a mplitude relati ons hip , accuracy, a nd latency a re no r ma l in both eyes, but uniocula r , vertical nystagmus is superimposed on saccades in left eye. Deflections up are upward ; down , downward.

15 B

c 60 degrees

I 2 sec I----i

Fig 3.-Vertical optokinetic nystagmus during sinusoidal drum rotation of 0.05 Hz and peak velocity of 60° I sec. A, OKN of normal subject. B, OKN of pa tient 4 (right eye). C , Drum velocity. Deflections up are upwa rd ; dGwn , downward.

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to rotation in the dark was 0.57+0.16 in the horizontal plane 14 and 0.40± 0.08 in the vertical plane. Comparable gains in the patients were 0.52±0.16 in the horizontal plane and 0.53±0.11 in the vertical plane, not significantly different from those in the normal subjects (P>.lO).

DISCUSSION

Severe loss of vision in one eye can produce a dissociated, vertical nystagmus of that eye. Visual loss can be present at birth or can be acquired in childhood or adulthood. The characteristics of the nystagmus observed in this study were similar to those described by Heinman. 15 The nystagmus is primarily vertical, although small horizontal components can also be present. The nystagmus has a pendular waveform, low frequency, and small amplitude. Characteristically, the frequency and the amplitude are irregular and are accentuated by eccentric gaze and refixation. The low frequency, small amplitude, and irregularity make the nystagmus difficult to detect during casual clinical observation. The fact that nine patients with this form of nystagmus were found during only a six-month period suggests that it is a common, although easily overlooked, sign in patients with uniocular visual loss. This form of nystagmus can be I differentiated from other forms of dissociated nystagmus in the primary position of gaze by its strict unilaterality, vertical direction, and low frequency. Uniocular, vertical nystagmus from other causes in humans, such as spasmus nutans and multiple sclerosis, as well as from an experimental lesion in the brain-

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stem of a monkey,16 have frequencies of at least 2 Hz. Although visual loss resulting in uniocular nystagmus was severe in all the patients, it was not necessarily permanent. Patient 10 had a mature, presenile cataract of the left eye and uniocular nystagmus with onset of visual loss in adulthood. After cataract surgery and aphakic correction with a contact lens in the left eye, the nystagmus disappeared. Quantitative study of the smooth pursuit, saccadic, optokinetic, and vestibuloocular systems in the horizontal and vertical planes in the ten patients demonstrates that these ocular motor systems are normal. Uniocular visual loss, therefore, is not associated with defects or adaptive changes in these systems. During attempted steady fixation of a target in normal subjects, the eyes are not stationary but are constantly making conjugate, micro-eye movements. 17 These movements are usually less than ten minutes in amplitude and consist of saccades, slow drifts of less than 20 mini sec in velocity, and an oscillatory tremor of usually greater than 20 Hz in frequency. The uniocular nystagmus observed in the ten patients does not appear to be an exaggeration of these micromovements. Most of the knowledge about the control of eye movements is of binocular movements. Little is known about central nervous system pathways controlling uniocular movements. Observations of uniocular nystagmus resulting from uniocular loss of vision, however, indicate that pathways for control of uniocular eye movements must

exist and that VISIOn in an eye is required for stabilization of that eye. The low velocity (less than 25° /sec) and unilaterality of the vertical oscillations suggest that uniocular nystagmus in the ten patients resulted from destabilized vergence eye movements. In a normal subject, vergence eye movements are induced by a change in the distance between the fixation point and the eyes and are disconjugate movements of low velocity (usually less than 20° /sec). If the fixation point is moved along the visual axis of one eye, that eye does not move, and a uniocular, vergence movement of the fellow eye is produced. 18 The vergence system is the only eye movement system capable of producing up.iocular movements in normal subjects. Elucidation of the anatomic location and physiologic function of unilateral pathways responsible for this uniocular nystagmus, however, must await other studies of the ocular motor control system in experimental animals and in humans.

ACKNOWLEDGMENT This work was supported by grant EY01853-02 from the National Institutes of Health and a grant from the Deafness Research Foundation.

Albrecht von Graefe's Arch Klin Ophthalmol 197:165-175, 1975. 4. Duane A: Unilateral and other unusual forms of nystagmus. NY State J Med 5:245-249, 1905. 5. Nathanson M, Bergman PS, Barker MB: Monocular nystagmus. Am J Ophthalmol 40:685-692, 1955. 6. Donin JF: Acquired monocular nystagmus in children. Can J Ophthalmol 2:212-215, 1967. 7. Duke-Elder S: System of Ophthalmology. St Louis, CV Mosby Co, 1971, vol 12, p 882. 8. Cogan DG: Neurology of the Visual System. Springfield, Ill, Charles C Thomas Publisher, 1966, p 191. 9. Duane A: Unilateral rotary nystagmus. Trans Am Ophthalmol Soc 11:63-67, 1906. 10. Vee RD, Wong EK, Baloh RW, et al: A study of congenital nystagmus: Waveforms. Neurology 26:326-333, 1976. 11. Sills AW, Honrubia V, Kumley W: Algorithm for the multi-parameter analysis of nystagmus using a digital computer. Aviat Space Environ Med 46:934-942, 1975. 12. Baloh RW, Sills A W, Kumley WE, et al: Quantitative measurement of saccade amplitude, duration and velocity. Neurology 25:1065-1070, 1975. 13. Baloh RW, Kumley WE, Sills AW, et al: Quantitative measurement of smooth pursuit eye movements. Ann Otol Rhinol Laryngol 85:111-119, 1976. 14. Honrubia V, Baloh RW, Lau CGY, et al: The patterns of eye movements during physiologic vestibular nystagmus in man. Trans Am Acad Ophthalmol Otolaryngol 84:0RL-339-0RL-347, 1977. 15. Heinman E: Einseitiger Nystagmus. Klin Monatsbl Augenheilkd 40:99-105, 1902.

REFERENCES 1. Cogan DG: Neurology of the Ocular Muscles, ed 2. Springfield, Ill, Charles C Thomas Publisher, 1956, p 192. 2. Kamel KS: Congenital nystagmus, report of a rare case of uniocular congenital nystagmus. Bull Ophthalmol Soc Egypt 67:349-352, 1974. 3. Komer F: Acquired and congenital monocular nystagmus, a comparative electronystagmographic study of two cases.

16. Jampel RS: Experimental monocular nystagmus in the monkey. Arch Ophthalmol 70:587, 1963. 17. Ditchbum RW: Eye Movements and Visual Perception. London, Clarendon, 1973, pp 78-93. 18. Zuber BL: Control of vergence eye movements, in Bach-y-Rita P, Collins C, Hyde J (eds): The Control of Eye Movements. New York, Academic Press Inc, 1971, pp 447-453.