reversed optokinetic nystagmus (okn): mechanism and clinical significance

Reversed Optohnetic Nystagmus (OKN): Mechanism and Clinical Signrficance

G. M. Halmagyi, FRACP, M. A. Gresty, PhD, and J. Leech

We studied reversed optokinetic nystagmus (OKN) in 31 patients and found that it is actually the patient’s own gaze-modulated spontaneous nystagmus shifted to the primary position of gaze by optokinetic stimulation. Two of our 3 1 patients were known to have congenital nystagmus. Most of the 29 others were adults who presented with neurological symptoms and nystagmus and were therefore suspected of having posterior fossa lesions. However, their nystagmographic findings and benign natural history suggest that they also had congenital nystagmus, which was unrecognized until they developed incidental neurological symptoms. These cases support the view that reversed OKN is pathognomonic of a benign, probably congenital, nystagmus.

Halmagyi GM, Gresty MA, Leech J: Reversed optokinetic nystagmus (OKN): mechanism and clinical significance. Ann Neurol 7:429-435, 1980

Normally the fast phases of optokinetic nystagmus (OKN) beat in the opposite direction to the movement of an optokinetic stimulus. O K N beating in the same direction, “reversed” OKN, was first described by Barany [ 2 ] , and later in more detail by Brunner [4], but its mechanism and clinical importance are still disputed. Since it occurs only in patients with spontaneous nystagmus, most explanations involve some interaction of spontaneous nystagmus with OKN [4, 121. While some writers hold that reversed OKN occurs exclusively in patients with congenital nystagmus [13, 141, others report its presence in patients with acquired neurological disease [ 12, 151. We have investigated 31 patients with reversed O K N and believe that the results clarify its mechanism and provide further evidence to show that it is pathognomonic of congenital nystagmus. (Throughout the text we follow the convention of designating the direction of a nystagmus by the direction of its beats or fast phases. Normally, a leftward moving optokinetic stimulus elicits a right-beating nystagmus. The beats of reversed OKN are in the same direction as the movement of the optokinetic stimulus.)

Materials and Methods Two of the 31 patients examined were known to have had nystagmus without other neurological abnormalities since infancy (i.e., congenital nystagmus) and were selected as controls to illustrate and explain the mechanism of reversed O K N . The other 29 were all those patients examined in the Hearing and Balance Unit between 1959 and

From the Medical Research Council, Hearing and Balance Unit, Institute of Neurology, and the Department of Neuro-oph- thalmology, National Hospital, Queen Square, London, En- gland.

1979 who were found to have reversed O K N but denied a lifelong history of spontaneous nystagmus. All had been referred for investigation of an obscure nystagmus of which they themselves had become aware only after seeking medical advice.

In addition to a routine clinical oculomotor examination, the following eye movements were examined by direct- current electrooculography:

1. Spontaneous nystagmus with the eyes held in at least three different positions ofgaze: the primary position (0 degrees), 30 degrees right, and 30 degrees left. Al- though we did not use a nystagmus velocity trace, we did try to identify the nystagmus waveforms according to the classification proposed by Dell’Osso and Daroff [81.

2. Optokinetic nystagmus. The stimulus was either a black-and-white striped curtain turning around the patient or a striped revolving drum 20 cm in diameter.

3. Pursuit. The stimulus which the patient tried to pursue was either an oscilloscope spot moving across a 60 cm screen with a triangular waveform or a small moving light bulb.

4. Visual suppression of vestibuloocular reflexes (VOR). This was assessed in 14 patients, who sat in a rotatable chair and were sinusoidally oscillated while viewing a small light fixed directly in front of them and moving with the chair.

Although the presence of latent nystagmus was specifically sought in each patient, binocular fixation was used in the experimental procedure.

Thirteen of the 29 patients not known to have congenital

Received June 12, 1979, and in revised form Aug 20. Accepted for publication Aug 30, 1979.

Address reprint requests to Dr Halmagyi, Medical Research Council, Hearing and Balance Unit, National Hospital, Queen Square, London W C l N 3BG, England.

0364-5134/80/050429-07$01.25 @ 1979 by Michael A. Gresty 429

@Right

- Drum Turning Right --Drum Turning L e f t - 1 sec U

nystagmus were examined on two o r more occasions, the interval between the first and last examination ranging from 6 months to 2 0 years. The other 16 patients were examined only once.

F i g 1 . Eye movement recordings in Patient I , with known congenital nystagmus. Spontaneous ny.itagmus beat t o the left on leftward gaze and in the primary position and beat t o the right on rightward gaze. There was right-beating nystagmuj with rightward optokinetic stimulation (reversed O K N ) and

Results Patients UJith Known Congenital Nystagmm PATIENT 1. This was a 10-year-old boy known since infancy to have nystagmus without any other neurological abnormalities. His pattern of spontaneous nystagmus during gaze holding is shown in Figure 1. When the patient tried to hold his eyes in the primary position (gaze angle, 0 degrees), he had a left-beating nystagmus with a saw-toothed waveform; 30 degrees to the right, a right-beating nystagmus with a pseudocycloid [81 waveform appeared. Around 20 degrees right there was a narrow zone of low-amplitude, pendular nystagmus-the neutral region.

When the patient looked straight ahead at either the drum or the curtain turning to the right, the nystagmus in the primary position changed from a left-beating, saw- toothed pattern to a right-beating, pseudocycloid type (Fig 1). When the curtain turned to the left, the left-beating nystagmus immediately reappeared. Because rightward optokinetic stimulation produced a right-beating nystagmus where before there was a left-beating nystagmus, one can confidently say that OKN to the right was reversed. However, since the patient already had a left-beating nystagmus in the primary position that remained basically un- changed during left optokinetic stimulation, one cannot be certain whether O K N to the left was truly reversed or whether the spontaneous left-beating nystagmus simply cancelled any tendency to develop a normal right-beating OKN.

PATIENT 2. This was a 20-year-old man also known to have nystagmus without other neurological abnormalities since infancy. His pattern of spontaneous nystagmus during gaze holding is seen in Figure 2. When the patient tried to hold his eyes in the primary position, he had a low- amplitude, bidirectional, jerk nystagmus [S]. With the eyes held at gaze angles greater than 15 degrees to the right, a right-beating nystagmus with a pseudocycloid waveform appeared. Similarly, gaze angles greater than 15 degrees to the left produced a left-beating nystagmus with a pseudocycloid waveform. Between 15 degrees right and 15 degrees left he had a wide neutral zone.

When the patient viewed the optokinetic curtain turning to the right at 35 degrees per second, the nystagmus in the primary position changed from a bidirectional jerk type to a right-beating, pseudocycloid nystagmus (Fig 2); when the curtain moved at 15 degrees per second this change was

left-beating nystagmus with leftward optokinetic stimulation (? reversed OKNi. See text for details.

less obvious. When the curtain moved at 30 degrees per second to the left, left-beating pseudocycloid nystagmus appeared in the primary position. The patient was asked to pursue a single stripe of the curtain as it moved across the field of gaze, and the results with four different stimuli are also shown in Figure 2. When he pursued a stripe moving to the right at 15 degrees per second, right-beating nystagmus first appeared as the eyes passed through the primary position; when the stripe moved at 35 degrees per seLond, right-beating nystagmus was evident throughout the field of gaze (30 degrees left to 30 degrees right). When he pursued a stripe moving to the left at 10 degrees per second, left-beating nystagmus first appeared as the eyes passed through the primary position; when the stripe moved at 30 degrees per second, left-beating nystagmus was evident throughout the field of gaze. Eye movements during pursuit of the oscilloscope spot were the same as these eye movements in pursuit of the single optokinetic stripe.

During VOR suppression, with the head moving at 13 degrees per second (0.5 Hz), there was nystagmus beating in the direction of head movement (Fig 2). It had a pseudocycloid waveform and its maximum slow phase velocity exceeded maximum head velocity.

Patients Not Known to Have Congenital Nystagmus Each patient had been referred by a neurologist for further investigation of obscure nystagmus. None of the patients themselves or any of their relatives interviewed had been previously aware of the nystagmus. There were 17 males and 12 females ranging in age from 10 to 58 years at the time of presentation (mean age, 35 years). Their chief complaints were headache in 17, dizziness or imbalance in 7, oscillopsia in 8, blurred vision in 7, diplopia in 4, loss of con- sciousness in 4, parasthesias in 2, and failing memory in 1. The 8 patients with oscillopsia had noted this symptom only on lateral gaze or when trying to follow a moving object; 4 had been aware of it most of their lives, whereas the other 4 had noticed it only recently. Two asymptomatic patients had first con-

430 Annals of Neurology Vol 7 No 5 May 1980

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Fig 2. Eye movement recordings in Patient 2, with Known congenital nystagmus. Spontaneous nystagmus from 15 degrees right to 15 degrees left had a bidirectional, jerk waveform. With gaze further t o the right the nystagmus was right beating; with gaze further left , left beating. During optokinetic stimulation the patient either looked straight ahead or followed a single stripe of the curtain. Wi th rightward stimulation, right-beating nystagmus appeared throughout the field of gaze; with leftward stimulation, left-beating nystagmus (bilaterally reversed OKN) was seen. Nystagmus during vestibuloocular reflex (VOR) suppression looked like the patient's own gaze-evoked congenital nystagmus. See text for details.

sulted optometrists. Six patients were having psychi- atric treatment for anxiety or depression, 3 were in- volved in compensation claims for injury, and 2 had been discharged from the Armed Forces with a diagnosis of presumed multiple sclerosis.

All patients except 1 had better than 6/12 vision. Eighteen had nystagmus to the left and right only in eccentric gaze; 11 had some nystagmus in the primary position as well. None of the patients who complained of blurred vision had major nonrefrac- tive visual sensory abnormalities, and none of those who complained of diplopia had a paralytic strabis- mus. All had normal vertical eye movements.

Sixteen patients were reported to have neurological signs other than nystagmus: in 14 these signs

could not be consistently elicited, and in 2 they were caused by peripheral neuropathy. Seventeen patients whose nystagmus was initially thought to be due to acquired neurological disease had special investiga- tions such as a CT scan, lumbar puncture, or air en- cephalogram, but no relevant abnormalities were detected. One patient had two air encephalograms 15 years apart. Two patients were thought to have hys- terical conversion reactions: 1 had bizarre involun- tary movements and the other an unexplained visual loss.

In 9 of the 18 patients who had spontaneous nystagmus only in eccentric gaze, the nystagmus was more marked to one side than the other. In the 11 patients who had primary position nystagmus as well, the nystagmus in the primary position was barely detectable. The predominant nystagmus waveform was saw-toothed in 19 and pseudocycloidal [8 ] or jerk with extended foveation [8] in 10. Four patients had latent nystagmus.

During optokinetic stimulation, O K N was bilaterally reversed in 21 patients and unilaterally reversed in 8. Nystagmus reversal tended to occur at certain specific optokinetic stimulus velocities for each patient and in each direction. There was no obvious re- lationship between stimulus velocity and the slow phase velocity of the reversed OKN. Pursuit was examined at several different velocities in 19 patients.

Halmagyi et al: Optokinetics in Congenital Nystagmus 431

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VOR Suppression

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Optokinetic Curtain Turning Right

Optokinetic Curtain Turning Left EOI ;

In each, pursuit was interrupted by nystagmus beating in the direction of target movement, so that during pursuit, nystagmus was evident at gaze angles which were free of nystagmus during gaze holding. In each of the 14 patients examined during VOR suppression, low-velocity head movement produced high-velocity nystagmus beating in the direction of head movement.

Thirteen patients were reexamined an average of 12 years after the nystagmus was first detected (range, 6 months to 27 years). None has developed any other neurological symptoms or signs so far, and none has shown any major change in the appearance of the nystagmus. Three other patients wrote that they were well after 10, 11, and 14 years. The 13 patients who did not return for review could no longer be contacted at their old addresses.

Two typical case histories follow.

PATIENT 3. A 23-year-old man who drank alcohol regularly complained of headaches, blurred vision, and numbness in his feet for 18 months. O n examination he had nystagmus to the left and right in eccentric gaze and some variable reflex and sensory changes in his legs. He denied oscillopsia but did admit that his vision blurred when he tried to follow moving objects with his eyes. He was suspected of having multiple sclerosis, but the visual evoked responses and cerebrospinal fluid immunoglobulin levels were normal.

At gaze angles between 30 degrees right and 5 degrees left, there was no spontaneous nystagmus (Fig 3). At 40 degrees right a right-beating, pseudocycloid nystagmus appeared; 10 degrees to the left a left-beating, saw-toothed nystagmus was seen although it became regular and sus- tained only at 40 degrees to the left.

During optokinetic stimulation at three different velocities to the right and to the left, the patient showed nystagmus (Fig 3). When the curtain turned to the right at 20

F i g 3 . Eye movement recordings in Patient 3 , not known t o have congenital nystagmus. Spontaneous nystagmus was absent with gaze from 30 degrees right t o 5 degrees left. Further right there was a right-beating nystagmus; further left, left- beating nystagmus. Rightward optokinetic stimulation at 40 degrees per second induced right-beating nystagmus (reversed OKNi. Leftward optokinetic stimulation did not produce left-beating nystagmus. Right-beating nystagmus occurred during attempted vestibuloocular reflex (VOR) suppression t o the right. See text for details.

degrees per second, left-beating nystagmus was seen in the primary position with a slow phase velocity of 14 degrees per second; at 30 degrees per second the nystagmus became disorganized, but at 40 degrees per second a regular, right-beating pseudocycloid nystagmus suddenly appeared in the primary position. When the curtain turned to the left up to 120 degrees per second, only right-bearing nystagmus was produced, although, unlike in normal subjects, the nystagmus slow phase velocity decreased with increasing stimulus velocity. This patient therefore had reversed OKN to the right.

During VOR suppression, with the head moving at 5 degrees per second (0.2 Hz), there was negligible nystagmus in either direction (Fig 3). When head velocity increased to 15 degrees per second (0.7 Hz), high-velocity, right- beating nystagmus appeared. During this part of the experiment the patient volunteered that rightward head turning reproduced precisely the “blurred” vision he had complained of. He also agreed that by “blurring” he meant an illusory movement of the target light.

We reexamined the patient after 18 months and found no change in his nystagmus. He had reduced his alcohol consumption, and his parasthesias had resolved. Slit-lamp examination of the iris at this time revealed numerous punctate areas of transillumination. As his hair is blond and his skin tans poorly, he probably has a form of ocuio- cutaneous albinism.


Right 30’

30’ ”A+-%- VOR suppression Left

Spontaneous Nysiagrnus

&- Optokinetic Curtain Turning Right -) Optoklnet tc Curiaon Turnlng L e t t 4 I100

F i g 4. Eye movement recordings in Patient 4, not known to have congenital nystagmus. Spontaneous nystagmus was absent with gaze from 15 degrees right to 5 degrees left. Bilaterally reversed OKN occurred with a stimulus moving at J degrees per second. Right-beating nystagmus was seen during rightward pursuit, left-beating nystagmus during leftward pursuit. Leftward pursuit reversed right-beating gaze-evoked nystagmus. Nystagmus velocity during vestibuloocular reflex (VOR) suppression exceeded head velocity. See text for details.

PATIENT 4 . A 38-year-old woman complained of headache and blurred vision. She had experienced blurred vision for many years, especially when she tried to look at moving objects. Apart from nystagmus to the right and left in eccentric gaze and a symmetrical sensorineural hearing loss for high tones, there was no neurological abnormality.

There was no spontaneous nystagmus between 15 degrees right and 5 degrees left (Fig 4). Further to the right a right-beating nystagmus developed, and further to the left a left-beating nystagmus appeared. The nystagmus waveform alternated between saw-toothed and pseudocycloid.

During optokinetic stimulation, when the curtain turned at 5 degrees per second to the right, right-beating nystagmus immediately appeared in the primary position; when the curtain turned to the left at 5 degrees per second, left- beating nystagmus appeared (Fig 4 ) . Therefore this patient had bilaterally reversed O K N .

When the patient tried to pursue a target moving at 7 degrees per second from 30 degrees left to 30 degrees right, right-beating nystagmus first appeared as the eyes passed through 15 degrees left (Fig 4). When she tried to pursue from 30 degrees right to 30 degrees left, left- beating nystagmus was seen throughout the entire movement. Figure 4 also shows the result of suddenly stopping the pursuit target as it passed through 25 degrees right: the left-beating nystagmus that was generated during the brief

period of leftward pursuit (from 30 degrees left to 25 degrees left) quickly changed to right-beating nystagmus, ap- propriate for gaze holding at 25 degrees right. When the target again moved to the left, the left-beating nystagmus immediately reappeared. This patient also remarked that the experiment reproduced the visual blurring she had noted in her daily life.

During VOR suppression, head movement at 10 degrees per second (0.2 Hz) produced nystagmus in the primary position, beating in the direction of head movement (Fig 4 ) . The maximum slow phase velocity of the nystagmus exceeded maximum head velocity.

Nine years later we reexamined this patient and found n o change in her nystagmus. She had developed no other neurological symptoms or signs, and her deafness was the same as before.

Discussion We interpret the results of our studies of nystagmus during pursuit as follows. In some patients with congenital nystagmus ( e g , Patient 2) as well as in others with reversed OKN, attempted smooth pursuit provokes spontaneous nystagmus beating in the direction of target movement. Consider for example the second patient’s primary position nystagmus (see Fig 2): when he tried to hold his eyes in the primary position he had a bidirectional jerk nystagmus; when his eyes passed through the primary position in pursuit of a rightward moving target he had a right- beating nystagmus; when he pursued leftward through the primary position he had a left-beating nystagmus. In fact, when he tried to pursue in either direction at 35 degrees per second, he had nystagmus beating in the direction of target movement throughout the field of gaze. All our patients with reversed


OKN who had adequate testing of pursuit at various velocities (19 out of 29 patients) showed this abnormality. Patient 4 had it to an exceptional degree: in her case, leftward pursuit actually reversed the right-beating nystagmus evoked by rightward gaze holding (see Fig 4).

The results in Patient 1 during optokinetic stimulation (see Fig 1) show that the right-beating, primary position nystagmus induced by rightward optokinetic stimulation was identical in waveform to the right- beating nystagmus with gaze held at 30 degrees right. That is, optokinetic stimulation induced reversal of the spontaneous primary position nystagmus. The second patient’s right-beating primary position nystagmus evoked by rightward optokinetic stimulation (i.e., the reversed OKN) was identical in waveform to his right-beating nystagmus during rightward pursuit through the primary position, and similarly, the left-beating nystagmus evoked by leftward optokinetic stimulation was identical to the left-beating nystagmus during leftward pursuit through the primary position. Reversed O K N is therefore the patient’s own gaze-modulated nystagmus shifted to the primary position by optokinetic stimulation. The recordings published by Adams and Staewen [ 13 actually show that the waveform of reversed O K N is identical to the patient’s own gaze-modulated nystagmus.

VOR suppression was abnormal in all the patients we tested. Whereas normal subjects are able to sup- press their VOR until head velocity reaches about 60 degrees per second (0.8 to 1.0 Hz) 131, our patients produced nystagmus at much lower head velocities. The fact that the nystagmus slow phase velocity exceeded head velocity and the distinctive shape of the nystagmus slow phases (pseudocycloid in patients with a pseudocycloid spontaneous nystagmus) sug- gested that attempted suppression of VOR, like attempted pursuit, provoked the patient’s own spontaneous nystagmus. Thus, nystagmus during VOR suppression may, wholly or in part, represent the patient’s own nystagmus combined with an indeter- minate amount of unsuppressed induced vestibular nystagmus.

These observations are consistent with the estab- lished association between pursuit and VOR suppression in both normal subjects 131 and patients with neurological disorders [9, 11, 161. With head movement to the right, the VOR tends to move the eyes to the left and is normally suppressed by a pursuit movement to the right. In these patients this pursuit movement shifts the neutral zone to the left so that a right-bearing congenital nystagmus appears in the primary position. Head movement to the left, by the same mechanism, induces a left-beating congenital nystagmus. These results show therefore that the position of the neutral zone in patients with congenital

nystagmus is not only a function of intended eye position but also a function of intended eye velocity.

We suggest that the spontaneous nystagmus in our 29 patients had actually been present unnoticed since infancy. That is, they had a form of congenital nystagmus. The diagnosis of congenital nystagmus is easily made in infancy if there is nystagmus in the primary position. If, however, nystagmus is present only on eccentric gaze and the patient has a wide neutral region around the primary position, the abnormality may well escape detection until a medical examination is performed in adult life.

Our 29 patients had the following in common with patients who are known to have congenital nystagmus: (1) the nystagmus was purely horizontal, and there were no vertical eye movement abnormalities; (2) 10 patients had congenital nystagmus by waveforms [8]; (3) 4 patients had latent nystagmus (a form of congenital nystagmus) and 1 had oculocutan- eous albinism (a disorder usually associated with congenital nystagmus); and (4 ) to our knowledge, none of the patients has developed any other relevant neurological abnormalities.

Eight of our 29 patients complained of oscillopsia in eccentric gaze. Godde-Jolly and Lanthony 1101 similarly reported that about a quarter of their patients with congenital nystagmus who had a useful neutral region complained of oscillopsia in eccentric gaze.

In the absence of other neurological signs, the combination of headache, visual disturbance, and imbalance is highly suggestive of a lesion at the level of the foramen magnum or within the fourth ventricle. O n this suspicion, 17 of our 29 patients had special investigation of the posterior fossa. The demonstra- tion of reversed O K N would have simplified diagnosis in these patients; it would have proved that the spontaneous nystagmus was not due to acquired or progressive neurological disease and that it was ir- relevant to the patient’s complaint of headache. Some have, however, reported the association of reversed O K N with acquired neurological disease [ 12, 141. Two possible explanations for this are: (1) the neurological disease was coincidental, as in our patient with peripheral neuropathy and reversed OKN, or (2) OKN was not truly reversed but was confused with spontaneous nystagmus evoked by gaze devia- tion in the direction of movement of the optokinetic stimulus.

Ordinarily, the predominant direction of gaze during OKN shifts in the direction of either the slow phases (“active” OKN) or the fast phases (“passive” OKN) 1121. Consider a patient with a right-beating gaze-evoked nystagmus who is subjected to rightward optokinetic stimulation. If his gaze deviates to the right-that is, the direction of optokinetic slow


phases (“active” 0KN)-the right-beating spontane- 011s nystagmus is evoked and may overcome any left-beating O K N that is induced. The result is a righ:-beating or apparently reversed O K N (we have actual!y recorded this in a patient with cerebellar de- generation and bilateral gaze-evoked nystagmus).

In contrast, our 3 1 patients showed no such shift in the predominant direction of gaze. For example, Pa- tient l had a left-beating nystagmus during gaze- holding in tht primary position. During rightward optokinetic stimdation, right-beating nystagmus appeared without any shift in the predominant direction of gaze (see Fig 1). Patient 4, who had no primary position nystagmus, produced reversed OKN in each direction without agaze shift to account for it. In fact, during leftw‘rd optokinetic stimulation (left-beating nystagmus), the eyes at first shifted slightly to the right, that is, opposite to the direction which would evoke a sp mtaneous left-beating nystagmus. Patients with revDrsed OKN have a unique eye movement abnormality that accounts for their reversed OKN: optokinei-ic (or pursuit) stimulation in one direction induces a shift in the neutral point of spontaneous nystagmus irl the opposite direction so that the nystagmus becomes evident in the primary position.

It is possible that in some patients with congenital nystagmus, reversal of opi okinetic and pursuit reflexes is due to abnormal decussation of the visual system and is the cause of the spontaneous nystagmus. Collewijn and van d:n Mark [ 5 ] have, for example, induced spontaneous nystagmus in rabbits by artificially reversing thei,- optokinetic reflexes. This experiment was based on open-loop positive feedback of position signals from a mobile covered eye to control the mobile visual scene of an immobile seeing eye. Albino rabbits normally show reversed OKN when the optokinetic stimulus is limited to the posterior (i.e., temporal) retina [b] . Congenital nystagmus is common in albino humans, and although we know of no comprehensive study of optokinetic OKN in such patients, our third patient with reversed OKN did have a form of albinism. Abnormal decussation of temporal retinal fibers, which occurs in albinos of many species, including humans [ 7 ] , may account for the reversal of OKN, at least in rabbits [61. Perhaps a similar abnormal decussation exists in hu-

mans with reversed O K N who are not overtly albino tic.

~ ~~ ~~~~ ~

Dr. Halmagyi was supported by an Alexander Piggott Wehrner Fellowship from the Medical Research Council and by a grant from the Mason Medical Foundation.

We are grateful to the physicians and surgeons of the National Hospital, Queen Square, who referred the patients, and to those patients and volunteers who took part in the study.

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reversed optokinetic nystagmus (okn): mechanism and clinical significance

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