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Vertical Ocular Dysmetria —Vertical Rebound Nystagmus and Optokinetic Vertical Ocular Dysmetria
Auris· Nasus· Larynx (Tokyo) 11, 91-100 (1984)
VERTICAL OCULAR DYSMETRIA -VERTICAL REBOUND NYSTAGMUS AND OPTOKINETIC VERTICAL OCULAR DYSMETRIAKyoko OHTSU Neurotological Clinic, Saitama Medical School, Saitama, Japan
Ocular dysmetria in vertical eye movement was confirmed by electronystagmographic recording in \ 00 cases. 1) Ocular dysmetria in spontaneous vertical ocular movement was reported in seven cases. It can be called vertical rebound nystagmus. This phenomenon was more prominent in vertical movement of the eyes returning from upward gazing to mid-position than in the movements of downward gazing. 2) Optokinetic vertical ocular dysmetria induced by vertical optokinetic stimulation was observed in 93 cases. This phenomenon was far more prominent in upward optokinetic nystagmus than in downward optokinetic nystagmus. 3) The pattern of optokinetic vertical ocular dysmetria was classified into the following four types: the dysrhythmic type, the overshoot type, the ataxic type and the saccadic (semi-inversive) type. 4) The pathophysiological mechanism of horizontal ocular dysmetria should be different from the mechanism of vertical ocular dysmetria. Ocular dysmetria was first described by OLZECHOWSKI in 1927. Thereafter Cogan described flutter-like oscillation (GOLDSTEIN and COGAN, 1961), KORNHUBER (1971) described Fixationsrucke, KIRIKAE and SAKATA (\965) described ataxic nystagmus and unregelmaessige Burste, and HOOD, KAYAN and LEECH (1973) described rebound nystagmus. Ever since, much attention has been paid to the cerebellar lesion as a cause of abnormal eye movement. However, concerning abnormal vertical ocular movement, only two papers have been published up to now; one by LESSER, SMITH and LEBENSON in 1973 and the other by ZEE et al. in 1976. There is no description of ocular dysmetria in the vertical plane, or of ocular dysmetria induced by optokinetic stimulation. The phenomenon of vertical ocular dysmetria which we describe in this report could be called rebound nystagmus in the vertical plane as it is very similar Received for publication June 7, 1983 91
92
K.OHTSU
to the rebound nystagmus in the horizontal plane reported by HOOD et al. (1973). Thus, we name this vertical ocular dysmetria "vertical rebound nystagmus (VRN)." We describe the existence of ocular dysmetria which is induced by vertical optokinetic stimulation and name this phenomenon "optokinetic vertical ocular dysmetria (OVOO)." We speculate on the pathophysiological mechanism of optokinetic vertical ocular dysmetria and vertical rebound nystagmus and we stress their importance for diagnosing lesions in the posterior fossa. CASES AND METHOD
One hundred cases of ocular dysmetria were subjected to electronystagmography. The chief complaints were mainly vertigo and dysequilibrium, and each case was examined neurologically and neurotologically. Neurotological examinations (SAKATA, SETOGUCHI and Hsu, 1968), mainly based on SAKATA'S maneuver (1970) were carefully performed, especially concerning spontaneous and induced nystagmus. In all the cases, the existence of a lesion in the posterior fossa was proved morphologically by studies such as CT-Scan, cerebral angiography and pneumoencephalography. Optokinetic nystagmus test was performed by using the apparatus of Ohm (SAKATA, 1971). Two different paper speeds were used to record optokinetic nystagmus: The optokinetic pattern (OKP) method (SAKATA, 1971) in which a paper speed of 0.1 em/sec is used to visualize the continuous optokinetic nystagmus as a simple pattern; and the optokinetic nystagmus (OKN) method with a faster paper speed of 0.5 em/sec, in order to examine the individual optokinetic nystagmus precisely. Optokinetic stimulations were given both in the horizontal and vertical planes. RESULTS
A.
Vertical rebound nystagmus (VRN) Rebound nystagmus was described by HOOD only in horizontal eye movement. However, the rebound phenomenon was also observed in vertical eye movement. In seven out of one hundred cases of ocular dysmetria, the vertical rebound phenomenon was observed. In all seven cases this phenomenon was observed in the movement of eyes returning from the eye position of upward gazing to the mid-position. But in only two cases out of seven was this phenomenon observed in the movement of the eyes returning to the mid-position from the eye position of downward gazing. Causal lesions of these cases varied. They consisted of three cases of occlusion of the superior cerebellar artery, two cases of occlusion of the basilar artery, etc. These lesions were all located relatively in the midline and also in the relatively rostral part of the posterior fossa (Table 1). Typical case. A thirty-two-year-old woman complained of dizziness on moving. After a while, the attacks of dizziness worsened and appeared frequently.
93
VERTICAL OCULAR DYSMETRIA Table 1. Seven cases of vertical rebound nystagmus with lesions confirmed morphologically. Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7
24F
Infarction of cerebellar vermis (occlusion of sup. cerebellar artery) 52F idem 36M Basilar artery syndrome (thrombosis of the perforating arteries) 63 F idem 32 F Sup. cerebellar artery syndrome 19 M Periaqueductal syndrome (atrophy of the sup. vermis) 36F Acoustic neurinoma (post-op)
M A
~ORWARD CA',
~~~ lO'CAL
~
M 1 1
2 sec
Fig. I. Case 5. 32-year-old female, sup. cerebellar artery syndrome. Upbeat nystagmus is seen during upward gazing, and the vertical rebound nystagmus is seen when the eyes are returning from the position of upward gazing to the mid-position or eye position of forward gazing. A: Horizontal component of eye movement. B: Vertical component of eye movement.
Two years before admission to our hospital, the patient suffered from sudden dizziness at midnight. The patient lay quietly, but her symptoms gradually worsened and severe nausea appeared. Dizziness continued until next morning and the patient was in a state of astasia and abasia; This condition continued over about three months, and Meniere's disease was diagnosed by an otolaryngologist. There was no improvement and the attacks of dizziness broke out spontaneously and more frequently. There was no noteworthy past history except for hypertension and allergy, and no abnormal findings in laboratory data of blood cell count, biochemistry and urinarysis. Neurological examination
94
K.OHTSU Table 2. Optokinetic vertical ocular dysmetria was observed in 93 cases in which the existence of lesions was confirmed. Vertical alone Number of D. alone or U. alone or cases D. dominant U. dominant
Periaqueductal synd. Basilar artery synd. Cerebel1ar vermis synd. Spinocerebel1ar degen. Cerebel1itis CP-angle tumor Meningioma Others
19
11
21
9
10
7
8
3
0
15 48
0 0 0 0 5
3 3 3 26 93
Both vertical & horizontal D . alone or U. alone or D. dominant U. dominant U.=D. 2
4 3
3
2
4
0 3
7
21
0
2
0 0 0 1 4
3 15
U.; upward; D.; downward.
R-OKN
L-OKN
DO-OKP
UP-OKP
,. ,
.
I'
I' lO·CAL
lO~cc
Fig. 2. Optokinetic patterns (OKP) of the patient who manifested optokinetic vertical ocular dysmetria. Marked dysmetria seen in the vertical OKP (lower two traces) both upward and downward, while the horizontal OKP (upper two traces) is completely intact.
VERTICAL OCULAR DYSMETRIA
95
lO'CAL
lOsec
Fig. 3. Optokinetic pattern (OKP) of the patient who manifested optokinetic vertical ocular dysmetria. Prominent dysmetria is seen in both right and left horizontal optokinetic patterns (A), while the vertical optokinetic pattern (B) shows dysmetria only in the downward and not the upward direction.
revealed trancal ataxia, and ataxic nystagmus on gazing laterally to both sides, as well as rebound nystagmus, was seen. During circular eye tracking testing (SAKATA, 1980), smooth pursuit of ocular movement was maintained in the horizontal component, but in the vertical component saccadic movements of the eyes were detected. Prominent vertical nystagmus was observed during upward gazing, and vertical rebound nystagmus was observed immediately after the eyes had returned to the mid-position from upward gazing (Fig. I). Optokinetic vertical ocular dysmetria (0 VO D) OVOD was observed and recorded by electronystagmogram in 93 cases. These cases consisted of various syndromes such as periaqueductal syndrome (19 cases), basilar artery syndrome (21 cases), cerebellar vermis syndrome (10 cases), etc. (Table 2). Representative optokinetic patterns are shown in Fig. 2 and Fig. 3. The majority of these cases (53 cases) showed optokinetic ocular dysmetria only in the vertical plane while 25 cases showed optokinetic ocular dysmetria both in the vertical and horizontal planes. B.
96
K.OHTSU
.11
. 1 .. .... '
DO-OKN
'. Fig. 4. Dysrhythmic type of optokinetic ocular dysmetria in the optokinetic nystagmus test. Disorders of regular rhythm of the fast and slow phase of optokinetic nystagmus.
Fig. 5. Overshoot type of optokinetic ocular dysmetria in the optokinetic nystagmus test. It is characterized by overshoot of the fast phase of the nystagmus.
Concerning vertical ocular dysmetria, the majority of the cases (69 cases) showed more prominent ocular dysmetria during downward eye movement than during upward eye movement. Only 9 cases showed more prominent ocular dysmetria during upward eye movement than during downward. Individual optokinetic nystagmus was examined precisely by faster paper speed study (0.5 em/sec) i.e. the OKN method. This enabled precise analysis of individual nystagmus which was impossible by the routine OKP method. In the examination by the OKN method, OVOD were classified according to their patterns of individual optokinetic nystagmus into the following four groups:
VERTICAL OCULAR DYSMETRIA
97
lO· CAr--:r-
Fig. 6. Ataxic type of optokinetic ocular dysmetria in the optokinetic nystagmus test. It is characterized by ataxic ocular movement in the slow phase of optokinetic nystagmus. UP-OKN
Fig. 7. Saccadic (semi-inversive) type of optokinetic ocular' ,dysmetria in the' .optokinetic nystagmus test. It is characterized by the disturbance of the smooth slow phase. Instead of smooth pursuit, prominent saccades are seen in the slow phase of optokinetic nystagmus.
a) the the b) the the
dysrhythmic type which is characterized by the disorder of the rhythm of fast and slow phase of the optokinetic nystagmus (Fig. 4). overshoot type which is characterized by overshoot of the fast phase of optokinetic nystagmus (Fig. 5).
98
K. OHTSU
c) the ataxic type which is characterized by the ataxic ocular movement in the slow phase of the optokinetic nystagmus (Fig. 6). d) the saccadic (semi-inversive) type which is characterized by saccades in the slow phase of the optokinetic nystagmus (Fig. 7). DISCUSSION
Dysrhythmic eye movements are already well known as a sign of lesion of the posterior fossa (COGAN, 1954; GOLDSTEIN and COGAN, 1961; HOOD et aI., 1973; KIRIKAE and SAKATA, 1965; KORNHUBER, 1971; LEssER et at., 1973). Dysrhythmic nystagmus which is induced by optokinetic stimulation is occasionally seen but is not yet well recognized. OLZECHOWSKI (1927) described ocular dysmetria in cases of multiple sclerosis and syphilitic angitis. COGAN (1954) described prominent ocular dysmetria in cases of cerebellar lesion, especially in those of unilateral lesion. He speculated that the phenomenon of ocular dysmetria is the overshoot phenomenon (UMEDA, SAKATA, and OHTSU, 1975) of horizontal eye movement. Concerning vertical eye movement, some characteristic abnormal eye movements have been described, such as spontaneous vertical downbeat nystagmus, upbeat nystagmus during upward gazing (KIRIKAE and SAKATA, 1965), vertical saccadic eye movement in the circular eye tracking test (SAKATA, 1980), directionchange vertical nystagmus in the positioning nystagmus test (KIRIKAE and SAKATA, 1965; SAKATA et at., 1968; SAKATA, 1970; ZEE et at., 1976), etc. LESSER et al. (1973) and ZEE et al. (1976) described vertical ocular oscillation. They reported that this phenomenon was observed in cases of cerebellar degeneration, astrocytoma in the fourth ventricle and of basilar artery syndrome. We also observed this phenomenon in 7 cases. The etiologies of our cases are atrophy of cerebellar vermis and vascular lesions in the basilar or superior cerebellar arteries. The phenomenon of vertical ocular oscillation, i.e., vertical ocular dysmetria, is very similar to the horizontal rebound nystagmus which was described by HOOD et al. (1973). Therefore we considered that the respective pathophysiological mechanisms involved might also be similar, and we propose naming this phenomenon "vertical rebound nystagmus." This phenomenon was observed in movement of the eye returning from the position of upward gazing to the mid-position in all seven cases, but in the eye movement returning to the mid-position from downward gazing, the phenomenon was observed in only two cases. This tendency, i.e. upward gazing dominance, suggests that the causal lesion related to this phenomenon possibly exists in the rostral region rather than the caudal region of the posterior fossa. This tendency also coincides with the fact that upbeat nystagmus is usually induced by a lesion of the rostral brainstem. And actually in our cases, this phenomenon was observed in the cases of superior cerebellar artery syndrome, or basilar artery
VERTICAL OCULAR DYSMETRIA
99
syndrome, and in the post-operative stage of a case of acoustic neurinoma of which the cyst extends deeply toward the rostral brainstem. We investigated OVOD in 93 cases which were confirmed to have a causal lesion in the posterior fossa. Vertical rebound nystagmus was induced by Ohmtype apparatus for optokinetic nystagmus, especially in the downward rather than the upward direction. Causal lesions were: superior cerebellar artery or basilar artery syndrome, cerebellitis, CP-angle tumors, tentorial meningioma, and cerebellar degeneration especially of the Ramsay-Hunt type. It is very suggestive for the localization of the causal lesion in the brain that, concerning cerebellar degeneration, horizontal ocular dysmetria is observed in all cerebellar degenerations except of the Friedreich type whereas vertical ocular dysmetria is only observed in degeneration of the Ramsay-Hunt type. In conclusion, disorder of cerebellar nuclei and their afferent tracts may be considered to be a causal lesion of horizontal rebound nystagmus and horizontal optokinetic ocular dysmetria, whereas disorder of cerebellar nuclei and their efferent tracts may be considered to be a causal lesion of vertical rebound nystagmus and vertical optokinetic ocular dysmetria. Optokinetic vertical ocular dysmetria can be classified into the following four groups: the dysrhythmic type, the overshoot type, the ataxic type, and the saccadic (semi-inversive) type. The saccadic type is very similar to the inversion phenomenon of optokinetic nystagmus, and this fact may become the key to solving the unknown pathophysiological mechanism of the above abnormal ocular movements. SUMMARY
Ocular dysmetria was observed and recorded on electronystagmograms in one hundred cases of posterior fossa lesion, especially of the midbrain and cerebellum. Observation and recording were carried out on vertical spontaneous ocular movement and vertical ocular movement induced by vertical optokinetic stimulation. 1) Ocular dysmetria which appears in the movements of the eyeballs in returning to the midpoint from the position of upward or downward gazing, is regarded as vertical rebound nystagmus. This phenomenon is more frequently observed in the movement of return to the midpoint from the upward gazing position than the downward. 2) Optokinetic vertical ocular dysmetria was recorded in 93 cases, and was more frequently induced by stimulation in the downward direction than the upward. The patterns of optokinetic vertical ocular dysmetria are classified into four types: a) the dysrhythmic type which is characterized by disorder of the rhythm of fast and slow phases. b) the overshoot type which is characterized and initiated by the overshoot
K.OHTSU
100
of the fast phase of nystagmus. c) the ataxic type which is characterized by ataxic ocular movement initiated by the disappearance of the distinction between fast and slow phases. d) the saccadic (semi-inversive) type which is characterized by disturbance of the smooth slow phase. 3) The respective neuronal systems of vertical and horizontal ocular dysmetria differ. The former usually appear in the case oflesions of the cerebellum and its afferent system, and the latter usually appear in those of the cerebellum and its efferent system. REFERENCES CoGAN, D. G.: Ocular dysmetria, flutter-like oscillations of the eyes, and opsoclonus. Arch. Opththal. 52: 318-328, 1954. GOLDSTEIN, J. E., and COGAN, D. G.: Lateralizing value of ocular motor dysmetria and skew deviation. Arch. Ophthal. 66: 517-521,1961. HOOD, J. D., KAYAN, A., and LEECH, J.: Rebound nystagmus. Brain 96: 507-527, 1973. KIRIKAE, I., and SAKATA, E.: Examinations of spontaneous and induced nystagmus. In Clinical Examinations of Otorhinolaryngology, pp. 176-197, Igaku-shoin PubJ., Tokyo, 1965. KORNHUBER, H. H. : Motor functions of cerebellum and basal ganglia: The cerebello-cortical saccadic clock, the cerebello nuclear hold regulator, and the basal ganglia ramp generator. Kybanetik 8: 157-162, 1971. LESSER, R. L., SMITH, J. L., and LEBENSON, D. S.: Vertical ocular dysmetria. Am. l. Ophthal. 76: 208-211, 1973. OLZECHOWSKI, K: De I'ataxie dysmetrique des yeux. Remarques sur I'ataxie des yeux dite myoclonique (Opsoclonie, opsoclonus). l. Psycho I. Neurol. 35: 1-13, 1927. SAKATA, E., SETOGUCHI, J., and Hsu, Y.: NeurotologicaI studies on cerebellar lesion. Practica Otologica (Kyoto) 61: 1642-1658, 1968. SAKATA, E.: How the examination of ocular movement with and without LeuchtbriIle can be help for diagnosis for the patients complaining vertigo. Practica Otologica (Kyoto) 63: 432-463, 1970. SAKATA, E.: Das neurootologische Studium uber die Liision des Kleinhirnwurms. Equilibrium Res. SuppJ. 1: 30-48, 1971. SAKATA, E.: Leitfaden der klinischen Neuro-Otologie, pp. 26-87, Ishiyaku Verlag, Tokyo, 1980. UMEDA, Y., SAKATA, E., and OHTSU, K.: Circular eye tracking test. l. Otolaryngol. lpn. 78: 218-224, 1975. ZEE, D. S., ROBERT, T. D., YEE, D. G., et al.: Oculomotor abnormalities in hereditary cerebellar ataxia. Brain 99: 207-234, 1976.
Request reprints from:
Dr. K. Ohtsu, Neurotological Clinic, Saitama Medical School, Moroyama 38, Iruma-gun, Saitama 350-04, Japan
VERTICAL OCULAR DYSMETRIA -VERTICAL REBOUND NYSTAGMUS AND OPTOKINETIC VERTICAL OCULAR DYSMETRIAKyoko OHTSU Neurotological Clinic, Saitama Medical School, Saitama, Japan
Ocular dysmetria in vertical eye movement was confirmed by electronystagmographic recording in \ 00 cases. 1) Ocular dysmetria in spontaneous vertical ocular movement was reported in seven cases. It can be called vertical rebound nystagmus. This phenomenon was more prominent in vertical movement of the eyes returning from upward gazing to mid-position than in the movements of downward gazing. 2) Optokinetic vertical ocular dysmetria induced by vertical optokinetic stimulation was observed in 93 cases. This phenomenon was far more prominent in upward optokinetic nystagmus than in downward optokinetic nystagmus. 3) The pattern of optokinetic vertical ocular dysmetria was classified into the following four types: the dysrhythmic type, the overshoot type, the ataxic type and the saccadic (semi-inversive) type. 4) The pathophysiological mechanism of horizontal ocular dysmetria should be different from the mechanism of vertical ocular dysmetria. Ocular dysmetria was first described by OLZECHOWSKI in 1927. Thereafter Cogan described flutter-like oscillation (GOLDSTEIN and COGAN, 1961), KORNHUBER (1971) described Fixationsrucke, KIRIKAE and SAKATA (\965) described ataxic nystagmus and unregelmaessige Burste, and HOOD, KAYAN and LEECH (1973) described rebound nystagmus. Ever since, much attention has been paid to the cerebellar lesion as a cause of abnormal eye movement. However, concerning abnormal vertical ocular movement, only two papers have been published up to now; one by LESSER, SMITH and LEBENSON in 1973 and the other by ZEE et al. in 1976. There is no description of ocular dysmetria in the vertical plane, or of ocular dysmetria induced by optokinetic stimulation. The phenomenon of vertical ocular dysmetria which we describe in this report could be called rebound nystagmus in the vertical plane as it is very similar Received for publication June 7, 1983 91
92
K.OHTSU
to the rebound nystagmus in the horizontal plane reported by HOOD et al. (1973). Thus, we name this vertical ocular dysmetria "vertical rebound nystagmus (VRN)." We describe the existence of ocular dysmetria which is induced by vertical optokinetic stimulation and name this phenomenon "optokinetic vertical ocular dysmetria (OVOO)." We speculate on the pathophysiological mechanism of optokinetic vertical ocular dysmetria and vertical rebound nystagmus and we stress their importance for diagnosing lesions in the posterior fossa. CASES AND METHOD
One hundred cases of ocular dysmetria were subjected to electronystagmography. The chief complaints were mainly vertigo and dysequilibrium, and each case was examined neurologically and neurotologically. Neurotological examinations (SAKATA, SETOGUCHI and Hsu, 1968), mainly based on SAKATA'S maneuver (1970) were carefully performed, especially concerning spontaneous and induced nystagmus. In all the cases, the existence of a lesion in the posterior fossa was proved morphologically by studies such as CT-Scan, cerebral angiography and pneumoencephalography. Optokinetic nystagmus test was performed by using the apparatus of Ohm (SAKATA, 1971). Two different paper speeds were used to record optokinetic nystagmus: The optokinetic pattern (OKP) method (SAKATA, 1971) in which a paper speed of 0.1 em/sec is used to visualize the continuous optokinetic nystagmus as a simple pattern; and the optokinetic nystagmus (OKN) method with a faster paper speed of 0.5 em/sec, in order to examine the individual optokinetic nystagmus precisely. Optokinetic stimulations were given both in the horizontal and vertical planes. RESULTS
A.
Vertical rebound nystagmus (VRN) Rebound nystagmus was described by HOOD only in horizontal eye movement. However, the rebound phenomenon was also observed in vertical eye movement. In seven out of one hundred cases of ocular dysmetria, the vertical rebound phenomenon was observed. In all seven cases this phenomenon was observed in the movement of eyes returning from the eye position of upward gazing to the mid-position. But in only two cases out of seven was this phenomenon observed in the movement of the eyes returning to the mid-position from the eye position of downward gazing. Causal lesions of these cases varied. They consisted of three cases of occlusion of the superior cerebellar artery, two cases of occlusion of the basilar artery, etc. These lesions were all located relatively in the midline and also in the relatively rostral part of the posterior fossa (Table 1). Typical case. A thirty-two-year-old woman complained of dizziness on moving. After a while, the attacks of dizziness worsened and appeared frequently.
93
VERTICAL OCULAR DYSMETRIA Table 1. Seven cases of vertical rebound nystagmus with lesions confirmed morphologically. Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7
24F
Infarction of cerebellar vermis (occlusion of sup. cerebellar artery) 52F idem 36M Basilar artery syndrome (thrombosis of the perforating arteries) 63 F idem 32 F Sup. cerebellar artery syndrome 19 M Periaqueductal syndrome (atrophy of the sup. vermis) 36F Acoustic neurinoma (post-op)
M A
~ORWARD CA',
~~~ lO'CAL
~
M 1 1
2 sec
Fig. I. Case 5. 32-year-old female, sup. cerebellar artery syndrome. Upbeat nystagmus is seen during upward gazing, and the vertical rebound nystagmus is seen when the eyes are returning from the position of upward gazing to the mid-position or eye position of forward gazing. A: Horizontal component of eye movement. B: Vertical component of eye movement.
Two years before admission to our hospital, the patient suffered from sudden dizziness at midnight. The patient lay quietly, but her symptoms gradually worsened and severe nausea appeared. Dizziness continued until next morning and the patient was in a state of astasia and abasia; This condition continued over about three months, and Meniere's disease was diagnosed by an otolaryngologist. There was no improvement and the attacks of dizziness broke out spontaneously and more frequently. There was no noteworthy past history except for hypertension and allergy, and no abnormal findings in laboratory data of blood cell count, biochemistry and urinarysis. Neurological examination
94
K.OHTSU Table 2. Optokinetic vertical ocular dysmetria was observed in 93 cases in which the existence of lesions was confirmed. Vertical alone Number of D. alone or U. alone or cases D. dominant U. dominant
Periaqueductal synd. Basilar artery synd. Cerebel1ar vermis synd. Spinocerebel1ar degen. Cerebel1itis CP-angle tumor Meningioma Others
19
11
21
9
10
7
8
3
0
15 48
0 0 0 0 5
3 3 3 26 93
Both vertical & horizontal D . alone or U. alone or D. dominant U. dominant U.=D. 2
4 3
3
2
4
0 3
7
21
0
2
0 0 0 1 4
3 15
U.; upward; D.; downward.
R-OKN
L-OKN
DO-OKP
UP-OKP
,. ,
.
I'
I' lO·CAL
lO~cc
Fig. 2. Optokinetic patterns (OKP) of the patient who manifested optokinetic vertical ocular dysmetria. Marked dysmetria seen in the vertical OKP (lower two traces) both upward and downward, while the horizontal OKP (upper two traces) is completely intact.
VERTICAL OCULAR DYSMETRIA
95
lO'CAL
lOsec
Fig. 3. Optokinetic pattern (OKP) of the patient who manifested optokinetic vertical ocular dysmetria. Prominent dysmetria is seen in both right and left horizontal optokinetic patterns (A), while the vertical optokinetic pattern (B) shows dysmetria only in the downward and not the upward direction.
revealed trancal ataxia, and ataxic nystagmus on gazing laterally to both sides, as well as rebound nystagmus, was seen. During circular eye tracking testing (SAKATA, 1980), smooth pursuit of ocular movement was maintained in the horizontal component, but in the vertical component saccadic movements of the eyes were detected. Prominent vertical nystagmus was observed during upward gazing, and vertical rebound nystagmus was observed immediately after the eyes had returned to the mid-position from upward gazing (Fig. I). Optokinetic vertical ocular dysmetria (0 VO D) OVOD was observed and recorded by electronystagmogram in 93 cases. These cases consisted of various syndromes such as periaqueductal syndrome (19 cases), basilar artery syndrome (21 cases), cerebellar vermis syndrome (10 cases), etc. (Table 2). Representative optokinetic patterns are shown in Fig. 2 and Fig. 3. The majority of these cases (53 cases) showed optokinetic ocular dysmetria only in the vertical plane while 25 cases showed optokinetic ocular dysmetria both in the vertical and horizontal planes. B.
96
K.OHTSU
.11
. 1 .. .... '
DO-OKN
'. Fig. 4. Dysrhythmic type of optokinetic ocular dysmetria in the optokinetic nystagmus test. Disorders of regular rhythm of the fast and slow phase of optokinetic nystagmus.
Fig. 5. Overshoot type of optokinetic ocular dysmetria in the optokinetic nystagmus test. It is characterized by overshoot of the fast phase of the nystagmus.
Concerning vertical ocular dysmetria, the majority of the cases (69 cases) showed more prominent ocular dysmetria during downward eye movement than during upward eye movement. Only 9 cases showed more prominent ocular dysmetria during upward eye movement than during downward. Individual optokinetic nystagmus was examined precisely by faster paper speed study (0.5 em/sec) i.e. the OKN method. This enabled precise analysis of individual nystagmus which was impossible by the routine OKP method. In the examination by the OKN method, OVOD were classified according to their patterns of individual optokinetic nystagmus into the following four groups:
VERTICAL OCULAR DYSMETRIA
97
lO· CAr--:r-
Fig. 6. Ataxic type of optokinetic ocular dysmetria in the optokinetic nystagmus test. It is characterized by ataxic ocular movement in the slow phase of optokinetic nystagmus. UP-OKN
Fig. 7. Saccadic (semi-inversive) type of optokinetic ocular' ,dysmetria in the' .optokinetic nystagmus test. It is characterized by the disturbance of the smooth slow phase. Instead of smooth pursuit, prominent saccades are seen in the slow phase of optokinetic nystagmus.
a) the the b) the the
dysrhythmic type which is characterized by the disorder of the rhythm of fast and slow phase of the optokinetic nystagmus (Fig. 4). overshoot type which is characterized by overshoot of the fast phase of optokinetic nystagmus (Fig. 5).
98
K. OHTSU
c) the ataxic type which is characterized by the ataxic ocular movement in the slow phase of the optokinetic nystagmus (Fig. 6). d) the saccadic (semi-inversive) type which is characterized by saccades in the slow phase of the optokinetic nystagmus (Fig. 7). DISCUSSION
Dysrhythmic eye movements are already well known as a sign of lesion of the posterior fossa (COGAN, 1954; GOLDSTEIN and COGAN, 1961; HOOD et aI., 1973; KIRIKAE and SAKATA, 1965; KORNHUBER, 1971; LEssER et at., 1973). Dysrhythmic nystagmus which is induced by optokinetic stimulation is occasionally seen but is not yet well recognized. OLZECHOWSKI (1927) described ocular dysmetria in cases of multiple sclerosis and syphilitic angitis. COGAN (1954) described prominent ocular dysmetria in cases of cerebellar lesion, especially in those of unilateral lesion. He speculated that the phenomenon of ocular dysmetria is the overshoot phenomenon (UMEDA, SAKATA, and OHTSU, 1975) of horizontal eye movement. Concerning vertical eye movement, some characteristic abnormal eye movements have been described, such as spontaneous vertical downbeat nystagmus, upbeat nystagmus during upward gazing (KIRIKAE and SAKATA, 1965), vertical saccadic eye movement in the circular eye tracking test (SAKATA, 1980), directionchange vertical nystagmus in the positioning nystagmus test (KIRIKAE and SAKATA, 1965; SAKATA et at., 1968; SAKATA, 1970; ZEE et at., 1976), etc. LESSER et al. (1973) and ZEE et al. (1976) described vertical ocular oscillation. They reported that this phenomenon was observed in cases of cerebellar degeneration, astrocytoma in the fourth ventricle and of basilar artery syndrome. We also observed this phenomenon in 7 cases. The etiologies of our cases are atrophy of cerebellar vermis and vascular lesions in the basilar or superior cerebellar arteries. The phenomenon of vertical ocular oscillation, i.e., vertical ocular dysmetria, is very similar to the horizontal rebound nystagmus which was described by HOOD et al. (1973). Therefore we considered that the respective pathophysiological mechanisms involved might also be similar, and we propose naming this phenomenon "vertical rebound nystagmus." This phenomenon was observed in movement of the eye returning from the position of upward gazing to the mid-position in all seven cases, but in the eye movement returning to the mid-position from downward gazing, the phenomenon was observed in only two cases. This tendency, i.e. upward gazing dominance, suggests that the causal lesion related to this phenomenon possibly exists in the rostral region rather than the caudal region of the posterior fossa. This tendency also coincides with the fact that upbeat nystagmus is usually induced by a lesion of the rostral brainstem. And actually in our cases, this phenomenon was observed in the cases of superior cerebellar artery syndrome, or basilar artery
VERTICAL OCULAR DYSMETRIA
99
syndrome, and in the post-operative stage of a case of acoustic neurinoma of which the cyst extends deeply toward the rostral brainstem. We investigated OVOD in 93 cases which were confirmed to have a causal lesion in the posterior fossa. Vertical rebound nystagmus was induced by Ohmtype apparatus for optokinetic nystagmus, especially in the downward rather than the upward direction. Causal lesions were: superior cerebellar artery or basilar artery syndrome, cerebellitis, CP-angle tumors, tentorial meningioma, and cerebellar degeneration especially of the Ramsay-Hunt type. It is very suggestive for the localization of the causal lesion in the brain that, concerning cerebellar degeneration, horizontal ocular dysmetria is observed in all cerebellar degenerations except of the Friedreich type whereas vertical ocular dysmetria is only observed in degeneration of the Ramsay-Hunt type. In conclusion, disorder of cerebellar nuclei and their afferent tracts may be considered to be a causal lesion of horizontal rebound nystagmus and horizontal optokinetic ocular dysmetria, whereas disorder of cerebellar nuclei and their efferent tracts may be considered to be a causal lesion of vertical rebound nystagmus and vertical optokinetic ocular dysmetria. Optokinetic vertical ocular dysmetria can be classified into the following four groups: the dysrhythmic type, the overshoot type, the ataxic type, and the saccadic (semi-inversive) type. The saccadic type is very similar to the inversion phenomenon of optokinetic nystagmus, and this fact may become the key to solving the unknown pathophysiological mechanism of the above abnormal ocular movements. SUMMARY
Ocular dysmetria was observed and recorded on electronystagmograms in one hundred cases of posterior fossa lesion, especially of the midbrain and cerebellum. Observation and recording were carried out on vertical spontaneous ocular movement and vertical ocular movement induced by vertical optokinetic stimulation. 1) Ocular dysmetria which appears in the movements of the eyeballs in returning to the midpoint from the position of upward or downward gazing, is regarded as vertical rebound nystagmus. This phenomenon is more frequently observed in the movement of return to the midpoint from the upward gazing position than the downward. 2) Optokinetic vertical ocular dysmetria was recorded in 93 cases, and was more frequently induced by stimulation in the downward direction than the upward. The patterns of optokinetic vertical ocular dysmetria are classified into four types: a) the dysrhythmic type which is characterized by disorder of the rhythm of fast and slow phases. b) the overshoot type which is characterized and initiated by the overshoot
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of the fast phase of nystagmus. c) the ataxic type which is characterized by ataxic ocular movement initiated by the disappearance of the distinction between fast and slow phases. d) the saccadic (semi-inversive) type which is characterized by disturbance of the smooth slow phase. 3) The respective neuronal systems of vertical and horizontal ocular dysmetria differ. The former usually appear in the case oflesions of the cerebellum and its afferent system, and the latter usually appear in those of the cerebellum and its efferent system. REFERENCES CoGAN, D. G.: Ocular dysmetria, flutter-like oscillations of the eyes, and opsoclonus. Arch. Opththal. 52: 318-328, 1954. GOLDSTEIN, J. E., and COGAN, D. G.: Lateralizing value of ocular motor dysmetria and skew deviation. Arch. Ophthal. 66: 517-521,1961. HOOD, J. D., KAYAN, A., and LEECH, J.: Rebound nystagmus. Brain 96: 507-527, 1973. KIRIKAE, I., and SAKATA, E.: Examinations of spontaneous and induced nystagmus. In Clinical Examinations of Otorhinolaryngology, pp. 176-197, Igaku-shoin PubJ., Tokyo, 1965. KORNHUBER, H. H. : Motor functions of cerebellum and basal ganglia: The cerebello-cortical saccadic clock, the cerebello nuclear hold regulator, and the basal ganglia ramp generator. Kybanetik 8: 157-162, 1971. LESSER, R. L., SMITH, J. L., and LEBENSON, D. S.: Vertical ocular dysmetria. Am. l. Ophthal. 76: 208-211, 1973. OLZECHOWSKI, K: De I'ataxie dysmetrique des yeux. Remarques sur I'ataxie des yeux dite myoclonique (Opsoclonie, opsoclonus). l. Psycho I. Neurol. 35: 1-13, 1927. SAKATA, E., SETOGUCHI, J., and Hsu, Y.: NeurotologicaI studies on cerebellar lesion. Practica Otologica (Kyoto) 61: 1642-1658, 1968. SAKATA, E.: How the examination of ocular movement with and without LeuchtbriIle can be help for diagnosis for the patients complaining vertigo. Practica Otologica (Kyoto) 63: 432-463, 1970. SAKATA, E.: Das neurootologische Studium uber die Liision des Kleinhirnwurms. Equilibrium Res. SuppJ. 1: 30-48, 1971. SAKATA, E.: Leitfaden der klinischen Neuro-Otologie, pp. 26-87, Ishiyaku Verlag, Tokyo, 1980. UMEDA, Y., SAKATA, E., and OHTSU, K.: Circular eye tracking test. l. Otolaryngol. lpn. 78: 218-224, 1975. ZEE, D. S., ROBERT, T. D., YEE, D. G., et al.: Oculomotor abnormalities in hereditary cerebellar ataxia. Brain 99: 207-234, 1976.
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Dr. K. Ohtsu, Neurotological Clinic, Saitama Medical School, Moroyama 38, Iruma-gun, Saitama 350-04, Japan