Auris路 Nasus路 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

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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.

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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

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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

UP-OKP

DO-OKP

,.
,

.

I'

I'
lO路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.

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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路 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 dysrhythmic type which is characterized by the disorder of the rhythm of
the fast and slow phase of the optokinetic nystagmus (Fig. 4).
b) the overshoot type which is characterized by overshoot of the fast phase of
the optokinetic nystagmus (Fig. 5).

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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.

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Dr. K. Ohtsu, Neurotological Clinic, Saitama Medical School,
Moroyama 38, Iruma-gun, Saitama 350-04, Japan