Arch. Oto-Rhino-Laryng. 214, 97--107 (1976)
Archivesof Oto-Rhino-Laryngology 9 by Springer-Verlag 1976
The Damped Pendular Rotation Test in Central Vestibular Disorders* Jin Kanzaki and Chiyoko Sakagami Department of Otolaryngology, School of Medicine, Keio University, 35 Shinanomach! Shinjyuku, Tokyo 150, Japan
Summary. Nystagmic rhythm in the damped pendular rotation test (DPRT) was analysed electronystagmographically both in healthy subjects (control) and patients with peripheral and central vestibular lesions. The patients were tested in a semi-dark room with eyes open and, in addition, a serial subtraction task was performed to maintain the state of alertness throughout the rotation. In the controls 49 years of age and under dysrhythmia was found in 11%, while in persons 50 years of age and over the abnormal rate was 29%. In patients with acoustic tumors, who had undergone surgery in which the translabyrinthine and middle fossa approach had been utilized, dysrhythmia was present post-operatively in only a few cases. In patients 49 years of age and under, operated on through the suboccipital approach, dysrhythmia was found post-operatively, or was at least more remarkable than pre-operatively in most cases. Nystagmic rhythm was, on the other hand, regular with cerebellar degenerative process or atrophy. Pre-operative dysrhythmia in patients with cerebellar and cerebral tumors was in some cases post-operatively converted to regular rhythmic nystagmus in pendular stimulations. Therefore, in cerebellar and cerebral tumors, dysrhythmia was thought to be due to secondary effects in brainstem, as these tumors can cause intracranial hypertension and circulatory disturbances in surrounding brain tissues. In Meni6re's disease and sudden deafness, dysrhythmia and salvos in D P R T were found in the age groups, 49 years of age and under and 50 years and over, as frequently as in the healthy and control group. In one case with Menibre's disease which showed dysrhythmia, labyrinthectomy was done. This surgical manipulation of the labyrinth did not eliminate dysrhythmia, though a temporary improvement was obtained. This result indicates that the dysrhythmi~t may be of central origin. * Presented at the fifth extraordinary meeting of the B/trfiny Society, October 1975, Kyoto, Japan
98
J. Kanzaki and C. Sakagami These findings also suggest that nystagmic rhythm in DPRT with mental arithmetic is significant in assessing brainstem dysfunctions, when the age and state of alertness of the patient are taken into consideration, or when comparing the pre- and post~operative findings in intracranial lesions. Key words: Damped pendular rotation test - Dysrhythmia - Alertness Acoustic neuroma -- Cerebellar lesions - Cerebral lesions - Meni6re's disease Sudden deafness.
-
The damped pendular rotation test (DPRT) was first brought into clinical use in 1960 by Greiner, Conraux and his associates [2] at Strasbourg University in France. Since that time this test has been widely used as one method of vestibular examination, mainly in France and Belgium. Only a few reports of this particular test, especially regarding its diagnostic value have been published in English [7]. As in other rotation tests, the directional preponderance and compensation process of an affected labyrinth can be detected using this test. The other finding in which we were interested was nystagmic rhythm during pendular rotation. Greiner et al. [2] speculated from their clinical studies that dysrhythmia in D P R T was due to brainstem lesions; however, detailed analyses of dysrhythmia based on observations of confirmed central vestibular lesions or comparative studies of pre- and post-operative nystagmic rhythm in brain tumor cases have been few. It should naturally be considered in these studies, as has been pointed out in the caloric test, that nystagmic rhythm could be affected by various factors, such as the patient's state of alertness during rotation, his age and whether he has taken drugs. Considering these factors, we have studied nystagmic rhythm in D P R T both in healthy persons and in patients with central and peripheral vestibular lesions.
Damped Pendular Rotation Test
99
Methods The apparatus is similar to that used at Strasbourg University. The chair rotates by torsion of wires (Fig. 1), and the rotation starts from 180 ~ twisted position, constantly decelerates and stops after 10-12 oscillations. Each rotation period is between 20 and 22 s. The patient was tested in a dark room with eyes open and in addition, subtraction task was performed to maintain the state of alertness throughout the rotation. The subject was in an ordinary chair-sitting position with his nose 30 ~ downward. The repeated trial was performed 2 - 3 min after the first test. The weight of the test subject is adjusted by placing lead cylinders symmetrically under the chair so that the constant period of the rotation can be obtained. Electronystagmographic recording was performed during the test. The rotation of 100 ~ was 10 mm on the recording chart. Recording was done with a paper speed of 15 mm/s. Clockwise rotation of the chair was recorded as a curve from upper left to lower right of the sine wave.
Subjects GroupA (Control): Subjects with no history of ear disease and vertigo. 56 cases. Group B: Subjects with pulmonary tuberculosis whose vestibular functions were repeatedly and regularly tested because of the administration of streptomycin sulfate, but who have no vertigo and no demonstrable objective abnormal findings in other vestibular examinations. 25 cases. Group C: Acoustic neuromas and other cerebellopontine angle tumors. 14 pre-operative cases. 21 post-operative cases. Group D: Cerebellar lesions. Atrophy or degeneration, 2 cases. Tumor, 5 cases. Group E: Brainstem tumor. 4 cases.
i.
~
,
IOme
A
i
9
-
-
8 s ~
Fig. 2. Upper: A: regular nystagmic rhythm. B: dysrhythmia (acoustic tumor case). Lower: A: regular nystagmic rhythm (one week after labyrinthectomy). B: dysrhythmia (a case with acoustic tumor operated on by the suboccipital approach). S: slow phase. H: horizontal recording. T.C.: 3.0 vertical bar indicates 10 ~
100
J. Kanzaki and C. Sakagami
8 ! I0"
b IlO"
C
.....
Fig. 3. Pathologic nystagmic rhythm, a: petite ~criture (high frequency nystagmus with low amplitude), b: salvos: occasional inhibition of nystagmus is seen. c: no response
GroupF: Cerebral lesions. Pre-operative tumors includingfour temporal lobe tumors, two parasellar tumors and one parietal lobe tumor, 7 cases. Post-operative tumors including 2 pineal body tumors, one third ventricle astrocytoma and one tumor arising from septum palcidum, 4 cases. Group G: Vascular lesions and others. Cerebral vascular lesions includingvertebro-basilar insufficiency, 18 cases. Criteria of Dysrhythmia The regularity of the nystagmic rhythm in pendular rotation was qualitatively evaluated in most cases. The irregular occurence of quick and slow phase of nystagmus, or nystagmic response with wide variety of amplitude was defined as dysrhythmia. The various types of nystagmic rhythm are shown in Figures 2 and 3. In selected cases, an interval of each nystagmus in control group was within a certain range of peak distribution, while in patients with central vestibular disorders, nystagmus intervals were scattered outside of the peak distribution.
Results
a) Nystagmic Rhythm in Group A and B (Table 1): Each Control group was divided into two, according to their age (49 years of age and under and 50 years of age and over). In 33 subjects 49 years of age and under in G r o u p A, dysrhythmia was observed in three (9%) and slight dysrhythmia in two (6%). In 23 subjects 50 years of age and over, six showed dysrhythmia (26%) and six narrow writing (petite ~criture) (26%). In G r o u p B, dysrhythmia was found in two out of sixteen subjects (13%) 49 years of age and under, and three of nine (33%) 50 years of age and over. Slight dysrhythmia was observed in two out of sixteen (13%) and narrow writing in two of sixteen subjects (13%) 49 years of age and under, and two of nine in subjects 50 years of age and over (22%) (Table 1). Therefore dysrhythmia and narrow writing (petite 6criture) were more frequently observed in subjects 50 years of age and over than in those 49 and under (Table 2).
Damped Pendular Rotation Test
101
Table 1. Nystagmic rhythm in group A and B. P.E.: petite 6criture means high frequency nystagmus with low amplitude 49 years of age and under Regular
Slightly dysrhythmic
Dysrhythmic
P.E.
Total
Control A Control B
28 10
2 2
3 2
0 2
33 16
Total
38
4
5
2
49
50 years of age and over Regular
Slightly dysrhythmic
Dysrhythmic
P.E.
Total
Control A Control B
11 4
0 0
6 3
6 2
23 9
Total
15
0
9
8
32
Table 2. Nystagmic rhythm and age distribution in group A Age
Regular
Slightly dysrhythmic
Dysrhythmic
Petite ~criture
Total
10-19 20-29 30-39 40-49 50-59 60-69 over 70
2 14 8 4 5 5 1
0 0 0 2 0 0 0
1 1 0 1 3 3 0
0 0 0 0 2 3 1
3 14 8 7 10 11 2
Total
39
2
9
6
56
b) Nystagmie Rhythm in Central Vestibular Disorders: 1. Acoustic n e u r o m a and other cerebellopontine angle tumors (Table 3 and 4). As shown in Table 3, surgical approach to an acoustic tumor was closely related to nystagmic rhythm in D P R T . All the cases with regular nystagmic rhythm could be operated on either through the translabyrinthine or middle fossa approach, while cases with dysrhythmia all had large tumors attached to the brainstem. Table 4 indicates that the postoperative nystagmic rhythm in patients operated on through the suboccipital approach becomes worse, that is, it becomes more dysrhythmic, than the preoperative state, while in cases where a translabyrinthine or middle fossa approach was used, there was no change postoperatively.
102
J. Kanzaki and C. Sakagami
Table 3. Nystagmic rhythm in acoustic tumor (49 years of age and under) Approach
Total Regular
Slight dysrhythmia
Dysrhythmia
Petite ~criture
Pre-op.
Translabyrinthine Middle fossa Suhoccipital
5 2 3
5 1 0
0 1 0
0 0 3
0 0 0
Post-op.
Translabyrinthine Middle fossa Suboccipital
8 2 8
6 1 1
1 1 1
0 0 6
1 0 0
Table 4. Post-operative nystagmic rhythm in acoustic tumor
Approach
Age
No change
Worse (dysrhythmia)
Translabyrinthine
< 49 > 50
5 1
0 0
Middle fossa
< 49 > 50
2 1
0 0
Suboccipital
< 49 > 50
0 0
3 3
Figure 4 shows the nystagmic rhythm in a patient with cerebellopontine angle meningeoma reoperated on 21 months after the first surgery because of tumor regrowth. The most striking findings in DPRT was the postoperative nystagmic rhythm which became gradually dysrhythmic and most evident just before the second operation and which recovered remarkably immediately after. In Figure 4, the uppermost recording indicates preoperative nystagmic rhythm, from B to C postoperative and D, ENG-recording one month after the reoperation, showing remarkable recovery in pendular nystagmus. K.G 44yrs cpa meningeorna
B
Fig. 4. A: Pre-operative nystagmic response. B: D
5ser
10 months after the first operation. C: 20 months after the first operation. D: One month after re-operation. Note: B and C: Nystagmic response reduced remarkably because of tumor regrowth. D: Recovery of nystagmic response
103
Damped Pendular Rotation Test 515r
h
prt.op
t=OSt-op
i 0' --
1o~
lo' I
Fig. 5. Patient with hemangioblastomaof right cerebellar hemisphere, a A: Pre-operative nystagmic rhythm. High frequency nystagmus with occasional inhibition are seen. B: Post-operative findings. H and h: horizontal recording. H: T.C. 3.0, h: T.C. 0.03. b Findings of pre- and post-operativeoptokinetic nystagmus pattern and Eye Tracking Test
Preoperative pendular nystagmus in a patient with hemangioblastoma in the right cerebellar hemisphere showed an increase of nystagmus frequency and slight dysrhythmia. Postoperatively, these findings disappeared and nystagmic rhythm in D P R T reverted to normal (Fig. 5a). After extirpation of cerebellar tumors eye tracking and optokinetic nystagmus became worse compared with preoperative findings (Fig. 5b). While pendular nystagmus in cerebellar atrophy or degeneration was regular and amplitude of nystagmus tended to increase (Fig. 6). 2. Brainstem lesions. In four patients diagnosed as having brainstem tumors, dysrhythmia and no response was observed in two cases respectively, one was found to have postinfectious lesions. This patient showed at first no pendular nystagmic response but improved later and gradually exhibited a nystagmic response. Dysrhythmia and reduced response or absence of response was frequently seen in large cerebellopontine angle tumors or other brain tumors. These findings appeared to be the effect of the direct compression of the tumor or by intracranial hypertension which in most cases can affect brainstem function. Figure 7 demonstrates a case with temporal lobe meningeoma in which preoperative dysrhythmia disappeared postoperatively. In most cases of irradiated brain tumors, dysrhythmia or reduced response was remarkable.
104
J. Kanzaki and C. Sakagami
IlO ~
B
}
1
~
II0~
5see
......
Fig. 6. Nystagmic rhythm in cerebellar atrophy cases. A: Patient with a late cerebellar cortical atrophy (male, 65 years old). B: Patient with a cerebellar atrophy (male, 39 years old). Note: Nystagmic rhythm in these cases was regular and the amplitude tended to increase. H: T.C. 3.0, h: T.C. 0.03. V: vertical recording. T.C. 0.03
l 10"
h
~
~
-
~
,
r.
h
11
......
I
10 ~
5sec
Fig. 7. Patient with a left temporal lobe meningeoma (male, 36 years old). A: Pre-operative nystagmic rhythm (dysrhythmic). B: Post-operative nystagmic rhythm (regular). H: T.C. 3.0, h: T.C. 0.03
3. Cerebral vascular diseases (18 cases). D y s r h y t h m i a in D P R T was also one of the most apparent nystagmic findings in cases with vertebro-basilar insufficiency. Cerebral vascular disease frequently showed a dysrhythmia and in some cases even a reduced response or a negative response was observed.
e) Nystagmic Rhythm in Peripheral Vestibular Lesions: In Meni~re's disease and sudden deafness, dysrhythmia and salvos in D P R T were found in either age groups, 49 years and under and 50 years and over, as frequently as in the healthy control group. In one patient with Meni6re's disease showing dysrhythmia in D P R T , labyrinthectomy was performed following an ineffective drainage operation of the endo-
Damped Pendular Rotation Test
105
lymphatic sac. For a few postoperative weeks dysrhythmia disappeared, but reappeared thereafter and remained. In this case EEG showed abnormal findings of paroxysmal slow waves in all leads which indicated hypothalamic epilepsy. These findings suggest that surgical manipulation of the labyrinth might temporally affect nystagmic rhythm although the route has yet to be determined. The fact that the labyrinthectomy did not eliminate dysrhythmia suggests that this might be caused by central mechanisms.
Nystagmic Rhythm and State of Alertness The effect of mental alertness by a subtraction task during pendular rotation on nystagmic rhythm was studied in ten normal subjects, in twenty-three cases -with peripheral vestibular disorders and in eighteen cases with central vestibular lesions. The test was done first with mental arithmetic and secondly without subtraction task. In about 40% of peripheral vestibular disorders, amplitude decreased when mental arithmetic tests were not given, but an affect on nystagmic rhythm was observed in only two out of sixteen cases under 49 years of age, in which regular nystagmic rhythm turned into dysrhythmia. In central vestibular disorders most patients showed dysrhythmia regardless of whether mental arithmetic was used or not. In three patients with central vestibular disorders; acoustic neuroma with wide extension into posterior fossa, pontine tumor and vertebro-basilar insufficiency, pathologic habituation according to the criteria of Greiner et al. [2] was found when mental arithmetic tests were not given. Discussion
A. Some Physiological Bases for Nystagmic Rhythm Anatomical and physiological bases related to nystagmic rhythm are complicated. In animal experiments in which vestibular nystagmus was evoked, unit discharge in vestibular nucleus, brainstem reticular formation and in abdecense nucleus were regular [4]. This is based on alternative rhythmic activities of IPSP and EPSP in antagonistic motoneurons [4]. Accordingly, lesions in the vestibular system could probably interfere with rhythmic unit discharges. In addition the pontine paramedian zone of reticular formation (PPRF) which might be a center for adduction and horizontal eye movement [1] could play an important role in producing nystagmic rhythm. It is not yet known whether oculomotor centers in diencephalon, whose role in evoking nystagmus has been reported [3, 5], are related to rhythmicity ofnystagmus or not. Pathways from vestibular nucleus and from brainstem reticular formation to oculomotor nuclei can be affected by circulatory disorders in the bralnstem, which are caused by arteriosclerosis or by the presence of a tumor or by secondary effect of the tumor. The rhythmicity of nystagmus might basically be a problem at synaptic levels, and lesions in these complex networks could interfere with the rhythmic activities of hyperpolarization and depolarization in antagonistic oculomotor neurons.
106
J. Kanzaki and C. Sakagami
B. Nystagmic Rhythm in Healthy Control Persons In these series slight and marked dysrhythmia are observed in 15% of the persons between 10 and 49 years of age. This percentage coincides with that reported by Van de Calseyde et al. [6]. In the age group 50 years of age and over, slight and marked dysrhythmia were found in 26% of the subjects, narrow writing in the same percentage which was seldom seen in younger age groups. Nystagmic rhythm in persons under 10 years of age is less regular than in other age groups 49 years of age and under. The state of alertness may affect nystagmic rhythm and in most cases the amplitude of nystagmus tends to be low without mental arithmetic. In the present series of studies the subjects were under a mental arithmetic task (subtraction) during rotation in order to keep them in a constant state of alertness. Without the subtraction task, the narrow writings, or slight dysrhythmia could be seen frequently both in healthy persons and subjects with peripheral vestibular lesions. Pathological habituation which could often be found in central lesions was more frequently observed by this test without mental arithmetic. Thus in evaluating nystagmic rhythm in the pendular test, the level of consciousness of the subject as well as age should always be considered.
C. Dysrhythmia and Central Vestibular Lesions In preoperative cases with acoustic tumors, three out of ten cases showing dysrhythmia in D P R T were those extended into posterior fossa with a diameter of more than 3.0 cm and attached to the brainstem. These preoperative dysrhythmia became worse postoperatively. In Figure 8 the upper recording is a preoperative one in a patient with an acoustic neurinoma. Nystagmic rhythm is relatively regular with small amplitude. The lower recording shows irregular postoperative nystagmic rhythm 8 weeks after the operation. While dysrhythmia was seen in almost all cases operated via the suboccipital approach, that is, in large tumors, there was only a few dysrhythmia in cases operated on via the translabyrinthine or middle fossa approach. In cerebellar degenerative lesions there was no dysrhythmia. In postoperative cases with cerebellar tumors, narrow writing or nystagmus of reduced response were A
J
Fig. 8. Acoustic neuroma, left (age 35, female). A: Pre-operative nystagmic response. B: Post-operative nystagmic response (8 weeks). Note: dysrhythmic nystagmus after suboccipital operation
Damped Pendular Rotation Test
107
found without dysrhythmia. In some cerebellar tumors preoperative dysrhythmia was not found postoperatively. Therefore, narrow writing and reduced response in postoperative cases with cerebellar tumors might be the effect of operative procedure during tumor surgery. In this respect nystagmic rhythm in D P R T is thought not to be closely related with the cerebellum. Nystagmic rhythm in cerebral or midbrain lesions varies according to the size and location of the tumor, or the degree of circulatory disturbances. In cases with slight or marked dysrhythmia the effect of intracranial hypertension to the brainstem should be considered. In fact, preoperative dysrhythmia disappeared postoperatively with a decrease of intracranial pressure after tumor removal. In all patients with irradiated brain tumors, dysrhythmia was found, and in some cases dysrhythmia which was present before irradiation became more significant after the procedure. Patients who required irradiation may therefore be those with intracranial hypertension. The cause of dysrhythmia in all irradiated cases cannot be ascribed only to irradiation, although irradiation may affect the brainstem circulation and cause a dysrhythmia. In patients with internal capsule bleeding, dysrhythmia was not observed. While in most patients with brain tumors and suspected infections cases in the brainstem, a marked reduction of nystagmic response was found. F r o m these observations, postoperative reduction in nystagmus in cerebellar tumors might be due to either direct or indirect disruption of the circulation in the brainstem due to surgical procedure. Also from the fact that there was only slight dysrhythmia in D P R T in patients with acoustic neuromas operated on through the translabyrinthine approach and in cerebellar degenerative lesions, while marked dysrhythmia was obtained postoperatively in cases of acoustic tumors or other cerebellopontine angle tumors operated on through the suboccipital approach, or in post-irradiated brain tumors in which no dysrhythmia was found preoperatively or pre-irradiation respectively and in vertebro-basillar insufficiency, dysrhythmia is thought to be related to brainstem lesions or dysfunction of the brainstem mechanisms related to the rhythmic activity-of the pendular nystagmus.
References
1. Cohen, B.: Vestibulo-ocular relations. The control of eye movements, p. 105--148. New YorkLondon: Academic Press 1971 2. Greiner, G. F. et al.: Vestibulometrie clinique. Paris: l~dit. Doin 1969 3. Lachmann, J. et al.: Central nystagmus elicited by stimulation of the mesodiencephalon in the rabbit. Amer. J. Physiol. 193, 328--334 (1958) 4. Maeda, M. et al.: Rhythmic activities of secondary vestibular efferent fibers recorded within the abducens nucleus during vestibular nystagmus. Brain Res. 34, 361--365 (1971) 5. Manni, E. et al.: Eye nystagmus elicited by stimulation of the cerebral cortex in the rabbit. Arch. ital. Biol. 102, 645--656 (1964) 6. Van de Calseyde, P. et al.: L'ENG dans l'~preuve rotatoire sinusoidale amortie. Acta oto-rhinolaryng, belg. 23, 1-335 (1969) 7. Van de Calseyde, p. et al.: The damped torsion swing test. Quantitative and qualitative aspects of the ENG pattern in normal subjects. Arch. otolaryng. 100, 449--452 (1974) Received March 1, 1976
Archivesof Oto-Rhino-Laryngology 9 by Springer-Verlag 1976
The Damped Pendular Rotation Test in Central Vestibular Disorders* Jin Kanzaki and Chiyoko Sakagami Department of Otolaryngology, School of Medicine, Keio University, 35 Shinanomach! Shinjyuku, Tokyo 150, Japan
Summary. Nystagmic rhythm in the damped pendular rotation test (DPRT) was analysed electronystagmographically both in healthy subjects (control) and patients with peripheral and central vestibular lesions. The patients were tested in a semi-dark room with eyes open and, in addition, a serial subtraction task was performed to maintain the state of alertness throughout the rotation. In the controls 49 years of age and under dysrhythmia was found in 11%, while in persons 50 years of age and over the abnormal rate was 29%. In patients with acoustic tumors, who had undergone surgery in which the translabyrinthine and middle fossa approach had been utilized, dysrhythmia was present post-operatively in only a few cases. In patients 49 years of age and under, operated on through the suboccipital approach, dysrhythmia was found post-operatively, or was at least more remarkable than pre-operatively in most cases. Nystagmic rhythm was, on the other hand, regular with cerebellar degenerative process or atrophy. Pre-operative dysrhythmia in patients with cerebellar and cerebral tumors was in some cases post-operatively converted to regular rhythmic nystagmus in pendular stimulations. Therefore, in cerebellar and cerebral tumors, dysrhythmia was thought to be due to secondary effects in brainstem, as these tumors can cause intracranial hypertension and circulatory disturbances in surrounding brain tissues. In Meni6re's disease and sudden deafness, dysrhythmia and salvos in D P R T were found in the age groups, 49 years of age and under and 50 years and over, as frequently as in the healthy and control group. In one case with Menibre's disease which showed dysrhythmia, labyrinthectomy was done. This surgical manipulation of the labyrinth did not eliminate dysrhythmia, though a temporary improvement was obtained. This result indicates that the dysrhythmi~t may be of central origin. * Presented at the fifth extraordinary meeting of the B/trfiny Society, October 1975, Kyoto, Japan
98
J. Kanzaki and C. Sakagami These findings also suggest that nystagmic rhythm in DPRT with mental arithmetic is significant in assessing brainstem dysfunctions, when the age and state of alertness of the patient are taken into consideration, or when comparing the pre- and post~operative findings in intracranial lesions. Key words: Damped pendular rotation test - Dysrhythmia - Alertness Acoustic neuroma -- Cerebellar lesions - Cerebral lesions - Meni6re's disease Sudden deafness.
-
The damped pendular rotation test (DPRT) was first brought into clinical use in 1960 by Greiner, Conraux and his associates [2] at Strasbourg University in France. Since that time this test has been widely used as one method of vestibular examination, mainly in France and Belgium. Only a few reports of this particular test, especially regarding its diagnostic value have been published in English [7]. As in other rotation tests, the directional preponderance and compensation process of an affected labyrinth can be detected using this test. The other finding in which we were interested was nystagmic rhythm during pendular rotation. Greiner et al. [2] speculated from their clinical studies that dysrhythmia in D P R T was due to brainstem lesions; however, detailed analyses of dysrhythmia based on observations of confirmed central vestibular lesions or comparative studies of pre- and post-operative nystagmic rhythm in brain tumor cases have been few. It should naturally be considered in these studies, as has been pointed out in the caloric test, that nystagmic rhythm could be affected by various factors, such as the patient's state of alertness during rotation, his age and whether he has taken drugs. Considering these factors, we have studied nystagmic rhythm in D P R T both in healthy persons and in patients with central and peripheral vestibular lesions.
Damped Pendular Rotation Test
99
Methods The apparatus is similar to that used at Strasbourg University. The chair rotates by torsion of wires (Fig. 1), and the rotation starts from 180 ~ twisted position, constantly decelerates and stops after 10-12 oscillations. Each rotation period is between 20 and 22 s. The patient was tested in a dark room with eyes open and in addition, subtraction task was performed to maintain the state of alertness throughout the rotation. The subject was in an ordinary chair-sitting position with his nose 30 ~ downward. The repeated trial was performed 2 - 3 min after the first test. The weight of the test subject is adjusted by placing lead cylinders symmetrically under the chair so that the constant period of the rotation can be obtained. Electronystagmographic recording was performed during the test. The rotation of 100 ~ was 10 mm on the recording chart. Recording was done with a paper speed of 15 mm/s. Clockwise rotation of the chair was recorded as a curve from upper left to lower right of the sine wave.
Subjects GroupA (Control): Subjects with no history of ear disease and vertigo. 56 cases. Group B: Subjects with pulmonary tuberculosis whose vestibular functions were repeatedly and regularly tested because of the administration of streptomycin sulfate, but who have no vertigo and no demonstrable objective abnormal findings in other vestibular examinations. 25 cases. Group C: Acoustic neuromas and other cerebellopontine angle tumors. 14 pre-operative cases. 21 post-operative cases. Group D: Cerebellar lesions. Atrophy or degeneration, 2 cases. Tumor, 5 cases. Group E: Brainstem tumor. 4 cases.
i.
~
,
IOme
A
i
9
-
-
8 s ~
Fig. 2. Upper: A: regular nystagmic rhythm. B: dysrhythmia (acoustic tumor case). Lower: A: regular nystagmic rhythm (one week after labyrinthectomy). B: dysrhythmia (a case with acoustic tumor operated on by the suboccipital approach). S: slow phase. H: horizontal recording. T.C.: 3.0 vertical bar indicates 10 ~
100
J. Kanzaki and C. Sakagami
8 ! I0"
b IlO"
C
.....
Fig. 3. Pathologic nystagmic rhythm, a: petite ~criture (high frequency nystagmus with low amplitude), b: salvos: occasional inhibition of nystagmus is seen. c: no response
GroupF: Cerebral lesions. Pre-operative tumors includingfour temporal lobe tumors, two parasellar tumors and one parietal lobe tumor, 7 cases. Post-operative tumors including 2 pineal body tumors, one third ventricle astrocytoma and one tumor arising from septum palcidum, 4 cases. Group G: Vascular lesions and others. Cerebral vascular lesions includingvertebro-basilar insufficiency, 18 cases. Criteria of Dysrhythmia The regularity of the nystagmic rhythm in pendular rotation was qualitatively evaluated in most cases. The irregular occurence of quick and slow phase of nystagmus, or nystagmic response with wide variety of amplitude was defined as dysrhythmia. The various types of nystagmic rhythm are shown in Figures 2 and 3. In selected cases, an interval of each nystagmus in control group was within a certain range of peak distribution, while in patients with central vestibular disorders, nystagmus intervals were scattered outside of the peak distribution.
Results
a) Nystagmic Rhythm in Group A and B (Table 1): Each Control group was divided into two, according to their age (49 years of age and under and 50 years of age and over). In 33 subjects 49 years of age and under in G r o u p A, dysrhythmia was observed in three (9%) and slight dysrhythmia in two (6%). In 23 subjects 50 years of age and over, six showed dysrhythmia (26%) and six narrow writing (petite ~criture) (26%). In G r o u p B, dysrhythmia was found in two out of sixteen subjects (13%) 49 years of age and under, and three of nine (33%) 50 years of age and over. Slight dysrhythmia was observed in two out of sixteen (13%) and narrow writing in two of sixteen subjects (13%) 49 years of age and under, and two of nine in subjects 50 years of age and over (22%) (Table 1). Therefore dysrhythmia and narrow writing (petite 6criture) were more frequently observed in subjects 50 years of age and over than in those 49 and under (Table 2).
Damped Pendular Rotation Test
101
Table 1. Nystagmic rhythm in group A and B. P.E.: petite 6criture means high frequency nystagmus with low amplitude 49 years of age and under Regular
Slightly dysrhythmic
Dysrhythmic
P.E.
Total
Control A Control B
28 10
2 2
3 2
0 2
33 16
Total
38
4
5
2
49
50 years of age and over Regular
Slightly dysrhythmic
Dysrhythmic
P.E.
Total
Control A Control B
11 4
0 0
6 3
6 2
23 9
Total
15
0
9
8
32
Table 2. Nystagmic rhythm and age distribution in group A Age
Regular
Slightly dysrhythmic
Dysrhythmic
Petite ~criture
Total
10-19 20-29 30-39 40-49 50-59 60-69 over 70
2 14 8 4 5 5 1
0 0 0 2 0 0 0
1 1 0 1 3 3 0
0 0 0 0 2 3 1
3 14 8 7 10 11 2
Total
39
2
9
6
56
b) Nystagmie Rhythm in Central Vestibular Disorders: 1. Acoustic n e u r o m a and other cerebellopontine angle tumors (Table 3 and 4). As shown in Table 3, surgical approach to an acoustic tumor was closely related to nystagmic rhythm in D P R T . All the cases with regular nystagmic rhythm could be operated on either through the translabyrinthine or middle fossa approach, while cases with dysrhythmia all had large tumors attached to the brainstem. Table 4 indicates that the postoperative nystagmic rhythm in patients operated on through the suboccipital approach becomes worse, that is, it becomes more dysrhythmic, than the preoperative state, while in cases where a translabyrinthine or middle fossa approach was used, there was no change postoperatively.
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Table 3. Nystagmic rhythm in acoustic tumor (49 years of age and under) Approach
Total Regular
Slight dysrhythmia
Dysrhythmia
Petite ~criture
Pre-op.
Translabyrinthine Middle fossa Suhoccipital
5 2 3
5 1 0
0 1 0
0 0 3
0 0 0
Post-op.
Translabyrinthine Middle fossa Suboccipital
8 2 8
6 1 1
1 1 1
0 0 6
1 0 0
Table 4. Post-operative nystagmic rhythm in acoustic tumor
Approach
Age
No change
Worse (dysrhythmia)
Translabyrinthine
< 49 > 50
5 1
0 0
Middle fossa
< 49 > 50
2 1
0 0
Suboccipital
< 49 > 50
0 0
3 3
Figure 4 shows the nystagmic rhythm in a patient with cerebellopontine angle meningeoma reoperated on 21 months after the first surgery because of tumor regrowth. The most striking findings in DPRT was the postoperative nystagmic rhythm which became gradually dysrhythmic and most evident just before the second operation and which recovered remarkably immediately after. In Figure 4, the uppermost recording indicates preoperative nystagmic rhythm, from B to C postoperative and D, ENG-recording one month after the reoperation, showing remarkable recovery in pendular nystagmus. K.G 44yrs cpa meningeorna
B
Fig. 4. A: Pre-operative nystagmic response. B: D
5ser
10 months after the first operation. C: 20 months after the first operation. D: One month after re-operation. Note: B and C: Nystagmic response reduced remarkably because of tumor regrowth. D: Recovery of nystagmic response
103
Damped Pendular Rotation Test 515r
h
prt.op
t=OSt-op
i 0' --
1o~
lo' I
Fig. 5. Patient with hemangioblastomaof right cerebellar hemisphere, a A: Pre-operative nystagmic rhythm. High frequency nystagmus with occasional inhibition are seen. B: Post-operative findings. H and h: horizontal recording. H: T.C. 3.0, h: T.C. 0.03. b Findings of pre- and post-operativeoptokinetic nystagmus pattern and Eye Tracking Test
Preoperative pendular nystagmus in a patient with hemangioblastoma in the right cerebellar hemisphere showed an increase of nystagmus frequency and slight dysrhythmia. Postoperatively, these findings disappeared and nystagmic rhythm in D P R T reverted to normal (Fig. 5a). After extirpation of cerebellar tumors eye tracking and optokinetic nystagmus became worse compared with preoperative findings (Fig. 5b). While pendular nystagmus in cerebellar atrophy or degeneration was regular and amplitude of nystagmus tended to increase (Fig. 6). 2. Brainstem lesions. In four patients diagnosed as having brainstem tumors, dysrhythmia and no response was observed in two cases respectively, one was found to have postinfectious lesions. This patient showed at first no pendular nystagmic response but improved later and gradually exhibited a nystagmic response. Dysrhythmia and reduced response or absence of response was frequently seen in large cerebellopontine angle tumors or other brain tumors. These findings appeared to be the effect of the direct compression of the tumor or by intracranial hypertension which in most cases can affect brainstem function. Figure 7 demonstrates a case with temporal lobe meningeoma in which preoperative dysrhythmia disappeared postoperatively. In most cases of irradiated brain tumors, dysrhythmia or reduced response was remarkable.
104
J. Kanzaki and C. Sakagami
IlO ~
B
}
1
~
II0~
5see
......
Fig. 6. Nystagmic rhythm in cerebellar atrophy cases. A: Patient with a late cerebellar cortical atrophy (male, 65 years old). B: Patient with a cerebellar atrophy (male, 39 years old). Note: Nystagmic rhythm in these cases was regular and the amplitude tended to increase. H: T.C. 3.0, h: T.C. 0.03. V: vertical recording. T.C. 0.03
l 10"
h
~
~
-
~
,
r.
h
11
......
I
10 ~
5sec
Fig. 7. Patient with a left temporal lobe meningeoma (male, 36 years old). A: Pre-operative nystagmic rhythm (dysrhythmic). B: Post-operative nystagmic rhythm (regular). H: T.C. 3.0, h: T.C. 0.03
3. Cerebral vascular diseases (18 cases). D y s r h y t h m i a in D P R T was also one of the most apparent nystagmic findings in cases with vertebro-basilar insufficiency. Cerebral vascular disease frequently showed a dysrhythmia and in some cases even a reduced response or a negative response was observed.
e) Nystagmic Rhythm in Peripheral Vestibular Lesions: In Meni~re's disease and sudden deafness, dysrhythmia and salvos in D P R T were found in either age groups, 49 years and under and 50 years and over, as frequently as in the healthy control group. In one patient with Meni6re's disease showing dysrhythmia in D P R T , labyrinthectomy was performed following an ineffective drainage operation of the endo-
Damped Pendular Rotation Test
105
lymphatic sac. For a few postoperative weeks dysrhythmia disappeared, but reappeared thereafter and remained. In this case EEG showed abnormal findings of paroxysmal slow waves in all leads which indicated hypothalamic epilepsy. These findings suggest that surgical manipulation of the labyrinth might temporally affect nystagmic rhythm although the route has yet to be determined. The fact that the labyrinthectomy did not eliminate dysrhythmia suggests that this might be caused by central mechanisms.
Nystagmic Rhythm and State of Alertness The effect of mental alertness by a subtraction task during pendular rotation on nystagmic rhythm was studied in ten normal subjects, in twenty-three cases -with peripheral vestibular disorders and in eighteen cases with central vestibular lesions. The test was done first with mental arithmetic and secondly without subtraction task. In about 40% of peripheral vestibular disorders, amplitude decreased when mental arithmetic tests were not given, but an affect on nystagmic rhythm was observed in only two out of sixteen cases under 49 years of age, in which regular nystagmic rhythm turned into dysrhythmia. In central vestibular disorders most patients showed dysrhythmia regardless of whether mental arithmetic was used or not. In three patients with central vestibular disorders; acoustic neuroma with wide extension into posterior fossa, pontine tumor and vertebro-basilar insufficiency, pathologic habituation according to the criteria of Greiner et al. [2] was found when mental arithmetic tests were not given. Discussion
A. Some Physiological Bases for Nystagmic Rhythm Anatomical and physiological bases related to nystagmic rhythm are complicated. In animal experiments in which vestibular nystagmus was evoked, unit discharge in vestibular nucleus, brainstem reticular formation and in abdecense nucleus were regular [4]. This is based on alternative rhythmic activities of IPSP and EPSP in antagonistic motoneurons [4]. Accordingly, lesions in the vestibular system could probably interfere with rhythmic unit discharges. In addition the pontine paramedian zone of reticular formation (PPRF) which might be a center for adduction and horizontal eye movement [1] could play an important role in producing nystagmic rhythm. It is not yet known whether oculomotor centers in diencephalon, whose role in evoking nystagmus has been reported [3, 5], are related to rhythmicity ofnystagmus or not. Pathways from vestibular nucleus and from brainstem reticular formation to oculomotor nuclei can be affected by circulatory disorders in the bralnstem, which are caused by arteriosclerosis or by the presence of a tumor or by secondary effect of the tumor. The rhythmicity of nystagmus might basically be a problem at synaptic levels, and lesions in these complex networks could interfere with the rhythmic activities of hyperpolarization and depolarization in antagonistic oculomotor neurons.
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J. Kanzaki and C. Sakagami
B. Nystagmic Rhythm in Healthy Control Persons In these series slight and marked dysrhythmia are observed in 15% of the persons between 10 and 49 years of age. This percentage coincides with that reported by Van de Calseyde et al. [6]. In the age group 50 years of age and over, slight and marked dysrhythmia were found in 26% of the subjects, narrow writing in the same percentage which was seldom seen in younger age groups. Nystagmic rhythm in persons under 10 years of age is less regular than in other age groups 49 years of age and under. The state of alertness may affect nystagmic rhythm and in most cases the amplitude of nystagmus tends to be low without mental arithmetic. In the present series of studies the subjects were under a mental arithmetic task (subtraction) during rotation in order to keep them in a constant state of alertness. Without the subtraction task, the narrow writings, or slight dysrhythmia could be seen frequently both in healthy persons and subjects with peripheral vestibular lesions. Pathological habituation which could often be found in central lesions was more frequently observed by this test without mental arithmetic. Thus in evaluating nystagmic rhythm in the pendular test, the level of consciousness of the subject as well as age should always be considered.
C. Dysrhythmia and Central Vestibular Lesions In preoperative cases with acoustic tumors, three out of ten cases showing dysrhythmia in D P R T were those extended into posterior fossa with a diameter of more than 3.0 cm and attached to the brainstem. These preoperative dysrhythmia became worse postoperatively. In Figure 8 the upper recording is a preoperative one in a patient with an acoustic neurinoma. Nystagmic rhythm is relatively regular with small amplitude. The lower recording shows irregular postoperative nystagmic rhythm 8 weeks after the operation. While dysrhythmia was seen in almost all cases operated via the suboccipital approach, that is, in large tumors, there was only a few dysrhythmia in cases operated on via the translabyrinthine or middle fossa approach. In cerebellar degenerative lesions there was no dysrhythmia. In postoperative cases with cerebellar tumors, narrow writing or nystagmus of reduced response were A
J
Fig. 8. Acoustic neuroma, left (age 35, female). A: Pre-operative nystagmic response. B: Post-operative nystagmic response (8 weeks). Note: dysrhythmic nystagmus after suboccipital operation
Damped Pendular Rotation Test
107
found without dysrhythmia. In some cerebellar tumors preoperative dysrhythmia was not found postoperatively. Therefore, narrow writing and reduced response in postoperative cases with cerebellar tumors might be the effect of operative procedure during tumor surgery. In this respect nystagmic rhythm in D P R T is thought not to be closely related with the cerebellum. Nystagmic rhythm in cerebral or midbrain lesions varies according to the size and location of the tumor, or the degree of circulatory disturbances. In cases with slight or marked dysrhythmia the effect of intracranial hypertension to the brainstem should be considered. In fact, preoperative dysrhythmia disappeared postoperatively with a decrease of intracranial pressure after tumor removal. In all patients with irradiated brain tumors, dysrhythmia was found, and in some cases dysrhythmia which was present before irradiation became more significant after the procedure. Patients who required irradiation may therefore be those with intracranial hypertension. The cause of dysrhythmia in all irradiated cases cannot be ascribed only to irradiation, although irradiation may affect the brainstem circulation and cause a dysrhythmia. In patients with internal capsule bleeding, dysrhythmia was not observed. While in most patients with brain tumors and suspected infections cases in the brainstem, a marked reduction of nystagmic response was found. F r o m these observations, postoperative reduction in nystagmus in cerebellar tumors might be due to either direct or indirect disruption of the circulation in the brainstem due to surgical procedure. Also from the fact that there was only slight dysrhythmia in D P R T in patients with acoustic neuromas operated on through the translabyrinthine approach and in cerebellar degenerative lesions, while marked dysrhythmia was obtained postoperatively in cases of acoustic tumors or other cerebellopontine angle tumors operated on through the suboccipital approach, or in post-irradiated brain tumors in which no dysrhythmia was found preoperatively or pre-irradiation respectively and in vertebro-basillar insufficiency, dysrhythmia is thought to be related to brainstem lesions or dysfunction of the brainstem mechanisms related to the rhythmic activity-of the pendular nystagmus.
References
1. Cohen, B.: Vestibulo-ocular relations. The control of eye movements, p. 105--148. New YorkLondon: Academic Press 1971 2. Greiner, G. F. et al.: Vestibulometrie clinique. Paris: l~dit. Doin 1969 3. Lachmann, J. et al.: Central nystagmus elicited by stimulation of the mesodiencephalon in the rabbit. Amer. J. Physiol. 193, 328--334 (1958) 4. Maeda, M. et al.: Rhythmic activities of secondary vestibular efferent fibers recorded within the abducens nucleus during vestibular nystagmus. Brain Res. 34, 361--365 (1971) 5. Manni, E. et al.: Eye nystagmus elicited by stimulation of the cerebral cortex in the rabbit. Arch. ital. Biol. 102, 645--656 (1964) 6. Van de Calseyde, P. et al.: L'ENG dans l'~preuve rotatoire sinusoidale amortie. Acta oto-rhinolaryng, belg. 23, 1-335 (1969) 7. Van de Calseyde, p. et al.: The damped torsion swing test. Quantitative and qualitative aspects of the ENG pattern in normal subjects. Arch. otolaryng. 100, 449--452 (1974) Received March 1, 1976
