Clinical verification of a unilateral otolith test

Acta Astronau6ca Vol.27, pp. 1 9 - 24, 1992 Printed in Great Britain

CLINICAL

J. We%zig*,

0094-5765/92 $5.00+0.00 Pergamon Press Ltd

VERIFICATION

OF A U N I L A T E R A L

K. H o f s % e % % e r - D e g e n * ,

Johannes-Gutenberg

University,

J. M a u r e r + *Dep%.

and R.J.

Physiology

TEST

yon B a u m g a r % e n *

and +ENT Dept.

2,3,5,7,9,11,12 Small d i f f e r e n c e s of otolith weight or the number of sensory cells or nerve fibres of %he otoli%h a p p a r a % u s in %he lef% or the right labyrin%hs respectively would p r o b a b l y be fully c o m p e n s a t e d on the ground. Such persons would be regarded as normal under %he ig condi%ion. In space the d i f f e r e n c e s of the o % o l i t h weigh% on bo%h sides would disappear and then %he c o m p e n s a t i o n itself w o u l d r e p r e s e n % a disturbing factor until recompensa%ion (space vestibular adap%a%ion) takes place.

ABSTRACT 13 In a p r e v i o u s study we r e p o r t e d p r o m i s i n g results for a new test to d i f f e r e n t i a t e in vivo unilateral o%olith functions. Tha% study p o i n t e d to a need for further validation on known pa%hological cases. In this presen%ation we will detail the results g a t h e r e d on a group of clinically v e r i f i e d v e s t i b u l a r defec%ives (verum) and a normal (control) group. The subjects in the verum group were former patients of the ENT clinic of %he u n i v e r s i t y hospital. These subjec%s had usually s u f f e r e d from neurinoma of the V I I t h cranial nerve or inner ear infec%ions. All had required surgical interven%ion including removal of the vestibular sys%em. The patients were c o n t a c % e d usually %wo or more y e a r s p o s t o p e r a tively. A g r o u p of s%udents clinical phase of served as con%rol.

OTOLITH

Experimen%al %esting of %his hypo%hesis requires a m e % h o d which allows the m e a s u r i n g of %he o % o l i % h i c activi%y on each side of the head separatly. The mos% c o m m o n l y used otolithic tests a~e %he ocular counter ro%ation ( O C R ) ' during lateral %ii% and ~he r e s e % t i n g of a luminous line (LL) in the dark to the subjective ver%ical. But these %es%s do no% separa%e between %he right and lef% o%olith system. To m e a s u r e o%oli%h asymme%ries OCR comparisons between %he left and %he rig%% eye due %0 la%~ral %ii%s were used bY LLackner a% al.-. D i a m o n d and M a r k h a m examined OCR-responses in an uprigh% p o s i % i o n during hypoand hypergravi%y o~ p a r a b o l i c fligh%s. K o r n i l o v a et al. used unila%eral g a l v a n i c n y s t a g m u s %o discover bilateral asymmetries. All authors found a positive c o r r e l a t i o n between space motion sickness susc e p % i b i l i t y and a s y m m e % r i c a l vestibular responses.

from the pre- and medical training

Bo%h groups were s u b j e c t e d to stand a r d i z e d clinical %es%s. T h e s e %es%s served to reconfirm %he in%raor p o s % o p e r a t i v e d i a g n o s i s of u n i l a % e r a l v e s % i b u l a r loss in %he verum group. In %he con%rol group they had to es%ablish the normalcy of the r e s p o n s e s of %he v e s t i b u l a r system. Both groups then u n d e r w e n t %es%ing on our e x c c e n % r i c ro%ary ~ a i r in %he manner d e s c r i b e d before P r e l i m i n a r y results of the trials indica%e %ha% this test may indeed for %he firs% time offer a chance to look at isolated otolith apparati in vivo.

For the i n v e s t i g a % i o n of u n i l a % e r a l otolith func%ions we have %ested a new m e t h o d which is based on the eccentric rotation o~3 an e l e c % r i c a l l y driven rotary chair

INTRODUCTION Space m o t i o n sickness is a complex p h e n o m e n o n which is o b s e r v e d in almost every space mission. Several authors p r o v i d e d s u p p o r t i n g evidence that bilateral asymmetries of the v e s t i b u l a r system would c o n t r i b u t e to space sickness susceptibility

HYPOTHESIS We hypothesized, that the luminous line set%ings of normal control subjects and of u n i l a t e r a l l y labyrin%hectomized subjects would differ 19

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considerably on the eccentric positions°

rotary

chair

in

METHODS Subjects T w o g r o u p s of s u b j e c t s took part. One group (verum) consisted of former patients of the ENT clinic. These subjects had suffered from neurinoma of the V I I t h cranial nerve, cholesteatoma or i n n e r ear i n f e c t i o n s and had required surgical intervention including removal of the vestibular s y s t e m on o n e side. T h e p a t i e n t s w e r e e x a m i n e d t w o y e a r s or m o r e p o s t o p e r a tively. The other of h e a l t h y Clinical

group young

(control) students.

consisted

Procedure

Both groups were subjected to s t a n dardized clinical tests, including electronystagmography under positional, t h e r m a l a n d o p t o k i n e t i c stimuli. In a d d i t i o n posture tests (Romberg) on a s t a b i l o m e t e r platform were undertaken. These tests served %o reconfirm the postoperative diagnosis of u n i l a t e r a l vestibular loss in the verum group. In the control group t h e y h a d to e s t a b l i s h t h a t no v e s t i bular disease or pertinent history was p r e s e n t . Rotary

chair

procedure

The subjects were seated in u p r i g h t position on t h e rotating chair. The chair was accelerated to 30 RpM. Thereafter the angular velocity on the chair was kept constant throughout the experiment propre to avoid canal stimulation. The subjects were then positioned eccentrically to the axis of rotation to effect stimulation of the otolith system. S t a r t i n g w i t h the a x i s of r o t a t i o n in the midline of the head and then slowly moving to e c c e n t r i c positions the following combinations of stimulation of b o t h l a b y r i n t h s would occur: I.

a x i s of r o t a t i o n in t h e m i d l i n e : both labyrinths are stimulated e v e n l y b u t in o p p o s i t e d i r e c t i o n

2.

axis of rotation e.g. to left: the right labyrinth s t i m u l a t e d m o r e t h a n the left and with opposite sign

3.

axis of r o t a t i o n e.g. t h r o u g h the left labyrinth: only the right l a b y r i n t h is s t i m u l a t e d

4.

axis of r o t a t i o n e.g. left from the left labyrinth: both labyrinths are s t i m m u l a t e d in the

the is one

same than

direction, the t h e left one.

right

more

The rotating c h a i r h a d a m o u l d e d seat m o u n t e d on a s l i d i n g p l a t f o r m resting on top of a s t a n d a r d rotating chair pedestal. Subjects were fixed by a four p o i n t h a r n e s s and a helmet type head restraint. The seat could be moved by r a d i o remote control l0 cm sideways to either side along the subject's y-(shoulder to shoulder] a x i s in ] cm i n c r e m e n t s . On the seat was f i x e d the m e a s u r e m e n t apparatus, consisting of a h e a d restraint helmet, covered by a c l o t h hood to further exclude ambient light. A t t a c h e d to this h e l m e t was a g o g g l e insert, which carried in f r o n t of one eye a luminous line (LL) stimulator. The LL-stimulator in t u r n presented the eye with a redly lit line subtending approx. 30 dego in the f i e l d of view. T h e L L s u p p l y u n i t was m o u n t e d in a small rack on the backside of the chair. The subject could manually rotate the outermost end of the tubular LL insert to control the orientation of the LL. The angle of r o t a t i o n was p i c k e d up by a precision potentiometer as v o l t a g e , P C M c o d e d in the s u p p l y unit and transmitted by r a d i o link to a d e c o d e r in t h e lab. T h e r e the v o l t a g e was displayed on a d~gital multimeter, read visually by t h e experimenter and noted manually~ The limiting factor for p r e c i s i o n of the measurement chain was the 8 bit resolution of the PCM link. Limiting the r o t a t i o n r a n g e of tlhe i n s e r t g a v e a final resolution of 0 5 deg. The intensity of the ]J[J c o u l d be c o n trolled before the s t a r t of the rot a t i o n by t h e o p e r a t o r on the s u p p l y unit. Care was taken to exclude external l i g h t by f i r m l y seating the goggle on the face a n d by t h e hood~ The lab was darkened, in a d d i t i o n . Subjects were required to confirm that no visual cues other than the line itself were visible before s t a r t i n g the chair. N e x t the subject was a s k e d to c l o s e the eyes, scramble the L L from the vertical to the right (clockwise; CW), open the e y e s and reset it to subjective vertical. T h i s was r e p e a t e d o n c e a n d t h e n the s a m e p r o c e d u r e was d o n e w i t h s c r a m b l i n g to t h e left (counterclockwise, CCW) ~ Following this the r o t a t i o n was s t a r ted. The subject was requested to scramble the line to the r i g h t and c l o s e the eyes. T h e i n i t i a l a c c e l e r a t i o n was suprathreshold. Thereafter, d u e to l i m i t a t i o n s of t h e m o t o r , it decreased, until, after approx. 20 s a final and constant rotational speed

9th IAA Man in Spac¢ Symposium

of 30 rpm was reached. To avoid influences of rotational n y s t a g m u s and o c u l o g y r a l illusions the test was begun only af£er another 60s of waiting.

21

fore e x p e r i e n c e a stimulus c o r r e s p o n ding to a static tilt angle of approx i m a t e l y 5.76 d e g r e e s about a sagittal axis. RESULTS

The subject was then again p r o m p t e d to set the line twice coming from the CW s c r a m b l e d a t t i t u d e and then twice coming from the CCW s c r a m b l e d attitude. Four values were thus o b t a i n e d for any p o s i t i o n of the seat. Following this the chair was m o v e d to the next position to the right by 1 cm steps and the p r o c e d u r e repeated at each position. When all ten positions had been reached, the chair was driven back to centre position and the same sequence as o u t l i n e d above followed, but this time moving the seat stepwise to the left. After this was done, the chair was again returned to the centre p o s i t i o n and decelerated. W h e n the p o s t r o t a t o r y sensations had abated, the subject followed the setting sequence for a p o s t r o t a t i o n calibration. The p r o c e d u r e o u t l i n e d above was rep e a t e d with the subjects, this time p r e s e n t i n g the LL to the other (left) eye The data noted by the operator was typed into a spreadsheet programme and reread to verify correctness once. V o l t a g e s were c a l i b r a t e d with the zero r e f e r e n c e value (for it's definition see below), converted to degree by formula and the means computed. The raw data values of i n d i c a t e d voltage were d e p e n d i n g on the individual fixation of the LL insert in the goggle and the subjective initial setting. To arrive at a n o r m a l i z e d angle therefore the mean over all data points was c o n s i d e r e d as a good candidate for a voltage value reference. H o w e v e r i£ turned out, that the settings p e r f o r m e d at rest when the chair had not yet started to rotate were often erratic and usually skewed the data such that the regr e s s i o n line would not go through the coordinate zero. Therefore the sum of settings e x c l u d i n g the first four settings was taken as voltage reference and all other angles were c o m p u t e d from this reference. Note that the stimulus is entered in all the figures as the e c c e n t r i c i t y in centimetres. The unit in the diagrams for the r e g r e s s i o n line slope is therefore d e g r e e s / c m lateral displacement. To arrive at an angle, the lateral d i s p l a c e m e n t has to be subs t i t u t e d with the arctan of the quotient of c e n t r i f u g a l force over 9.81 m/s/s of gravity. An object p l a c e d at an e c c e n t r i c i t y of i0 cm would there-

The results of the clinical evaluation will not be d e t a i l e d here. For this series of the rotary i.e. the chair from above. Normal

only right r o t a t i o n s chair are reported, turned CW when seen

Subjects

Two of the control subjects could not finish the trial. One had an ongoing viral infection with general malaise, w o r s e n e d by the rotation onset to the point of major discomfort. Another one succumbed to a mild case of c l a u s t r o p h o b i a under the h e l m e t with hood and e l e c t e d to terminate the exp e r i m e n t prematurely. A total of ten normal control subjects participated. 4 were female, 6 male. Ages ranged from 20 to 28, with a mean of 23.2 years. The data of all of control subjects could be fully evaluated. The subject's left and right eye's settings were e x a m i n e d usually on the same day. A listing of the individual data points and the mean data of the four c o n s e c u t i v e settings at each p o s i t i o n is not given here for sheer volume.

..................... !.......~'

i

x i

[..... j.

-10

-8

-6 -4 -2 0" 2 4 e Choir Eccentricity [ c m ] ( + : - right shoulder)

8

Figure i: Subject HS. Dots and d o t t e d line are data points and first order regression line for the left eye, crosses and dashed line are for the right eye respectively.

10

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9th IAA Man in Space Symposium

I

....... L .......

....... i ....... i ....................

I

.............

4 t .............. !

'

~

1

:

:

4t...............

~........

!

ix!

I i

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I .l I i, kl i Jo,'""i" ]..-."-~ 0 i' l I '. ~ I......................... [ F l....... "r':.'~-x[ Ii x |

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....... "[ 't / * l

.......t.......!.......I.......+ .......

! i

:

I i : +,....... ~, ........... F"X

I ~

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]

hx

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i i

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0

2

,t

~

~

/ Choir Eccentricity [cm]

-,o

(+ : = right shoulder)

Figure 2: Regression lines for d a t a of all control subjects. Dotted lines are left eyes, dashed l i n e s are r i g h t eyes. A typical e x a m p l e of a c o n t r o l ject is s h o w n in the f i g u r e i.

summary

of

sub-

the

The "gain" of the m e t h o d a p p e a r s to be a b o u t 2.29 d e g r e e s of L L A n g l e for i0 cm d i s p l a c e m e n t , w h i c h c o r r e s p o n d s to 5.76 d e g r e e s v i r t u a l roll tilt. LABYRINTHECTOMIZED

-4. -2 Chair Eccentricity

-~

[cm] (4- :~

SUBJECTS

Of the e l e v e n l a b y r i n t h e c t o m i z e d subjects invited, one did not undergo the test. Four more did not finish the i n v e s t i g a t i o n . In the four cases one subject d e v e l o p e d m a l a i s e at the o n s e t of the r o t a t i o n for the s e c o n d h a l f of the trials, after the chair had been decelerated for the change of the luminous line insert to the other eye.

:0

right ~houtder)

Figure 3: Subject n o m e n c l a t u r e as i.

N o t e the s m a l l s c a t t e r of d a t a p o i n t s and the g o o d c o i n c i d e n c e b e t w e e n left and r i g h t e y e ' s r e g r e s s i o n lines. Figure 2 displays a r e g r e s s i o n l i n e s now.

-e

RO. Same in f i g u r e

As can be seen in this case ( f i g u r e 3) t h e d a t a v a r i e s m o r e t h a n in the normal control subjects. C l e a r l y t h e r e is a l s o a m a r k e d a n g l e that opens between ]eft and right eye's settings. However, i9 m u s t be noted, that in one of the six subjects (WF) the regression lines coincided very well for left and right eye while in a n o t h e r (AO) the a n g l e was of c o n t r o l g r o u p size only. We t h u s h a v e two s u b j e c t s which, even while being verifyably labyrinthectomized, showed "normal" regression line b e h a v i o r . F i g u r e 4 r e p r e s e n t s the s l o p e s of the regression lines for all verum s u b j e c t s , as was d o n e for the c o n t r o l subjects.

i

,,

i

i

:,

:~

b<::}<';?;r,d ',

Three more elected not to c o n t i n u e the experiment with the second (right) eye due to s u b j e c t i v e d i s c o m fort. In t o t a l ten s u b j e c t s participated, six of t h e m w i t h b o t h e y e ' s s e t t i n g s .

..-"'L /

_.

-1o

Of the ten s u b j e c t s 6 w e r e f e m a l e , 4 male. Of the six f i n i s h i n g t h e full set of t r i a l s 4 w e r e f e m a l e , two w e r e male, i.e. the sex ratio was the same. A g e s r a n g e d from 20 to 68 in all subjects. Since the extremes a l s o in the g r o u p of the f i n a l t h e r e the r a n g e was the same, the m e a n d e c r e a s i n g ~ o w e v e r f r o m in the full g r o u p to 49.3 in the group.

ten were six, with 51.7 six-

>'"i -t

i

i ..-i'i" -4

-6 Choir

.' -2

o

F'ccen~ici'b/ [cm] (+ := right shoulder)

Figure 4: Regression lines for d a t a of the f i n a l six verum group subjects. Same nomenclature as in f i g u r e 3.

J

i i

9th IAA Man in Space Symposium

DISCUSSION All

subjects

Visus was s u f f i c i e n t for the task at hand in all subjects. Experience shows, that the image of the line need not be sharply f o c u s s e d over the full viewing angle. This was not po s s i b l e anyway, owing to the lens refraction errors of the high diopter lens used in the goggle. Even for subjects with 20/20 vision a distortion with the line either frayed at the ends or b u l g i n g in the middle, d e p e n d i n g on focussing, existed. Obviously, the edge d e t e c t i o n c i r c u i t r y of the visual a p p a r a t u s can cope with the distortions introduced in our device. Normal

23

forces, as outlined in the introduction. The slope of the data, as e v i d e n c e d by the r e g r e s s i o n lines fitted £o each subjects data varies, but not more than can be e x p e c t e d for biological data c o l l e c t e d by a subjective p s y c h o m o t o r task. Labyrinthectomized

subjects

In view of our hypothesis there was a 66.4% success. Four of our six subjects showed a clear deviation from the normal control group settings. Age may have played a role in the verum group. However we note, that the verum group c o n t a i n e d one subject even y o u n g e r (20) than the average of the control group (23.2).

Subjects

Methodical

considerations

It m i g h t be argued, that the m e t h o d of d e t e r m i n i n g the zero r e f e r e n c e for the LL indications is arbitrary. However we believe that the grand mean is the i n d i v i d u a l zero point of the system. This system then relates to the outside world r e f e r e n c e system in an i n d i v i d u a l l y d i f f e r e n t fashion. No person has the head absolutely vertical in normal life. Most people will even show a visible roll and pitch attitude. We therefore believe that it is p e r m i s s i b l e to n o r m a l i z e by r e f e r r i n g all values to this individual "normal" position. Experience showed that the first four settings were rather often "off" and not in line with the rest of the settings, "spoiling" the mean. We therefore left them out of the zero r e f e r e n c e calculation. However, it should be noted, that they i n t r o d u c e d only a linear bias into the y-scale. Therefore all our s t a t e m e n t made, referring to angles are not affected, since they would be invariate £o linear bias. Procedural For a normal unusual, but ence.

Stresses person the chair is an non-provocative experi-

Rather one has to beware of not falling asleep during the about 30 m i n u t e s of rotation in the dark. This pitfall deliberately is guarded against by the investigator, constantly prompting the subject by voice to set the line and to indicate the c o m p l e t e d setting. The LL a n g l e s set by the "normal" subjects show no major surprises. The settings of the luminous line follow the course of the e f f e c t i v e c o m b i n e d gravitational plus centrifugal

The two falsely negative results in subjects AO and WF cannot at this time be explained. We initially considered adaptation. In view of the ages of 59 and 61 years of the two "false negative" subjects this would be rather unlikely. E x a m i n i n g more closely the clinical data for clues, whether there may have been a lesion on the n o n - o p e r a ted side was u n s u c c e s s f u l so far too. Such a d o u b l e s i d e d lesion would at least explain why the left and right values did not differ greatly. The m e t h o d p r e s e n t e d cannot localize the location of any p o s s i b l e inequality of the vestibular apparati. While we have gained our results on patients with d e m o n s t r a t e d p e r i p h e r a l lesions, we cannot exclude more central lesions other than from circumstantial clinical evidence. It is commonly accepted that the s e m i c i r c u l a r canals are not stimulated by linear acceleration, except maybe under ~he paradigm of the barbecue spit . We will therefore insist, that the effects we have seen, be they equal or with side differences, were o t o l i t h mediated. We were slightly astonished at the apparent gain of only 2.29/5.76 = 0.40 of LL setting vs. p s e u d o tilt. We suggest, working ~ o m e v i d e n c e of Gray~el and Clarke and Miller et al. --~' as r e p o r t e d in the H a n d b o o k of Sensory Physiology, that the proprioceptive cues are partially r e s p o n s i b l e for the almost unity gain r e p o r t e d for luminous line settings and tilts of up to 30 degrees in subjects sitting in a tilt chair.

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9th IAA Man in Space Symposium

Kornilova, L.N.; Yakovleva, l.Ya.; Tarasov, I.K.; Gorgiladze~ G.I. V e s t i b u l a r d y s f u n c t i o n in cosmonauts during a d a p t a t i o n to zero-G and r e a d a p t a t i o n to i G. Physiologist, Suppl. ]983;26,6

CONCLUSIONS A d i f f e r e n c e in slope of the left and right eye's settings with an angle of more than I0 d e g r e e s / c m is a necessary but not s u f f i c i e n t c o n d i t i o n for diagnosis of otolithic labyrinthine inequality.

hackner, James R.; Graybiel, Ashton; Johnson, W a l t e r H.; Money, K e n n e t h E. A s y m m e t r i c otolith function and i n c r e a s e d s u s c e p t i b i l i t y to motion sickness during exposure to v a r i a t i o n s in gravitoinertial acceleration level. Aviat. Space Environ. Med. 1987;58

The method p r e s e n t e d can serve to indicate otolithic inequalities. It cannot ensure that NO such state exists, nor can it localize the lesion. In contrast to e.g. the method applied by Diamond and M a r k h a m , which separates inequalities under zero-G, we can separate under normal gravity conditions and with little more effort than a standard r o t a t i n g chair investigation.

i0

Miller,E.F., Fregly, A.R.; Graybiel, A. Visual h o r i z o n t a l p e r c e p t i o n in relation to otolith function. AMI-989, Pensacola, FL, Naval Aerospace Medical I n s t i t u t e (1966)

ii

Trinus, K.F.; Studies of the otolithic a s y m m e t r y with subjective s e n s a t i o n s and p o t e n t i a l s evoked by the action of the linear a c c e l e r a t i o n s d i r e c t e d upward. A b s t r a c t s of the r e p u b l i c a n scientific and practical conference, 22-23 October 1987, Kiev, USSR.

12

Yegorov, B.B.; Samarin, G.I. Possible change in the paired operation of the vestibular a p p a r a t u s during weightlessness. Kosm. Biol. Aviakosm. Med. 1970;4

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Wetzig, J.; Reiser, M.; Bregenzer, N. ; Baumgarten, R.J.v.. Effects of o f f - c e n t e r rotation of the head on p e r c e p t i o n of the subjective vertical. P f l G g e r s Archly 1990; 415:R ii0.

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