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THE EFFECT OF GRAVIlOINERTIAL FORC, UPON

OCULAR COUNTERROLLING

Earl F. Miller II, and Ashton Graybiel

Bureau of Medicine and Surgery

MF] 2.524.005-5024B

NASA Order T-81633

NASA Order R-93

Released by

Captain M. D. CourtneyCommanding Officer

23 March 1970

This study was supported by the Biomedical Research Office, Manned Spacecraft Center,and the Office of Advanced Research and Technology, National Aeronautics and SpaceAdministration.

NAVAL AEROSPACE MEDICAL INSTITUTENAVAL AEROSPACE MEDICAL CENTER

PENSACOLA, FLORIDA 32512

SUMMARY PAGE

THE PROBLEM

To measure and compare normal subjects and persons with severe or completei nss na . . I... ;,t..iutl h, ,, uIIIV ,, O N ..... .. ..

antiles as a function of g-load'ng.

FINDINGS

A group of six normal subjects manifested a compensatoiy eye roll which increasedas a direct and essentially linear function of the component of the gravitoinertial forceacting laterally upon the subjeJct. This increase in response was not observed in thefive deaf subjects wih severe or complete bilateral loss of their vestibular organs.

',se findings confirmed similar results found by other authors using other measuring'chniques which show that the reflex eye movement is dependent upon and limitedthe magnitude of the grovitoinertial stimulus (within the range used) when the otolitho-

ocular system is functioning normally. However, when this function is impaired or lost,the magnitude of the compensatory eye roll is limited to that manifested at Ig andpossibly to nonotolithic contributions. These findings offer means for differentiationbetween otolithic defective individuals and "normal" persons who exhibit little counter-rolling.

A41

lN[II•oDJ JICINI IThe study of ol•lith activity in man is dependent upon a limited few overt

indicators which vary iH their specificity and mecuri-bi lity (1, 2, 4,6,9, 10,11,13,15). At thepresent time, ocular counterrolling represents the best objective means to explore theresponse ihatacteristics of the oloiith orquns at the reflex level. The usefulness of thisexternal indicator has been increased with the deveiopmenT Of a higliy precise phnio-graphic measuring technique and testing methods which minimize the influence of extra-labyrinthine factors upon ocular torsion (6-8, 12). The precision afforded by this pro-cedute reduces the need for itsing centrifugal force to magnify the response, and thuseases the difficulties in measurement of ocular roll. However,centrifugation may stilloffer u means by these meacuremernts of exploring etiological differences between smallamourt-i of ocular counterrolling manifested by apparently normal subjects and by thosepersons with severe bilateral labyrinthine defects.

Woeltner and Graybiel have demonstrated that ocular counterrol'ing as reflectedby the relative movement of two silk sutures in the conjunctiva was increased substantiallyin direct response to the amount of centrifugation (lateral p force) among five normalsubjects, but the procedure failed to produce similar results for two totally deaf subjectswith labyrinthine defects (16). Colenbrander recorded changes in the position of thesubject's blind spot which indicated increases in magnitude of normal counterrolling aswell as a steepening of the typical "S" shape response curve among his normal subjectsi n progressin3 from 1.0 to 1.5 to 2.0 resultant 9.(1).

The purpose of the present study was to explore further, by the photographicmethod, counterrolling as a function of hypergravic stimulation in six normal subjectsand in five deaf subjects with established functional losses of the semicircular canalsand otolith organs.

PROCEDURE

SUBJECTS

Six healthy young male medicai students volunteered as subji:ts for this studyduring their Navy officer clerkship training at Pensacola. Each demonstrated substantialocular counterrolling as measured by the standard photographic technique (6), and wasfree of any defect, disease, or disorder.

Five totally deaf men with complete or severe bilateral functional lass of thecupular and macular organs were chosen from a'group of instructors and students atGallaudet College to serve as the labyrinthine-lefective comparison group of subjects.Their clinical i4 sumr, which includes the results of mecisuring appropriate eye move-ment responses to thermal stimulation (5) and static body tilts (7), is given in Table I.

I l a,0

.2' -~ I0 -p_,

Cc- 0

44)

az z z I 2i

o ~0

-0 I' 4) Q 0

m vn

2 E

OZ AlIZ Al Al

'S.

0vE

S.. -- 04

0 VI

4)M

2zLI.>

APPARATUS

A tiit cliir was ontumA -ii tloohe u uf the Pensacola human centrifuge, 15 feet10 inches from the center of rotation, and was completely covered by a light-tightI,,=iu; t7n•iuur. 'inc Lhu;r wua 3u cornsrFucied ihai 4 cou; de 6iired iefirward or righ- Iward up to 90* by hydraulic power or held fixed in its upright position. A gimbal ring-- r. ---

with the subject's ' ,ngitudinal body axis, for pro-positioning the subject to face in or180' counter to the direction of centrifuge rotation for effective rightward or leftwardtilting, respectively. A hollow rubber appliance, filled with fine particles describedin detail previously (13), was used as the chair's inner liner. With proper manipulationthis liner could be rnade to conform closely to the subject's torso, neck, and head, andwhen evacuated, it became a rigid, form-fitting support. The head portion of theappliance was completely encased in a large helmet which was in turn attached to thetilt chair. Additioiol straps were used to secure the appliance as well as the subject'slegs and feet to the chair.

A 35-mm camera cnd electronic strobe system fully described elsmvhere (6-8, 12)was bolted to the ti It-chair supporting frome. A biteboard extended from the camerabase, and this entire assembly could be moved along its three principal axes for properimaging of the subject's eye being photographed. The camera was equipped for remotefiring by the experimenter from within the room at the center of the centrifuge. Voiceand buzzer (hand vibmator) communication systems were available between the subjectand experimenter as well as between the experimenter and the centrifuge external con-trol room.

METHOD

1. Tilt of the Subject With Res tto the Gravitational Vertical

The subject was positioned in the tilt choir and properly secired with the suppor-tive appliance and straps. The camera/strobe apparatus with its biteboard attachmentwas bvited immediately in front of the subject on the chair frame. The biteboard wasinserted in the subject's mouth, and he bit firmly into the temporarily softened dentalmaterial deposited on it. The camera was then racked into its proper position to focusupon the subject's right eye; his left eye was covered with an opaqua patch. One dropof pilocarpine hydrochloride I per cent was instilled in the eye being recorded to reducethe over-all size and physiological oscillations of its pupil (15), important factors in thesubsequent analysis of the film records.

During this phase of the experiment the observer conducted the test within themetal enclosure. While the subject was in the upright position, several photographicrecordings were made. The neah recorded eye position measured among these recordingsseW is the basis for computing eye roll deviation found for the various tilt positions.On, cording was used as the reference for comparing all other recordings by themethod of superimposing two projected images, as described elsewhere (6).

3

UI

111-3 chrir wur first tilted slowly from upright either in rightward (+) or leftward(-) direction (randomized among subjects) and according to the following sequence: I2 5 0. 50°. 58*. 63'. One recordinu was made at each of these tilt oositions. At 63'a second recording was made before initiating the same tilt procedure but in the descend-i tj order of the degree of tilt in retturning to upright; passing through upright Ihe sameascending-descending tilt order was repeated in the opposite quadrant. This procedurewas continued until at least three recordings had been mude at each of the eight tiltpositions and upright.

2. Tilt of the Grvitoin- rtial Vertcal with Respect fa the Upright Subject

Immediately following the static test of counterrolling and without removing thesubject from the chair, the chair was rigidly fixed in its upright position. The observermoved to the central room of the centrifuge where controls were provided for firing thecamera remotely and for communicating with the subject. The centrifuge was rotatedslowly (within approximately 60 reconds) in the counterclockwise direction up to thevelocity required to change the graviioinertial upright in the same amounts (250, 50*,580, 638) and in the same sequ'ential order rightward oe leftward as in the static testing.Calculation of the gravitoinertial vector was based upon the radial distance from theaxis of rotation to the center of the subject's head. Thus the essential differencebetween the static and dynamic forms of tilt was the difference (P) between the magni-tude of the gravitatiunal and gravitoinertial force which increased as a direct functionof apparent tilt (displacement of gruvitoinertial force vector) during rotation. Accuracyin the rate of rotation was mraintained within plus ;r mir,.;s I per cent. The subject facedforward in the direction of rotation for effective rightword "tilting" and was turned1800 to ttavel backward along the path of rotation for left-,,ard "tilting." The order oftilt direction was selected at random among the subjects. After slowly accelerating toeact, desired velocity, a 60-second delay was timed before the first photographicrecording was made. As in the static phase, the test ended when the eye was photo-graphed at least three times at each 0, the angle formed between the gravitational andgrwitoinertial force vectors.

RESULTS

The results are summarized in Figure 1. Mean counterrolling data in minutes ofarc of thr two groups of subjects are plotted as a function of tilt angle in degrees withrespect to the gravitational (closed circles) and 'he gravitoinertial upright (open circles).Individual counterrolling data were simflar to those representing the group data, but insome instances, a given subject's responses were substantially more variable than theaverage. This i;, to be expected with limited eye recordings at each position since theeye is physiologically active and may be phoiographed while it is undergoing anoccasional yet considerable spontaneous torsional shift (6). To reduce the effect ofthis influence which would be expected to occur in opposite directions at random amongsubjects, the results of the six normal as well as the five labyrinthine-defective subjectswere averaged and compared as groups.

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No, rall Subjects Lobr~nthkie-Detective

G 0 0 ;ujecrza- * Centrifuge Stolionury ', ....

C) ' o.......o Centrifuge Rotating " .

S~:400i.-

0

0 -200z

0

n-J

I--z -400

0 "s,5

-600

-'•-63 -50 -25 0 25 50 63

BODY TILT (DEGREES) WITH RESPECT

TO GRAVITY/GRAVITOINERTIAL FORCEFigure 1

Counterrolling of Normal and Lobyrinthirie-Defective SubjectGroups as a Function of Body Tilt with Respect to Gravitational cr Grovitoinertiol Force

5

I1;

rhoe two~ ruirves r,ý±presentirug the data of the normal group tested under the staticand dynamic conditions appear to be nearly coincident at the smallest angle of tilt(Figure 1). With greater tilt angles in both the right and left directions, the. curvesbecoun ri~orna nd inuire c~immmtrnt rpeve~dhvi fka aff~t iinnn nrIdnr _ ~ian~arrnlliif nf Amever-increasing amount of centrifugal force added to that of gravity. It is impossible todeterniinn a dire-d- rlutinr-rihip bfptwoozn counterrolli-ig rind margnitude of the inEcrtialforc.e since the angle, and, the~refore, direction of tile applied stimulus relative to theotolith organs'W'e also varied. As suggested by Woellner and Graybiel (16), an approx-imation of the comb~ined effect of magnitude antd direction is possible by consideringonly the inertial force component acting sagittally and perpendicul'ar to the subject'slong cc is. The intensity of this laterally directed force equal4,under the static condi-tion, fhe sine of the angle (0) formed between the body axis and the gravitational up-r -ght, and underlie dynamic conditions, the product of the gravitoinertial force (GIF)and the cosine of the angle (0) formed between the body axis and the gravitoinertial up-right. The difference between these values represents the difference (Aa) in otolithic

rK shear force generated bythe two test conditiotis, centrifugation and tilting:

41 g=GIF cos - sin 0

Figure 2khows the linear relationshIp Eound in normals between the change in oculartcounterrolling (6 CR) us 4~ functioni of th,.4 change in shear force (Ay~). The datu ofWot~llner and Graybiel were recalculated by this format and revealed remarkable agree-ment with our data (Figure 2) even though the two groups of normal subjects differed intheir basic counterrolling respnse levels.

The rt~ultN firom the labyrinthine-defective group of subjects are also presentedin Figure LThbes- subjects, in contrast to the normals, revealed no apparent difference

tA in counterrolling measured under the dynamic and static test conditions.

DISCUSSION

The counterrolling response to static tilt (centrifuge stationary) shown in FigureI is typical of normal subjects; under these test conditions, eye rollI compensation isgreatest between upright and 250, less between 250 and 5DO, and tends to reach a l imitmound 60*. This pattern of response changes dramatically when the magnitude of theresultant force is increased as a byproduct of the centrifugation required to effect anapparent tilt with the subject maintained in alirnment with gravity. At 250 of tilt underdynamic conditions, with only a slight increase in gravitoinertial force (11 .09 ,R), theamount of eye roll is comparable to that measured under static conditions. Above this

.. t.tilt angle a discrepancy between. the results of the static and dynamic ~modes begins toappear ans' to wax in direct relation to the angle of tilt; at the maximum tilt angle (63'0)the dynamic, unlike the static response, shows no sign of reaching or approaching a

6

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4. 0[ I /i 3.60

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i_ E 3.60 0

z

-2.40

z

0ac 1.80-

w

z 1.20-

0

1 .60

00

OO

0 .25 .50 .75 1.00 1.25 1.50

,A SHEAR FORCE (g UNITS)Figure 2

Average Change in Counterrolling for Normal Subjects as c FunctionI!• of the Chnnge in Shear Force. Data from Present Study Coded as Solid Circles,Those of Woeliner and Graybiel (16), Recalculated for This Format, os Dotted CirclesI7

Individually, as well cis a q'r~ -up t xc & .- c uqii~i~dfC. Irevealed no essential change in fl',oir savill, but definite basic counterrolling responsew~ifi hicreased E-looding. These resul'os confirm ifhose ,;{ Wouliner ar-d Gruybiul (16)

I. S.r'; No z.y m,, T.NI one'ln o of a norrna;wi ijc ;ri..UPf up

limited, within the range tested, by the strsength of tbo itit--iiaI force stimulus, that of

loss of his otolithiic or ans or by thie contribution of nonokolith!c gravireceptor systems.Evide.. e that this response is gwuvit', dependent is provided by data which show changesin the amount of cutroln uJ udcr 1-9 ~ton us o functifen of tilt, us wellas 6y the findings of a previous study which revealed that the small oniounts of ocularcounterrolling manifested by suck individuals was reduced or essentiully eliminatedwhen gravity was counteracted partially or completely by Keplariari flight (15). Theinnervation Source Of Such small cmounts of counterrol ling, however, rerndins in question.

Differentiation of whether a residuum of otolithic function e>Asts oý whether noni-otolithic grovireceptor activity can account fi-r reduced amoursts of counten'rolling m2'aydepend upon the independent but complementary stud iez of this reflex with a subjectimmersed in water or exposed to cantrifugation. Water immersion is highly effective inreducing, if not eliminating, the influence of the nonotolithic groviraceptor systemsupon the perception of the oculogravic illusion (3), but it rerrig ins to be shown that t. iswnvlronment would influence ocular caunteviolling. If watei imersion is effective,Ithen~ the question of origin of th--- counterrolling reflex is im'mediateiv solvad. If not,

centrifugation could be used in an attempt to drive this low-level function and toexplore the possibility that it represents a physiologically normol variation in this res-ponse characteristic.

RE FLRE NCES

1. Golenbrander, A., Eyes and otoliths. Aerorned. Attu, 9- 45-91, 1964.

2. Graybiel, A., Oculogravic illusion. Arch. thI,48 605-615, 19052.

3. Gry~l A., Miller, E. F. 1I, Newsom, B. D., and K.enne4di, R. S., Th'seffect of water imme 5ion on percept ion of the oculogravic illusion in nonmaland labyrinthine-.defective subjects. Acto otaoar~nq., Stockh., 64~ 599-610,1968.

4. Jongkaes, L. 6. W.., The parallel1 swing test. In: Wc-'son, R. .J. (Ed.), TheVestibular ýysteni and Its Disl ses. Phil~aelpful, P(3.- University ;r

5. McLeod, M. E., and Meek, J. C., A threshold caloric tesh Results in normalsubjects. NSAM-834. NASA R-47. Pensacola, Fla.: Navol School ofAviation Medicine, 1962.

V 6. MiP13r, E. F. 11, Counterrolllng of the human eyes produced by head tilt with respectto ait.Acta otolaryng., Stockh., 54, 479-501, 1961 .

7. Miller, E. F. ~[Ocular counterrolling. In: Wolfson, R. J. (Ed.), The VestibularSystemn and Its Diseases. Philadelp~ia, Pa.- University of Penivylvani

8. MIilr, E. F. 11, Evaluation of otolith function by means of ocular counterrollingmneasuerements. Irt Stahle, J. (Ed.), Vestibular Function on Earth and inSpare. QCbord'nqiland: Pergamon Press, 90P7iY

9.Miller, E. F. 11, Fregy, A. R., and Graybiel, A., Visual horizontal perception inrelation too.tolith fijnct~on. Amer. J. Psco. 81.-488-496, 1968.

10. Millasr, E. F. I1, and Graybiel, A,,. Comparison of autokinetic movement perceivedby normal cinr deaf subjects with bilateral labyrinthine defects. Aerospace

M~,33:1077-1080, '962.

11i MIioar: E. F. HI, cind Graybiei, A... Rotary autokinesis and displacement of the4--afl horizontal associated with head (body) position. Aeopc e.34c 915-919, 1963.

12. Miller. E. F. 11, ond Graybiel, A., A comparison of ocular counterrolling mnove-mentý, [eatw~gn normal persons and deaf subjects with bilateral labyrinthineI defect-,. Ann. Ot.,lI., 72 8835-893, 1963.

J 9

13, Miller, r. F I11, ond Iraphiel, A,, Magnitude of gravitoinertial force, an indo.-pendent vurkible ir, egoc miric visuwl localization of the horizontal.I .A-. P.,-1- 71.A9..4-,An 1QAA

1-T. Milbr. E. F. I1, and Gravbiel, A., Role of the otolith organs in the perception ofhorizontality. Amer. J. Psydhol., 79:24-37, 1966.

15. Miller, E. F. II, Graybiel, A., and Kellogg, R. S., Otolith organ activity with-in earth standard, one-half standard, and zero gravity environments.Aerospace Mt.J., 37:399-403, 1966.

10'. yW li,.ar, R. C., and Grayuiel, - ,u,,,rollir,. of the eyes and its dependenceon the magnitude of grr'•itational or inertial force actinqi laterally on thebody. J. appl. Physiol., 14:632-634, 1959.

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DOCUM 'NT CONTROL DATA • -& u ~il I" 1".,IrJA* t111 A[4TI40 .v (PlEP I lvfll t) r rORT NKCeU ITV CLAssIFICATION

Naval Aerospace Medical Institute UnclassifiedPensucula, Florida 32512 VA _ __ __

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THE EFFECT OF GRAVITOI JERIIAL FORCE UPON OCULAR COUNTERROLLING

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23 Marc h 1970 11l, j or I' 161. , 1. ,,,W1 OAlGlu:TOR'S k.,Po ,NIT INN

NASA T-81633 and NASA R-93 NAMI-1104

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11 SUI'ILI I AVTAII 10T. S 1i SPONSORING MILITARV ACTIVITY

N/A A

The effect in tcrms of magnitude of ocular counterrolling of giLoading at various angles oftilt up to 630 was measured on normal subjects and compared with the effect upon persons withsevere or complete loss of otolith function. The group of six normal subjects manifested a com-pensotory eye roll which increased as a direct and essentially linear function of the componentof the gravitoinertial force acting laterally upon the subject. This increase in response was not

observed in the five deaf subjects with severe or complete bilateral loss of their vestibular organs.These findings confirmed similar results found by other authors using other measuring techniqueswhich show tha* the reflex eye movement is dependent upon and limited to the magnitude of thegruvitoinertial stimulus (within the range used) when ihe otolitho-ocular system is functioningnormally. However, when this function is impaired or lost, the magnitude of the compensatoryeye roll is limited to that mcnifested at 1 a and possibly to non-otolithic contributions. Thesefindings offer means for differentiation between otolithic defective individuals and "normal"persons who exhibit little countenolling.

DD 1 3 "" )UaFOIM1AAedDD by r147 Unclassified

Undl, ,;fied. .�-� ,�tt tity ClommifIcetion

Otol ith urouws

Ocular counterrl ing

Eye moviement

Labyrinthine defects

g-loading

D D,'o ..14 73 (BACK Unclassified

(PA•GE 2) Security Clan-ificaltion

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