OCULAR COU~RROLLlNG

Eaal F. Millet II cnsd A o h Graybiel

NAVAL AEROSPACE MEDICAL INSTITUTE

WTIQML AEW3MUTiCS AND SPACE ADMINISTMTIQW

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THE EFFECT OF GRAYlTOlNERTlAL FORCE UPON

OCULAR COUNTERROLLING

Earl F. Mil ler II, and Ashton Graybiel

Bureau of Medicine and Surgery MF 1 2.524.005-50248

NASA Order T-8 1633

NASA Order R-93

Released by

Captain M. Do Courtney Commanding 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 Space Administration.

NAVAL AEROSPACE MEDICAL INSTITUTE NAVAL AEROSPACE MEDICAL CENTER

PENSACOM, FLORIDA 3259 2

SUMWRY PAGE

THE PROBLEM

To measure and compre norme l subiects and persons with severe or complete loss of otolith function in the amount of ocular counterroll associated with several tilt angles as a hnct isn of g-iwding, -

FINDINGS

A group of six normal subjects manifested a compensatory eye roll which increased as a direct and essentially linear function of the component of the gravitoinertial force acting lateraily upon the subiect, 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 techniques which show that the reflex eye movement i s dependent upon and limited to the magnitude of the gravitoinertial stimulus (within the range used) when the otolitho- ocular system i s functioning normally. However, when this function i s impaired or lost, the magnitude of the compensatory eye rol l i s limited to that manifested at 1 g and possibly to nonotoli thic contributions. These findings offer means for differen3ation beween otolithic defective individuals and "normal" persons who exhibit l i t t le counter- rol I ing.

The study of otolith ac t i v i v in man i s dependent upon a limited Few overt indicators which vary in their specificib and measurabiliv ( I , %,4,6,9,'IO, I f , 13,15). A t the present time, ocular counterrolling represents the best objective means to explore the response characteristics of the otolith organs at the reflex level, The usefulness s f this externai indicator has been increased with the developiiient of a highly precise photo- graphic measuring technique and testing methods which minimize the influence of extra- labyrinthine facton upon ocular tarsion (6-8, 121, The precision afforded by this pro- cedure reduces the need for using centrifugal force to magnify the response, and thus eases the difficulties in measurement of ocular roll, However,centrifugation may sti l l offer a means by these measurements s f exploring etiological differences beheen small amounts of ocular counterrol l ing manifested by apparently normal subjects and by khose pemons with severe bilateral labyrinthine defects,

Woe1 Lner and Gray biel have demonstrated that ocular counterrol l ing as reflected by the relative movement of two silk sutures in the conjunctiva was increased substantially in direct response to the amount of centrifugation (lateral g force) among five normal subjects, but the procedure failed to produce similar resulgfor two totally deaf subjects with labyrinthine defects (16). Colenbrander recorded changes in the position of the subject's bi ind spot which indicated increases in magnitude of normal counterrolling as well as a steepening of the iypica l "S" shape response curve among his normal subjects i n progressing from 1 .0 to 1.5 to 2.0 resultant g - (1).

The purpose of the present study was to explore further, by the photographic method, counterrolling as a function of hypergravic stimulation i n six normal subjects and i n five deaf subjects with established functional losses of the semicircular canals and otolith organs.

PROCEDURE

SUBJECTS

Six healthy young male medical students volunteered as subjects for this study during their Navy officer clerkship training a t Pensacola. Each demonstrated substantial ocular counterrol ling as measured by the standard photographic technique (6), and was free of any defect, disease, or disorder.

Five total ly deaf men with complete or severe bilateral functional loss of the cupular and macular organs were chosen from a group of instructors and students at Gal laudet College to serve as the labyrinthine-defective comparison group of subjects. Their c linica l r&surnk, which includes the results of measuring appropriate eye move- ment responses to themai stimulation (5) and static body t i l t s (7), i s given in Table I .

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--

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s"

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l

iz

tt

A tilt chair was mounted on the arm of the Pensacoia human centrifuge, 15 feet 16 "iches from the center of rotation, and was completely covered by a light-tight mehI encIosureB The chair was so constructed that it could be t i l ted l e f ~ a r d or right- ward up to 9OBby hydraulic power or held fixed in its upright position. A g i m h l ring shsppo~ allowed the chair to be rotated compieteiy about its yaw axis, which coincided w f h the subiect" longitudinal body axis, for pre-positioning the subiect to face i n or 180" counter to the direcf-ion ~f centrifuge retation for effective r ighhard or Ief%~ard tilting, respectively , A hollsw rubber appliance, f i l led with fine pgrl.isfes described in detail previously (131, was used as the chaires inner liner, With proper manipulation this liner could be made to conform closely to the subject's tosso, neck, and head, and when evacuated, it became a rigid, form-fitting support, The head portion of the appliance was completefy encased in a large helmet which was i n turn attached to the tilt chair, Additional stmps were used to secure the appliance as well as the subject's legs and feet to the chair,

A 35-mm camera and electronic strobe system fully described elsewhere (6-8, 12) was bolted to the t i it-chair suppoding frame, A biteboard extended from the camera base, and this entire assembly could be moved along its three principal axes for proper imaging of the subiect6s eye being photwraphed. The camera was equipped for remote firing by the experimenter from within the room at the center of the centrifuge, Voice and buzzer (hand vibmtor) communication systems were available beheen the subject and experimenter as well as bebfssn the experimenter and the centrifuge external con- t ro l room @

METHOD

1 . "%It of -- to the -- The subject was positioned i n the tilt chair and properly secured with the suppor-

tive appliance and stmps, The oamem/strobe apparatus with its biteboard atbchment was bolted immediately in front of the subject on the chair frame, The bitebmrd was inserted in the subiect's mouth, and he bi t firmly into the temporarily softened dental material deposited on it, The camera was then racked into i t s proper position to focus upon the subject's right eye; his left eye was covered with an opaque patch. One drop of pilocarpine hydrochloride 1 per cent was instilled Yn the eye being recorded to reduce the over.-all size and physiological oscillations of its pupil (Is), impoPi-ant factors in the subsequent analysis of the fiY m records.

During this phase of the experiment the obsewer conducted the test within the metal enclosure, While the subject was in the upright position, several photographic recordings were made. The m a h recorded eye position megsured among these recordings served as the k s i s for computing eye roll deviation found for the various tilt positions, One recording was used as the reference for compring a l l other recordings by the method of superimposing hvs projected images, as described elsewhere (6).

The chair was first t i l ted slowly from upright either in rightward (+) or leftward (-) direction (randomized among subjects) and according io the following sequence: 2 5 O , So, 58", aO, One recording was made at each of these tilt ~ s i t i o n s . At & O

a second recording was made before initiating the same t i l t procedure but in the descend- ing order of the degree of tilt in returning to upright; passing through upright the same ascending-descending t i l t order was repeated in the opposite quadrant. Phis procedure was continued until at least three recordings had been made at each of the eight tiit p s itions and upright . 2. T i l t of the Gravitoinertial Vertical with Respect to the Upright Subject ---------

Immediately following the static test of counterrailing and without removing the subject from the chair, the chair was rigidly fixed in its upright position. The observer moved to the central room of the centrifuge where controls were provided for firing the camera remotely and for communicating with the subject. The centrifuge was rotated slowly (within approximately 60 seconds) in the counterclockwise direction up to the velocity required to change the gravitoinertial upright in the same amounts ( 2 5 O , No, 58", 6 3 O ) and in the =me sequential order r ighbard or le fhard as in the static testing. Calculation of the gravitoinertial vector was ksed upon the mdial distance from the axis of rotation to the center of the subiect8s shed, Thus the essential difference between the static and dynamic forms of tilt was the difference (4 beheen the magni- tude of the gravitational and gravitoineri"ia1 force which incrmsed as a direct function of apprent tilt (displacement of gravitoinertial force vector) during rotation. Accuracy i n the rate of rotation was maintained within plus or minus 1 per cent. The subject faced fornard in the direction of rotation for effective righkvard ""t ilking" and was turned 980" to tmvel k c h a r d along the path of rotation for le fbard ""li.Iting ." The order of t i l t direction was selected at random among the subjects, After slowly accelerating to each desired velocity, a 60-second delay was timed before the first photographic recording was made, As in the static phase, the test ended when the eye was photo- graphed at least three times at each @, the angle formed between the gravitational and gravitsinertia I force vectols.

RESULTS

The results are summarized i n Figure 1 . Mean counterrol ling data in minutes of arc of the b o groups of subjeck are plotted as a function of tilt angle i n degrees with respect to the gravitatisna l (c fosed circles) and the gmvitoinertial upright (open circles), individual counterrolling data were similar to those representing the group data, but in some instances, a given subject's responses were substantially more variable than the average, This i s to be expected with limited eye recordings at each position since the eye i s physiologically active and may be photogmphed while it i s undergoing an occasionaB yet considerable spontaneous tonional shift (6). To reduce the effect sf this influence which would be expected to occur in opposite directions at random among subjects, the resulb of the six normal as well as the five labyrinthine-defective subjects were averaged and compared as groups,

Normal Subjects Lsbyrinthine- Defective Subjects

el sl Centrifuge Stationary &-------A

0 - - - - - - 0 Centrifuge Rotating A - - - - - - - A

BODY "$LT (DEGREES) WITH RESPECT TO GGA~~!TYdGRAVOTOINERTIAL FORCE

Figure 1

Counterrolling o f Norma! and Labyrinthine-Defeei-ive Subject Groups as a Function of Body Ti l t with Respect to Gravitational or Gravitoinertiai Force

5

The two curves representing the data of the normal group tested under the static and dynamic conditions appear to be nearly coincident at the smallest angle of f i i t (Figure I ) , With greater kill. angles in both the right and left directions, the curves become more and more disparate, revealing the effect upon ocular counterrolling of the ever-increasing amount of centrifugal force added to that of gravity. It is impossible to determine a direct relationship between counterrolling and magnitude of the inertial force since the angle, and, therefore, direction of the applied stimulus relative to the otol i th organswe aiso varied. As suggested by Woel Iner and Graybiel (1 61, an approx- imation o f the combined effect of magnitude and direction i s possible by considering only the inertia! force component acting sagittally and perpendicular to the subiectgs long a x i s . The intensity of this laterally directed force equalsf,under the static condi- tion, the sine of the angle (@)formed between the body a x i s and the gravitatisnai up- right, and under h e dynamic conditions, the product of the gravitoinerfial force (G IF) and the cosine of the angle (@I formed bemeen the body m i s and the gravitoinertiai up-- right. The difference between these values represents the difference (A9 i n stsl i this shear force generated by the two test conditions, centrifugation and t i l t ing :

@ g = GIF cos @ - sin $ - Figure 2 bhows the linear relationship bund in normals between the change in ocular countermiling (@ CR) as a function of the change in shear Force (Ag) . The data of Woe! lner and Graybiel were recalculated by this format and revealgd remarkable agree- ment with our data (Figure 2) even though the two groups of normal subjects differed in their basic counterrol l ing response leve is,

The results from the labyrinthine-defective group s f subjects are also presented in Figure 1 . These subieck, i n contrast to the normals, reveared no apparent difference in counterrof ling measured under the dynamic and static test conditions.

DISCUSSION

The counterrol l ing response to static t i It (centrifuge statisnar)~) shown in Figure 1 i s bp ica l of normal subjecb; under these test conditions, eye rol l compensation i s greatest between upright and 25', less b e ~ e c t n 25' and %;and tends to reach a l imit around Me. This pattern of response changes dramatically when the magnitude of the resultant force i s increased as a byproduct of the centrifugation required to effect an apparent tilt with the subject maintained in alignment with gravity. A t 25' of tilt under dynamic conditions, with only a slight increase in gmvitoinertial force ( I .09 g), the amount s f eye ro l l i s comparable to that measured under static conditions. c eve this tiit angle a discrepancy beween the results of the static and dynamic.modes begins to appear and to wax in direct relation to the angle of tilt; a+ +he maximum tiit angle (Be) the dynamic, unlike the static respsnse, shows no sign of reaching or approaching a plateau,

a SHEAR FORCE ( ~ U N I T S ) Figure 2

Average Change i n Counterrolling for Normal Subjects as m Function sf the Change i n Shear Force, Data from Present StudY Coded as Solid Circles, Those of Woe! lner and Graybiel (16), Recalculated for This Format, as Dotted Circles

Individually, as weti as a group, the subjects with severe labyrinthine defeck revea led no essential change in their smal I , but def itsite &sic counterrol iing response with increased 9-lscrding, These results eonfim those of Woellner and Graybiel (16) and indicate thglf, wherws the eye roll of a normal subject i s dependent upon and limited, within the range tested, by /he strength of the inertial farce stimulus, that of individuals with labyrinthine defects wilt be dictated either by the extenhf functionai loss of his otol ithie organs or by the contribution of nonstoi ithic gravireceptor systems, Evidence that this response i s graviv dependent i s provided by dafa which show changes in the amount of counterr~lling feund under 1-g conditions as a function of tilt, as \BIOII as by the findings of a previous study which reyealed that the small amounk of ocular counterrol ling manifested by such individuals was reduced or essentially eliminated when graviv was counteracted padially or completely by Keplerian flight (15). The innervation source of such small amounts of eounterrolling, however, remains in question.

Differentiation of whether a residuum of otolithic function exists sr whether none- otol i thic gravireceptor act iv ib can account for reduced amounts of counterrol ling may depend upon the independent but complementary studies of this reflex with a subject immersed in water or exposed to centrifugation, Water immersion i s highly effective in reducing, if not eliminating, the influence of the nonotolithic gmvireceptor systems upon the perception of the oculogmvic illusion (3), but it remciins to be shown that this environment would influence ocular csunterrolling. If water immession i s effective, then the question of origin of the counterrolling reflex i s immediately solved. If not, centrifugation could be used in an attempt to drive this low-level function and to explore the possibiliiy that i t represenb a physiologically nomal variation in this res- ponse characteristic.

REFERENCES

i . Coienbrander, A., Eyes and otol iths. Aeromed . Acta, 9: 45-91, 194%. - - 2. Graybiel , A ., Oculogravic illusion. - Arch. Ophthal . , M 48: 605-61 5, 1952,

3. Gra~biel, A., Miller, E. F. I I , Newsom, B e D., and Kennedy, R. S., The effect of water immersion on perception of the oculogra;ic illusion in normal and labyrinthine-defective subjects. - Acta otolaryng . , - Stockh., - 64. 599-610, 1968.

4. Jongkees, L. B. W., The parallel swing test. In: Wolfson, R. J. (Ed .), - The Vestibular System and Its Diseases. Phi laelphia, Pa .: University of

ia hess7966. Pp 218-228.

5. McLeod, M. E., and Meek, J. C., A thresholdcalorictesl: Results in normal subjects. NSAM-834. NASA R-47. Pensacola, Fla .: Naval School of Aviation Medicine, 1962.

6. Miller, E. F. II, Counterrolling of the human eyes produced by head tilt with respect to gravity. Acta otolaryng . , Stockh., %. 479-!%l, 1961 ,

P P - 7. Miller, E. F. [I, Ocular counterr~ i l in~. In: Wolfson, R. J. (Ed.), - The Vestibular

System and Its Diseases. PhiladelpKa, Pa .: University of Pennsylvania

8. Miller, E. F. II, Evaluation of otolith function by means of ocular counterrolling measurements. In: Stahle, J . (Ed .), Vestibular Function on Earth and in Space. OxfordTEngland: Pergamon Press, 1970. Pp 9 7 - n 7 7 - -

9. Miller, E. F. I], Fregiy, A. R., and Graybiel, A., Visual horizontal perception in relation to otolith function. Amer. J . - - 8 1 :488-496, 1968. -

10. Miller, E . F. 1 I, and Graybiel, A,, Comparison of autokinetic movement perceived by normal and deaf subjects with bilateral labyrinthine defects. Aerospace Med,, 33: 1077-1080, 1962.

1 9 . Miller, E . F. I I, and Graybiel, P I . , Rotary autokinesis and displacement of the visual horizontal associated with head (body) position. Aerospace - Med . , 34: 915-919, 1963. A

1 2. Miller, E. F. II, and Graybiel, A., A comparison of ocu!ar counterso!ling move- men& bemeen normal persons and deaf subjects with bilateral labyrinthine defeck. Ann, Otol . , 72 885-893, 1 9 a , -- 7

13, Miller, E, F, [I, and Graybiel, A,, Magnitude sf grervibine~ial force, an inde- pendent variable in egocentric visual loca lizatisn of the horizontar , J . exp, Psyehoi *, 79 :452-4Qr 1966. - -

14, Miller, E, F , I ! , and Grsaybiel, A,, Role of the ofolith organs in the perception of' horizontaliv. ., - 79:24-37, 9966,

15, Miller, E, F, I I , Graybiel, A,, and Kellogg, R. S., Otolith organ aet iv iv with- Ir! mrrh standard, ~ne-hal f stcndard, and zero gravikf environments, Aerospace Med . , - 37:399-403, 1966,

16, Woel lner, R, C,, and Graybiel, A,, Counterrolling of the eyes and its dependence on the magnitude of gravitational or inedial force acting lateraily on the body. J . appl , Physiol ., 14:632-634, 1959. - - -

Unclassif ied Srcuril . Class i f ica t ion

THE EFFECT OF GWVITO1NERTiAb FORCE UPON OGUMR COUNTERROLLING

I P T I V E N O T E S (Type ol report and inclusive dates)

tnitiai,

Ashto

SA 7-81 633 and NASA 8-93 b . P R O J E C T N O .

d. I 3 10. D I S T R I B U T I O N S T A T E M E N T

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13 A B S T R A C T

The effect in terms of magnitude of ocular counterrolling of g l m d i n g a t various angles of t i l t up to 63' was mmsured on normal subjects and compared with the effect upon persons with severe or complete loss of otolith function, The group of six normal subjects manifested a com- pensatory eye ro l l which increased as a direct and essentially linear function of the component of the gravitoinertial force acting laterally upon the subject, This increase i n response was not observed in the f ive deaf subjects with severe or complete bilateral loss of their vestibular organs, These findings confirmed similar results found by other authors using other measuring techniques which show that the reflex eye movement i s dependent upon and limited to the magnitude of the gmvitoinertial stimulus (within the range used) when the otoiitho-ocular system i s functioning normal lye However, when this function i s impaired or losf, the magnitude of the compensatory eye rol l is limited to that manifested at 1 g and possibly to non-otolithic contributions, These findings offer means For differentiation beGeen otolithic defective individuals and 'fnormali' persons who exhibit l i t t le counterrolting.

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