Adaptation of otolith organ activity was investigated by monitoring the ocular counterrolling response of four normal individuals and three persons with severe bilateral loss of labyrinthine function. Several eye photographs were recorded every 30 minutes during a period of 8 hours in which the subject was held in a lateral tilt (60 deg) position. The recorded eye roll position varied to an expected small extent within each test session; this variation about a given mean roll position was similar among the test sessions for all subjects. The mean roll position, on the other hand, changed from session to session in substantial amounts, but these changes appeared to be random with respect to time and among subjects. Furthermore, the intersessional variation in the mean torsional eye position of the normal subjects was equivalent to that of the labyrinthine-defective subjects who displayed little or no counterrolling. These results suggest that the human counterrolling response is maintained either by essentially nonadapting macular receptors or by extremely fine movements of the head in the gravitational field, such as may have been allowed by the biteboard/headrest restraint system used in this study, which served as an everchanging accelerative stimulus

Graybiel, A.

Miller, E. F., II

English

NASA Technical Reports Server

NAMRL- 1154
OCULAR COUNTERROLUNG MEASURED DURING \
,: , EIGHT. HOURS OF SUSTA||sip BODTTIO*
Ecirl f> Miller II, and Ashton Graybiel
^ I
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AER09^CE MEDICAL RESEARCH
Januaiy T972
tite
IWIOWAL AERONAUTICS
SRftCE M)MINISTRATION
https://ntrs.nasa.gov/search.jsp?R=19720018408 2020-03-11T18:05:34+00:00Z
Approved for public release; distribution unlimited.
OCULAR COUNTERROLLING MEASURED DURING
EIGHT HOURS OF SUSTAINED BODY TILT
Earl Fo Miller II, and Ashton Graybiel
NASA Order T-81633
Biomedical Research Office, Manned Spacecraft Center
NASA Order L-43518
Office of Life Sciences
Released by
Captain N. W. Allebach, MC USN
Officer in Charge
4 January 1972
Naval Aerospace Medical Research Laboratory
Naval Aerospace Medical Institute
Naval Aerospace Medical Center
Pensacola, Florida 32512
SUMMARY PAGE
THE PROBLEM
To measure changes in amount of ocular counterfoil ing as a function of duration of
body tilt in the frontal plane.
FINDINGS
Four normal individuals and three persons with severe bilateral loss of labyrinthine
function served as test and control subjects, respectively. Each subject was held in a
lateral tilt position, 60 degrees from upright, fora period of 8 hours. During this
period the roll position of his right eye was measured eighteen times immediately upon
reaching the terminal tilt position and in like number at 30-minute intervals thereafter.
The recorded eye roll position varied to an expected small extent within each test
session; this variation about a given mean roll position was similar among the test
sessions for all subjects. The mean roll position, on the other hand, changed from
session to session in substantial amounts, but these changes appeared to be random with
respect to time and among subjects. Furthermore, the intersessional variation in the mean
torsional eye position of the normal subjects was equivalent to that of the labyrinthine-
defective subjects who displayed little or no counterrolling. These results suggest that
the human counterrolling response is maintained either by essentially nonadapting macular
receptors or by extremely fine movements of the head in the gravitational field, such as
may have been allowed by the biteboard/headrest restraint system used in this study,
which served as an everchanging accelerative stimulus.
ii
INTRODUCTION
Maintenance of equilibrium without a visual framework while the head (body) is
held in a given position must rely upon nonvisual stimulus-response mechanisms that
provide continuous valid information on the relative direction of gravity. It is well
known that the cilio-otolith system as a specialized gravireceptor mechanism acts as a
major influence in man's nonvisual perception of the upright, at least in those measure-
ments made during a typically brief course of an experiment, and a physiological basis
for this system's possible role in sustained static orientation has been indicated by the
recordings of vestibular neural signals in animals0 The frequency of these signals was
found by several investigators to be significantly different in a tilted animal position
compared to an upright reference level and showed little accommodation over periods up
to several minutes' duration (1, 2,4,5,8). Man's ability to orient himself to a gravito-
inertial frame of reference without empirical visual cues over much longer periods of
time was well demonstrated by the relative constancy of the oculogravic illusion as
observed by four experienced subjects throughout a 4-hour period of exposure to
constant lateral centripetal acceleration (3). The cilio-otolith system under these
conditions probably acted as the primary sensory mechanism,but nonotolirhic systems,
including touch, pressure, and kinesrhesis,responding to the resultant acceleration vector
could have played a part in these observations (7). In order to monitor more directly the
effect of sustained gravitational stimulation upon man's otolithic activity with relative
freedom from nonotolithic gravireceptor influences, the ocular counterrolling reflex was
selected as the test parameter for the present study (11). This choice, however, did
not necessarily rule out all extraneous factors such as spontaneous changes in extraocular
muscle tonus which would affect eye roll position during the 8-hour recording period.
For this reason, bilateral labyrinthine-defective individuals who were apparently normal
in all other respects were included in this study as our control subjects.
PROCEDURE
SUBJECTS
Four healthy Navy enlisted men, 19 or 20 years of age, served as the normal
subjects, and tests revealed normal hearing, as well as normal nonacoustic labyrinthine
function; their counterrolling response was in the high normal range (Counterrolling
Index = 383 to 456) (9-1 !)„ The control group comprised three deaf persons with severe
loss of vestibular function as detailed in Table 10
METHOD
The counterrolling test device, described elsewhere (11,12) and portrayed in
Figure 1, was used for positioning the subject with respect to gravity. The subject was
first stationed erect in the carrier portion of the device in a semistanding position, with
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Figure 1
Diagram Showing Subject Positioned in the Counterfoil ing Test Device and Tilted
at 60 Degrees from Upright. Camera Recording System Shown on Platform
in Front of Subject's Face .
3
his weight distributed between a saddle-type seat arrangement and an adjustable foot-
rest platform. A locked headrest and biteboard assembly kept the subject's head pre-
cisely, yet comfortably in this position. The platform was raised or lowered by a
hydraulic mechanism, and the subject was shifted sidewise until the center of the pupil
of his right eye, during proper fixation of a ring target supplied for this purpose, fell
on the optic axis of the camera system,, Coincidence was determined when the pupillary
image was concentric with specific circular markings on the camera's ground-glass
viewing screen. In this position several straps and a tight-fitting vest constructed of
velcro material secured the subject's body to the device. Foam-rubber padding was
used in this particular study to cushion the right side and arm of the subject when held
in the tilted position.
One or two drops of 1 per cent pilocarpine hydrochloride was instilled
approximately 15 minutes prior to the initial testing and subsequently as required to
reduce the overall size and physiological oscillations of the pupil, which aided the
subsequent analysis of eye position based upon natural iris landmarks. The analytical
procedure has been described elsewhere (10).
Thirty-six photographic recordings of the subject's right eye were made when
he was upright; then the subject was slowly tilted 60 degrees in the rightward direction.
Sixty seconds after reaching this tilt position, the first of 18 photographs was taken; an
identical number was recorded every 30 minutes during the 8-hour period of sustained
tilt. After 8 hours the subject was slowly returned to the upright, and his iris photo-
graphed 36 more times over a period of approximately 5 minutes. The average roll
positions of his eye as recorded in the initial and terminal upright positions were
averaged and used as the baseline (zero) position to which all other measurements were
related. During the several minutes that separated the test sessions, the subject remained
fixed in his tilted position, but his biteboard was removed for comfort,,
RESULTS
Figures 2 and 3 summarize the changes in ocular counterrolling of the
normal and labyrinthine-defective (L-D) subjects as a function of time within and among
the various test sessions, respectively. Figure 2 portrays the extremely small intrasessional
torsional variations (average deviations) of the eyeball about the mean position measured
for each session; the variability found for subjects of both groups throughout the 8-hour
test period was relatively small, but somewhat greater deviations were recorded within
the normal group. Figure 3 presents the mean ocular roll position of each subject as
recorded during each of the several test sessions. As expected from the preliminary
calibration tests, the L-D subjects clearly manifested less ocular counterrolling than the
normals, but their individual data tended to complement those of the normal subjects in
forming a continuum of response over a range from essentially none to greater than 10
degrees of arc,. Within the 8-hour test period each normal and L-D subject manifested
substantial intersessional changes (up to approximately ± 2 degrees) in mean eye roll
position, but this appeared to be independent of the duration of sustained tilt,, A
measure of the randomness of the intersessional changes was provided by averaging
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NORMAL SUBJECTS
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TIME (HOURS)
Figure 3
Average Ocular Counterrolling Values of the Normal and Labyrinthine-Defective
Subjects Plotted Individually and as Groups as a Function of Time
Held in the 60-Degree Body Tilt Position. Each of the Individual
Data Points Represents an Average of Eighteen Eye Roll Recordings.
individual data according to subject group. The resultant average curves of the normal
and L-D subjects are relatively smooth and appear to follow essentially horizontal and
therefore time-independent courses. The break in the curves of the normal group (Figure
3) marks the session in which the data of HO were lost for technical reasons.
DISCUSSION
Although constant error changes in the eye roll position were recorded
for the normal and labyrinthine-defective subjects, the amount was relatively small and
inconsistent throughout the 8-hour test period. On the basis of these data and the
previously found evidence that this response closely reflects otolith activity (12, 14, 15),
it would appear that the macular source of tonic innervation to the extraocular muscles
was effectively undiminished by time. These results can be explained either by the
existence of nonadapting macular receptors in man or by some artifact in the test pro-
cedure. In the present experiment, for example, the subject's head was stabilized by
the simplest and most practical method available: a biteboard/headrest system. This
restraint method assured a high degree of head rigidity (otolith organ stabilization), but
it is conceivable that extremely fine movements might have occurred, particularly when
the biteboard was removed between test sessions, which could have served as an ever-
changing accelerative stimulus to the otolith organs. The extreme precision in the
measuring techniques, on the other hand, precluded any significant error being intro-
duced by this factor.
The different sources of tonic innervation that influenced the measurements
in this study can be differentiated to some extent by comparisons of the results of the
normal and the L-D subjects who manifested little or no counterrolling. The latter
subjects provided data on extraocular muscle tonus under the prolonged test conditions
which was primarily dependent upon nonotolithic neurochemical processes. The intra-
sessional variations in eye roll position among these L-D subjects was extremely small,
which tends to confirm the evidence that the basic tonic equilibrium of the extraocular
muscles is more persistently maintained than that of other skeletal muscles (2) and
indicates that this activity can be independent of normal otolithic inputs. In fact, the
slightly greater general intrasessional variability in the recordings of normal subjects
would suggest that otolithic activity acts to decrease ocular stability.
Some support of this possibility is offered by the recordings of spontaneous
irregular firing activity of the otolith organs in animals. Fujita et al. reported, for
example,that the neuronal signal recorded from cells of the lateral vestibular nucleus
in cats held in a specific tilt position was marked by a wide scatter of interspike
interval values which they judged would require a probabilistic approach to identifying
head position (5). These spontaneous variations in otolith signals with a given body
position may also offer partial explanation for the perceptual phenomenon of rotary
autokinesis (13). However, it is unknown whether the eyes fluctuate in their torsional
position in simple accord with this perceptual illusion; more likely, the illusion is
based upon the complex neural activity resulting from an interplay of nonotolithic and
otolithic gravireceptor inputs that have undergone central processing. This hypothesis
is supported by the finding that prolonged lifting of the g-load tends to reduce
variability in the judgment of horizontally (6).
The slower rates of change in the eye roll position that were recorded
among sessions, separated by approximately 30 minutes, would appear to be nonotolithic
in origin since the L-D subjects, and in particular subject HR with essentially complete
functional loss of his otolith organs, revealed variations in mean ocular roll position
that were indistinguishable from those of the normals.
REFERENCES
1. Adrian, E0 D0/ Discharges from vestibular receptors in the cat. J_. Physiol.,
J£l_:389-407, 1943.
2o Bjb'rk, A,, and Kugelberg, E0, The electrical activity of the muscles of the eye and
eyelids in various positions and during movement. Electroencephalogra
Clin. Neurophysiol., 5:595-602, 1953.
3o Clark, Bo, and Graybiel, A0/ Visual perception of the horizontal during prolonged
exposure to radial acceleration on a centrifuge, J_. exp. Psycho I,,, 63:294-
301, 19620 ~ ~"
4. Cramer, R. L., Response of mammalian gravity receptors to sustained tilt0 Aerospace
Med., 33:663-666, 19620
5. Fujita, Y., Rosenberg, J., and Segundo, J0 P., Activity of cells in the lateral
vestibular nucleus as a function of head position,, Jj> Physiol., 196:1-18,
1968. ~
6. Graybiel, Ao, Miller, E. F. II, Billingham, J0, Waite, R0, Berry, C0 A., and
Dietlein, L., Vestibular experiments in Gemini flights V and VII. Aerospace
Med,, 38:360-370, 1967.
7e Graybiel, A«, Miller, Ee F. II, Newsom, B0 D0, and Kennedy, R0 S., The effect
of water immersion on perception of the oculogravic illusion in normal and
labyrinthine-defective subjectso Acta otolaryng., Stockho, 65:599-610,
1968.
8. Lowenstein, O., and Roberts, T0 D8 M., The equilibrium function of the otolith
organs of the thomback ray (Raja clavata). J_. Physiol., ]_[0:392-415, 1950.
9. McLeod, M. E0, and Meek, J. C., A threshold caloric test: Results in normal
subjects. NSAM-8340 Pensacola, Fla.: Naval School of Aviation
Medicine, 1962.
10. Miller, Eo Fo II, Counterrolling of the human eyes produced by head tilt with
respect to gravity. Acta otolaryng., Stockh., 54:479-501, 1962.
11. Miller, E. F. II, Ocular counterrolling. In: Wolfson, R. J0 (Ed,), The Vestibular
System and Its Diseases, Philadelphia, Pa.: The University of Pennsylvania
Press, 1966. Pp 229-241.
12. Miller, E, F, II, Evaluation of otolith function by means of ocular counterrol I ing
measurements. In; Stahle, J. (Ed.), Vestibular Function on Earth and in
Space. Oxford: Pergamon Press, 1970. Pp 97-107.
9
13. Miller, E0 F. ll/ and Graybiel, A., Rotary autokinesis and displacement of the
visual horizontal associated with head (body) position. Aerospace Med.,
32:915-919, 1963.
140 Miller, Ee F. II, and Graybiel, A0, The effect of gravitoinertial force upon ocular
counterfoil ing. J_. appl. Physio I., 3_h697-700, 19710
15. Miller, E0 F» II, Graybiel, A0/ and Kellogg, R. S., OtoIith organ activity within
Earth standard, one-ha If standard, and zero gravity environments. Aerospace
Med0, 37:399-403, 19660
10
Unclassified
Security Classification
DOCUMENT CONTROL DATA - R & D
(Security classification of title, body of abstract and indexing annotation muxt bo entered when the overall report is classified)
ORIGINATING A C T I V I T Y (Corporate author)
Naval Aerospace Medical Research Laboratory
Pensacola, Florida 32512
Unclassified
2b. GROUP
N/A
3. REPORT T lTL E
OCULAR COUNTERROLLING MEASURED DURING EIGHT HOURS OF SUSTAINED BODY TILT
4. DESCRIPTIVE NOTES (Type of report and inclusive dates)
N/A
5- AUTHOR(S) (First name, middle initial, last name)
Earl F. Miller II, and Ash ton Graybiel
6. REPORT D A T E
4 January 1972 11
7b. NO. OF RE FS
15
8a. C O N T R A C T OR GRANT NO. 9a. ORIGINATOR'S REPORT NUMBER(S)
NASA Orders T-81633 and L-43518 NAMRL-1154
b. PROJEC T NO.
9b. OTHER REPORT NO(S) (Any other numbers that may be assigned
this report)
10. DISTRIBUTION STATEMENT
Approved for public release;distribution unlimited,,
. SUPPLEMENTARY NOTES
Prepared for the National Aeronautics and
Space Administration
12. SPONSORING M I L I T A R Y A C T I V I T Y
N/A
I 3 . A B S T R A C T
Adaptation of otolith organ activity was investigated by monitoring the ocular counter-
rolling response of four normal individuals and three persons with severe bilateral loss of labyrinthine
function. Several eye photographs were recorded every 30 minutes during a period of 8 hours in
which the subject was held in a lateral tilt (60°) position. The recorded eye roll position varied
to an expected small extent within each test session; this variation about a given mean roll position
was similar among the test sessions for all subjects. The mean roll position, on the other hand,
changed from session to session in substantial amounts, but these changes appeared to be random
with respect to time and among subjects. Furthermore, the intersessional variation in the mean
torsional eye position of the normal subjects was equivalent to that of the labyrinthine-defective
subjects who displayed little or no counterrolling. These results suggest that the human counter-
rolling response is maintained either by essentially nonadapting macular receptors or by extremely
fine movements of the head in the gravitational field, such as may have been allowed by the
biteboard/headrest restraint system used in this study, which served as an everchanging accelerative
stimulus.
(PAGE 1)
Unclassified
S/N 0 1 0 1 - 8 0 7 - 6 8 0 1 Security Classification
Unclassified
Security Classification
1 4.
KEY WO R OS
Eye movements
Ocular counrerrol ling
Otolirh organs
Labyrinthine defects
Tonic reflex
LINK A
R O L E W T
LINK B
R O L E W T
LINK C
RO L E W T
DD ,F°oRvM.,1473 (BACK) Unclassified
(PAGE 2) Security Classification


Ocular counterrolling measured during eight hours of sustained body tilt

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