Influence of otolith organs on visual horizontal perceptio

Fregly, E. A.

Graybiel, A.

Miller, E. F., II

English

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VISUAL HORIZONTAL PERCEPTION IN RELATION TO OTOLITH FUNCTION* 
Earl F. Miller II, Alfred R. Fregly, and Ashton Graybiel 
I 
Bureau of Medicine and Surgery 
MR005.04-0021 
NASA Order R-93 
Released by 
Captain J. W. Weaver, MC USN 
Commanding Officer 
23 December 1966 
*This research was conducted under the sponsorship of the Office of Advanced 
Research and Technology, National Aeronautics and Space Administration. 
NAVAL AEROSPACE MEDICAL INSTITUTE 
NAVAL AEROSPACE MEDICAL CENTER 
PENSACOIA, FLORIDA 32512 
https://ntrs.nasa.gov/search.jsp?R=19680009826 2020-03-12T09:27:54+00:00Z
SUMMARY PAGE 
THE PROBLEM 
To determine the influence of the otolith organs on visual localization of  the 
horizontal during nineteen positions of body tilt within *90 degrees of  gravita- 
tional vertical. 
FINDINGS 
The mean constant and variable errors shown by a group of fifteen normal per- 
sons and a group of ten deaf subjects with bilateral labyrinthine defects were com- 
pared. High test-retest reliabil i ty was demonstrated for both groups. Although 
the general pattern of  results was similar for the two groups, the labyrinthine-de- 
fective group was found to be more variable and manifested greater E- and A-effects 
in their settings in  several of the tilt positions. A significantly larger E-effect 
was observed in  those subjects (L-Ds) with l i t t le or no ocular counterroll. 
.. 
I I  
INTRODUCTION 
In a recent study (12) the visual localization of  a group of  normal subjects was 
compared with that o f  a group of  deaf persons with known bilateral labyrinthine 
defects. Each subject was required to set a luminous line to the gravitational hori- 
zontal when he was placed in 1) an erect, 2) a recumbent (left side), and 3) an in- 
verted head (body) position. In the absence of  visual reference cues, significant 
intergroup differences were found in  the settings made when the subject was in  the 
erect and in the recumbent positions. That these differences were quantitative, 
i.e., the normals showed less errors, rather than qualitative emphasized the 
contribution of  the sensory receptors in the otolith organs. Other studies comparing 
the visual localization of  normal and labyrinthine-defective (L-D) subjects tended 
to confirm this conclusion (8, 11). 
The present study, in which both normal and L-D subjects were also tested, was 
designed to determine the influence of the otolith organs on the visual localization 
of  the horizontal at 10' intervals of  body tilt through 90" leftward and rightward 
from the gravitational vertical. It i s  well known that in  this range of  body tilt, a 
subject wi l l  usually manifest a bias in making settings f i r s t  by undercompensating 
(E-phenomenon) (1 4), then overcompensating (A-phenomenon) (1 ). One theory 
that has been advanced to explain at  least partially the cause of  the E-phenomenon 
i s  the ocular counterrolling reflex (7) associated with head t i l t .  Inasmuch as that 
reflex i s  greatly suppressed in L-D subjects (9 ) ,  it was taken into account in this 
study. 
PROCEDURE 
SUBJECTS 
Fifteen healthy male subjects ranging in age from 24 to 35 years formed the 
normal group; ten deaf subjects aged 20 to 47 years served as the comparison group. 
In addition to their deafness these latter subjects had lost completely, or nearly 
completely, function of the semicircular canals and otolith organs (Table I )  as 
measured by caloric (3), ataxia (4,5), and counterrolling (7) test methods. 
A P PA RAT US 
The apparatus used for t i l t ing a seated subject and measuring his visual judg- 
ments of horizontality was identical to that of  a previous study in  which a detailed 
description was reported (1 3). 
The apparatus consisted of a hydraulically powered chair which could be 
ti l ted and held stationary in any given position within *90° from gravitational 
upright. The subject was secured in the chair wi th  seat bel t  and shoulder harness. 
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A target, which was positioned approximately 36 inches in  front o f  him, consisted 
o f  a dimly illuminated line of collimated light on a dark background. The subject 
could rotate the target clockwise or counterclockwise about i t s  center by means 
o f  a knob provided at his right hand. A similar control was available to the 
observer seated behind the subject at the control panel. This panel contained 
circular protractor scale readouts o f  the angular position o f  the target and tilt 
chair which could be read within *O .25 degree. The entire testing system was 
placed in  a light tight room. A buzzer signal heard by the normal subjects and 
fel t  on the fingertips by the deaf subjects provided a l l  the necessary communication 
between subject and observer. 
METHOD 
After subject was secured upright in  the t i l t  chair, his left  eye was covered 
by an opaque patch. Then the target was adiusted so that, to the subject, it ap- 
peared to be centered within i t s  cylindrical housing. The room lights and target 
light were then turned off.  The observer at the control console slowly t i l ted the 
subject at the rate o f  approximately 1 degbec 
but randomly scheduled body positions (0, *lo,  *a, *30, *a, *50, *60, *70, 
i80, *90 degrees). After thirty seconds in the tilted position the target was 
illuminated and the subject was signalled to make his first setting. Upon making 
his setting the subject signalled the observer, who then turned off the target light, 
offset the line (direction and magnitude were random), then turned on the target 
light for subject's next setting. This procedure was repeated unti l  ten settings 
were recorded. The subject was then tilted to the second randomly scheduled 
body position, which was in  the opposite direction. Leftwardbightward t i l t ing 
was alternated with the exception that the final position within each block of  
ten trials was always upright for al l  subjects. To determine test-retest reliability, 
a l l  subjects were re-tested by the same procedure within one to ten days. 
to the first o f  nineteen pre-selected 
RESULTS AND DISCUSSION 
Test-retest reliability as computed by correlating (Spearman rank order) the 
constant error curve configuration o f  the f i r s t  experimental test session with that 
of the second experimental test session was 0.94 for the normal and 0.81 for the 
L- D subjects. 
The mean constant and variable errors o f  the two groups of  subjects as measured 
for the various tilt positions ( f i r s t  experimental test session) are shown in Figures 
1 and 2, respectively. At each tilt position the means o f  the first three and last 
three o f  the ten settings o f  each subject group at each tilt position are plotted as 
coded points, together with the respective mean o f  a l l  ten settings indicated as the 
group curve. No constant error i s  shown in Figure 1 for the 0-degree tilt position 
inasmuch as the mean setting at  upright (Point of Subjective Horizontal) was used as 
3 

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5 
a basis for calculating the deviation of the mean setting o f  a l l  other positions. 
This was done to eliminate any procedural or equipment bias that may have existed, 
for example, variations in  the way the subject was secured in  the tilt chair. The 
judgments o f  the normal group were typical for normal subjects (13) and revealed 
the characteristic A- and E-phenomena in  fairly symmetrical fashion for the 
clockwise ( + )  and counterclockwise (-) direction of tilt. The maximum E-bias 
(4.6 to 8.4 degrees) occurred at the f 30 to 50 degrees of tilt. Beyond this 
tilt the bias tended to reverse rather slowly and became an A-bias when the 
longitudinal axis o f  the body approached horizontal. 
The group of L-D subjects revealed the same general pattern of  localization 
with bodily tilt, but their settings deviated more in the E- and A-directions than 
did those of  the normal group. The variable error (standard deviation) of  the set- 
tings tended to increase with increasing bodily t i l t in  both groups but to a greater 
extent i n  the L-D subjects, particularly when they were tilted toward their left 
side. In the L-D subjects significant changes in  the constant and variable errors 
occurred in certain tilt positions within the time required to make ten settings and 
were observed in  more positions of  tilt and to a greater degree. At the top of 
Figures 1 and 2, the confidence (P) levels of the significant (P 5 .05) intergroup 
differences in the first three and last three settings are indicated above the corre- 
sponding degree o f  body tilt. Between the first (1-3) and last (8-10) three groups 
o f  measurements the number of  positions o f  tilt at which significant intergroup dif- 
ferences in constant errors were seen increased from six to nine; for such differ- 
ences in variable error the number o f  positions increased from four to nine. 
The most likely explanation o f  the intergroup differences observed i s  that they 
represent principally the influence o f  the otolith organs, which appear to provide 
effective cues for visual localization since subjects without normally functioning 
otoliths were significantly less accurate (greater A- and E-deviations) and more 
variable in visual localization. However, visual localization i s  based also upon 
nonotolithic factors, which in certain body positions are as effective alone as in  
combination with those o f  otolithic origin. No significant intergroup differences 
were found in  more than half the tilt positions within the 180-degree range tested, 
and, wi th  few exceptions, the L-D subjects using primarily nonotolithic cues mani- 
fested a general pattern of  response which was qualitatively similar to that of the 
normal subjects. Notable intergroup differences occurred with small (* 10') and 
large (*80', *90') angles of  tilt, which i s  a finding consistent with other studies 
(1 1, 12). These results indicate that when the L-D subject i s  ti lted slightly from 
his usual upright position, the available cues impress an exaggerated sense o f  tilt, 
whereas at or near recumbency these cues lead to his underestimation of  tilt. A 
visual localization task in positions near upright i s  now being explored as a simple 
means of  differentiating normal and otolithic defective individuals. 
6 
Based upon recent visual localization studies carried out on normal individuals 
during weightlessness ( 6 ) ,  the greater variability in  settings shown by the L-D 
subjects in  the present study probably reflects the interplay o f  the active non- 
otolithic sensory inputs rather than a reduction in sensory information caused by 
the functional loss o f  the otolith organs. 
Although temporal changes in  constant errors and in variable ermrs were found 
in the present study, further investigation of the visual localization of  L-D subjects 
as a function of time duration at a given tilt position i s  required to define possible 
''adaptation" effects o f  nonotolithic receptors. When nonotolithic inputs are 
combined with vestibular (otolithic) information, as indicated by the settings of  
normal subjects, adaptation effects upon visual localization do not appear to 
occur in any typical pattern: 
remain unchanged when observed during long periods in  a t i l ted position (10, 14). 
In related studies (2, 15) it was shown that after a relatively short ini t ial  lag 
period following a sudden change in the magnitude as well as the direction of  
resultant force, the oculogravic illusion in normal subjects developed quickly to 
a peak and then underwent no systematic change during test periods up to four 
hours, whereas L-D subjects demonstrated only a gradual change in  the illusion 
and required one-hour exposure to reach the magnitude shown by the normal 
subiects. 
The A-phenomenon may increase, decrease, or 
The possible influence o f  ocular counterrolling on the E- and A-phenomena 
(Figures 3 and 4) i s  depicted by the average value of  ocular counterrolling measured 
in nine of the normal and a l l  of the L-D subjects of this study. If the E-phenom- 
enon were to be explained simply on the basis of ocular counterrolling and 
concomitant shift o f  the 'I horizontal retinal meridian, 'I  the pattern of  counter- 
rolling should mirror the E-effect; i .e., surnsof the two curves should equal 
zero in  normal subjects (Figure 3) and, essentially, be absent in the L-D subjects 
(Figure 4). 
invalid since not only i s  the patterning o f  these two responses different in subjects 
with normal counterrolling values, but their E-deviations are equalled or ex- 
ceeded by the L-D subjects. The elimination of the E-effect by manipulation of  
kinesthetic cues as reported for both normals and L-D subjects (16) demonstrates 
further the multiple basis o f  this visual phenomenon. 
It i s  apparent from these data plots that such a simple explanation i s  
7 
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NORMAL SUBJECTS 
---- COUNTERROLLING (CR) 
V I SUA L LOCAL I Z AT I 0 N 
OF HORIZONTAL (VLH) 
I I I I I I I I I I I I I 
- 60 -40 - 20 + 2 0  +40 +60 0 
BODY TILT - DEGREES 
Figure 3 
A comparison of counterrol ling results and constant errors in visual horizontal 
localization of nine normal subjects as a function of body t i l t  within *60° of 
gravitational vertical. 
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VI SUA L LO C A LI Z AT ION 
OF HORIZONTAL (VLH) 
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BODY TILT - DEGREES 
Figure 4 
A comparison of counterrolling results and constant erron in visual horizontal 
localization of ten deaf subjects with bilateral labyrinthine defects as a function 
of body tilt  within 560' of gravitational vertical. 
9 
REFERENCES 
1 . Aubert, H., Eine scheinbare bedeutende Drehung von Objekten bei Neigung des 
Kopfes nach rechts oder links. Virchows - -  Arch., 20:381-393, 1861 . 
2. Clark, B., and Graybiel, A., Visual perception of the horizontal during 
prolonged exposure to radial acceleration on a centrifuge. - -  J. exp. 
PS chol 63:294-301, 1962. 
Y O ,  - 
3. McLeod, M. E., and Meek, J. C., A threshold caloric test: Results in normal 
subjects. NSAM-834. NASA R-47. Pensacola, Fla.: Naval School of 
Aviation Medicine, 1962. 
4. Graybiel, A., and Fregly, A. R., A new quantitative ataxia test battery. Acta -
otolaryng . , S toc kh . , 6 1 :292-3 1 2, 1 966 . - -  
5. Fregly, A. R., and Gmybiel, A., An ataxia test battery not requiring the use 
of mils. NAMI-985. NASA R-93. Pensacola, Fla.: Naval Aerospace 
Medical Institute, 1966. 
6. Graybiel, A., Miller, E. F. 11, Billingham, J., Waite, R. E., Berry, C. A., 
and Dietlein, L. F., Vestibular experiments in Gemini flights V and VII. 
Aerospace Med . , 38:360-370, 1967. - -  
7. Miller, E. F. II, Counterrolling of the human eyes produced by head tilt with 
respect to gravity. Acta -otolaryng., Stockh., 54.479-501, 1961. 
8. Miller, E. F. II, and Gmybiel, A., Comparison of autokinetic movement per- 
ceived by normal persons and deaf subjects with bilateral labyrinthine 
defects. Aerospace Med., 33:1077-1080, 1962. - -  
9. Miller, E. F. II, and Gmybiel, A., A comparison of ocular counterrolling 
movements between normal persons and deaf subjects with bilateral 
labyrinthine defects. Ann. Otol., 72:885-893, 1963. - - - 
10. Miller, E. F. 11, and Graybiel, A,, Rotary autokinesis and displacement of the 
visua I horizonta I associated with head (body) position. Aerospace - Med. , 
34:9 1 5-9 19, 1963 . -
11. Miller, E. F. II, and Graybiel, A., Magnitude of gmvitoinertial force, an 
independent variable in egocentric visual localization of the horizontal. 
J. exp. Psychol., 71:452-460, 1966. - - 
12. Miller, E. F. II, and Graybiel, A., Role of the otolith organs in the perception 
of horizontality. Amer. L. Psychol., z24 -37 ,  1966. 
10 
13. Miller, E. F. II, Fregly, A. R., van den Brink, G., and Graybiel, A., 
Visual localization of the horizontal as a function of body tilt up 
to S O o  from gravitational vertical . NSAM-942. NASA R-47. 
Pensacola, Fla.: Naval School of Aviation Medicine, 1965. 
14. Miiller, G. E., Uber das Aubertsche Phanomenon. Z. Sinnesphysiol., 49: - -
Part 11.,109-244, 1916. 
15. Clark, B., and Gmybiel, A., Perception of the visual horizontal in  normal and 
labyrinthine defective subjects during prolonged rotation. Amer. J . 
Ps chol 79.608-61 2, 1966. Y*,-* 
- -  
I 16. Clark, B., and Gmybiel, A., The egocentric localization of the visual 
~ 
horizontal in  normal and labyrinthine-defective observers as a function 
of head and body ti l t. Percept. and Psychophys., 2:609-611, 1967. 
1 
- - 
11 
Unclassified 
Security Classification 
I .  
K E Y  W O R D S  
~ 
Counterrol ling 
Deafness 
Gravita tiona I ‘effects 
La by r i n t h i ne defects 
Otolith apparatus 
Spatia I loca I izat ion 
Visual horizontal perception 
L I N K  A I L I N K  B -
R O L E  W T  R O L E  W T  
L I N K  c 
R O L E  W T  - 
(PAGE 2 )  
Unclassified 
Security Classification 
Unclassified 
0 4  I G I N  a T I  N G  A c T I  v i  T Y f l ' c > f p ~ ~ r . 7 1 e  .rcrrhor) 
Naval Aerospace Medical Institute 
Pensacola, Florida 32512 
- 
2.. R € P O  R T SE C u R I  T Y C L A  S S I  F I C A  TION 
UNCLASSIFIED 
2 b .  G R O U P  
N/A 
N/A 
Earl F. Miller, II, Alfred R .  Fregly, and Ashton Graybiel 
A U  T H O R I I I  ( F i r a t  n n m r .  m , d d l r  intl ,al .  last  name) 
R E P O R T  D A T E  
23 December 66 
a. C O N T H A C T  O R  G R A N T  N O  
R-93 
7 8 .  T O T A L  N O  O F  P A G E S  7 6 .  NO. O F  R E F S  
12 16 
9a. O R 1 6 1 N A T O R ' s  R E P O R T  N U M B E R I S )  
NAMI-989 
9 b .  O T H E R  R E P O R T  N O I S )  (Any other numbers that may be assigned 
this reporl) 
141 
b .  P R O J E C T  N O  
1 S U P P L E M E N T A S Y  N O T E S  
MR005.04-0021 
c .  
I2 S P O N S O R I N G  M I L I T A R Y  A C T I V I T Y  
I d. 
0 D I S T R I B U T I O N  S T A T E M E N T  
This document has been approved for public release and sale; i t s  distribution i s  unlimited. 
TO determine the influence of the otolith organs on visually perceived direction of 
space the constant and variable errors of normal persons and deaf persons with bilateral 
labyrinthine defects during nineteen positions of body tilt within =k90° of gravitational vertical 
were compared. The general perceptual pattern was similar for the two groups, although that 
of the labyrinthine-defective group was found to be more variable, and greater E- and A-effects 
were manifested during several of the tilt positions. A significantly larger E-effect was 
observed in those subjects (L-Ds) with l i t t le or no ocular counterroll. 
I D  1F,",M,,1473 ( P A G E  ) Unclassified 
S / N  0 I O  1 .  8 0 7 -  680 1 Security C l a s T l f l c a t l o n  


Visual horizontal perception in relation to otolith function

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