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Directional changes in the vestibular ocular response as a result of adaptation to optical tilt
VivonRtwurchVol.22.pp 37lo 42.1982 Printedin GreatBritain
DIRECTIONAL RESPONSE
0042.6989:X2.010037-06M300’0 Perpamon PressLtd
CHANGES IN THE VESTIBULAR AS A RESULT OF ADAPTATION OPTICAL TILT
JUDITH W. CALLAN
and
SHELWN
OCULAR TO
M. EBENHOLTZ
Department of Psychology, University of Wisconsin, 1202 West Johnson Street, Madison, WI 53706. U.S.A. (Receioed
24 April 1980: in rrrisedJorm 8 Junr
1981)
Abstract-Before and after exposure to clockwise optical tilt, subjects’ compensatory eye movements were recorded, as the head was oscillated around a vertical axis by the experimenter. An analysis of the horizontal and vertical components of eye movements showed a change in eye movement path in the clockwise direction. This corresponded to similar changes in visual spatial orientation judgments indicative of perceptual adaptation. It was suggested that long-term visual feedback serves to restore the compensatory nature of the eye movements which was altered by the introduction of the prism transformation.
INTRODUCTION Previous studies investigating adaptive responses due to exposure to an optical tilt transformation have found changes in visual orientation perception (Ebenholtz, 1966; Mack and Rock, 1968; Mikaelian and Held, 1964; Morant and Belier, 1965), contrast thresholds and orientation-dependent visual evoked responses (Fiorentini et al., 1972), and the orientation of the McCollough effect (Mikaelian, 1976). Studies using transformations other than tilt, have investigated changes, not in visual perception, but in the vestibulo-ocular reflex (VOR). They have found adaptive shifts in the VOR with reversal (man, Gonshor and Melvill Jones, 1973, 1976a and b), and with minification and magnification (man, Gauthier and Robinson, 1975; monkey, Miles and Fuller, 1974). These changes have occurred when head movements were made during exposure to the transformation. It was suggested that this type of oculomotor adaptation may be related to the visual adaptation which occurs to minimize the apparent background movement most noticeable when the transformation is first introduced (Gonshor and Melvill Jones, 1973; Robinson, 1975), however, with one exception, relations between the VOR and perception have not been tested directly.* In a recent tilt study in which adaptation occurred during movement in the environment (Callan and Ebenholtz, 1981) changes were found in the direction of voluntary saccades corresponding to the adaptation of visual orientation. The present experiment attempted to determine if changes in VOR also resulted from exposure to optical tilt. While previous studies of VOR tested for increases or decreases in the * Oman ef al. (1980) looked for corresponding changes in VOR and circular vection following reversal, but did not attempt to look for changes in risual perception. 37 Y.R.22 I--r
gain of the horizontal VOR, changes due to tilt would have to be manifest as eye movements along an oblique axis, i.e. as shifts in the horizontal and vertical directions simultaneously. In addition, the present study examined the possibility of corresponding adaptive changes in VOR and visual orientation perception. METHODS Each session started with a 20min period of dark adaptation, followed by a series of calibration eye movements. Eye movements were recorded by d.c. electro-oculography, using a Beckman R411 Dynograph with nystagmus couplers. Horizontal electrodes were placed adjacent to the outer canthus of each eye, vertical electrodes above and below the right eye and the vertical and horizontal components of eye movements were recorded on separate channels. The settings were adjusted on the Dynograph and preliminary calibration eye movements were made by having the subject look back and forth between pairs of spots set opposite each other on a large lighted circular contour, in a dark room, with the head stabilized by a bite bar. Due to crosstalk, or in some cases a slight misalignment of the electrodes, there was often a small regular signal on the minor channel when the eye movement was being made in the orthogonal direction, which usually changed direction in phase with, or 180’ out of phase with, the signal on the major channel. Since the results were to consist of the differences between pre- and post-exposure recordings, this did not introduce an artifact. In addition to calibrations for horizontal and vertical eye movements, recordings were also taken on eye movements to targets placed 5’ clockwise (CW) and 5’ counterclockwise (CCW) of the major orientations. This was to ascertain that for
JUDITH W. CALLAN and SHELDON M. EBENHOLTZ
38
each subject it would be possible to detect slight changes in the orientation of the eye movement path, and was used to screen subjects. According to an extensive analysis done by Callan and Ebenholtz (1981). it should be possible to detect differences in eye movement path angle at least as small as I.3 deg. Before and after tilt exposure compensatory eye movements and tilt adaptation were measured, in that order. One of the problems of taking measures after tilt exposure is the possibility of decay of the effect starting soon after exposure is ended (Ebenholtz, 1968. 1969). This makes it imperative that any responses which might be affected in this way be measured as soon as possible after the end of the exposure period. One implication of this is that only one dependent variable can be measured before decay progresses very far in any one session, and thus still be regarded as an accurate measure of the size of the effect of tilt exposure. Adaptation results were obtained immediately after exposure in the screening session, and. since compensatory eye movements (the VOR) were the main object of interest in the present study. they were measured immediately after exposure in the experimental session. A second point relates to the state of light adaptation at the time of eye movement measurement. The normal procedure is to darkadapt the subject to bring about a more stable eye movement response. Since decay would start before dark adaptation could be completed, subjects were not dark-adapted after tilt exposure in the lighted hallway. Accordingly, in order to make the pre- and post-exposure measurements under approximately comparable conditions, subjects were light-adapted for 5 min prior to the pre-exposure measure. To produce the VOR, the bit was attached to a frame that could be tilted forward 30’. The frame mechanism was oscillated by hand by the experimenter, through an angle of 30’. at a frequency of 0.25 Hz. for about 8 cycles.* This period, which preceded, and followed the tilt adaptation session, began and ended with a static calibration test for sensitivity changes. For the VOR measures reported in this study, the subject was given a fixation point straight ahead, which was turned off when the head movements began. The subjects were not told to do anything with their eyes, but were given standard mental arithmetic instructions, which generally insure purely compensatory eye movements (Barr et al., 1976; Gauthier and Robinson, 1977). A dynamic calibration, in which eye fixation was maintained on a fixed target during head oscillation, was taken before the final static calibration; since the two should have been the same (Barr et al.. 1976) a deviation indicated an equipment adjustment that was needed to bring the head into proper alignment before the experimental session. * These were the values found during the best combination
nome aided timing.
of amplitude
pilot studies to be and frequency, A metro-
The level of tilt adaptation was measured by having the subject direct the experimenter in the setting of a thin luminous line in an otherwise dark room. The line was set by the subject so as to be oriented from “12 to 6” or from “9 to 3” o’clock, according to instructions, with the subject’s head used as the reference for egocentric orientation. During each session with electrodes in place the subject was exposed to a 30” optical tilt while walking about in a hallway. To produce the optical tilt, the subject wore a helmet which allowed an eyepiece to be positioned over the right eye; the left eye was covered. The eyepiece contained two dove prisms mounted in tandem, one of which was stable while the other was rotated, to produce a tilted visual field, 14” in diameter, without left-right reversal. Potential subjects were screened in an initial session to find those with voluntary and compensatory eye movements regular and consistent enough to be measured objectively with some degree of confidence, and who also could exhibit orientation adaptation. This procedure yielded six subjects who returned for an experimental session a week later, and a control session at least one week after that. Subjects received a 10min exposure to a 30. tilt during the screening session and a 20min exposure to a 30” tilt during the experimental session. The 20min time period was chosen to make it more likely that the subject would achieve a stable level of adaptation (Ebenholtz and Callan. 1980) before undergoing the series of postexposure tasks. During the control session the subjects received 20min exposure to 0’ tilt.
RESULTS
A typical VOR record is shown in Fig. 1, which has both the compensatory segments, opposite the direction of head movement, and the anticompensatory segments returning the eye to the center position. To measure the total amplitude of compensatory eye movements it was necessary to construct cumulative eye position (CEP) curves (Meiry, 1966). In the VOR retraining studies described previously, the measure of interest was the gain of the compensatory eye movements with respect to the head movement. In those cases the only change in the eye movement was an increase or decrease in horizontal amplitude. The gain was computed as the ratio of eye angular ~&city to head angular velocity, and in some cases (Gonshor and Melvill Jones, 1976a and b) the peak eye angular velocity was calculated from the CEP curves. In the present study a more important measure was the angle of eye movement, which could be readily obtained from the eye position curves. The gain in this case, then, was taken as the ratio of horizontal eye position amplitude to head position amplitude. Segments of 8-10 horizontal half-cycles and corresponding vertical half-cycles were measured, and the means, in mm, were taken for each and used to com-
Adaptation to optical tilt
ward eye movement, contributing to the mean were not necessarily successive. It was more important that the half-cycles correspond in the two components than that they be successive, so whenever there was a break in the vertical CEP curve due to a blink or vertical saccade, the measurements were not taken on either curve.
pute the slope of the given eye movement. The mean of the minor component (the vertical) was divided by the mean of the major component. Since the slope equals tan 0, the angle (0) of the eye movement path was then computed. These angles (0) were compared from data generated before and after exposure. In the present study the half-cycles, i.e. a rightward or leftA
39
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Fig. I. Sample of compensatory eye movement records, from subject A.J., during mental arithmetic task. The upper part of each record is the horizontal component, and the lower is the vertical. Spots at the bottom of each record indicate times at which the head reached rightmost point.
40
JUDITH W. CALLAN and SHELDON M. EBENHOLTZ Table
I. Before-after
difference scores (deg arc) from compensatory eye movements*
tests of adaptation
Experimental session (20 min at 30’)
Screening
session (lOminat30’)
Control session (20min at 0
Eye Subject
Adaptation
Adaptation
movements
C.C. F.G. J.H. S.K. B.B. A.J.
3.25 2.12 3.12 3.00 3.50 3.50
2.62 0.62 1.88 1.50
5.51 0.63 2.1 I 3.66 5.80 10.05
M 0.U
3.0w 0.2 I
1.60t 0.27
4.63t 1.35
* Adaptation 7 Significant
1.75
I .25
scores averaged at P < 0.05.
over horizontal
The results shown in Table 1 are from VOR eye movements made while the subject was doing mental arithmetic.* The direction of eye movement path did change after exposure to tilt, the path becoming more oblique in the CW direction following exposure to 30’ CW tilt, t(5) = 3.33, P < 0.05. In the records of some subjects, as shown in Fig. 1, the change in the vertical component could be clearly seen, even before the measurement techniques were applied. There was no change following exposure to the 0” tilt in the third session. Wheq the mental arithmetic instruction is used during head oscillation in the dark, reports of the normal gain of horizontal eye angular velocity with respect to the head vary from 0.60 (e.g. Gonshor and Melvill Jones, 1975; Barr rt (I/., 1976; Gauthier and Robinson, 1977) to 0.80 (Takahashi et al. 1980). The gain? of horizontal eye position, which was measured in this study was within this range, averaging 0.73 and 0.61 in the 30“ and 0. conditions before exposure. After exposure in the 30’ condition it was reduced to 0.58, and to 0.58 in the 0” condition. Only the decrease in was statistically significant, the 30. condition r(5) = 5.00, P < 0.01. This is fully consistent with the
is the result from the first session of were obtained under the combination mental arithmetic and straightahead eye position instruction only. When the eye movements for the second session were examined it was found that the eye movements using the mental arithmetic instruction and the ones using the combination instruction were identical. It was assumed that this would have been the case in the first session and hence that the scores from that session are equivalent to those obtained under mental arithmetic alone. t The geometric mean of the two static calibrations that preceded and followed each VOR measurement session was taken as the measure of a 30’ head movement amplitude. The gain was defined as the ratio of the mean amplitude of the CEP curve and the geometric mean of the static calibrations. *The one exception
the first subject from which eye movements
Adaptation
) Eye
movements
0 0.12 0.25 0.25 0.12
0.52 -0.73 -0.58 -0.50 -0.37 -2.39
- 0.08 0.24
-0.68 0.39
-
I.25
and vertical
and
settings.
angular shift in VOR found in the adaptation condition. An analysis of variance compared spatial adaptation under the two conditions of exposure (30” and 0’ tilt) separately for horizontal and vertical settings. There was no difference between the two directions. so in subsequent tests these scores were combined. There was a significant difference between the two tilt conditions, as shown in Table 1, F(l, 5) = 22.67, P < 0.05. While the level of adaptation in the 30” tilt condition is low, it should be remembered that this test was taken about 8 min after the helmet was removed. The level of adaptation found after only 1Omin of exposure. but measured immediately after prism exposure in the screening session, was higher, averaging 3.08 deg. However, despite the reduction in the size of the adaptation measurement in the experimental session compared to the screening session, it was significantly different from zero, t(5) = 5.93, P < 0.05, while that obtained in the control condition was not. The assumption which is therefore assumed to be creditable is that significant levels of tilt adaptation were present during the VOR rests under the experimental conditions. It is difficult to make exact comparisons of the size of the effects in this study, since the compensatory eye movements were measured within a few minutes after the end of the exposure period. while adaptation measures were taken about 6min after that. This would give the adaptation a chance to decay (Ebenholtz, 1968, 1969), with the decay rates possibly different for each subject. There was no significant correlation between the adaptation and VOR change in the 30” tilt experimental condition. However, a correlation also was computed on the compensatory eye movement change in that condition and the adaptation measures of the screening session. The exposure period was shorter in the screening session and the level of adaptation probably less than it was right after the 20min exposure, but at least both measures
Adaptation to optical tilt could be compared without the effects of decay. This correlation, r = 0.80, was significant, t(4) = 2.67, P < 0.05. DISCUSSION
Compensatory eye movements due to the VOR were examined before and after exposure to 30” and 0” optical tilts. The angle of the eye movement path changed significantly in the direction of tilt in the 30 tilt condition; in the 0” condition there was no change. The angular shift that occurred in the 30” condition can be seen as adaptive in that such an
adjustment during exposure to an optically tilted environment would reduce the need for visual feedback control of fixation during head and body movement. It may also be noted that, since with mental arithmetic the VOR is automatically elicited, these eye movement changes could not have been due to any con-
scious effort on the part of the subject. It follows that the subject’s eye movements could not have been influenced by the subject’s perception of orientation (whether egocentric or exocentric) as might be argued in the case of voluntary eye movements (Callan and Ebenholtz, 1981). This result seems to preclude the possibility of accounting for changes in eye movements, particularly VOR movements, by referring to changes in visual orientation. It is proposed that the shifts in eye movement direction occurred as part of a feed-forward mechanism of the compensatory eye movement system to lessen the need for error correction in visual feedback control, as occurs during exposure to prism transformation. Under normal conditions for adaptation the subject moves about in an optically tilted environment. During this time his head is moving almost continuously, and each head movement is accompanied by a compensatory eye movement, generated by vestibular and neck muscle stimulation. When the environment is viewed through tilting prisms each eye movement so generated is only partially effective, since the reflex portion of the movement is programmed to compensate for normal head movement, whereas normal head movement now leads to altered retinal image displacement. With a clockwise tilt transformation, the VOR would take the eye to the right during a leftward head movement, but visual feedback would be essential to get the eye to move downward in order to maintain fixation. The effort and the time required to complete a compensatory eye movement would be greater than normal; but the difference would eventually be reduced, to the extent that the VOR could be adjusted to be consistent with image displacement contingent upon a head movement. This adjustment would entail that a horizontal head movement, for example, elicit a somewhat oblique compensatory eye movement, rather than a purely horizontal one. With a regular transformation, such as that caused by tilting prisms, and sufficient movement on the part of the subject, the present
41
results demonstrate that such an adjustment can be made in the VOR. As was expected, there was significant visual adaptation in the 30” tilt condition, but not in the 0” condition. Tilt adaptation was manifest despite the fact that the subjects were well into the decay period when this was measured and as anticipated, adaptation was higher in the screening session when it was measured immediately after exposure. The individual differences found in amount of adaptation seem also to apply to the change in VOR. When the two measures taken immediately after exposure were compared, a significant correlation was found. We are left with the possibility either of a common mechanism behind the observed changes or that the VOR mechanism determines egocentric angular orientation.
Acknowledgements-This research was supported in part bv arant EY02264 from the National Eve Institute to SIMTE.to whom reprint requests should be addressed. This work was submitted by J.W.C. in partial fulfillment of the requirements for the Ph.D. degree, Department of Psychology, University of Wisconsin, 1979. We thank Wes Handrow for constructing the special apparatus used in this experiment. J.W.C. also thanks the members of the dissertation committee, Sheldon Ebenholtz, William Epstein, Leonard Ross, Ulker Keesey and Fred Dretske for their helpful comments.
REFERENCES
Barr C. C., Schultheis L. W. and Robinson D. A. (1976) Voluntary, non-visual control of the human vestibuloocular reflex. Acta otolar. 81, 365375. Callan J. W. and Ebenholtz S. M. (1981) Effects of tilt adaptation on the direction of voluntary saccades. Perception. In press. Ebenholtz S. M. (1966) Adaptation to a rotated visual field as a function of degree of optical tilt and exposure time. J. exp. Psycho/. 72, 629-634. Ebenhdltz S. M. (1968) Readaptation and decay after exnosure to ontical tilt. J. exn Psvchol. 78. 350-351. Edenholtz S. ‘M. (1969) Transfer-and decay functions in adaptation to optical tilt. J. exp. Psycho/. 81, 170-173. Ebenholtz S. M. and Callan J. W. (1980) Tilt adaptation as a feedback control process. J. exp. Psychol. Hum. Percept. Perform. 6, 413-432. Fiorentini A., Ghez C. and MatTei L. (1972) Physiological correlates of adaptation to a rotated visual field. J. Physiol. 227, 313-322. Gauthier G. M. and Robinson D. A. (1975) Adaptation of the human vestibuloocular reflex to magnifying lenses. Brain Res. 92, 331-335. Gonshor A. and Melvill Jones G. (1973) Changes of human vesticuloocular response induced by vision-reversal during head rotation. 2. Physiol. 234, iO2-103P. Gonshor A. and Melvill Jones G. (1976a) Short-term adaptive changes in the human vestibulo-ocular reflex arc. J. Physiol. 256, 361-379. Gonshor A. and Melvill Jones G. (1976b) Extreme vestibulo-ocular adaptation induced bv Drotonaed ontical reversal of vision.-J. Physiol. 256, 381-1414. * Ito M. (1972) Neural design of the cerebellar motor control system. Brain Res. 40, il-84. Mack A. and Rock I. (1968) A re-examination of the Stratton effect: Egocentric adaptation to a rotated visual image. Percept. Psychophys. 4, 57-62.
42
JUDITHW. CALLANand SHELDONM. EBENHOLTZ
Meiry J. L. (1966) The vestibular system and human dynamic space orientation. NASA CR-628. Washington DC, N.A.S.A. Mikaelian H. H. (1976) Plasticity of orientation specific chromatic aftereffects. Vision Res. 16, 459-462. Mikaelian H. and Held R. (1964) Two types of adaptation to an optically-rotated visual field. Am. J. Psycho/. 77. 257-262. Miles F. A. and Fuller J. (1974) Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey. Brain Res. 80. 5 12-5 16.
Morant R. B. and Belier H. K. (1965) Adaptation of prismatically rotated visual fields. Science 148, 53&531.Oman C. M.. Bock 0. L. and Huang J.-K. (1980) Visuallv induced self-motion sensation adapts rapidly to’ left-righi visual reversal. Science 209, 706-708. Robinson D. A. (1975) How the oculomotor system repairs itself. Incest. Ophthal. cisual Sci. 14, 413-415. Takahashi M., Uemura T. and Fujishiro T. (1980) Studies of the vestibulo-ocular reflex and visual-vestibular interactions during active head movements. Acta of&w. 90, 115-124.
DIRECTIONAL RESPONSE
0042.6989:X2.010037-06M300’0 Perpamon PressLtd
CHANGES IN THE VESTIBULAR AS A RESULT OF ADAPTATION OPTICAL TILT
JUDITH W. CALLAN
and
SHELWN
OCULAR TO
M. EBENHOLTZ
Department of Psychology, University of Wisconsin, 1202 West Johnson Street, Madison, WI 53706. U.S.A. (Receioed
24 April 1980: in rrrisedJorm 8 Junr
1981)
Abstract-Before and after exposure to clockwise optical tilt, subjects’ compensatory eye movements were recorded, as the head was oscillated around a vertical axis by the experimenter. An analysis of the horizontal and vertical components of eye movements showed a change in eye movement path in the clockwise direction. This corresponded to similar changes in visual spatial orientation judgments indicative of perceptual adaptation. It was suggested that long-term visual feedback serves to restore the compensatory nature of the eye movements which was altered by the introduction of the prism transformation.
INTRODUCTION Previous studies investigating adaptive responses due to exposure to an optical tilt transformation have found changes in visual orientation perception (Ebenholtz, 1966; Mack and Rock, 1968; Mikaelian and Held, 1964; Morant and Belier, 1965), contrast thresholds and orientation-dependent visual evoked responses (Fiorentini et al., 1972), and the orientation of the McCollough effect (Mikaelian, 1976). Studies using transformations other than tilt, have investigated changes, not in visual perception, but in the vestibulo-ocular reflex (VOR). They have found adaptive shifts in the VOR with reversal (man, Gonshor and Melvill Jones, 1973, 1976a and b), and with minification and magnification (man, Gauthier and Robinson, 1975; monkey, Miles and Fuller, 1974). These changes have occurred when head movements were made during exposure to the transformation. It was suggested that this type of oculomotor adaptation may be related to the visual adaptation which occurs to minimize the apparent background movement most noticeable when the transformation is first introduced (Gonshor and Melvill Jones, 1973; Robinson, 1975), however, with one exception, relations between the VOR and perception have not been tested directly.* In a recent tilt study in which adaptation occurred during movement in the environment (Callan and Ebenholtz, 1981) changes were found in the direction of voluntary saccades corresponding to the adaptation of visual orientation. The present experiment attempted to determine if changes in VOR also resulted from exposure to optical tilt. While previous studies of VOR tested for increases or decreases in the * Oman ef al. (1980) looked for corresponding changes in VOR and circular vection following reversal, but did not attempt to look for changes in risual perception. 37 Y.R.22 I--r
gain of the horizontal VOR, changes due to tilt would have to be manifest as eye movements along an oblique axis, i.e. as shifts in the horizontal and vertical directions simultaneously. In addition, the present study examined the possibility of corresponding adaptive changes in VOR and visual orientation perception. METHODS Each session started with a 20min period of dark adaptation, followed by a series of calibration eye movements. Eye movements were recorded by d.c. electro-oculography, using a Beckman R411 Dynograph with nystagmus couplers. Horizontal electrodes were placed adjacent to the outer canthus of each eye, vertical electrodes above and below the right eye and the vertical and horizontal components of eye movements were recorded on separate channels. The settings were adjusted on the Dynograph and preliminary calibration eye movements were made by having the subject look back and forth between pairs of spots set opposite each other on a large lighted circular contour, in a dark room, with the head stabilized by a bite bar. Due to crosstalk, or in some cases a slight misalignment of the electrodes, there was often a small regular signal on the minor channel when the eye movement was being made in the orthogonal direction, which usually changed direction in phase with, or 180’ out of phase with, the signal on the major channel. Since the results were to consist of the differences between pre- and post-exposure recordings, this did not introduce an artifact. In addition to calibrations for horizontal and vertical eye movements, recordings were also taken on eye movements to targets placed 5’ clockwise (CW) and 5’ counterclockwise (CCW) of the major orientations. This was to ascertain that for
JUDITH W. CALLAN and SHELDON M. EBENHOLTZ
38
each subject it would be possible to detect slight changes in the orientation of the eye movement path, and was used to screen subjects. According to an extensive analysis done by Callan and Ebenholtz (1981). it should be possible to detect differences in eye movement path angle at least as small as I.3 deg. Before and after tilt exposure compensatory eye movements and tilt adaptation were measured, in that order. One of the problems of taking measures after tilt exposure is the possibility of decay of the effect starting soon after exposure is ended (Ebenholtz, 1968. 1969). This makes it imperative that any responses which might be affected in this way be measured as soon as possible after the end of the exposure period. One implication of this is that only one dependent variable can be measured before decay progresses very far in any one session, and thus still be regarded as an accurate measure of the size of the effect of tilt exposure. Adaptation results were obtained immediately after exposure in the screening session, and. since compensatory eye movements (the VOR) were the main object of interest in the present study. they were measured immediately after exposure in the experimental session. A second point relates to the state of light adaptation at the time of eye movement measurement. The normal procedure is to darkadapt the subject to bring about a more stable eye movement response. Since decay would start before dark adaptation could be completed, subjects were not dark-adapted after tilt exposure in the lighted hallway. Accordingly, in order to make the pre- and post-exposure measurements under approximately comparable conditions, subjects were light-adapted for 5 min prior to the pre-exposure measure. To produce the VOR, the bit was attached to a frame that could be tilted forward 30’. The frame mechanism was oscillated by hand by the experimenter, through an angle of 30’. at a frequency of 0.25 Hz. for about 8 cycles.* This period, which preceded, and followed the tilt adaptation session, began and ended with a static calibration test for sensitivity changes. For the VOR measures reported in this study, the subject was given a fixation point straight ahead, which was turned off when the head movements began. The subjects were not told to do anything with their eyes, but were given standard mental arithmetic instructions, which generally insure purely compensatory eye movements (Barr et al., 1976; Gauthier and Robinson, 1977). A dynamic calibration, in which eye fixation was maintained on a fixed target during head oscillation, was taken before the final static calibration; since the two should have been the same (Barr et al.. 1976) a deviation indicated an equipment adjustment that was needed to bring the head into proper alignment before the experimental session. * These were the values found during the best combination
nome aided timing.
of amplitude
pilot studies to be and frequency, A metro-
The level of tilt adaptation was measured by having the subject direct the experimenter in the setting of a thin luminous line in an otherwise dark room. The line was set by the subject so as to be oriented from “12 to 6” or from “9 to 3” o’clock, according to instructions, with the subject’s head used as the reference for egocentric orientation. During each session with electrodes in place the subject was exposed to a 30” optical tilt while walking about in a hallway. To produce the optical tilt, the subject wore a helmet which allowed an eyepiece to be positioned over the right eye; the left eye was covered. The eyepiece contained two dove prisms mounted in tandem, one of which was stable while the other was rotated, to produce a tilted visual field, 14” in diameter, without left-right reversal. Potential subjects were screened in an initial session to find those with voluntary and compensatory eye movements regular and consistent enough to be measured objectively with some degree of confidence, and who also could exhibit orientation adaptation. This procedure yielded six subjects who returned for an experimental session a week later, and a control session at least one week after that. Subjects received a 10min exposure to a 30. tilt during the screening session and a 20min exposure to a 30” tilt during the experimental session. The 20min time period was chosen to make it more likely that the subject would achieve a stable level of adaptation (Ebenholtz and Callan. 1980) before undergoing the series of postexposure tasks. During the control session the subjects received 20min exposure to 0’ tilt.
RESULTS
A typical VOR record is shown in Fig. 1, which has both the compensatory segments, opposite the direction of head movement, and the anticompensatory segments returning the eye to the center position. To measure the total amplitude of compensatory eye movements it was necessary to construct cumulative eye position (CEP) curves (Meiry, 1966). In the VOR retraining studies described previously, the measure of interest was the gain of the compensatory eye movements with respect to the head movement. In those cases the only change in the eye movement was an increase or decrease in horizontal amplitude. The gain was computed as the ratio of eye angular ~&city to head angular velocity, and in some cases (Gonshor and Melvill Jones, 1976a and b) the peak eye angular velocity was calculated from the CEP curves. In the present study a more important measure was the angle of eye movement, which could be readily obtained from the eye position curves. The gain in this case, then, was taken as the ratio of horizontal eye position amplitude to head position amplitude. Segments of 8-10 horizontal half-cycles and corresponding vertical half-cycles were measured, and the means, in mm, were taken for each and used to com-
Adaptation to optical tilt
ward eye movement, contributing to the mean were not necessarily successive. It was more important that the half-cycles correspond in the two components than that they be successive, so whenever there was a break in the vertical CEP curve due to a blink or vertical saccade, the measurements were not taken on either curve.
pute the slope of the given eye movement. The mean of the minor component (the vertical) was divided by the mean of the major component. Since the slope equals tan 0, the angle (0) of the eye movement path was then computed. These angles (0) were compared from data generated before and after exposure. In the present study the half-cycles, i.e. a rightward or leftA
39
BEFORE
EXPOSURE
HORIZONTAL
.
COMPONENT
:
:
,LEFt
:
I I I
1 .
.”
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Fig. I. Sample of compensatory eye movement records, from subject A.J., during mental arithmetic task. The upper part of each record is the horizontal component, and the lower is the vertical. Spots at the bottom of each record indicate times at which the head reached rightmost point.
40
JUDITH W. CALLAN and SHELDON M. EBENHOLTZ Table
I. Before-after
difference scores (deg arc) from compensatory eye movements*
tests of adaptation
Experimental session (20 min at 30’)
Screening
session (lOminat30’)
Control session (20min at 0
Eye Subject
Adaptation
Adaptation
movements
C.C. F.G. J.H. S.K. B.B. A.J.
3.25 2.12 3.12 3.00 3.50 3.50
2.62 0.62 1.88 1.50
5.51 0.63 2.1 I 3.66 5.80 10.05
M 0.U
3.0w 0.2 I
1.60t 0.27
4.63t 1.35
* Adaptation 7 Significant
1.75
I .25
scores averaged at P < 0.05.
over horizontal
The results shown in Table 1 are from VOR eye movements made while the subject was doing mental arithmetic.* The direction of eye movement path did change after exposure to tilt, the path becoming more oblique in the CW direction following exposure to 30’ CW tilt, t(5) = 3.33, P < 0.05. In the records of some subjects, as shown in Fig. 1, the change in the vertical component could be clearly seen, even before the measurement techniques were applied. There was no change following exposure to the 0” tilt in the third session. Wheq the mental arithmetic instruction is used during head oscillation in the dark, reports of the normal gain of horizontal eye angular velocity with respect to the head vary from 0.60 (e.g. Gonshor and Melvill Jones, 1975; Barr rt (I/., 1976; Gauthier and Robinson, 1977) to 0.80 (Takahashi et al. 1980). The gain? of horizontal eye position, which was measured in this study was within this range, averaging 0.73 and 0.61 in the 30“ and 0. conditions before exposure. After exposure in the 30’ condition it was reduced to 0.58, and to 0.58 in the 0” condition. Only the decrease in was statistically significant, the 30. condition r(5) = 5.00, P < 0.01. This is fully consistent with the
is the result from the first session of were obtained under the combination mental arithmetic and straightahead eye position instruction only. When the eye movements for the second session were examined it was found that the eye movements using the mental arithmetic instruction and the ones using the combination instruction were identical. It was assumed that this would have been the case in the first session and hence that the scores from that session are equivalent to those obtained under mental arithmetic alone. t The geometric mean of the two static calibrations that preceded and followed each VOR measurement session was taken as the measure of a 30’ head movement amplitude. The gain was defined as the ratio of the mean amplitude of the CEP curve and the geometric mean of the static calibrations. *The one exception
the first subject from which eye movements
Adaptation
) Eye
movements
0 0.12 0.25 0.25 0.12
0.52 -0.73 -0.58 -0.50 -0.37 -2.39
- 0.08 0.24
-0.68 0.39
-
I.25
and vertical
and
settings.
angular shift in VOR found in the adaptation condition. An analysis of variance compared spatial adaptation under the two conditions of exposure (30” and 0’ tilt) separately for horizontal and vertical settings. There was no difference between the two directions. so in subsequent tests these scores were combined. There was a significant difference between the two tilt conditions, as shown in Table 1, F(l, 5) = 22.67, P < 0.05. While the level of adaptation in the 30” tilt condition is low, it should be remembered that this test was taken about 8 min after the helmet was removed. The level of adaptation found after only 1Omin of exposure. but measured immediately after prism exposure in the screening session, was higher, averaging 3.08 deg. However, despite the reduction in the size of the adaptation measurement in the experimental session compared to the screening session, it was significantly different from zero, t(5) = 5.93, P < 0.05, while that obtained in the control condition was not. The assumption which is therefore assumed to be creditable is that significant levels of tilt adaptation were present during the VOR rests under the experimental conditions. It is difficult to make exact comparisons of the size of the effects in this study, since the compensatory eye movements were measured within a few minutes after the end of the exposure period. while adaptation measures were taken about 6min after that. This would give the adaptation a chance to decay (Ebenholtz, 1968, 1969), with the decay rates possibly different for each subject. There was no significant correlation between the adaptation and VOR change in the 30” tilt experimental condition. However, a correlation also was computed on the compensatory eye movement change in that condition and the adaptation measures of the screening session. The exposure period was shorter in the screening session and the level of adaptation probably less than it was right after the 20min exposure, but at least both measures
Adaptation to optical tilt could be compared without the effects of decay. This correlation, r = 0.80, was significant, t(4) = 2.67, P < 0.05. DISCUSSION
Compensatory eye movements due to the VOR were examined before and after exposure to 30” and 0” optical tilts. The angle of the eye movement path changed significantly in the direction of tilt in the 30 tilt condition; in the 0” condition there was no change. The angular shift that occurred in the 30” condition can be seen as adaptive in that such an
adjustment during exposure to an optically tilted environment would reduce the need for visual feedback control of fixation during head and body movement. It may also be noted that, since with mental arithmetic the VOR is automatically elicited, these eye movement changes could not have been due to any con-
scious effort on the part of the subject. It follows that the subject’s eye movements could not have been influenced by the subject’s perception of orientation (whether egocentric or exocentric) as might be argued in the case of voluntary eye movements (Callan and Ebenholtz, 1981). This result seems to preclude the possibility of accounting for changes in eye movements, particularly VOR movements, by referring to changes in visual orientation. It is proposed that the shifts in eye movement direction occurred as part of a feed-forward mechanism of the compensatory eye movement system to lessen the need for error correction in visual feedback control, as occurs during exposure to prism transformation. Under normal conditions for adaptation the subject moves about in an optically tilted environment. During this time his head is moving almost continuously, and each head movement is accompanied by a compensatory eye movement, generated by vestibular and neck muscle stimulation. When the environment is viewed through tilting prisms each eye movement so generated is only partially effective, since the reflex portion of the movement is programmed to compensate for normal head movement, whereas normal head movement now leads to altered retinal image displacement. With a clockwise tilt transformation, the VOR would take the eye to the right during a leftward head movement, but visual feedback would be essential to get the eye to move downward in order to maintain fixation. The effort and the time required to complete a compensatory eye movement would be greater than normal; but the difference would eventually be reduced, to the extent that the VOR could be adjusted to be consistent with image displacement contingent upon a head movement. This adjustment would entail that a horizontal head movement, for example, elicit a somewhat oblique compensatory eye movement, rather than a purely horizontal one. With a regular transformation, such as that caused by tilting prisms, and sufficient movement on the part of the subject, the present
41
results demonstrate that such an adjustment can be made in the VOR. As was expected, there was significant visual adaptation in the 30” tilt condition, but not in the 0” condition. Tilt adaptation was manifest despite the fact that the subjects were well into the decay period when this was measured and as anticipated, adaptation was higher in the screening session when it was measured immediately after exposure. The individual differences found in amount of adaptation seem also to apply to the change in VOR. When the two measures taken immediately after exposure were compared, a significant correlation was found. We are left with the possibility either of a common mechanism behind the observed changes or that the VOR mechanism determines egocentric angular orientation.
Acknowledgements-This research was supported in part bv arant EY02264 from the National Eve Institute to SIMTE.to whom reprint requests should be addressed. This work was submitted by J.W.C. in partial fulfillment of the requirements for the Ph.D. degree, Department of Psychology, University of Wisconsin, 1979. We thank Wes Handrow for constructing the special apparatus used in this experiment. J.W.C. also thanks the members of the dissertation committee, Sheldon Ebenholtz, William Epstein, Leonard Ross, Ulker Keesey and Fred Dretske for their helpful comments.
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