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Adaptation of the human vestibuloocular reflex to magnifying lenses
Brain Research, 92 (1975) 331-335
331
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Adaptation of the human vestibuloocular reflex to magnifying lenses
GABRIEL M, GAUTHIER ANDDAVID A. ROBINSON Laboratoire de Psychophysiologie, Universitd de Provence, Marseilles (France) and The Wilmer Institute, The Johns Hopkins University, Baltimore, Md. (U.S.A.)
(Accepted April 1st, 1975)
The function of the vestibuloocular reflex (VOR) is to maintain stable vision of the environment during head movement. Normally, eye movement should be equal but opposite to head movement, in which case the gain or ratio of eye to head velocity is 1.0. When prisms or lenses change this normal relationship, images, at first, slip on the retina when the head turns. This stimulates adaptive brain mechanisms which alter the gain of the VOR until images no longer slip. This was first demonstrated by Gonshor and Melvill Jones 2 in man wearing reversing prisms (which caused the VOR to actually reverse!). Similar results have been demonstrated in rabbit a and in cat s. Adaptive increases as well as decreases in gain were demonstrated by Miles and Fuller 4 in the monkey wearing telescope lenses. Only the latter study 4 demonstrated a clear, large increase in gain and, although our results are not surprising, we wanted to verify in man that the gain could go up as well as down 2 and also obtain the benefits of subjective description, especially with respect to the spatial localization ability of the Subject (S). The results have practical implications, e.g., the magnifying effect of the water-air interface means that the VOR of a diver, who spends long periods under water, is exposed to a similar adaptive pressure. This situation also occurs in patients with bilateral aphakia who must be corrected with spectacle lenses which inadvertently magnify. Gne S was fitted with telescope lenses with a magnification of 2.1 x . Masking goggles restricted the S's visual world to that seen only through the lenses. They were worn for 5 full days during which the S made every attempt to live a normal life compatible with physical safety. The VOR gain was measured thoroughly before, during, and after the adaptation period. For several hours after the lenses were put on, the S had a mild headache and slight nausea. Head movements were not compensated for correctly by eye movements and stabilized vision was greatly impaired. The visual surround seemed to move in the direction opposite to that of head movements. Correct evaluation of distance and size of objects and calibration of eye-body coordination was regained in about one day. Visual stability during head movements improved more slowly and was only adequate after 4 days. The restricted visual field (about 6 °) was a source of disorientation throughout the experiment. When the lenses were removed after 5 days, nausea
332 occurred again for 2 h and visual stability during head movements was again lost for the first 5-6 h. The next morning, visual instability was again experienced for several minutes after rising. The V O R was tested by rotating the S horizontally, sinusoidally, at about 0.25 Hz over a 40 ° range. Eye movements were recorded with the DC-EOG. Thirty minutes were allowed for dark adaptation and stabilization of electrode drift. Subsequently, calibration o f eye and chair signals were simultaneously rechecked about every 1-3 min by using a dim, red target light. Most testing was done without goggles but the S was then kept in darkness and not rotated when target lamps were visible except for special tests o f short duration. Eye and chair velocity were obtained by electronic differentiation over the bandwidth 0-1.6 Hz (time constant 0.1 sec). The eye velocity trace recovered from quick-phase interference within 0.3 sec and eye velocity could thus be estimated correctly because quick phases seldom occur closer together. The chair was rotated by hand (the necessary heavy machinery being unavailable) so that head velocity was not exactly sinusoidal and o f constant peak velocity. Never-
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2.SEC. MENTAL ARITHMETIC
IMAGINARY SPOT OR WALL
IM A C,I~4AR '~ SPOT ON .~i, ,',1R
Fig. 1. The subject's vestibuloocular response before (upper 4 traces) and after (lower 4 traces) wearing 2.1 × magnifying lenses for 5 days. All tests were done in the dark. For each test, head (chair) position, head velocity, eye position (in the head) and eye velocity are shown. A : subject performing mental arithmetic. B: subject looking at an imaginary target on the wall. C: subject looking at an imaginary target moving with him on the rotating chair. In all cases, peak eye velocity increased after wearing lenses (bottom traces).
333 theless, by comparing peak eye to peak head velocity within a single half cycle, the gain can be measured with good accuracy. For each trial, the gain of at least 20 individual half cycles was averaged. Fig. 1A shows a few typical cycles. When the S was performing mental arithmetic in the dark, the gain rose from 0.61 ± 0.07 S.D. (e.g., Fig. 1, top traces) to 1.08 i 0.14 (bottom traces) after 5 days of adaptation; an increase of 70~. The frequency of quick phases did not increase significantly but their amplitude also increased by about 50~. When a target was visible, the gain was 1.0 when it was fixed to the wall and seen without lenses. It was 2.0 when seen with lenses. It was zero when the lamp was on the chair and rotated with the S. Previous experiments (unpublished observations by Gauthier and Voile, and Barr et al.) have shown that, even without vision, the mental effort to fixate an imaginary target can change the gain from the mental arithmetic value of about 0.6, up to almost 1.0 if the imaginary target is on the wall and down to about 0.3 if it is on the chair. Similar mental tasks were given the S to demonstrate the results ot VOR adaptation. Fig. 1B shows the results of looking at an imaginary target on the wall in darkness. The gain rose from 0.81 4- 0.12 (upper traces) to 1.24 :~ 0.15 (lower traces); an increase of 53~. The ability to suppress the VOR diminished. When trying to look at an imaginary target on the chair (Fig. 1C) the gain rose from 0.18 (upper traces) to 0.45 (lower traces); an increase of 150~. Thus, 5 days of wearing 2.1 × magnifying lenses increased the gain of the VOR by large amounts under all conditions of testing: by 1.7 × with mental arithmetic, by 1.53 × when attending to an unseen earth-fixed surround and, by 2.5 x when trying to suppress the VOR. These results might explain the findings of Gauthier 1 who tested 2 professional deep-sea divers and found that when the gain of their VOR was measured in the dark, it intermittently rose above 1.0 for brief periods. The magnification they experienced in looking at the aquatic world through masks or bell windows is about 1.35. It is possible that these men have developed a schismatic VOR with one gain for land activity and another for undersea activity (where automatic, clear vision and visual stability has some survival value) either of which might sporadically appear during testing in the dark. In Fig. 2 the S was first shown a target on the wall, then it was turned out and he was rotated 20 or 40 ° with instructions to keep looking at the now invisible target. Normally, the S did this well (upper traces) and when the target reappeared he was looking right at it. After 5 days of adaptation, the eye over-compensated by 30-50~ (6-10 °, lower traces). When the target reappeared, a large corrective saccade was needed for refixation. More importantly, the target, subjectively, appeared to have moved during the dark period in the direction of the chair motion. If the light were left on during the rotation, the eye stayed on target but, subjectively, the target appeared to move in space with the chair but by a lesser amount. This raises the issue of how Ss localize seen targets. Skavenski et al. 6 have shown that this is based on an extraretinal knowledge of eye position from outflow or efference copy. When a S is rotated, his subjective calculation of relative target position must be the subjective estimate of how far he has moved from the vestibular signal, minus how much he thinks his eye has moved from efference copy, plus retinal
334
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Fig. 2. Subject's ability to look at the remembered position of a fixed target lamp when rotated 20 or 40 ° in the dark before (upper 2 traces) and after (lower 2 traces) wearing magnifying lenses. Chair (head) and eye position are shown in each test. At the down arrows the target lamp disappears, the subject is rotated and attempts to keep looking at the target location. At the up arrows, the lamp reappears and the subject refixates it. After lens adaptation, subject mislocates target.
e r r o r if any. I n the a d a p t e d state, o u r S mislocated targets in space because o f a false i n t e r n a l r e c a l i b r a t i o n o f one o f these signals. Eye m o v e m e n t s with the h e a d s t a t i o n a r y d i d n o t suggest a n y r e a s o n to suspect a r e c a l i b r a t i o n o f retinal error or efference copy. T h e p h e n o m e n a c o u l d be m o s t simply explained b y assuming the semicircular canal signal itself was r e c a l i b r a t e d b y a factor o f a b o u t 1.5. Thus, when r o t a t e d 20 °, the S t h o u g h t he was r o t a t e d 30 °. H e m a d e w h a t was to h i m a correct 30 ° c o m p e n s a t o r y eye m o v e m e n t . I n fact, his eyes were n o w 10 ° on the w r o n g side o f the target. W h e n it r e a p p e a r e d , it was 10 ° off the f o v e a in the d i r e c t i o n o f chair movement. T o the S, the c o n c l u s i o n was t h a t the target h a d m o v e d 10 ° in t h a t direction. If the light stayed on d u r i n g the m o v e m e n t , he h a d to m a k e a 10 ° ' p u r s u i t ' m o v e m e n t to stay on target. To the S, the p u r s u i t m o v e m e n t was needed n o t to cancel an excess V O R m o v e m e n t b u t instead to pursue the target because, to the S, it a p p e a r e d to move. In s u m m a r y , these experiments confirm the finding that the V O R is plastic a n d
335 responds adaptively to any disturbance, external or internal, that creates vestibuloocular dysmetria. This adaptation also creates internal changes that cause Ss to mislocate objects in space and suggests an interesting technique for separating out the way in which various signals are used by the brain in calculating the relative location of seen objects. We thank A. R. Friendlich for technical assistance and P. Speros of the Wilmer Laboratory of Physiological Optics for providing the telescope glasses. The authors' laboratories are supported by Research Grants 73048 from the D.R.M.E. and ERA272 from the C.N.R.S. (G.M.G.), and Research Grant EY00598 from the Eye Institute and the National Institutes of Health of the U.S. Public Health Service (D.A.R.).
1 GAUTHIER, G. M., Plong6e profonde simul6e Sagittaire IV h 610 m6tres sous Heliox, Rapp.
pr61im., (1974) 1-7. 2 GONSHOR,A., ANDMELVILLJONES,G., Changes of human vestibulo-ocular response induced by vision-reversal during head rotation, J. Physiol. (Lond.), 234 (1973) 102-103P. 3 |TO, M., SHIIDA,T., YAGI, N., AND YAMAMOTO,M., The cerebellar modification of rabbit's horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation, Proc. Jap. Acad., 50 (1974) 85-89. 4 MILES,F.A., AND FULLER,J. H., Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey, Brain Research, 80 (1974) 512-516. 5 ROBINSON,D. A., Oculomotor control signals. In P. BACrI-Y-RITAANDG. LENNERSTRAND(Eds.), Basic Mechanisms of Ocular Motility and their Clinical Implications, Pergamon Press, Oxford~ 1975, in press. 6 SKAVENSKI,A. A., HADDAD,G., ANDSTEINMAN,R. M., The extraretinal signal for the visual perception of direction, Percept. Psychophys., 11 (1972) 287-290.
331
© Elsevier Scientific Publishing Company, Amsterdam - Printed in The Netherlands
Adaptation of the human vestibuloocular reflex to magnifying lenses
GABRIEL M, GAUTHIER ANDDAVID A. ROBINSON Laboratoire de Psychophysiologie, Universitd de Provence, Marseilles (France) and The Wilmer Institute, The Johns Hopkins University, Baltimore, Md. (U.S.A.)
(Accepted April 1st, 1975)
The function of the vestibuloocular reflex (VOR) is to maintain stable vision of the environment during head movement. Normally, eye movement should be equal but opposite to head movement, in which case the gain or ratio of eye to head velocity is 1.0. When prisms or lenses change this normal relationship, images, at first, slip on the retina when the head turns. This stimulates adaptive brain mechanisms which alter the gain of the VOR until images no longer slip. This was first demonstrated by Gonshor and Melvill Jones 2 in man wearing reversing prisms (which caused the VOR to actually reverse!). Similar results have been demonstrated in rabbit a and in cat s. Adaptive increases as well as decreases in gain were demonstrated by Miles and Fuller 4 in the monkey wearing telescope lenses. Only the latter study 4 demonstrated a clear, large increase in gain and, although our results are not surprising, we wanted to verify in man that the gain could go up as well as down 2 and also obtain the benefits of subjective description, especially with respect to the spatial localization ability of the Subject (S). The results have practical implications, e.g., the magnifying effect of the water-air interface means that the VOR of a diver, who spends long periods under water, is exposed to a similar adaptive pressure. This situation also occurs in patients with bilateral aphakia who must be corrected with spectacle lenses which inadvertently magnify. Gne S was fitted with telescope lenses with a magnification of 2.1 x . Masking goggles restricted the S's visual world to that seen only through the lenses. They were worn for 5 full days during which the S made every attempt to live a normal life compatible with physical safety. The VOR gain was measured thoroughly before, during, and after the adaptation period. For several hours after the lenses were put on, the S had a mild headache and slight nausea. Head movements were not compensated for correctly by eye movements and stabilized vision was greatly impaired. The visual surround seemed to move in the direction opposite to that of head movements. Correct evaluation of distance and size of objects and calibration of eye-body coordination was regained in about one day. Visual stability during head movements improved more slowly and was only adequate after 4 days. The restricted visual field (about 6 °) was a source of disorientation throughout the experiment. When the lenses were removed after 5 days, nausea
332 occurred again for 2 h and visual stability during head movements was again lost for the first 5-6 h. The next morning, visual instability was again experienced for several minutes after rising. The V O R was tested by rotating the S horizontally, sinusoidally, at about 0.25 Hz over a 40 ° range. Eye movements were recorded with the DC-EOG. Thirty minutes were allowed for dark adaptation and stabilization of electrode drift. Subsequently, calibration o f eye and chair signals were simultaneously rechecked about every 1-3 min by using a dim, red target light. Most testing was done without goggles but the S was then kept in darkness and not rotated when target lamps were visible except for special tests o f short duration. Eye and chair velocity were obtained by electronic differentiation over the bandwidth 0-1.6 Hz (time constant 0.1 sec). The eye velocity trace recovered from quick-phase interference within 0.3 sec and eye velocity could thus be estimated correctly because quick phases seldom occur closer together. The chair was rotated by hand (the necessary heavy machinery being unavailable) so that head velocity was not exactly sinusoidal and o f constant peak velocity. Never-
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2.SEC. MENTAL ARITHMETIC
IMAGINARY SPOT OR WALL
IM A C,I~4AR '~ SPOT ON .~i, ,',1R
Fig. 1. The subject's vestibuloocular response before (upper 4 traces) and after (lower 4 traces) wearing 2.1 × magnifying lenses for 5 days. All tests were done in the dark. For each test, head (chair) position, head velocity, eye position (in the head) and eye velocity are shown. A : subject performing mental arithmetic. B: subject looking at an imaginary target on the wall. C: subject looking at an imaginary target moving with him on the rotating chair. In all cases, peak eye velocity increased after wearing lenses (bottom traces).
333 theless, by comparing peak eye to peak head velocity within a single half cycle, the gain can be measured with good accuracy. For each trial, the gain of at least 20 individual half cycles was averaged. Fig. 1A shows a few typical cycles. When the S was performing mental arithmetic in the dark, the gain rose from 0.61 ± 0.07 S.D. (e.g., Fig. 1, top traces) to 1.08 i 0.14 (bottom traces) after 5 days of adaptation; an increase of 70~. The frequency of quick phases did not increase significantly but their amplitude also increased by about 50~. When a target was visible, the gain was 1.0 when it was fixed to the wall and seen without lenses. It was 2.0 when seen with lenses. It was zero when the lamp was on the chair and rotated with the S. Previous experiments (unpublished observations by Gauthier and Voile, and Barr et al.) have shown that, even without vision, the mental effort to fixate an imaginary target can change the gain from the mental arithmetic value of about 0.6, up to almost 1.0 if the imaginary target is on the wall and down to about 0.3 if it is on the chair. Similar mental tasks were given the S to demonstrate the results ot VOR adaptation. Fig. 1B shows the results of looking at an imaginary target on the wall in darkness. The gain rose from 0.81 4- 0.12 (upper traces) to 1.24 :~ 0.15 (lower traces); an increase of 53~. The ability to suppress the VOR diminished. When trying to look at an imaginary target on the chair (Fig. 1C) the gain rose from 0.18 (upper traces) to 0.45 (lower traces); an increase of 150~. Thus, 5 days of wearing 2.1 × magnifying lenses increased the gain of the VOR by large amounts under all conditions of testing: by 1.7 × with mental arithmetic, by 1.53 × when attending to an unseen earth-fixed surround and, by 2.5 x when trying to suppress the VOR. These results might explain the findings of Gauthier 1 who tested 2 professional deep-sea divers and found that when the gain of their VOR was measured in the dark, it intermittently rose above 1.0 for brief periods. The magnification they experienced in looking at the aquatic world through masks or bell windows is about 1.35. It is possible that these men have developed a schismatic VOR with one gain for land activity and another for undersea activity (where automatic, clear vision and visual stability has some survival value) either of which might sporadically appear during testing in the dark. In Fig. 2 the S was first shown a target on the wall, then it was turned out and he was rotated 20 or 40 ° with instructions to keep looking at the now invisible target. Normally, the S did this well (upper traces) and when the target reappeared he was looking right at it. After 5 days of adaptation, the eye over-compensated by 30-50~ (6-10 °, lower traces). When the target reappeared, a large corrective saccade was needed for refixation. More importantly, the target, subjectively, appeared to have moved during the dark period in the direction of the chair motion. If the light were left on during the rotation, the eye stayed on target but, subjectively, the target appeared to move in space with the chair but by a lesser amount. This raises the issue of how Ss localize seen targets. Skavenski et al. 6 have shown that this is based on an extraretinal knowledge of eye position from outflow or efference copy. When a S is rotated, his subjective calculation of relative target position must be the subjective estimate of how far he has moved from the vestibular signal, minus how much he thinks his eye has moved from efference copy, plus retinal
334
HEAD POSITION
40*
Lp R
EYE
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L HEAD POSITION
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40* R
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2.SEC.
Fig. 2. Subject's ability to look at the remembered position of a fixed target lamp when rotated 20 or 40 ° in the dark before (upper 2 traces) and after (lower 2 traces) wearing magnifying lenses. Chair (head) and eye position are shown in each test. At the down arrows the target lamp disappears, the subject is rotated and attempts to keep looking at the target location. At the up arrows, the lamp reappears and the subject refixates it. After lens adaptation, subject mislocates target.
e r r o r if any. I n the a d a p t e d state, o u r S mislocated targets in space because o f a false i n t e r n a l r e c a l i b r a t i o n o f one o f these signals. Eye m o v e m e n t s with the h e a d s t a t i o n a r y d i d n o t suggest a n y r e a s o n to suspect a r e c a l i b r a t i o n o f retinal error or efference copy. T h e p h e n o m e n a c o u l d be m o s t simply explained b y assuming the semicircular canal signal itself was r e c a l i b r a t e d b y a factor o f a b o u t 1.5. Thus, when r o t a t e d 20 °, the S t h o u g h t he was r o t a t e d 30 °. H e m a d e w h a t was to h i m a correct 30 ° c o m p e n s a t o r y eye m o v e m e n t . I n fact, his eyes were n o w 10 ° on the w r o n g side o f the target. W h e n it r e a p p e a r e d , it was 10 ° off the f o v e a in the d i r e c t i o n o f chair movement. T o the S, the c o n c l u s i o n was t h a t the target h a d m o v e d 10 ° in t h a t direction. If the light stayed on d u r i n g the m o v e m e n t , he h a d to m a k e a 10 ° ' p u r s u i t ' m o v e m e n t to stay on target. To the S, the p u r s u i t m o v e m e n t was needed n o t to cancel an excess V O R m o v e m e n t b u t instead to pursue the target because, to the S, it a p p e a r e d to move. In s u m m a r y , these experiments confirm the finding that the V O R is plastic a n d
335 responds adaptively to any disturbance, external or internal, that creates vestibuloocular dysmetria. This adaptation also creates internal changes that cause Ss to mislocate objects in space and suggests an interesting technique for separating out the way in which various signals are used by the brain in calculating the relative location of seen objects. We thank A. R. Friendlich for technical assistance and P. Speros of the Wilmer Laboratory of Physiological Optics for providing the telescope glasses. The authors' laboratories are supported by Research Grants 73048 from the D.R.M.E. and ERA272 from the C.N.R.S. (G.M.G.), and Research Grant EY00598 from the Eye Institute and the National Institutes of Health of the U.S. Public Health Service (D.A.R.).
1 GAUTHIER, G. M., Plong6e profonde simul6e Sagittaire IV h 610 m6tres sous Heliox, Rapp.
pr61im., (1974) 1-7. 2 GONSHOR,A., ANDMELVILLJONES,G., Changes of human vestibulo-ocular response induced by vision-reversal during head rotation, J. Physiol. (Lond.), 234 (1973) 102-103P. 3 |TO, M., SHIIDA,T., YAGI, N., AND YAMAMOTO,M., The cerebellar modification of rabbit's horizontal vestibulo-ocular reflex induced by sustained head rotation combined with visual stimulation, Proc. Jap. Acad., 50 (1974) 85-89. 4 MILES,F.A., AND FULLER,J. H., Adaptive plasticity in the vestibulo-ocular responses of the rhesus monkey, Brain Research, 80 (1974) 512-516. 5 ROBINSON,D. A., Oculomotor control signals. In P. BACrI-Y-RITAANDG. LENNERSTRAND(Eds.), Basic Mechanisms of Ocular Motility and their Clinical Implications, Pergamon Press, Oxford~ 1975, in press. 6 SKAVENSKI,A. A., HADDAD,G., ANDSTEINMAN,R. M., The extraretinal signal for the visual perception of direction, Percept. Psychophys., 11 (1972) 287-290.