0042-6989/92 $5.00 + 0.00 Copyright © 1992 Pergamon Press pIc Vision Res. Vol. 32, No.1, pp. 167-171, 1992 Printed in Great Britain. All rights reserved Research Note Eye Movements During Motion After-effect s. H. SEIDMAN,* R. J. LEIGH,*tt c. W. THOMAS* Received 6 February 1991; in revised form 23 May 1991 Using the magnetic search coil technique, we measured torsional eye movements in four male subjects during and after rotation of a visual display around the line of sight. During rotation of the display, subjects developed a torsional nystagmus with slow-phases in the direction of target rotation that had a typical gain of < 0.01. Upon cessation of display motion, subjects experienced a motion after-effect (MAE) in the direction opposite prior target rotation, which persisted for > 15 sec. During this MAE, slow-phase eye movements of low velocity were in the same direction as the MAE, but did not persist as long as perceptual effects. In separate experiments, horizontal eye movements were recorded during horizontal stimulus motion; during MAE, no eye movements occurred due to stronger fixation mechanisms. We conclude that MAE is not caused by retinal slip of images, but MAE and the accompanying eye movements might be produced by shared or similar mechanisms. Motion after-effect Human ocular torsion Magnetic search coil INTRODUCTION The motion after-effect (MAE) is an illusory motion perception which follows the viewing of a moving target. After the target stops moving, it appears to move in the opposite direction (Holland, 1965; Wohlgemuth, 1911). This phenomenon, for historical reasons, is also known as the waterfall effect. Eye movements during MAE have not been measured, although there has been speculation as to their presence and effects (Masland, 1969). A popular stimulus for the study of MAE has been a rotating spiral. According to Cavanagh and Favreau (1980), one justification for this particular stimulus has been that rotation of a target around the line of sight involves stimulation of all directions equally, giving rise to the assumption that the eyes do not move during stimulation. This is thought to rule out eye movements as an artifactual cause of the MAE. The eyes, however, are perfectly able to move about the line of sight during this type of stimulation (i.e. torsional, or cyclorotatory eye movements), and therefore the veracity of this assumption requires investigation. It has been shown by Collewijn, Van der Steen, Ferman and Jansen (1985) and by Morrow and Sharpe *Department of Biomedical Engineering, University Hospitals, Case Western Reserve University and Cleveland Veteran Affairs Medical Center, Cleveland, OH 44106, U.S.A. tDepartments of Neurology, Neuroscience and Otolaryngology, University Hospitals, Case Western Reserve University and Cleveland Veterans Affairs Medical Center, Cleveland, OH 44106, U.S.A. tTo whom all correspondence should be addressed at the Department of Neurology, University Hospitals, 2074 Abington Road, Cleveland, OH 44106, U.S.A. 167 Eye movement Optokinetic nystagmus (1989) that torsional optokinetic nystagmus (OKN) and optokinetic after-nystagmus (OKAN), although low in gain, do occur when a subject is exposed to a full-field visual stimulus rotating around the line of sight. If OKAN occurs when the target stops, then the retinal slip caused by the OKAN would be in the appropriate direction to cause an apparent reversal of target motion. This would suggest that MAE is, at least in part, due to drift of images on the retina, i.e. "retinal slip". MAE can also be induced by sustained visual motion in the horizontal plane, but the properties of horizontal fixation and pursuit differ greatly from the torsional case. Our goals, therefore, were to (1) observe eye movements during torsional and horizontal MAE and (2) to determine if MAE was caused by retinal slip following the motion of the target. Some of these findings have been presented in abstract form (Seidman, Thomas, Huebner, Billian & Leigh, 1990). METHODS Four male human subjects, ages 24-43, were studied. All gave informed consent. Two subjects were myopes, one of whom habitually wore contact lenses; none wore corrections during the experiments. Torsional and horizontal rotations of one eye were recorded using a "double-loop" silastic search coil (Skalar, Delft, the Netherlands) and 6 ft field coils (CNC Engineering, Seattle, W A) that employed a rotating field in the horizontal plane and an alternating field in the torsional plane (Seidman & Leigh, 1989). The search coil RESEARCH NOTE 168 was precalibrated on a protractor device prior to placement on the subject's eye. The measurements of eye position were 98.5% linear over an operating range of ± 20°. The SD of the noise of our coil system was < 1 min arc. The crosstalk artifact on the torsional channel produced by horizontal or vertical rotations was ｾ＠ 0.025° torsion per deg of horizontal or vertical movement. Crosstalk of this magnitude did not effect our results. Data were filtered (0-40 Hz) using 4-pole maximally flat filters (Krohn-Hite Corporation, Avon, MA) and digitized at 100 Hz using a 16-bit data acquisition board (Data Translation, Marlborough, MA) installed in an IBM PC-AT computer. Because the torsional eye movements produced by our stimuli were small in magnitude, instantaneous eye velocity was estimated at approx. 75 instances during each trial using an interactive program. This provided a convenient method to view slow-phase direction. Visual targets were generated using an IBM PC-AT with a dedicated board used to create the images. These images were recorded directly on to videotape. A 19" monitor was used to present the stimuli to the subjects. The monitor was placed outside of the magnetic field, and was thus approx. 3 ft from the subject. At this distance, the monitor sub tended > 30° of the visual field of the subject, who viewed the display binocularly. Two different groups of stimuli were generated. The first group consisted of circular targets which incorporated 8 or 16 alternating light and dark sectors with a fixation spot in the center, and rotated around the line of sight with angular velocities of 60 or 90 degjsec [Fig. 1(A)]. Although this stimulus is not a spiral, MAE is still elicited, and the torsional optokinetic system is stimulated without the presence of complicating linear components. Subjects were requested to fixate upon the center of the rotating display. The second group consisted of 8 or 16 alternating vertical light and dark bars, with a central fixation spot [Fig. 1(B)]. These targets moved to the right, and, at the viewing distance of 3 ft, had linear velocities of 6 or 9 degjsec. Neither the torsional or the horizontal stimuli elicited circularvection (CV) in any subjects. Subjects reported perceptions of motion through use of a continuous potentiometer, which they were asked to rotate at a velocity matching the apparent velocity of the display stimulus. This signal was filtered and digitized in the same manner as the eye position signal. The stationary target was presented on the monitor for a period of 20 sec. At the end of this time period, the target started to move, and continued to do so for 20 sec. The target then stopped moving, but remained visible for a further 60 sec. Data collection began approx. 10 sec prior to target movement, and continued for 60 sec. RESULTS Typical responses are shown in Fig. 2, while the responses of all subjects are summarized in Table 1. During rotation of the circular targets, all subjects TABLE 1 Post-movement duration (sec) Target Subject Mode Sectors Velocity e/sec) Perception Eye movement Peak/ steady state T 16 16 8 16 16 8 16 16 8 16 16 8 16 16 8 16 16 8 16 16 8 16 16 8 60 90 60 6 9 6 60 90 60 6 9 6 60 90 60 6 9 6 60 90 60 6 9 6 21.0 24.6 >33.9 12.6 23.7 27.6 23.3 17.7 18.0 5.9 6.9 6.8 18.7 20.8 16.0 t 11.8 17.1 24.9 t t 5.4 5.0 15.0 17.2 19.6 26.9 * * * 17.5 12.1 5.6 * * * 6.9 13.2 7.5 t * * 10.0 20.8 11.3 * * * 0.01/ <0.01 <0.01/ <0.01 0.01/<0.01 0.72/0.20 0.87/0.08 0.57/0.15 0.04/<0.01 0.06/ <0.01 0.04/<0.01 0.70/0.11 0.55/0.11 0.70/0.15 0.04/0.02 0.03/ <0.01 0.03/<0.01 t 0.79/0.33 0.62/0.13 0.03/0.01 0.02/<0.01 0.03/ <0.01 0.05/0.03 0.04/<0.01 0.08/0.07 H 2 T H 3 T H 4 Gain T H T, torsional; H, horizontal; Gain, optokinetic gain during target motion. *Not applicable (suppressed by fixation, see text). tNot measured. RESEARCH NOTE FIGURE 1. Typical stimuli: (A) torsional and (B) horizontal. See text for details. 169 170 RESEARCH NOTE (A) TARGET MOTION ｾ＠ "0 <V "2 :e "0 () c 2...... 0... <V ｾ＠ <V CL 4.0 3.0 + velocity 3.0 + 2.0 ,..-.., 0' 1.0 <V 3 c 0 :;:; -position + + 0.0 -1.0 <V 0' II> + Ｎ［Ｋｾ＠ ＧＺＮＭＫｾ＠ + + ·w -2.0 0 o ＱＮＰｾ＠ + + + + +++ + ................... +- 2.0 0.0 3 ｾＧＫ＠ 1::- + 'g -1.0 CL q; -3.0 -2.0 > -4.0 -5.0 '---'---'--.L.----L_'---'---'---'---1_'---'---'---'----'-_'---'---'---'--'-_L..-.J.-o-'---'---' 0 20 10 30 40 50 -3.0 60 Time (sec) (B) TARGET MOTION ...... "0 ｾ＠ .! 2 '5 () c 20ｾ＠ III III CL 3.0 4.0 2.0 ....... 0'1 III + velocity -position + 2.0 ＱＮＰｾ＠ 0.0 --.. U II> 0' II> 3 -2.0 0.0 3 'w0 -4.0 -1.0 'g c :3 1::- CL Gi -2.0 > -6.0 -8.0 0 10 20 40 30 50 Time (sec) FIGURE 2. Typical responses to torsional and horizontal motion stimuli. Lower traces show eye position (line) and instantaneous estimates of eye velocity (crosses). Upper trace shows perception, as reported by subjects with a continuous potentiometer. (A) Torsional motion stimulus of 180 deg/sec and (B) horizontal motion stimulus of 9 deg/sec, followed by fixation on center of still target. Note reversal of slow phase direction following cessation of target movement in (A) and the lack of a reversal in (B). signaled stimulus motion and developed a torsional nystagmus with slow-phase eye movements going in the same direction as the target. The gain of the slow-phases of this nystagmus was low, with a steady state value usually < 0.01. Peak slow-phase velocity, occurring near the onset of target motion, tended to be slightly higher in gain. Upon motion cessation of the circular target, all subjects reported an illusory reversal in the direction of target motion, or MAE. This illusory motion persisted for a median time of 20.9 sec (range 16.0->33.9 sec). During this period slow-phase eye movements also reversed direction, with one subject actually developing torsional nystagmus. This reversed nystagmus was usually of lower velocity than that developed during target rotation, and declined to zero in a median time of 12.6 sec [range 5.6-26.9 sec, Fig. 2(A)]. Horizontal eye movements were monitored during torsional trials, and were found to deviate < 2° from the center of the target with velocities < 2 deg/sec. These movements would be expected to produce < 0.05 deg and < 0.05 deg/sec of crosstalk artifact on the torsional channel, which is too small to bias our results. During horizontal target motion, subjects developed a small horizontal nystagmus, once again with slowphases in the same direction as the target. The 171 RESEARCH NOTE steady-state gain of the slow-phases of this nystagmus was low (mean = 0.125) presumably because of the suppression of OKN by fixation mechanisms. Following horizontal target movement, subjects experienced a small, short-lived MAE which was reported to be less compelling than torsional MAE. The MAE lasted for a median time of 11.5 sec (range 5.0-27.6 sec). Reversal of horizontal nystagmus did not occur following cessation of target motion [Fig. 2(B)]. DISCUSSION activity of secondary visual areas in cerebral cortex that encode both torsional visual stimuli and eye movement signals (Graziano, Andersen & Snowden, 1990; Newsome, Wurtz & Komatsu, 1988). REFERENCES Brandt, T., Dichgans, J. & Biichele, W. (1974). Motion habituation: Inverted self-motion perception and optokinetic after-nystagmus. Experimental Brain Research, 21, 337-352. Cavanagh, P. & Favreau, O. E. (1980). Motion aftereffect: Global mechanism for the perception of rotation. Perception, 9, 175-182. Collewijn, H., Van der Steen, J., Ferman, L. & Jansen, T. C. (1985). Human ocular counterroll: Assessment of static and dynamic properties from electromagnetic scleral coil recordings. Experimental Brain Research, 59, 185-196. Ferman, L., Collewijn, H., Jansen, T. C. & Van den Berg, A. V. (1987). Human gaze stability in the horizontal, vertical, and torsional direction during voluntary head movements, evaluated with a three dimensional scleral induction coil technique. Vision Research, 27, 811-828. Graziano, M., Andersen, R. & Snowden, R. (1990). Stimulus selectivity of neurons in Macaque MST. Society for Neuroscience Abstracts, 16,6. Holland, H. C. (1965). The spiral after-effect. Oxford: Pergamon Press. Masland, R. H. (1969). Visual motion perception: Experimental modification. Science, 165, 819-821. Morrow, M. J. & Sharpe, J. A. (1989). Effects of head and body position on torsional optokinetic and vestibular eye movements in humans. Society for Neuroscience Abstracts, 15, 514. Newsome, W. T., Wurtz, R. H. & Komatsu, H. (1988). Relation of cortical areas MT and MST to pursuit eye movements. II. Differentiation of retinal from extraretinal inputs. Journal of Neurophysiology, 60, 604-620. Seidman, S. H. & Leigh, R. J. (1989). The human torsional vestibuloocular reflex during rotation about an earth-vertical axis. Brain Research, 504, 264-268. Seidman, S. H., Thomas, C. W., Huebner, W. P., Billian, C. & Leigh, R. J. (1990). Eye movements during motion aftereffect. Society for Neuroscience Abstracts, 16, 902. Wohlgemuth, A. (1911). In the after-effect of seen movement. British Journal of Psychology, Monograph Supplement 1. We have shown that there are eye movements associated with torsional MAE. These eye movements are present both during and after the motion stimulation. During stimulation, torsional eye movements were in the same direction as the motion stimulus. Following stimulation, the eye movements reversed direction. The torsional eye movements during the perception of illusory motion were not in the direction which would have produced the retinal slip necessary to cause the perception. Therefore, we conclude that retinal slip is not responsible for MAE. Although there are small eye movements during horizontal motion stimulation, there are no horizontal eye movements during the MAE. This difference between torsional and horizontal MAE may be due to the strength of the horizontal fixation system: gaze stability during fixation of a stationary target is much less precise torsionally than horizontally (Ferman, Collewijn, Jansen & Van den Berg, 1987). The reversal of eye movements during torsional MAE may be linked to the illusory reversal of the direction of the visual stimulus. Similar observations have been made by Brandt, Dichgans and Biichele (1974) for horizontal eye movement during CV, in which a reversal in the direction of CV is accompanied by a reversal in slowphase eye movement. However, since "velocity storage" in the human torsional optokinetic-vestibular system is weak or absent (Morrow & Sharpe, 1989; Seidman & Leigh, 1989), this mechanism is unlikely to contribute to eye movements during MAE. Acknowledgements-This work was supported by NIH grant EY06717 Another possibility is that the reversal of torsional eye (to Dr Leigh), the Department of Veterans Affairs, and the Evenor movements that occurs during MAE may reflect the Armington Fund.