Experimental Brain Research

Exp. Brain Res. 37, 317-336 (1979)

@ Springer-Verlag i979

Smooth Pursuit Eye Movements and Optokinetic Nystagmus Elicited by Intermittently Illuminated Stationary Patterns F. Behrens and O.-J. Grtisser Department of Physiology,Freie Universitfit Berlin, Arnimallee 22, D-1000 Berlin 33

Summary. Stationary periodic visual patterns (row of equally spaced dots or black-white stripes) of the period P~ illuminated stroboscopically with a flash frequency f~ induce an apparent movement perception (o-movement) when slow eye movements are performed across the periodic pattern. The movement appears in the direction of the eye movements when the angular speed VE of the eyes corresponds to the following condition: Ve = k - P ~

.f~ [ d e g ' S-1]

(1)

k is a constant and equals 1 (or exceptionally 2 or 3). The o-movement induces a o - O K N with an average angular speed of its slow phases corresponding to Eq.(1). o - O K N can be elicited when identical foveal or identical extrafoveal stimulus patterns are applied from flash to flash. A considerable random variablility of the flash sequence does not interrupt the o-movement and the o-OKN. Both phenomena can also be elicited by a stimulus pattern with its periodicity hidden in spatial noise and this periodic pattern only becomes visible during the eye movements. It is argued that the o-phenomena are caused by efference copy signals of the gaze control system, which interact with the afferent signals (displacement of visual stimuli on the retina) at different levels of the afferent visual system. One interaction is supposed at a cortical level where the extrapersonal visual space is represented.

Key words: Optokinetic nystagmus - Sigma-movement - Efference copy Visual psychophysics

Visual movement perception might be elicited by two different mechanisms: The signals of retinal stimulus displacement or the motor command signals changing position of gaze (afferent retinal and efferent oculomotor motion

Offprint requests to." Prof. O.-J. Griisser (address see above)

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perception; Jung, 1972, 1973). Hermann von Helmholtz (1866) was probably the first to describe efferent visual motion perception: The attempt to fixate in darkness a longlasting parafoveal afterimage shifts the eyes toward it, but the afterimage "moves" away, keeping an equal distance. Slow pursuit eye movements are elicited if the distance between afterimage and fovea centralis is 3 degrees away from the fovea centralis, intended fixation leads to saccades and an apparent fast shift of the afterimage (Heywood and Churcher, 1971, 1972; Kommerell and Klein, 1971; Kommerell and Tfiumer, 1972). Hermann von Helmholtz assumed that signals controlling eye movements ("effort of will") interact within the central nervous system (CNS) with the afferent signals caused by the displacement of the image across the retina during the eye movements (Sechenow, 1878; Mach, 1886; von Uexkiill, 1920; von Weizs~cker, 1940; Gregory, 1958). The problem of how the signals informing the CNS about the motor outflow (~efference copy" of yon Holst and Mittelstaedt, 1950; von Holst, 1954; "corollary discharge" of Sperry, 1950; and Teuber, 1960) are added to the sensory inflow signal ("reafference") is still not settled, however. In the model of von Holst and Mittelstaedt, a linear subtractive interaction between efference copy and reafference signals is assumed, while MacKay (1973) favors the idea that the corollary discharge leads to a general "informational evaluation" of the input signals, for which no simple quantitative model has been established so far. Filehne's (1922) observations, on the other hand, indicate that during slow pursuit eye movements, complete "cancellation" between efference copy and reafference signals does not exist. In addition, Dichgans et al. (1969) demonstrated that scaling of the afferent and the efferent visual movement perception is different with respect to stimulus speed (Wist et al., 1976). In the light of present knowledge about the interaction of efference copy and reafference signals, psychophysical experiments by which the interaction of afferent and efferent visual motion perception can be quantitatively studied and which are applicable to animal studies are therefore desirable. Lamontagne (1972, 1973) described a new experimental paradigm derived from a model similar to that of von Holst and Mittelstaedt: Apparent visual movement without movement of the retinal image is elicited when the eyes move across a stationary, but intermittently illuminated pattern, which contains a certain amount of spatial periodicity. Lamontagne illuminated a straight row of stationary dots stroboscopically (Fig. lb) and induced pursuit eye movements by fixating a real moving target. As soon as the eye movements reach the appropriate speed, i.e., the speed at which the center of gaze moves from one dot to the next during the dark interval between successive flashes, the row of dots appears to move in the direction of the eye movements and continues to move when the initiating stimulus disappears (Rock and Ebenholtz, 1962; Heywood, 1973; Stoper, 1973; Korn, 1974). This movement illusion induces an optokinetic nystagmus (OKN), which in turn maintains the apparent movement of the row of dots. Hereafter, we will call this apparent visual motion perception sigma-movement and correspondingly, the eye movements sigma-pursuit

S i g m a - m o v e m e n t and S i g m a - O K N in Man

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movements (o-PM) or sigma-optokinetic nystagmus (o-OKN, Behrens and Griisser, 1977, 1978). As will be demonstrated in this report, the quantitative measurements of o-movement and o-OKN provide the possibility for exploring the properties of efferent visual movement perception. More recent experiments have indicated that monkeys (Macaca fascicularis) and rabbits as well exhibit o-OKN. Therefore, the phenomena described in the following are, at least in part, measurable in animals and can be studied by means of the microelectrode technique (Grtisser et al., 1979; Grtisser et al., 1979).

Methods T h e vertical and/or horizontal eye m o v e m e n t s were measured with the head fixed in 12 adult subjects (age 20 to 46 years) by m e a n s of conventional DC-electro-oculography ( E O G ; Jung, 1953; Mackensen, 1959). Sintered Ag/AgCl-plate electrodes were placed at the temporal rim of the left and right orbita (horizontal E O G ) and at the upper and lower rim of the right orbita (vertical E O G ) . T h e signals were fed into DC-ampliflers with remote DC-control and via an optocoupling amplifier displayed on an oscilloscope. The frequency limits of the recording-set were set between 0 and 30 or 0 and 100 Hz. In some of the experiments, the head was not fixed and the head position of the subject was also recorded. For this purpose, the subject wore a helmet fixed on a vertical axis which was connected to a linear potentiometer. The verbal report by the subject was recorded by m e a n s of a microphone and tape-recorder (Fig. la). The subjects wore earphones through which either white noise or music was presented, masking any other auditory stimuli. Visual Stimulation. In the experiments performed from 1973-1977, the visual stimulus pattern shown in Fig. 1 and other stimulus patterns were placed on a transparent screen of opaque lucite placed at 90 or 130 cm distance from the subject's eyes. The screen was fixed to the larger end of a funnel and a stroboscope (van Gogh, A m s t e r d a m ) was positioned at the smaller end. Between the screen and stroboscope, a second, thin transparent screen was placed to obtain h o m o g e n e o u s illumination of the tangent screen seen by the observer. The visual patterns were illuminated by short flashes of about 50 bts half-time; the intensity was varied between 890 and 1150 cd . m -2 which corresponded to a time-average luminance of 0.9 to 1.2 cd . m -2 at 20 flashes . s -1 for the white part of the patterns (Fig. 1 in Behrens and Grtisser, 1978). In the more recent experiments the stimulus pattern was projected by m e a n s of an optical system to a reflecting screen 110 cm away from the subject (Fig. la, flash duration 56 bts, stimulus luminance 4550 cd 9 m -2, corresponding to a time-averaged luminance of the stimulus pattern white parts of 5.1 cd . m -2 at 20 flashes 9 s-l). (a) The flash intensity was constant within the frequency range investigated ( 5 - 1 2 0 flashes . s-l). If not otherwise mentioned, the contrast of the black and white patterns was about 0.7, except for the r a n d o m dot pattern m e n t i o n e d in section 3.7 for which the black/white contrast was about 0.6. The flash frequency fs was controlled by a Wavetek pulse generator providing pulse sequences of a constant frequency and recorded by m e a n s of a photocell placed near the stroboscope bulb. (b) In part of the experiments, the flash frequency was modulated in time according to a sinewave, squarewave, or triangular wave by m e a n s of an amplitude frequency converter. (c) In other experiments, flash series of an average constant flash rate but of a r a n d o m interval variation were applied using a digital computer on line or prerecorded sequences of impulses. The interval distributions were analyzed and characterized by their m e a n and standard deviation (Fig.

6c). D a t a Analysis. The flash sequence was automatically m e a s u r e d during the experiments by a rate meter (Eckmiller and Petsch, 1975). The E O G recordings, the signals from the photocell, head position, and the signals modifying the flash frequency were recorded together with the instantaneous flash rate on paper (Siemens Mingograph or modified Siemens Cardirex), from which further m e a s u r e m e n t s were taken. In more recent experiments, the O K N slow phase velocity was m e a s u r e d automatically.

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F. Behrens and O.-J. Grtisser

Results

1. The Sigma-movement (Lamontagne-effecO When one looks at a straight horizontal line of equally spaced dots or periodic vertical black and white stripes (Fig. lb, c) which are intermittently illuminated at 20 flashes 9 s -1, e.g., one perceives a stationary flickering pattern. As the eyes follow a small target moving horizontally across the flicker pattern at an appropriately adjusted speed, one suddenly perceives the flickering pattern as moving in the direction of the eye movements. The "appropriate speed" is that which shifts the projection of the fovea during a flash interval from one black dot or stripe to the next. After a training period of 2 to 3 min, most of our subjects were able to see the apparent motion (o-movement) of the flicker pattern, even after the initiating target was removed. Recordings of the eye movements indicate that during the apparent motion perception, the subject had an optokinetic nystagmus (o-OKN) with a slow phase pointing in the direction of the apparent motion of the pattern (Fig. 2b). Any spatial inhomogeneity of the dots or stripes larger than 0.1 deg was perceived as a slight irregularity in the otherwise very homogeneous o-movement, as soon as the image of the irregular part of the pattern was seen with the fovea centralis. When a closed figure of equally spaced dots was used, the o-movement was also visible. In the case of a dot circle (Fig. ld), the subject perceived this circle as continuously rotating in the direction of the pursuit eye movements (o-PM). This apparent movement perception was not disturbed by an additional apparent movement seen in t h e region of the circle on the side opposite the center of gaze. That region was perceived as rotating in the opposite direction to the o-PM. This "paradoxical" movement perception did not prevent the subjects, however, from reporting initially that the "whole" circle was moving in the direction of the movement of the foveal and parafoveal regions. The opponent movement was perceived far outside the region of the fovea centralis and therefore in a region of low visual acuity (diameter of the circle 23 or 29 deg, dot diameter 0.42 or 0.51 deg). Circular eye movements were performed by the subjects during the o-PM elicited by the dot circle. These circular eye movements led to sinewave EOG-recordings of the horizontal and vertical E O G with a phase shift of 90 deg (Fig. 3a). Evidently, the information transmitted by the fovea centralis "dominates" the movement perception of the whole circle. When one considers the changes in the image position of the stimulus patterns lb, lc, ld, during the o-movement and the o-PM or o-OKN, one finds considerable differences. With the patterns of Fig. l b and lc, large parts of the retina receive an approximately identical stimulus with every flash as the center of gaze moves during the flash intervals from one bar or dot to the next. Thus, the condition "eye movement without changes in the retinal image position" is more or less fulfilled. With the dot circle, however, only the foveal region receives the same stimulus during each flash, viz., a single dot. During the circular eye movements, the images of all other dots change their relative retinal position from flash to flash; the image of the circle rotates on the retina around the fovea centralis.

Sigma-movement and Sigma-OKN in Man

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When the eye m o v e m e n t velocity was not properly adjusted to the flash frequency, the n u m b e r of perceived dots or stripes suddenly increased by about two to five times and within 0.5-2 s, the apparent motion disappeared and a stationary flickering pattern was seen. Besides dot circles, ellipses or m o r e complex "closed" dot figures as well could also elicit (J-movement and o-PM. In

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these cases the eye m o v e m e n t s also followed the configuration of the dot pattern (Fig. 3b). The o - m o v e m e n t was also seen when the subject was allowed to move his head. The o - p h e n o m e n a are therefore correlated to the gaze control signals and are not pure oculomotor phenomena.

2. Is Foveal Fixation Necessary to Elicit Sigma-movement? Applying pattern lb, we examined whether foveal fixation is necessary to elicit the o - m o v e m e n t and o - O K N . Firstly, the o - m o v e m e n t was generated by pattern l b during foveal fixation. Thereafter, the center of gaze was shifted by a vertical saccade into the " e m p t y field" of the tangent screen up to 15 deg above or below the horizontal row of dots. As a rule, the o - m o v e m e n t continued after

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such vertical saccades and the subject correspondingly had a regular o - O K N during which he kept his fixation point in the empty field while paying attention to the extrafoveally moving row of dots (Fig. 2a). This finding allows the conclusion that the o-phenomena do not depend on foveal fixation and are not interrupted when the stimulus pattern is displaced on the retina. The first part of this statement was corroborated in a further series of experiments. The pattern of Fig. lc was divided into two halves by a horizontal black bar of 5-20 deg width with a horizontal white mid-line of 0.1 deg height (Fig. 4). The subject was asked to fixate this line, but to pay attention (without

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corresponding eye movements) to the vertical periodic gratings placed in the periphery of his visual field above and below the horizontal black bar. By keeping the center of gaze on the horizontal white mid-line (which was also illuminated stroboscopically), o-movement and o - O K N could be initiated by a small target moving along the horizontal line and continued when the initiating target was withdrawn (Fig. 4). A quantitative analysis of the average angular v e l o c i t y ~'re of the eyes during the slow periods of the o - O K N revealed that ~s was somewhat smaller when the stripe patterns of Fig. 4 were seen with the extrafoveal retina, as compared to foveal vision (e.g., at 20 flashes 9 s -1 We ---- 14.0 --+ 0.7 deg 9 s -1 for foveal stimulation, Ve ~-- 13.0 + 0.8 deg 9 s -1 for 7 deg extrafoveal presentation, Ps = 0.75 deg; t-test: p < 0.001).

3. The Effect of Flash Frequency In Fig. 2b, recordings of the eye movements during o - O K N elicited by the stripe pattern of 1 deg period (Fig. lc) are shown. As the subject changed the amplitude of the o - O K N voluntarily, the angular velocity of the eyes during the slow phase of the O K N remained the same. Ve increased linearly with the frequency f~ of the flashes (Figs. 2b, 5b): Ve = k '

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whereby Ps is the period of the stripe pattern und k a constant which was normally 1 or near 1. Depending on the speed of the initiating target and the flash frequency, however, k could also reach the values 2 or 3. In these cases, the fixation point moved from one stripe to the next but one or the next but two,

Sigma-movementand Sigma-OKNin Man

325

during the dark interval between two successive flashes. Extensive studies on Eq. (1) were only performed for k ~ 1. At a given flash frequency, the speed of the o-OKN slow phase could vary considerably (Fig. 5a). This indicates that the "appropriate speed" of the eye movement eliciting o-movement and o-OKN need not be so precise to produce identical or "stabilized" retinal stimulus patterns by each flash. The subjects did not perceive the variability in their o-OKN slow phase velocity and reported seeing smooth movements of a constant speed. Sometimes, the movement perception seemed to be temporarily interrupted by a bright or "dark" flash correlated with a backward saccade. The speed of the circular eye movements during o-PM elicited by the circle of Fig. ld also depended on the flash frequency as described by Eq. (1) (Fig. 5c): fe = k " ?

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f-e is the average sinewave frequency of the EOG, n the number of dots in the circle and the constant k was again 1. In contrast to the fluctuation of V~ during o-OKN, a trained and attentive observer produced circular eye movements which exactly fulfilled Eq. (2). Deviations from Eq. (2) appeared as the subject's attention lowered or the subject performed voluntary saccades across the apparently moving circle (p. 323, 327). The upper frequency limit of fe was about 1.2 Hz and corresponded to the upper following frequency of the eyes elicited by a moving, continuously illuminated spot of light rotating in a circle of the diameter of Fig. ld (23 or 29 deg). Equations (1) or (2) were not affected by reducing the stimulus intensity by neutral density filters up to 2.61~ units.

4. Flash Frequency and Perceived Velocity of Sigma-movement The perceived velocity of the o-movement depended on the flash frequency. The subjects were asked to change a flash frequency fl (set by the experimenter) in such a way that the perceived velocity of the apparently moving stripe pattern (Fig. lc) or dot circle (Fig. ld) doubled. Figure 5d shows the correlation between the initial flash frequency fl and the flash frequency f2 set by the subject (vertical stripe pattern): f2 = _afl + b [flashes 9 s -1]

(3)

The constant a = 2 would be expected if doubling the average velocity of the slow pursuit eye movements Ve (Eq. (1)) led to a doubling in the perceived o-motion velocity. The constant a of Eq. (3) was in three subjects in six experimental sessions on the average 1.3 _+ 0.3. Hence, a doubling of the apparent motion velocity was perceived when the angular speed of the eyeball only increased by 30-35%. Thus, the relative "gain" in the velocity of the o-movement perceived at different velocities of eye movements was about 2/1.3 = 1.54. Within the range investigated (flash frequency 6 to 45 flashes 9 s -1,

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Sigma-movementand Sigma-OKNin Man

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angular speed Ve -< 70 deg 9 s-a), the gain did not change. In testing the validity of Eq. (3) with the dot circle (Fig. ld), the constant a was also significantly smaller than 2 (a = 1.3 _+ 0.3, 8 subjects, 16 experimental sessions; Fig. 5e).

5. Voluntary Saccades do Not Interrupt Sigma-movement As already mentioned, the backward saccades of the o-OKN did not interrupt the apparent motion perception. At low flash frequencies (8 -< fs -< 15 flashes 9 s-a), most of the observers regularly became aware of some of their saccades and frequently reported a short " d a r k " or bright flash and sometimes a horizontal "jitter" or shift in the whole stimulus pattern before the smooth o-movement proceeded. Voluntary saccades in the direction of or perpendicular to the o-movement also did not interrupt the o-PM or o-OKN. The subjects could also gaze around the dot circle during o-PM without interrupting the apparent movement perception (Fig. 3a). These saccades as well did not lead to an apparent shift in the stimulus pattern. Despite the interruption in the smooth pursuit movements by voluntary saccades and the rapid shift of the whole pattern across the retina, the dot circle not only seemed to remain at its location in the extrapersonal space, but also continued to rotate smoothly.

6. The Effect of Different Amounts of Temporal Noise Disturbing the Regular Flash Sequences The velocity distribution of the o-OKN slow phases (Fig. 5a) indicated that without losing the o-phenomena, o-OKN slow phases need not correspond exactly to that speed at which identical retinal stimuli are produced with every flash. This observation led to the hypothesis that o-movement is generated by signals representing an approximate average of the eye velocity and signals of average stimulus position, both averaged over several hundred milliseconds. To investigate the temporal tolerance of the u-effects or the " m e m o r y " of the system responsible for the o-movement in more detail, we applied random interval flash sequences with a variable degree of scatter around the average stimulus interval (Fig. 6c). For a flash rate of 20 flashes - s-* and a coefficient of variation of < 0.12, the vertical stripes of Fig. lc (1 deg period) were still perceived in very regular o-movement. At a coefficient of variation 0.12 < c.v. 0.30, however, the subjects saw the smooth movement interrupted by irregular jerky shifts, but the o-OKN went on (Fig. 6a). Only when the coefficient of variation was larger than 0.36 did the subjects fail to produce a longer lasting o-OKN and were not able to initiate o-movement perception. As Fig. 7 demonstrates, even a fairly high temporal irregularity of the flash sequence only slightly affected the average velocity ~re of the o-OKN slow phase. The random variation of the f a s h sequence and of Ve (expressed as standard deviation or coefficient of variation) increased together. When the dot circle of Fig. l d was illuminated stroboscopically with irregular flash sequences of a constant average rate, smooth o-PM and o-movement were elicited at a coefficient of variation _< 0.1. At higher flash irregularities (0.10
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tested by a n o t h e r series of e x p e r i m e n t s : T h e r e g u l a r flash s e q u e n c e s ( 8 - 3 0 flashes 9 s -a) were i n t e r r u p t e d at r a n d o m times d u r i n g the slow phases of the o - O K N . T h e d u r a t i o n of these pauses was varied. W h e n the flash s e q u e n c e was i n t e r r u p t e d for l o n g e r t h a n 1 s, the o - m o v e m e n t a n d the o - O K N g e n e r a t e d by the vertical stripe p a t t e r n were always i n t e r r u p t e d . Pauses s h o r t e r t h a n 200 ms, however, were always t o l e r a t e d a n d the o - O K N a n d o - m o v e m e n t p e r c e p t i o n w e n t o n s m o o t h l y as the flashes r e a p p e a r e d . Flash pauses b e t w e e n these two limits s o m e t i m e s i n t e r r u p t e d the o - p h e n o m e n a , s o m e t i m e s not. T h e p r o b a b i l i t y t h a t the o - p h e n o m e n a c o n t i n u e d d e p e n d e d on the flash f r e q u e n c y , the flash p a u s e d u r a t i o n a n d the a n g u l a r d i s p l a c e m e n t of the eyes d u r i n g the flash pause (Fig. 9).

8. Experiments with Spatial Noise Patterns A s a next step in exploring the o - p h e n o m e n a , we designed a stimulus p a t t e r n in which the spatial periodicity was h i d d e n by u n c o r r e l a t e d spatial noise a n d only b e c a m e visible w h e n o - p u r s u i t m o v e m e n t s were correctly p e r f o r m e d . The pattern displayed in Fig. le consisted of a regular sequence of vertical stripes of 1.5 deg period. This pattern was composed of identical (correlated) stripes interspersed with uncorrelated stripes, All stripes were produced from a noise pattern of the same average distribution of black and white squares. To produce pattern le, we cut out 32 identical stripes from enlarged photographs of a Julesz random dot pattern (Julesz, 1968) and 32 non-identical stripes from the same patterns. To facilitate the inspection of Fig. le, dots are placed below the correlated vertical stripes, while the uncorrelated spatial noise stripes are placed between the dots. Correlated and uncorretated stripes were of equal width and height. As one can see, such a pattern of correlated and uncorrelated noise stripes does not give the appearance of vertical stripes when the pattern is illuminated continuously. On the contrary, most subjects looking at pattern le first report seeing some horizontal bands in the middle and the upper region of this figure.

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5s Fig. 8. Sigma-pursuit eye movements elicited by the dot circle of Fig. l d illuminated with flashes at an average flash rate of 20 flashes 9 s -a. The temporal noise of the flash sequence was increased in steps (s.d. = 0 ms; c.v. = 0; s.d. = 5 ms, c.v. = 0.10; s.d. = 15 ms, c.v. = 0.3; s.d. = 25 ms, c.v. = 0.5). Slow pursuit eye movements are interrupted by small saccades as c.v. was larger than 0.2. In the lower half of the figure at s.d. = 15 ms and s.d. = 25 ms, the interruption of the o-PM is seen. At s.d. = 15 ms, the subject saw some jitter, while at s.d. = 25 ms, the subject saw a strong irregular jitter of the apparently moving clot circle, whereby the continuation o f the ~J-PM was possible only with great attention and effort on the part of the subject

When Fig. le or similar patterns were illuminated stroboscopically, except for the flicker impression, subjects perceived the same as under continuous illumination 9 When, however, smooth pursuit eye movements were initiated by a target moving at an appropriate speed and medium frequency stroboscopic illumination (15-25 flashes - s-t) was applied, the subject could suddenly see a

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Fig. 9. Sigma-OKN elicited by t deg vertical stripe pattern. The flash sequence was interrupted for different durations. The probability that the o-movement ceased ("sigma-interrupt") is plotted as a function of the pause duration (a) and of ocular displacement during the flash pause (b). Curves are computed integrals of Gaussian distributions (minimal quadratic deviation from the experimental data). In (c) the average duration of flash pauses leading to sigma-interrupt and the average ocular displacement during this flash pause are plotted as a function of flash frequency fs

vertical grid pattern composed of identical stripes moving at a constant speed in front of a "snowstorm" background. At a viewing distance of 90-110 cm, the apparent distance between the background and the moving stripe pattern appeared to be about 2-3 cm. This value was independent of whether the pattern was seen with only one or with both eyes. The apparent distance to the horizontally moving grid was optimal between 12 and 20 flashes - s-r. We tried to illustrate the subjects' impression of pattern le during o-OKN in Fig. If. Being accustomed to seeing the o-phenomena with pattern le, the subjects could voluntarily gaze about the o-moving pattern of correlated stripes, whereby the areas with larger black "figures" were especially prominent landmarks of.

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F. Behrens and O.-J. Grtisser

fixation. Thereby horizontal, vertical, or oblique saccades shifted the image of the whole stimulus pattern across the retina, but the cJ-movement as well as the o-OKN continued. It was also possible to inspect in detail the fine structure of the apparently moving stripes by small saccades superimposed on the slow phase of the o-OKN. When spatial noise was combined with temporal noise, the o-OKN and o-movement were disturbed at somewhat lower temporal noise levels, as compared to the stripe pattern of Fig. lc. The limiting coefficient of variation for an average flash rate of 20 flashes 9 s-1 was found to be at approximately 0.2. Otherwise, the results obtained were similar to those described in section 3.6 (Fig. 6b). As we suspected that the appearance of the apparent stripes in the stimulus pattern of Fig. le during o-OKN was caused by spatio-temporal autocorrelation within the visual system and not by efference copy signals, we performed the necessary control experiment: The subject fixated a stationary dot and the stroboscopically flashed stimulus pattern of Fig. le was moved across the tangent screen at angular velocities corresponding to Eq. (1). Here again, random dot stripes moving in front of a "snowstorm" background became visible.

Comments

Sigma-movement perception and the oculomotor phenomena induced by and maintaining o-movement can be interpreted as being aroused by the interaction of efference copy signals representing the internal feedback of the motor command signals for gaze movement and the signals in the visual system (Lamontagne, 1973). The (J-phenomena confirm the traditional v. Helmholtz notion rephrased in more modern language by Yasui and Young (1975, 1977) that perceived visual motion rather than real visual movement is the effective stimulus for pursuit eye movements. From our present findings, some general properties of a model explaining G-phenomena can be deduced; they are included in the qualitative block diagram of Fig. 10: a) The stroboscopic stimuli during simple ~J-experiments (periodic row of stripes or dots) provide a time-sampled position signal 1~ with respect to the fovea center for the afferent visual system. From a sequence of these signals, a change in position signal V*r = dt~/dt can be computed by movement sensitive visual neurons (e.g., Griisser-Cornehls, 1968). V*r corresponds to the "retinal slip velocity" during normal horizontal OKN. Somewhere in the visuomotor system, the V*r average computed with a time constant of about 0.3-0.5 s is obtained. This assumption is derived from the data obtained with flash sequences containing a certain amount of temporal noise (p. 327). Due to the temporal jitter of the flashes, the retinal position of the successive images is shifted in the direction of the eye movements or in the opposing direction. The system leading to G-movement does not seem to evaluate the individual but rather the time-averaged retinal position or position change V*r of the apparently moving stimulus pattern. For gaze control the signals providing V*r

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afferent visual afferent visual systemA systemB I ~ e ~ i ' t visual field central visual I~1.~ representation system 1

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interact with efference copy signals. Some of our experimental data indicate that V*r might be 0 (Fig. 5c), while under all experimental conditions in which the constant k of eq. (1) is somewhat smaller than 1 (Fig. 5b, flash frequencies > 20 flashes - s-l), V*, is a non-zero apparent retinal slip velocity. b) Efference copy and afferent visual signals might interact simultaneously at different levels within the CNS. At a subcortical niveau shch an interaction might occur in visuovestibular neurons of the vestibular nuclei (e.g., Waespe and Henn, 1977), in visuovestibular neurons of the cerebellum (Ansorge and Griisser-Cornehls, 1977; Simpson and Hess, 1978) or in the polymodal neurons of the nucleus praepositus hypoglossi of the brain stem (e.g., McCrea et al., 1979). An interaction of visual signals and gaze control signals also has to be postulated, however, for a cortical level beyond retinotopic projection. A trained subject can easily gaze about the dot circle (Fig. ld) and not interrupt o-phenomena by his saccades, despite the fact that the pursuit eye movements changed direction after the saccade. During o-movement, the apparently moving stimulus in space and not its retinal image is pursued. This statement extends Lamontagne's original paradigm and is further corroborated by the more recent observation that horizontal o-movement and o-OKN are elicitable by stroboscopically illuminated random dot stereograms in which vertical stereostripes (generated on the "cyclopean retina") are visible (Adler and Grtisser, 1979). The o-phenomena observed with the noise-stripe pattern of Fig. le are also in accordance with this notion (p. 330, 331). In these experiments, the subjects were able to gaze about the apparently moving random dot stripes by means of horizontal, vertical or oblique saccades. Hereby, the stripe pattern and its apparent movement, both "generated" in the brain, were maintained,

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despite the fact that the image shifted across the retina during each saccade. Thus, the hypothesis that interaction between afferent visual signals and efference copy feedback signals are also present at a cortical level where the visual stimulus in space is represented and not the retinal location became plausible (Fig. 10). The parietal lobe is a candidate for such an interaction. c) Finally, the question of whether eye position signals from peripheral mechanoreceptors (inflow hypothesis) might play a role in o-phenomena cannot be answered to date. Since the early findings of Kornmiiller (1931) with experimental palsy of the external eye muscles and repeated clinical observation it is known that a sudden complete palsy of the external eye muscles leads to apparent movement of the stationary visual world whenever the subject intends to move his paretic eye in the direction of the paretic muscles. Therefore, one could assume that the efference copy signals would be sufficient to explain the perceived movement in the afterimage experiments mentioned in the introduction. More recent experimental data (Siebert, 1954; Brindley et al., 1976; Stevens et al., 1976), however, indicate that with pharmacological paresis of all external eye muscles (curarine or succinylcholine experiments), displacement without apparent movement of stationary visual signals is seen during goal-oriented voluntary eye movements. Apparent movement in the direction of the eye movements regularly occurs when the paresis is incomplete. These observations indicate that besides efference copy signals and afferent retinal signals, signals from mechanoreceptors (sclera, eye muscle or tendon receptors) might also play a role in visual movement perception. They are therefore considered for a model explaining o-phenomena (Fig. 10). In summary, we think that the experimental data available to date on o-phenomena and efferent visual movement perception suggest that a hierarchy of feedback mechanisms might be present by which the afferent signals and efference copy signals interact in the control of gaze movement and visual movement perception. In addition, predictive mechanisms present in the control system of pursuit eye or gaze movements also play a role in o-phenomena. The interaction of efference copy and reafference at a low visual center as postulated by v. Holst (1954) might be only one of several mechanisms leading to apparent movement in the o-experiments or to stabilization of the visual world under normal viewing conditions. On the other hand, the interaction at higher cortical regions where the external visual space is represented, might be close to a mechanism postulated by MacKay (1966, 1973) for which a continuous reevaluation of afferent signals in the informational context of performed movements is assumed.

Acknowledgements. The work was supported by a grant of the Deutsche Forschungsgemeinschaft (Gr 161). The careful technical assistance of Mrs. J. Dames is gratefullyacknowledged. We thank Mr. H. Dannenberg, Mr. J. Lerch, Mr. J. Petsch, and Mr. P. Rickmeyer for their help in mechanical and electronic problems. The circuit design for the device measuring the OKN slow phase angular velocitywas kindlyprovided by Mr. Corti from the Department of Neurology,Universityof Z~rich.

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Received March 1, 1979