Characteristics of" anti" saccades in man

between 80 ms and 120 ms (Express saccades) followed by another ... were then left without a visual stimulus for 200 to 500 ms before a ...... Res 27:1745 1762.
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Exp Brain Res (1992) 89:415 424

nResearch (~) Springer-Verlag1992

Characteristics of "anti" saccades in man B. Fischer and H. Weber Department of Neurology and Neurophysiology, University of Freiburg, HansastraBe 9, W-7800 Freiburg, Federal Republic of Germany Received March 7, 1991 AcceptedNovember 21, 1991 Summary. Four subjects all made large numbers of Express saccades in the normal gap task were instructed to make saccades in the direction opposite to the side where a visual stimulus appeared ("anti" task). Gap and overlap trials were used. Saccadic reaction time (SRT), velocity and amplitude of the corresponding eye movements were analysed and compared to those of saccades made in the normal task. The velocity of "anti saccades" was found to be slightly (up to 15%) but significantly slower in two subjects. The distributions of SRTs in normal gap tasks show a small group of anticipatory saccades (with SRT below 80 ms and slower velocities) followed by a group of saccades with fast reaction times between 80 ms and 120 ms (Express saccades) followed by another large group ranging up to 180 ms (regular saccades). In the gap anti task there are anticipatory saccades and saccades with SRTs above 100 ms; Express saccades are missing. The distribution of SRTs obtained in the overlap anti task was unimodal with a mean value of 231 ms as compared to 216 ms in the normal task. The introduction of the gap therefore clearly decreases the reaction times of the anti saccades. Control experiments show that the delay of anti saccades is not due to an interhemispheric transfer time but must be attributed to the saccade generating system taking more time to program a saccade to a position where no visual stimulus appears. These data are discussed as providing further evidence for the existence of a reflex-like pathway connecting the retina to the oculomotor nuclei mediating the Express saccade.

Key words: Anti saccades - Saccadic reaction time Express saccades Human

Introduction The preparation and initiation of visually guided saccades is still not fully understood. It is known that there exist at Offprint requests to.

B. Fischer

least two visual-to-oculomotor pathways. One includes the superior colliculus, the other the frontal eye field (Schiller et al. 1979, 1980). However, other cortical and subcortical structures such as the striate cortex, the parietal cortex, or the pulvinar may also contribute certain details to the complete preparation of a visually guided saccade. Whereas the pulvinar seems to play a minor role (Robinson et al. 1986), striate cortex is needed to generate Express saccades (Boch 1988), but not to generate just any saccade (Mohler and Wurtz 1977). The same is true for the superior colliculus (Schiller et al. 1987). The minimum latency of a visually guided saccade is in the order of 70 ms in monkey (Fischer and Boch 1983) and about lOOms in man (Fischer and Ramsperger 1984); other authors found a minimum latency of 110 to 130 (Kalesnykas and Hallett 1987b). Still others found a surprisingly early transition in the normalized peak velocity versus latency scatter plot at about 30 to 70 ms, but they do not believe that this demarcates the minimum latency for a visually guided saccade (Smit and van Gisbergen 1989). The extremely short latency saccades form - in most subjects - a clearly discernable first peak in the distribution of saccadic reaction times. The saccades contributing to this peak, between 80 and 120 ms, are called Express saccades. To obtain Express saccades, striate cortex and the superior colliculus must be intact and it has been argued that these two structures are parts of a pathway by which the optomotor system can react in a reflex-like way to the sudden occurrence of a visual target, given this pathway is disinhibited at the time the target appears in the field of view (Fischer 1987). This interpretation implies that the occurrence of Express saccades depends critically on the physical event of the target's appearance, which elicits the corresponding responses of the cells in several visual structures; in the retina, the lateral geniculate body, the superior colliculus, striate, and prestriate cortex. It has in fact been shown that Express saccades are absent if the target stimulus is present all the time, the saccade being elicited by the command of fixation point offset (Boch and Fischer 1986). It remains,

416 however, still o p e n whether or n o t the "Express way" can be a c t i v a t e d a n d utilized b y the onset of a visual stimulus which is n o t the target of the required saccade, b u t the a p p e a r a n c e of which is the physical c o m m a n d the cue to m o v e the eye. A special case of such a s p a t i o - t e m p o r a l a r r a n g e m e n t is given b y the anti saccade t a s k (Hallett 1978, H a l l e t t a n d A d a m s 1980), in which the subject is i n s t r u c t e d to m a k e a saccade into the direction o p p o s i t e to the side where the visual stimulus appears. This p a r a d i g m has been used in patients with frontal lobe lesions: they could rarely prevent their eyes from m o v i n g to the stimulus (rather t h a n to the o p p o s i t e side) ( G u i t t o n et al. 1985). The latencies of these erratic saccades were in the o r d e r of 150 ms. T h e subjects were then left w i t h o u t a visual stimulus for 200 to 500 ms before a small p a t t e r n a p p e a r e d . T h e frontal lobe patients - n o t the n o r m a l c o n t r o l subjects then m a d e saccades to the p a t t e r n after a l m o s t c o n s t a n t a n d extremely short r e a c t i o n times of 100 ms. These saccades could be identified with the Express saccades. The first erratic saccade was largely a b s e n t in h e a l t h y subjects, w h o can easily follow the instruction to m a k e anti saccades. Anti saccades of n o r m a l subjects have p r o l o n g e d latencies ( D o m a a n d H a l l e t t 1988). H o w e v e r , these a u t h o r s m a d e no special a t t e m p t to investigate the occurrence of Express saccades in the anti task experiment, neither did they analyse the direction errors. D i r e c t i o n errors in the anti task are c o r r e c t e d earlier when their size is large a n d later when they are small ( K a l e s n y k a s a n d H a l l e t t 1987a). A n o t h e r type of n o n - t a r g e t saccades are the anticip a t o r y or predictive saccades. Their velocity is smaller t h a n for n o r m a l saccades a n d they can be identified on the basis of their velocity-latency t r a n s i t i o n function. The t r a n s i t i o n h a p p e n s quite early, certainly below 1 0 0 m s (Smit a n d van G i s b e r g e n 1989) while Express saccades occur b e y o n d this point. This shows that they are clearly visually guided saccades. In the present study we therefore used the g a p p a r a digm (which favours the occurrence of Express saccades) with two instructions: n o r m a l - anti. W e used subjects who were t r a i n e d in the n o r m a l g a p p a r a d i g m a n d therefore m a d e large a m o u n t s of Express saccades right at the b e g i n n i n g of the e x p e r i m e n t (Fischer a n d R a m s p e r g e r 1986). The o v e r l a p p a r a d i g m was also used for c o m parison. As a c o n t r o l we a p p l i e d the n o r m a l saccade t a s k a n d two other " n o n - t a r g e t " tasks: (i) a stimulus a p p e a r e d in one q u a d r a n t of the visual field (say the u p p e r right) a n d the i n s t r u c t i o n was to m a k e a saccade to the same hemifield b u t in the o t h e r (lower right) q u a d r a n t (oblique task); (ii) a stimulus a p p e a r e d on one side a n d the instruction was to m a k e a saccade half as large as the stimulus eccentricity, t h e r e b y u n d e r s h o o t i n g the stimulus by a b o u t a factor of two. I n all cases the saccades were below 10 deg in size, which is well within the n a t u r a l o c u l o m o t o r range ( F r o s t a n d P 6 p p e l 1976). The analysis of the latency, a m p l i t u d e a n d velocity shows t h a t n o n t a r g e t - s a c c a d e s are g e n e r a t e d in a different way t h a n n o r m a l saccades. Express saccades are a b s e n t o r largely reduced in n u m b e r if the saccades are a i m e d at a spatial p o s i t i o n which does n o t c o r r e s p o n d to the " n a t u ral" goal for the saccade.

Methods Four subjects participated in most of the experiments, all members of the department. Some control tests were carried out with three or two of them. All subjects made Express saceades in a normal gap task. They were then trained in the anti task for 10 15 days (see Results). Although pooled data for several subjects is shown, it is representative for all individual subjects included. Subjects were comfortably placed on a chair with their heads stabilized by a chin rest 57 cm in front of a colour monitor. Their horizontal eye movements were recorded by a simple infrared reflection method (LED and photo cells mounted on a spectacle frame) with a precision of 0.2 deg and with a linear range of more than 8 deg to either side of the fixation point (Gauthier and Volle 1975). To measure oblique saccades the photo cells were adjusted obliquely such that the signals for the eye movements to the different stimuli used were of different polarity. Quantitative measurement of the oblique saccade size was not attempted. The central fixation point (6 min of arc) and the stimuli (0.25 deg of arc) - were generated on a computer RGB colour display unit (Nec Multisync II) using a frame rate of 80 Hz. The green background (20 x 15 deg) had a luminance of 19 cd/m 2, the red fixation point and the white stimuli had luminances of 60 cd/m 2. Saccadic reaction times (SRT) as measured from the actual target onset time (as determined by the frame synchronization) to the beginning of the electronically detected saccade (velocity threshold detection) were displayed on line as a histogram (bin---10 ms) and could be reconstructed offline using bins of 10 ms or 5 ms. All other parameters were determined off line on the basis of the A-D-converted eye position signal stored on disc (sample time 1 ms). 200 saccades were measured in one session, 100 for each stimulus condition. The subjects' task was to fixate the central fixation point for 2 s until the visual stimulus appeared randomly either 4 deg to the right or left. In the anti task the instruction was to make a saccade to the opposite side. In the normal task the instruction was to look at the stimuli. For further classification two other tasks were used: in one the subjects had to make saccades to the same side (constantly left or constantly right) while the stimulus occurred randomly at the left or right, such that some saccades happened to be normal and others happened to be anti saccades. In still another control experiment the stimulus positions were randomized between 4 deg obliquely up and 4 deg obliquely down in the same hemifield (oblique task). The subjects were instructed to aim the saccades to the other quadrant in the same hemifield. In a final control test the targets appeared again at the right or left but the instruction for the subjects was to make saccades about half as large, i.e. clearly undershooting the target position (half-way task). Two paradigms with different timing of the stimuli were used: in gap trials (GAP) the fixation point disappeared 200 ms before target onset, in overlap trials (OVL) the fixation point remained on until the end of the trial. The data were analysed as to the reaction time (SRT), amplitude (A), and maximum velocity (V) of the saccades. To compare the velocities of saccades of different sizes we computed the normalized velocity defined by the linear regression line through the scatter plot of velocity versus amplitude. If the equation v = c" A + d represents the regression line the normalized velocity is given by vn=vl/v, where v~is the velocity of the saccade under consideration. Using a 2 term polynomial fit we obtained the same results. The details of this analysis are given in the appropriate sections of the Results.

Results The first p a r t of the results will deal with the r e a c t i o n times, the o t h e r p a r t with the velocity a n d a m p l i t u d e of the saccades.

417

Reaction time Gap paradigm. The main parameter analysed in this study was the saccadic reaction time (SRT). It will turn out that as in earlier studies the distribution of SRTs provides the basis of a distinction between anticipatory, Express, and regular saccades. All subjects participating in this study produced a clear peak of Express saccades in the normal gap task with the target position randomized between _ 4 deg, as can be observed in the individual SRT distributions given in Fig. 1A. In Fig. 1B the distributions from the 4 subjects are-sampled. The upper panel was obtained by pooling the individual data obtained in the normal gap paradigm shown in Fig. 1A. Note that pooling of the data did not destroy the multimodality of the individual distributions: four peaks can be seen in the summed spectrum: the first peak is small and contains values between 25 and 80 ms; the second peak represents the Express saccades and contains values between 80 and 120 ms; the third peak represents the fast regular saccades with values between 120 and 180 ms; and the last small peak at about 200 ms (sometimes not very clearly separated) contains the slow regular saccades. For the further analysis fast and slow regular saccades will be treated as one group. The second and third panel of Fig. 1B show reaction times obtained in the gap anti task (same subjects, same physical conditions). Saccades contributing to the second panel were made unvoluntarily to the stimulus rather than to the opposite side and therefore are assigned "direction errors" in the sense of the anti task. Note that their SRTdistribution very closely resembles that of the normal saccades (upper panel). This is confirmed by the two sample two-tailed T-test of the SRT mean values ( > 8 0 ms), which were 125.2_+32.3 ms in the normal task and 123.5 _+50.7 ms for the direction errors in the anti task, with a p-value of 0.6. The anti saccades show a small peak of values below 80 ms and a broad distribution ranging from just above 100 ms to 300 ms. The basic observation is that the peak of Express saccades at 100 ms, so clearly present in the upper panel (normal task) is completely absent in the third panel (anti task), whereas the Express saccades are again clearly present in the second panel (direction errors of the anti task). The difference in SRTs as obtained in the normal and the anti task is evident (p 0.9) while those for SRTs > 8 0 m s showed a highly significant difference (p •

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Fig. 3. Saccadic reaction times in normal (upper) and anti conditions (lower). Pooled data of three subjects (HW, MB, HK). Left side: data collected when both target position and saccade direction were kept constant. Right side: saccade direction was constant, but stimulus direction was randomized. Note: under neither anti condition was there an Express peak

saccades which were followed by a second saccade opposite in direction of the primary saccade. Mean amplitudes of the primary saccades were 6.82_ 1.11 deg to the left and 5.26 + 1.06 deg to the right. In the latter cases we assume that the subjects unvoluntarily made saccades directed to the visual stimulus and then made a second saccade back to the 4 deg location. The lower panel clearly resembles the pattern of the upper one, whereas the middle panel contains some Express saccades; the majority of values, however, fall clearly beyond 135 ms and up to 275 ms.

Overlap paradigm. Since

in overlap trials, where the fixation point remains on, saccadic latencies are rather long, the question arises whether or not anti saccades under this condition would still need an extra time. The upper panel of Fig. 6 shows the SRT-distribution obtained with the overlap normal task, the lower panel that obtained with the overlap anti task. The comparison reveals that anti saccades have latencies between 175 and about 375 ms, whereas the distribution of normal saccades starts at 140 ms and ranges up to 350 ms. The corresponding mean values of 216 ms for the normal saccades and 231 ms for

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Fig. 4. Data from the modified normal (upper) and the modified anti task (lower two). Pooled data of two subjects (HW, BF). Even though the targets appear in the same hemifield into which the anti saccades are being made (lower panel) there is no distinct peak at 100 ms as there is in the normal control condition (upper panel)

the anti saccades were statistically different (p