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Motor Systems NeuroReport NeuroReport 10, 2665±2670 (1999) THE gain of visually triggered saccades depends on orbital position. Centrifugal saccades have smaller gains and are slower than centripetal saccades elicited by the same target amplitude. We determined whether internally triggered saccades, e.g. scanning or memory saccades, exhibit the orbital position dependency evident in visually guided saccades. The search coil technique was used to record eye movements of healthy subjects while they performed horizontal 12.58 saccades under three paradigms (gap, scanning and memory saccades). Orbital position in¯uenced externally triggered gap saccades but not the gain or peak eye velocity of scanning or memory saccades. These ®ndings do not support the idea that position dependency caused by orbital mechanics is compensated for at the level of the common brainstem burst generator. Instead our results are consistent with the view that cortical output re¯ects the differences evident in the gain of visually triggered centrifugal and centripetal saccades. NeuroReport 10:2665±2670 # 1999 Lippincott Williams & Wilkins. Key words: Centrifugal; Centripetal; Craniotopic; Orbital eye position; Orbital mechanics; Retinotopic Introduction The gain of visually triggered saccades partly depends on the position of the eye at the start of the saccade. Centripetal saccades are signi®cantly larger than centrifugal saccades. In addition, the peak eye velocities of centrifugal saccades . 158 are smaller than those of centripetal saccades of the same size [1,2]. This position dependency may be caused by the elastic force of the extraocular muscles and tendons which tend to pull the eyeball back to the primary position near straight ahead [3]. The elastic force assists centripetal saccades and opposes centrifugal saccades. The neuronal signal driving the eye muscles must compensate for the effect of the elastic force on the eye. An incomplete compensation for this force could explain the gain and velocity differences between centrifugal and centripetal saccades. Compensation for orbital position is thought to occur in two regions of the cerebellum: the oculomotor vermis and the caudal fastigial nucleus (CFN). Lesions of these areas cause an abnormally large difference in the gains of centrifugal and centripetal saccades [4,5]. The CFN receives input from the oculomotor vermis and projects to the premotor network in the paramedian pontine reticular formation, which is common to all saccades, i.e. the brain stem burst generator. Thus, current evidence suggests that visually triggered saccades are depen0959-4965 # Lippincott Williams & Wilkins Orbital position dependency is different for the gain of externally and internally triggered saccades Thomas Eggert, Frank Mezger, Farrel Robinson1 and Andreas StraubeCA Department of Neurology, Ludwig-Maximilians University, 81377 Munich, Germany; 1 Department of Biological Structure, University of Washington, Seattle, USA CA Corresponding Author dent on eye position because the oculomotor vermis and CFN provide incomplete compensation via the brain stem burst generator. We could infer more about the origin of position compensation if we knew more about the position dependency of internally triggered saccades, such as memory and scanning saccades. There is increasing evidence that different circuits in the cerebral cortex are responsible for generating externally (visually triggered or re¯exive) saccades and internally triggered saccades [6]. Re¯exive saccades probably depend mostly on pathways from the posterior parietal cortex to the superior colliculus via the posterior part of the internal capsule. Internally triggered saccades probably depend more on direct pathways from the frontal or supplementary eye ®elds to the brain stem [6,7,8]. Currently no data are available from normal subjects which indicate if position dependency is the same for externally and internally triggered saccades. There are some signs that the cerebellum may be less involved in internally triggered than externally triggered saccades. Straube et al. [9] examined a patient with a large cerebellar midline lesion due to tumor surgery who showed a pronounced hypermetria for the re¯exive saccades but normal internally triggered scanning saccades. This suggests that the position dependency may be stronger in internal saccades. In this study, we investigated whether different types Vol 10 No 12 20 August 1999 2665 NeuroReport of saccades exhibit different position dependency in healthy subjects. Materials and Methods Six healthy subjects (ages 27±40 years, one female and ®ve males) participated in the study. Each subject was recorded at least twice on different days. Subjects were seated in front of a screen at a distance of 1.40 m in darkness. A red laser spot, which was controlled by a mirror galvanometer (General Scanning G120D, USA), served as visual target. Eye movements were recorded with the magnetic search coil technique. A 1.5 3 1.5 3 1.5 m three-®eld coil was used (Remmel System, USA) and a 2-dimensional scleral coil (Scalar, Delft, Netherlands) was attached to the right eye of the subjects. Eye movement signals were sampled at 1 kHz and were stored on the hard disk of the computer. For calibration of the eye movements a thirdorder polynomial calibration was applied. In each session intervals of stable eye positions of .300 ms were collected from the late ®xation periods (within a period of 500 ms immediately before the target stepped). These ®xations were used to compute the coef®cients of the polynomial. This method provided a reliable calibration within the examined range of horizontal eccentricities ( 258). Saccades were detected and marked on the basis of velocity criteria. All movements with peak absolute eye velocity . 1008/s were analyzed. The start and the end of the saccade were de®ned as the points where the saccade velocity rose to or dropped below, respectively, 10% of the peak eye velocity. Thus, the computer automatically marked the onset, the end, and the peak velocity of the saccades. From these marks the gain (ratio eye to target amplitude), the saccade duration, the peak velocity, and the skewness of the velocity pro®le were calculated offline. The skewness was computed according to the method of Van Opstal and Van Gisbergen [10]; positive values indicate a deceleration period longer than the acceleration period. In all paradigms the subject had to perform saccades to one of ®ve target locations that were at the center, 12.58, and 258 on the horizontal meridian at eye level. The sequence of target locations was a pseudo random sequence with length of 200 and was identical for all experiments. We elicited three different types of saccade. (1) Gap saccades were elicited when the ®xation spot was switched off and 100 ms later the laser spot reappeared at the new target position. (2) Scanning saccades were elicited when the subject could always see the ®ve targets. The sequence of the targets to be scanned was indicated by a slight increase of the 2666 Vol 10 No 12 20 August 1999 F. Eggert et al. luminance of the next target. (3) Memory guided saccades were elicited when the next target was ¯ashed for 50 ms while the ®xated target stayed on. After a delay period of 1 s the ®xated target was switched off, and the subject had to perform a saccade to the remembered position of the brie¯y illuminated target. After this saccade, the laser spot reappeared at the location where it had brie¯y appeared. The new trial started from this position 2 s later, an interval which was suf®cient for corrective saccades. The latency of the saccade was de®ned as the interval between the blanking of the ®xation spot and the start of the primary saccade (gap and memory-guided saccades) or the increase of the luminance of the target location and the start of the saccade (scanning saccades). Each subject was examined in two recording sessions. In each session we ®rst elicited 100 gap saccades and then 200 scanning or memory-guided saccades. Finally, we recorded 100 gap saccades again to measure the effect of fatigue on our measurements. We discarded all saccades that crossed the midline from our analysis. Our statistical comparisons always used a signi®cance level of 0.01. Results The data were divided into two saccade directions and ®ve different starting positions (08, 12.58, 258).This resulted in eight subgroups because saccades starting at 258 were in only one direction, i.e. centripetal. In each of these eight resulting subgroups, the median of the number of saccades analyzed per subject was 27 gap saccades, 17 memory saccades, and 10 scanning saccades. Figure 1 shows for all subjects the dependence of the gain, the peak velocity and the skewness on initial eye position for gap saccades, memory, and scanning saccades with an amplitude of 12.58. We discuss each type of saccade separately. Gap saccades: As can be seen in the left-most column of Fig. 1, there was a signi®cant correlation of the eye position and the gain (leftward saccades: r 0.7, p , 0.001; rightward saccades: r 0.7, p , 0.001) with centripetal saccades larger than centrifugal saccades. A similar highly signi®cant relationship was also seen for the peak velocity, which was slower for the centrifugal saccades than for the centripetal saccades (leftward: r 0.79, p , 0.001; rightward: r ÿ0.78, p , 0.001; leftmost panel, Fig. 1). Table 1 lists the average gain and the average peak velocity of all subjects for saccades to 12.58 targets at larger orbital eccentricities (i.e. saccades between 12.58 and 258), where the difference be- Dependency of saccades on orbital position A Gap NeuroReport Memory Scanning 140 130 Gain (%) 120 110 100 90 80 70 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 B 600 Peak velocity (deg/s) 500 400 300 200 100 C 0.5 0.4 Skewness 0.3 0.2 0.1 0.0 20.1 20.2 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 218.75 26.25 0 6.25 18.75 FIG. 1. The individual means of the six subjects (open circles) as well as the group means ( s.d.) for saccades starting at the center (08), at 12.58 or at 258 eccentricity on the left (negative values) or on the right (positive values) with petal direction (gray symbols) or fugal direction (dark symbols) for the gap, memory, and scanning saccades are presented. For more clarity the mean eccentricity of the saccades (18.758 and 6.258) are plotted slightly offset from each other. (A) Saccadic gain plotted against orbital eye position. (B) Peak eye velocity against orbital eye position. (C) Skewness against orbital eye position. The linear regression slopes of the gain and peak eye velocity were much steeper for the gap saccades than for the memory and scanning saccades. These differences were highly signi®cant. tween centrifugal and centripetal saccades was largest. For the skewness the correlation with orbital position was not signi®cant (leftmost panel Fig. 1C; Table 1). Memory saccades: In contrast to gap saccades, memory saccades showed no position dependency. There was no signi®cant correlation between gain and eye position (leftward: r ÿ0.27, p , 0.2; rightVol 10 No 12 20 August 1999 2667 NeuroReport F. Eggert et al. Table 1. Values (mean s.d.) of the 12.58 saccades between 12.58 and 258 eccentricity Condition Petal abduction Petal adduction Fugal abduction Fugal aduction Gain (%) Gap Scanning Memory 102.9 5.8 95.2 2.5 85.9 5.2 103.4 8.8 89.8 6.9 85.2 8.3 87.8 3.0 97.6 2.8 93.6 20.7 86.7 6.1 93.2 4.3 91.5 7.7 Velocity (8) Gap Scanning Memory 431.4 26.9 415.9 25.2 309.5 29.9 401.9 37.4 354.3 39.7 268.4 39.7 316.3 39.9 320.4 74.8 230.8 64.9 301.6 26.6 298.4 45.3 237.7 48.8 Skewness Gap Scanning Memory 0.12 0.04 0.12 0.07 0.29 0.08 0.04 0.1 0.08 0.08 0.24 0.1 0.02 0.1 0.13 0.14 0.31 0.14 ÿ0.016 0.06 0.01 0.1 0.19 0.15 ward: r 0.18, p , 0.38, middle panel, Fig. 1A). The dependency of the peak velocity on the orbital position was less than that for gap saccades (leftward: r 0.26, p , 0.21; rightward: r ÿ0.57, p , 0.004; middle panel, Fig. 1B). Finally, skewness did not show a correlation with the orbital position (leftward: p , 0.6; rightward: p , 0.79; middle panel, Fig. 1C). Scanning saccades: Like memory saccades, but in contrast to the gain differences evident in the gap saccades, there was no consistent correlation between gain and orbital position (leftward: r ÿ0.18, p , 0.4; rightward: r 0.47, p , 0.02; rightmost panel, Fig. 1A). The small tendency observed for rightward saccades was in the direction opposite to that for gap saccades. There was a slightly stronger in¯uence of the orbital position on the peak eye velocity than on memory saccades (leftward: r 0.5, p , 0.02; rightward: r ÿ0.6, p , 0.003; rightmost panel, Fig. 1B). The skewness showed no signi®cant correlation (leftward: p , 0.2, rightward: p , 0.85; rightmost panel, Fig. 1C). The overall mean of the latency of the primary saccade was 114 ms in the gap paradigm, 233 ms in the memory paradigm, and 585 ms in the scanning paradigm. Differences between the conditions: It is critical to determine if the differences in position dependency of the different types of saccades are signi®cant. To test this, we compared the slopes of the relationships between initial position and gain, velocity and skewness for the three types of saccades tested. The initial position vs gain slopes for gap saccades were signi®cantly different from those for memory ( p , 0.003) and scanning saccades ( p , 0.0001). Thus, position dependency is signi®cantly higher for the gain of gap saccades than for the gain of either type of internally guided saccades (Fig. 1A). In contrast, there was no signi®cant difference between the three 2668 Vol 10 No 12 20 August 1999 types of saccades we tested in the position dependency of peak eye velocity or skewness. In summary, the gain, but not peak eye velocity or skewness, of gap saccades depends more on initial eye position than does the gain of memory and scanning saccades. Discussion Our data for the visually guided re¯exive saccades (gap saccades) are in agreement with previous published results [1,2,11] and show that there is strong in¯uence of the orbital position on the amplitude and velocity of the saccade. Centrifugal saccades generally have a smaller gain and a slower peak eye velocity than centripetal saccades of the same desired amplitude. This difference may be related to the mechanical properties of the tissue around the globe in the orbit. The elastic force of the orbital tissue tends to pull the eye toward a primary position [3]. Thus, this force is larger at eccentric orbital position and should add to the forces obtained by the muscle activation, giving a net result of a higher acceleration and peak velocity for saccades towards the primary eye position. Pelisson and Parblanc [12] propose another explanation. They speculate that the force accelerating the eyes (agonist force minus antagonist force) is highest at eccentric orbital positions, because here the step activity of the agonist is largest and the antagonist is deactivated during a saccade. Our ®ndings that there is no centrifugal±centripetal difference in the gain of internally triggered scanning and memory-guided saccades cannot be explained by such an effect. A position dependency of the signals to the extraocular muscles would, contrary to our ®ndings, induce the same centripetal±centrifugal differences in gain for all types of saccades. The variability of internally triggered saccades Dependency of saccades on orbital position cannot explain the absence of centrifugal±centripetal gain differences. The gain of scanning saccades showed less variability than did the gain of gap saccades. Even memory saccades were only slightly more variable than gap saccades. Functional consequences: Our results are not consistent with the idea that the dependency of saccade gain on initial eye position is compensated for at the level of the brainstem burst generator. If this were true, we would expect that the difference in the gain of centrifugal and centripetal saccades would be the same for all types of saccades. This is clearly not the case. Our results are also not compatible with our initial hypothesis that the cerebellum is less involved in the compensation of position dependency of internal saccades. That the gap saccades show a dependency on position and scanning/memory saccades do not, implies that the compensation for initial eye position is done upstream from the brain stem burst generator where the saccade signals are still handled by separate channels. Our results do not reveal whether the position dependency of gap saccades originates with orbital tissue and/or the position dependency of the signals to the extraocular muscles. Whatever the origin of position dependency, the signals diving the burst generator must be different to explain our results. In contrast to the gain the position dependency of the peak velocity and the skewness was nearly identical for all saccade types. This indicates that the position dependency of the peak eye velocity does not have the same origin as the position dependency of the saccade amplitude and that the coupling between both is not fully explained by the well known amplitude±velocity relationship of saccades, i.e. the main sequence. Peak velocity is not exclusively determined by the saccade amplitude but also by the saccade type, the initial position, and the direction. This is supported by our results concerning the reduced peak velocities in the memory task which are in agreement with the results of Smit et al. [13] and by the observation that scanning saccades with identical amplitudes but different positions and different directions have different peak velocities (see Fig. 1). Previous evidence indicates that position-sensitive signals are present in several locations in the brain upstream from the brainstem burst generator. The brain stem burst generator receives direct input from the superior colliculus. Eye position in¯uences the activity of presaccadic neurons in the superior colliculus of monkeys in such a way that the peak ®ring rate of the neurons is changed [14]. Whether this position dependency of the neuronal discharge re¯ects the cortical input or is a consequence of NeuroReport positional feedback signals from the nucleus prepositus hypoglossi to the superior colliculus is not clear. There is also increasing evidence that the discharge of neurons in the lateral intraparietal sulcus and in some other areas is in¯uenced by the orbital eye position [15±21]. Microstimulation at different locations of the intraparietal sulcus evoked saccades with similar direction but different amplitudes depending on the eye position (vector saccades) [15]. Apparently the dependency of these saccades on the orbital eye position was not completely compensated. In contrast, at distinct locations (e.g. the ¯oor of the sulcus) the evoked saccades were independent of the starting position (goal-directed saccades) and convergent toward a goal in head-centered space (compensating for the orbital position) [15]. Neuronal network models have been suggested to explain how a combination of visual information in retinotopic coordinates and eye position signals can form a representation in head-centered coordinates [16]. In these networks the vector saccade neurons represent an earlier step of the saccade processing, the goal directed saccade neurons a later step. The superior colliculus receives projections from the lateral intraparietal area as well as from the frontal eye ®eld [22]. Thus, a possible explanation for the differences in the compensation for the orbital position we observed is that the visual triggered re¯exive saccades, which in our experiment always had much shorter latencies than the internally guided saccades, are generated by signals originating more from neurons representing the target in retinal coordinates, whereas the internally triggered saccades originated more from neurons representing a target position in head coordinates. Conclusion The gain of externally triggered saccades depends more on the orbital position of the eye than the gain of internally triggered saccades. In contrast, the position dependency of the peak velocity and the skewness was similar for all saccade types. The contribution of the cerebellum to the compensation of orbital position dependencies of saccades cannot explain these ®ndings. 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Bremmer F, Graf W, Ben Hamed S and Duhamel JR. NeuroReport 10, 1±6 (1999). 22. Blatt GJ, Andersen RA and Stoner GR. J Comp Neurol 299, 421±445 (1990). ACKNOWLEDGEMENTS: We are grateful to J. Benson for her help in editing the paper. This work was supported by the Deutsche Forschungsgemeinschaft (DGF) and NIH grants RR-00166 and EY10578. Received 21 April 1999; accepted 24 June 1999