Difference Between Visually and Electrically Evoked Gaze Saccades Disclosed by Altering the Head Moment of Inertia

Alexandre J. F. Coimbra,1,2 Philippe Lefèvre,1,2 Marcus Missal,1 and Etienne Olivier1

 1Laboratory of Neurophysiology, Université Catholique de Louvain, B-1200 Brussels, Belgium; and  2Centre for Systems Engineering and Applied Mechanics (CESAME), Université Catholique de Louvain, B-1348 Louvain-la-Neuve, Belgium


    ABSTRACT
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Coimbra, Alexandre J. F., Philippe Lefèvre, Marcus Missal, and Etienne Olivier. Difference Between Visually and Electrically Evoked Gaze Saccades Disclosed by Altering the Head Moment of Inertia. J. Neurophysiol. 83: 1103-1107, 2000. Differences between gaze shifts evoked by collicular electrical stimulation and those triggered by the presentation of a visual stimulus were studied in head-free cats by increasing the head moment of inertia. This maneuver modified the dynamics of these two types of gaze shifts by slowing down head movements. Such an increase in the head moment of inertia did not affect the metrics of visually evoked gaze saccades because their duration was precisely adjusted to compensate for these changes in movement dynamics. In contrast, the duration of electrically evoked gaze shifts remained constant irrespective of the head moment of inertia, and therefore their amplitude was significantly reduced. These results suggest that visually and electrically evoked gaze saccades are controlled by different mechanisms. Whereas the accuracy of visually evoked saccades is likely to be assured by on-line feedback information, the absence of duration adjustment in electrically evoked gaze shifts suggests that feedback information necessary to maintain their metrics is not accessible or is corrupted during collicular stimulation. This is of great importance when these two types of movements are compared to infer the role of the superior colliculus in the control of orienting gaze shifts.


    INTRODUCTION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The study of movements elicited by electrical stimulation has been widely used to infer the function of different brain structures. For example, the finding that the metrics of gaze shifts elicited by electrical stimulation of the superior colliculus (SC) are determined by the location of the stimulating electrode on the collicular map led to the hypothesis that the role of the SC is to generate a motor command corresponding to the desired gaze displacement (e.g., Freedman et al. 1996; Paré et al. 1994). In addition, because of the similarity between visually evoked orienting movements and those elicited by collicular stimulation, it has been assumed that these two types of movements share the same control mechanism (e.g., Freedman et al. 1996; Paré et al. 1994; Roucoux et al. 1980). Indeed, it has been suggested that both electrically and visually evoked gaze movements are controlled by a closed loop system that allows the desired displacement signal to be continuously compared with an internal copy of the actual displacement (Robinson 1975). The observations that, despite alterations of their dynamics, the amplitude of visually evoked orienting movements remained unaffected support this hypothesis (Guitton et al. 1984; Jürgens et al. 1981; Pélisson et al. 1995; Zee et al. 1976). However, similar evidence has never been provided for electrically evoked gaze saccades.

The goal of the present study was to test the hypothesis that both electrically and visually evoked gaze movements are controlled by a similar closed loop system. To do so, we altered artificially the dynamics of both electrically and visually evoked gaze saccades in head-free cats by increasing the head moment of inertia, and the consequences of this maneuver on their metrics were investigated. Our results show that visually and electrically evoked gaze displacements are affected differently, suggesting that these two types of movements are controlled by different mechanisms and that feedback information is not accessible, or is corrupted, during electrical stimulation of the SC.


    METHODS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

All procedures were approved by the University of Louvain Ethics Committee and were in accordance with the National Institutes of Health guide for care and use of animals.

Under deep anesthesia (6-10 mg/kg Ketamine and 0.1 mg/kg Xylazine IM) a scleral search coil was implanted, and a plastic rod was cemented on the skull in four adult cats. This rod was subsequently used to fix a coil to record head position and to attach the load used to increase the head moment of inertia. A small craniotomy centered on the midline (AP0-A2) was also made to allow access to both SC with microelectrodes, and a stainless steel chamber was cemented over this craniotomy.

SC stimulation experiments were performed in three cats (GN, RX, and NB). Cats were held in a box with the head unrestrained, and they had to fixate a central target (~0.5°) for ~1 s. Electrical SC stimulation was delivered, with a probability varying from 0.7 to 1.0, following a constant 50 ms gap interval after the fixation point was switched off. Stimulation was then followed by the presentation of a target at an eccentricity of 10-20°. The cats received a reward if they made a saccade to this target within a tolerance window of 4° radius and maintained fixation for 300-500 ms. Electrical stimulation was delivered through an epoxy-insulated tungsten microelectrode positioned using a hydraulic microdrive. The electrode was advanced through the SC until stimulation produced a short-latency (<40 ms) gaze saccade with a threshold <15 µA. Electrical stimulation (250 ms train, 0.5 ms pulse width, 400 Hz) was then delivered with a current of 2 to 2.5 times threshold.

In the so-called "loaded" condition, the head moment of inertia was increased using a small plastic device whose mass was 156 × 10-3 kg; it was designed to affect mainly the moment of inertia of the head in the horizontal plane. The increment in the head mass was estimated at 50-60%, and the head moment of inertia was ~3.5 times larger than in the control condition.

Experiments on visually evoked gaze saccades were performed in two cats (NB and PN). After a steady fixation of 1 s, the fixation point was turned off and a target located at 20 or 40° on the horizontal meridian was flashed for 50 ms to avoid any visual feedback during gaze shifts. Food reward was contingent to fixation of the remembered target for 300-500 ms within a tolerance window of 6° radius.

Because stimulation sites were selected to obtain gaze shifts with a horizontal component larger than 90% of their vectorial amplitude, only the horizontal gaze component was analyzed. When stimulation elicited a staircase, only the initial movement was considered for analysis. Gaze movement onset was determined by a 20°/s velocity criterion; trials where eye or head velocity was higher than 10°/s at the stimulation onset were discarded. Gaze movement offset was determined by an acceleration criterion (1,200°/s2). In visually evoked movements, only the main gaze saccades were analyzed; corrective movements were ignored.


    RESULTS
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ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

Electrically evoked movements

An increase in the head moment of inertia reduced the amplitude of gaze shifts evoked by SC stimulation. In the example illustrated in Fig. 1, electrically evoked gaze saccades had a mean amplitude of 37.5 ± 3.2° (mean ± SD, n = 33) in the control condition, and it was significantly reduced (24.9 ± 6.5°, n = 41) when the head moment of inertia was increased (t-test, P < 0.0001). The amplitude distributions of gaze saccades evoked from this site in the control and "loaded" conditions are compared in Fig. 1B. As shown in Fig. 1A, an increase in the head moment of inertia also reduced the peak velocity of evoked gaze movements. In this example, the averaged peak velocity of evoked gaze saccades was 593 ± 70°/s (n = 33) in the control condition and dropped to 393 ± 79°/s (n = 41) in the loaded condition (t-test, P < 0.0001). However, an increased head moment of inertia did not alter the duration of electrically evoked gaze saccades. Indeed, the mean duration of gaze saccades elicited from this site was not statistically different in the control (109.0 ± 10.0 ms, n = 33) and in the loaded (107.3 ± 19.2 ms, n = 41) condition (t-test, P = 0.22, Fig. 1C).



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Fig. 1. Effect of an increased head moment of inertia on gaze movements elicited by collicular stimulation (cat NB). A: horizontal gaze (G), head (H) and eye (E) position (top) and velocity (bottom) traces of a representative movement elicited by collicular stimulation in the control (- - -) and "loaded" (---) conditions. B: distributions of gaze saccade amplitude in control () and loaded () conditions. Averages and standard deviations of each population are represented by a triangle and a horizontal line, respectively (triangle , control; black-triangle, loaded). C: distributions of gaze saccade duration obtained from the same stimulation site (same conventions as before).

Similar effects of the load were observed when data from the three cats (43 sites) were pooled together. An increased head moment of inertia reduced both the amplitude (paired t-test, P < 0.05) and peak velocity (paired t-test, P < 0.0001) of electrically evoked gaze shifts but had no effect on their duration (paired t-test, P = 0.30). The decrease in gaze shift amplitude subsequent to an increase in the head moment of inertia was due to a significantly smaller head contribution to the gaze saccades (paired t-test, P < 0.05, 43 sites, 3 cats). This resulted from a smaller head acceleration peak in the loaded than in the control condition (paired t-test, P < 0.0001, 43 sites, 3 cats) and explains why the effect of the load on gaze saccade dynamics was more important for larger gaze shifts (see Fig. 3). Neither the eye contribution nor peak velocity of eye saccades were affected by an increased head moment of inertia.

Visually evoked movements

The dynamics of visually evoked gaze saccades were similarly affected by an increase in the head moment of inertia. In the example illustrated in Fig. 2A, gaze shifts toward a target flashed at an eccentricity of 40° had a peak velocity of 606 ± 86°/s (n = 34) in the control condition; it diminished to 488 ± 72°/s (n = 27) when the head moment of inertia was increased (t-test, P < 0.0001). This decrease in the gaze velocity was similar to that observed in electrically evoked gaze shifts of comparable amplitude. However, the amplitude of visually evoked gaze saccades was not affected by the load. Indeed, in the example of Fig. 2A, the mean amplitude of gaze saccades was 35.8 ± 2.2° (n = 34) and 36.6 ± 2.2° (n = 27) in the control and in the loaded condition, respectively (Fig. 2B, t-test, P = 0.15). This lack of effect of the load on the amplitude of visually evoked gaze shifts was due to an increase in the gaze saccade duration that accurately compensated for the changes in movement dynamics: the mean duration of gaze saccades was 102.6 ± 12.0 ms (n = 34) in the control condition, and it was 118.6 ± 10.7 ms (n = 27) in the loaded condition (Fig. 2C, t-test, P < 0.001). Similar results were obtained for all visually evoked saccades (n = 246, 2 cats).



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Fig. 2. Effect of an increase of the head moment of inertia on visually evoked gaze saccades (cat NB). A: position (top) and velocity (bottom) traces of a typical gaze shift recorded in the control (- - -) and loaded (---) conditions (same conventions as in Fig. 1A). B and C: distributions of amplitude and duration of visually evoked gaze shifts obtained in the control and the loaded conditions (same conventions as in Fig. 1, B and C).

The peak of head acceleration in visually evoked gaze shifts was also reduced in the loaded condition when compared with the control condition (paired t-test, P < 0.01). This effect was similar to that observed in electrically evoked gaze shifts. However, an increased head moment of inertia also significantly decreased the peak velocity of eye saccades (paired t-test, P < 0.01); this contrasts with results obtained in electrically evoked movements.

Figure 3 summarizes data gathered in the present study. It shows plots of peak velocity, amplitude, and duration of gaze shifts obtained in the loaded versus control condition for electrically (left column) and visually (right column) evoked saccades. For electrically evoked gaze saccades, both the peak velocity (Fig. 3A) and amplitude (Fig. 3C) were smaller in the loaded than in the control condition, whereas their duration remained unchanged (Fig. 3E). In contrast, whereas the load decreased the peak velocity of visually evoked saccades (Fig. 3B), their amplitude remained constant (Fig. 3D) and their duration increased (Fig. 3F).



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Fig. 3. Effect of the increase in head moment of inertia on the peak velocity (A and B), amplitude (C and D), and duration (E and F) of electrically (left column) and visually (right column) evoked gaze saccades. A, C, and E: each point in the scatter plots represents average values of loaded vs. control data from a single superior colliculus (SC) site. Different symbols represent data from different cats (GN, open circle , n = 9; RX, triangle , n = 15; NB, , n = 19). B, D, and F: each point represents average values of loaded vs. control data from saccades executed by each cat to visual targets located at 20 or 40° eccentricity. Different symbols represent data from different cats (NB, , n = 2; PN, star , n = 2). In each panel, dotted lines are equality lines (slope = 1).


    DISCUSSION
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

The main finding of the present study is that, whereas an increase in the head moment of inertia affected the dynamics of visually and electrically evoked gaze saccades in a similar way, it had a different effect on their metrics. Indeed, the duration of visually evoked gaze shifts was precisely increased to compensate for changes in gaze dynamics, whereas a similar adjustment was never observed for electrically evoked movements.

Because flashed targets were used in the present study, a contribution of visual information cannot explain the adjustment in duration of visually evoked gaze saccades. This adjustment is in accordance with earlier studies showing that an adequate compensation occurs during visually evoked gaze saccades when the SC is briefly stimulated (Pélisson et al. 1995) or when a transient brake interrupts head displacement (Guitton et al. 1984). Together with these previous studies, our results support the idea that visually evoked movements are not ballistic but that feedback signals provide on-line information about the movement execution (Robinson 1975). Because accurate compensation also occurs for external perturbations of the head movement (Guitton et al. 1984; Laurutis and Robinson 1986; Tomlinson 1990), it suggests that the efference copy of motor commands is probably not the exclusive source of feedback information and that proprioceptive or vestibular signals, or both, are also involved.

An alternative explanation for the duration adjustment observed in visually evoked movements is that it may result from a progressive change in the eye and head motor programs in a predictive way, without involving the internal feedback loop. An observation compatible with this hypothesis is the decrease of saccadic peak eye velocity in the loaded condition. This was only observed in visually evoked movements and suggests that the eye motor program could be modified to take into account expected changes in the dynamics of the head movement. This hypothesis is compatible with recent studies showing that eye and head components of gaze shifts are programmed relative to each other in a predictive way. In human subjects, Stahl (1999) showed that the amplitude of head movements is a function of the eye eccentricity that would have resulted from an orienting movement executed solely with a saccadic eye movement. It was concluded that head movements are preprogrammed to keep the final eye eccentricity within a restricted zone of the oculomotor range. Furthermore, it has been shown that, in the monkey, the eye motor program anticipates the slow phase of the vestibuloocular reflex (VOR) to control the final position of the eye in the orbit (Crawford et al. 1999). Therefore the present results could be explained by a change in preprogrammed eye and head movements following an adaptation to the load. This change would only be observed in visually evoked movements because SC stimulation probably triggers a default motor program. However, we did not find any evidence for a progressive adaptation to the load, although we cannot exclude that such an adaptation took place in a very short period of time. The decrease in peak eye velocity that we observed in visually evoked movements could be due to a coupling between the eye and head through the vestibular quick phase mechanism (Guitton et al. 1984).

In electrically evoked movements, a decrease in the head acceleration was never compensated by an increase in the gaze duration, and therefore this resulted in gaze shifts of smaller amplitude. Two mechanisms could explain this absence of adjustment in the gaze duration. First, the desired gaze displacement command generated by SC stimulation could be modified in the loaded condition because of abnormal proprioceptive information about the head plant. This is, however, unlikely because the parameters of stimulation were kept constant in the two conditions and because changes in the displacement command should also influence the gaze duration. The second possible explanation is that the gaze amplitude varies because the dynamic motor error is not correctly approximated. If true, this suggests that feedback information carrying the estimate of instantaneous gaze displacement is not accessible or not correct during electrical SC stimulation and that electrically evoked gaze movements are controlled as ballistic movements.

Therefore it is reasonable to hypothesize that the end of gaze saccades is triggered differently for visually and electrically evoked movements. For visually evoked gaze saccades, our results, together with perturbation experiments (Guitton et al. 1984; Pélisson et al. 1995), suggest that the metrics of gaze saccades are precisely controlled by on-line feedback information about movement execution. In most models (Lefèvre and Galiana 1992; Lefèvre et al. 1998), this feedback is provided by the displacement integrator (DI) that receives an internal copy of the gaze velocity. The saccadic system compares the desired gaze displacement command with the feedback and thus computes an estimate of the dynamic motor error (ME). When ME approaches zero, the gaze saccade is stopped by inhibiting the saccade generator and by reactivating the VOR. For electrically evoked gaze saccades, feedback information is probably not accessible to the controller and ME is incorrectly estimated because the metrics of gaze saccades are affected by changes in movement dynamics. We hypothesize that the internal copy of gaze velocity is replaced at the input of DI by a signal that is a function of both the locus and parameters of stimulation. Consequently, the duration of electrically evoked gaze saccades is also a function of the electrical stimulation but is not influenced by changes in gaze dynamics. On the basis of these assumptions, two mechanisms can be suggested to explain how the end of electrically evoked gaze saccades is controlled. If the gaze comparator is located in the SC, the reduction of ME to a null value could produce the reactivation of collicular fixation neurons (FNs), which have been hypothesized to terminate saccades (Lefèvre and Galiana 1992; Munoz et al. 1991). The propagation of neural activity due to SC stimulation could trigger an artificial and stereotyped reactivation of FNs. This reactivation of FNs could in turn provoke the end of gaze saccades by reactivating brain stem omnipause neurons. Even though FNs are not the only input to omnipause neurons (Everling et al. 1998), this collicular input could be predominant during SC stimulation. Another possible hypothesis is that saccades are controlled by the synergistic action of the SC and cerebellum, the comparator being located in the latter (Lefèvre et al. 1998; Quaia et al. 1999). During SC stimulation, the cerebellum could be inappropriately recruited and the input of the DI could also be a stereotyped signal that is a function of the electrical stimulus.


    ACKNOWLEDGMENTS

This work was supported by the Fonds National de la Recherche Scientifique (FNRS, Belgium), Belgian Program on Inter-university Poles of Attraction, initiated by the Belgian State, Prime Minister's Office for Science, Technology and Culture (SSTC), Actions de Recherche Concertées (ARC, Belgium) and Fonds de la Recherche Scientifique Médicale (FRSM, Belgium). A.J.F. Coimbra was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, Brazil).


    FOOTNOTES

Address for reprint requests: P. Lefèvre, Laboratory of Neurophysiology, UCL-NEFY 5449, 54, avenue Hippocrate, B-1200 Brussels, Belgium.

The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

Received 19 July 1999; accepted in final form 20 October 1999.


    REFERENCES
TOP
ABSTRACT
INTRODUCTION
METHODS
RESULTS
DISCUSSION
REFERENCES

0022-3077/00 $5.00 Copyright © 2000 The American Physiological Society