Espace et Action, Institut National de la Santé et de la Recherche Medicale Unité 94, 69500 Bron, France
![]() |
ABSTRACT |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|
Goffart, Laurent, Alain Guillaume, and Denis Pélisson. Compensation for gaze perturbation during inactivation of the caudal fastigial nucleus in the head-unrestrained cat. J. Neurophysiol. 80: 1552-1557, 1998. Muscimol injection in the caudal part of the fastigial nucleus (cFN) leads, in the head-unrestrained cat, to a characteristic dysmetria of saccadic gaze shifts toward visual targets. The goal of the current study was to test whether this pharmacological cFN inactivation impaired the ability to compensate for unexpected perturbations in gaze position during the latency period of the saccadic response. Such perturbations consisted of moving gaze away from the target by a transient electrical microstimulation in the deep layers of the superior colliculus simultaneously with extinction of the visual target. After injection of muscimol in the cFN, targets located in the contralesional hemifield elicited gaze shifts that fell short of the target in both "perturbed" and "unperturbed" trials. The amplitude of the compensatory contraversive gaze shifts in perturbed trials coincided with the predicted amplitude of unperturbed responses starting from the same position. Targets located in the opposite hemifield elicited hypermetric gaze shifts in both trial types, and the error of compensatory responses was not statistically different from that of unperturbed gaze shifts. These results indicate that inactivation of the cFN does not interfere with the ability of the head-unrestrained cat to compensate for ipsiversive or contraversive perturbations in gaze position. Thus the gaze-related feedback signals that are used to compute a reference signal of desired gaze displacement are not impaired by cFN inactivation.
It was proposed that saccadic shifts of the visual axis are controlled by a feedback mechanism. First formulated for head-restrained saccadic eye movements (Jürgens et al. 1981 A detailed description of the methods can be found in previous papers (Goffart and Pélisson 1998 Muscimol-induced inactivation of the cFN produced a marked hypermetria of ipsiversive gaze shifts and hypometria of contraversive ones, as described in previous reports (Goffart and Pélisson 1994 Target in the contralesional visual hemifield
Compensatory gaze shifts were still observed after muscimol injection in the left cFN of cat H (experiment H/lcFN/rSC), as illustrated in Fig. 1A, showing representative responses elicited by a target located 27° to the right. The temporal courses of horizontal gaze and head position are plotted for two unperturbed (Fig. 1A, left panel) and one perturbed trials (Fig. 1A, right panel). Stimulation of the right SC shifted gaze to the left ("perturbation") and was followed by a rightward gaze shift ("compensation") toward the remembered target location. Note that because of the cFN inactivation, all three target-elicited gaze shifts markedly undershot the target location. Note further that the compensatory gaze shift was more hypometric than the unperturbed gaze shift that started from a gaze position corresponding to the preperturbation position (Fig. 1A, trajectory a). Nevertheless, the amount of hypometria (error = -15.7°) was similar to that of the other unperturbed gaze shift (error = -15.6°), which started from a position comparable with the gaze position reached at the end of the perturbation (Fig. 1A, trajectory b). For a given target position when gaze starts from the same position, the similarity between gaze-shift amplitude in the perturbed and unperturbed trials suggests that the gaze perturbation was adequately taken into account in the production of the compensatory gaze shift. To evaluate the consistency of this observation, the amplitude of each unperturbed and compensatory gaze shift recorded during cFN muscimol inactivation is plotted as a function of the amplitude of the desired horizontal gaze displacement (Fig. 1B). For unperturbed trials (
Target in the ipsilesional visual hemifield
Figure 2 shows the data obtained after muscimol injection in the left cFN of cat L (experiment L/lcFN/lSC). The time course of the horizontal component of gaze and head movements toward a target located 19° to the left are shown in Fig. 2A. All gaze shifts were hypermetric and ended at the same position beyond the target. In the perturbed trial, the left SC stimulation quickly shifted gaze to the right (perturbation). This perturbation was shortly followed by a leftward gaze shift (compensation) toward the remembered target location. This compensatory gaze shift was markedly hypermetric and overshot the target location by 13.5°, an error relative to the target virtually identical to that of the two unperturbed gaze shifts. The amplitude of each unperturbed and compensatory gaze shift was plotted as a function of the amplitude of the desired horizontal gaze displacement (Fig. 2B). First, note that the "unperturbed relationship" is displaced toward negative values of actual gaze displacement (see equation of regression in Fig. 2 legend). This result illustrates the characteristic hypermetria of gaze shifts directed toward the inactivated cFN, which is largely related to a bias of the response end points relative to the target. Second, the overlap between the perturbed data points and the unperturbed ones indicates that the relationship between the amplitude of compensatory gaze shifts and the desired gaze displacement is similar to that of unperturbed responses. The average compensation error was not statistically different from zero [0.73 ± 3.92°, t (15) = 0.74, P > 0.05]. In addition, as shown in Fig. 2C, there was no correlation between compensation error and perturbation size. In the same cat we injected muscimol in the right cFN, and compensatory responses to a target presented in the ipsilesional hemifield (experiment L/rcFN/rSC) provided the same results. Table 1 shows that the average value of compensation error and its correlation with perturbation size did not reach a significant level in any experiment.
These results provide some clues regarding the origin of the head-unrestrained gaze dysmetria observed after muscimol inactivation of the cFN (Goffart and Pélisson 1994
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
; Robinson 1975
), this hypothesis was later extended to gaze shifts resulting from combined eye and head movements (for review see Guitton 1992
). The displacement of the line of sight would be driven by a reference signal specifying the gaze displacement required to foveate the target (desired gaze displacement command). The basic idea of this feedback control hypothesis is that gaze accuracy is preserved regardless of how the movement is executed, as long as the feedback mechanisms accurately inform about the actual performance. Compatible with this prediction is the demonstration in behaving animals of a preserved accuracy of eye or gaze saccades despite perturbations induced by intracerebral electrical microstimulation (e.g., Keller et al. 1996
; Pélisson et al. 1989
, 1995
; Sparks and Mays 1983
).
), but its specific role in the context of the feedback control hypothesis is still unclear. The loss of gaze accuracy after inactivation of the caudal fastigial nucleus (cFN) (head-fixed monkey: Ohtsuka et al. 1994
; Robinson et al. 1993
; head-free cat: Goffart and Pélisson 1998
) could result either from an inadequate feedback control (i.e., a mismatch between the actual movement and its internal representation) or from an impaired specification of the reference signal of desired gaze displacement.
; Sparks and Mays 1983
). To test the effectiveness of compensations independently from the dysmetria related to cFN inactivation, we compared the compensatory gaze shift of such perturbed trials to the primary gaze shift of unperturbed trials with a similar desired gaze displacement. The predictions are as follow. If the dysmetria induced by cFN inactivation results from inadequate feedback signals, gaze perturbations may be miscoded and compensation failures are expected. On the other hand, if the dysmetria results from a change in the reference signal, full compensations for gaze perturbations are expected.
METHODS
Abstract
Introduction
Methods
Results
Discussion
References
; Pélisson et al. 1989
). Briefly, two cats were prepared for the experiments under general anesthesia and aseptic conditions following the guidelines from the French Ministry of Agriculture (87/848) and from the European Community (86/609/EEC). Two coils were implanted for the recording of gaze and head position by the search-coil-in-magnetic-field technique (Robinson 1963
). Signals from eye and head coils were linearized (see equation in Judge et al. 1980
) and scaled on-line by a custom-written computer program with calibration parameters defined before implantation and checked after surgery in the behaving animal (details in Goffart and Pélisson 1998
). A recording chamber was implanted stereotaxically over the cerebellum. A second chamber was implanted over the SC in one animal (cat L), whereas in the other animal (cat H), four bundles of four microwires each were stereotaxically implanted in each deep SC. Finally, a plastic head-holding device was fixed to the skull with cement. After recovery from surgery, each cat was placed in a hammock that gently restrained the body, without constraint on natural movements of the head. The visual target was a spoon filled with a food puree and fitted with two infrared diodes that permitted us to continuously record its position (Urquizar and Pélisson 1992
). The sudden presentation of this food target on either side of an opaque panel placed in front of the animal (41-cm distance) elicited coordinated eye and head movements that shifted gaze (eye-in-space) in a saccadic manner. Different panels were used to elicit gaze shifts toward ±19, ±27, and ±35° targets in the horizontal plane. The ambient lights were turned off ~80 ms after target presentation by an electronic shutter so that the orienting response was triggered and completed in darkness. In about one-third of the trials (perturbed trials), initial gaze position was perturbed by applying a short microstimulation train to the SC at the time of target offset; in these trials the target location was chosen to elicit compensatory gaze shifts in a direction opposite to the gaze perturbation. Both perturbed and unperturbed trials were randomly presented during a 1-2 h recording session initiated 15-20 min after the onset of muscimol injection in the cFN. In one animal, control recordings were performed several days before injection to verify that the accuracy of gaze shifts was preserved despite the stimulation-induced gaze perturbation (Pélisson et al. 1989
).
RESULTS
Abstract
Introduction
Methods
Results
Discussion
References
, 1998
). Because these modifications in accuracy occurred predominantly in the horizontal plane, the analysis of the compensation abilities after muscimol injection in the cFN is restricted to the horizontal component of gaze shifts. We report on the compensatory responses elicited by a target presented in the hemifield contralateral and ipsilateral, respectively, to the inactivated cFN.
) the desired gaze displacement corresponds to the distance between target and gaze during the target presentation time, and for perturbed trials (
) it represents the new distance between target and gaze after the electrically induced change in gaze position. The regression analysis that was performed for unperturbed gaze shifts confirmed the typical gain reduction of contraversive gaze shifts (regression equation in legend). It is remarkable that the amplitude values of the compensatory gaze shifts (
) are distributed along the regression line fitting the unperturbed responses. This observation was analyzed further by computing for each perturbed trial the inaccuracy of compensation as defined relative to comparable unperturbed responses. This value of compensation error was obtained by subtracting from the compensatory gaze-shift amplitude the amplitude of the predicted unperturbed gaze response to the same target (i.e., distance between each perturbed data point and the regression line in Fig. 1B). A positive value corresponds to an overcompensation and a negative one to an undercompensation. As seen in Fig. 1C, the compensation error did not depend on the perturbation size (
, regression); in addition, it was not statistically different from zero (-0.7 ± 2.9°, mean ± SD; t (df = 17) = 1.0, P > 0.05). The values of compensation error differed clearly from the theoretical values predicted from the hypothesis of no compensation (- - -).
View larger version (37K):
[in a new window]
FIG. 1.
Compensatory responses toward a target located in the contralesional visual hemifield (experiment H/lcFN/rSC). A: time course of horizontal gaze and head position during representative responses elicited by a target briefly presented (hatched column) at 27° to the right and recorded during inactivation of the left caudal fastigial nucleus (cFN). In the unperturbed trials (A, left) gaze and head movements markedly undershot the target position. In the perturbed trial (A, right) the perturbation in gaze position evoked by superior colliculus (SC) stimulation (darker shaded column) was shortly followed by a compensatory gaze shift that also was hypometric. Note that the amplitude of the compensatory gaze shift matched that of the unperturbed gaze shift initiated from a similar starting position (trajectory b). B: relationship between actual and desired amplitude of horizontal gaze displacement achieved during the primary response of unperturbed trials ( ) or during the compensatory response of perturbed trials (
). Desired gaze displacement amplitude refers to the horizontal distance between starting gaze position and target position. - - -, unitary slope;
, regression fitting the unperturbed data (y = 0.65x - 2.41, R2 = 0.77). C: relationship between gaze compensation error and perturbation size (absolute value of gaze horizontal perturbation). Compensation horizontal error corresponds to the distance between the amplitude value of each perturbed data point and the regression line shown in B. Regression lines (intercept set to 0) are shown for the theoretical relationship predicted from the hypothesis of no compensation (- - -, slope corresponding to that of regression line in B) and for the relationship fitting the actual data (
, y = -0.12x, slope not statistically different from 0, t (17) = -1.7, P > 0.05). B and C, arrow: compensatory gaze shift shown in A. Ipsi, ipsiversive; contra, contraversive.
View larger version (36K):
[in a new window]
FIG. 2.
Compensatory responses toward a target located in the ipsilesional visual hemifield (experiment L/lcFN/lSC). Same conventions as in Fig. 1. A: time course of horizontal gaze and head position during representative responses elicited by a target briefly presented at 19° to the left and recorded during inactivation of the left cFN. B: relationship between actual and desired amplitude of horizontal gaze displacement achieved during the primary gaze shift of unperturbed trials ( ) or during the compensatory gaze shift of perturbed trials (
). Equation of regression: y = 1.24x - 10.36 (R2 = 0.89). C: relationship between gaze compensation horizontal error and perturbation size [
, equation: y = 0.06x, slope not statistically different from 0, t (15) = 0.8, P > 0.05]. B and C, arrow: compensatory gaze shift shown in A.
View this table:
TABLE 1.
Perturbation size and compensation horizontal error computed for each experiment
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, 1998
; Goffart et al. 1998
). It is shown that inactivation of the cFN did not interfere with the ability of the head-unrestrained cat to compensate for collicular-induced perturbations moving gaze away from the target of an impending gaze shift (Pélisson et al. 1989
). Irrespective of whether the perturbation was directed toward or away from the inactivated cFN, the amplitude of the compensatory gaze shifts to a given target was inaccurate but nevertheless comparable with the amplitude of unperturbed gaze shifts starting from similar positions. In both cases, the compensation error was not related to the size of the perturbation within the tested range, and its average value was virtually zero. These findings indicate that the gaze perturbation is taken into account to update the command specifying the required gaze displacement for foveating a visual target. This result in turn suggests that neither the feedback mechanism informing about the gaze position perturbation nor the combination of this gaze perturbation with the memorized retinal signals of initial gaze error, to update the desired gaze displacement command, are affected by the muscimol cFN inactivation.
, 1998
) and for the unchanged dynamics of contraversive gaze shifts (Goffart et al. 1998
). On the other hand, if distinct gaze-related feedback signals are used for updating the reference signal and for the dynamic control of gaze shift (Fig. 3B), the current findings have some implication regarding the hypometria of contraversive gaze shifts during cFN inactivation. Indeed, the correct updating of the desired gaze displacement after gaze perturbation (see long feedback pathway in Fig. 3B) implies that the gain reduction of contraversive gaze shifts takes place downstream from this updating. In addition, the unchanged dynamics of contraversive gaze shifts (Goffart et al. 1998
) would again place this gain reduction upstream from the dynamic feedback loop.
View larger version (32K):
[in a new window]
FIG. 3.
Hypothetical block diagrams of the control system for gaze shift showing the postulated level of cFN action (shaded areas). These highly simplified diagrams represent 2 putative structures of the gaze control system but do not address the exact nature of the feedback signals (position vs. displacement, gaze vs. eye and head). The 2 dynamic controllers (premotor centers + feedback generators) are each recruited either by the presentation of the visual target or by the SC electrical microstimulation. Eye and head premotor centers are driven by a signal of horizontal dynamic motor error (hDME), which itself results from the permanent comparison between a reference signal specifying the desired horizontal gaze displacement (hDGD) and feedback signals estimating the current horizontal displacement of gaze (hEGD). In A, the feedback signals (hEGD) that accurately encode the SC microstimulation-induced perturbation of gaze position are involved in the dynamic control of the gaze shift. Gaze dysmetria induced by muscimol inactivation of the cFN results from an impairment in the translation of retinal signals into the hDGD reference signal (gain reduction for the hypometria of contraversive gaze shifts, addition of bias K for the hypermetria of ipsiversive gaze shifts). In B, the feedback signals (hEGD) encoding gaze perturbation and allowing to update the reference signal are distinct from those used for the dynamic control of gaze shift, constraining the site of gain reduction for the hypometria of contraversive gaze shifts (see text).
![]() |
ACKNOWLEDGEMENTS |
---|
We thank M. Riley and C. Urquizar for writing some of the display/parameter extraction software, N. Boyer-Zeller for providing essential support for histology, and M.-L. Loyalle for taking care of the animals.
This study was supported by Human Frontier Science Program Organization Grant RG58/92B. L. Goffart was supported by a fellowship from the French Ministry of Research and Technology.
![]() |
FOOTNOTES |
---|
Present address of L. Goffart: Division of Neuroscience, Baylor College of Medicine, One Baylor Plaza, Houston, Texas 77025.
Address for reprint requests: D. Pélisson, Espace et Action, INSERM U 94, 16 Avenue Doyen Lépine, 69500 Bron, France.
Received 17 March 1998; accepted in final form 14 May 1998.
![]() |
REFERENCES |
---|
![]() ![]() ![]() ![]() ![]() ![]() |
---|