Modifications in end positions of arm movements following short-term saccadic adaptation.

We investigated whether short-term saccadic adaptation modifies hand pointing. Subjects were presented with double-step targets, the second target jump occurring during the saccade to the first one and bringing the target back to 66% of the first target eccentricity, in order to reduce the gain of their gaze saccades. Before and after this adaptation phase, they pointed with their hand to single step targets while keeping their gaze straight ahead. The results show that the hand movements terminated at positions that were significantly less eccentric following the adaptation phase, resembling the adaptive modification seen in the gaze movements. These results suggest that the motor systems controlling gaze and hand use common information about target position.

A simple method for constructing microinjectrodes for reversible inactivation in behaving monkeys.

A method for constructing a simple, durable injection-microelectrode (injectrode) is described. The injectrode can record neuronal activity, stimulate neuronal tissues, or inject substances locally through its tip. The injectrode is lightweight and is easy to construct from commercially available parts, and it can be used repeatedly for multiple recordings and injections. Since dura penetration can damage fragile electrode tips, a reliable method to pass the injectrode through an intact dura matter is described.

Early head movements elicited by visual stimuli or collicular electrical stimulation in the cat.

During the course of previous recordings of visually-triggered gaze shifts in the head-unrestrained cat, we occasionally observed small head movements which preceded the initiation of the saccadic eye/head gaze shift toward a visual target. These early head movements (EHMs) were directed toward the target and occurred with a probability varying between animals from 0.4% to 16.4% (mean=5.2%, n=11 animals). The amplitude of EHM ranged from 0.4 degrees to 8.3 degrees (mean=1.9 degrees ), their latency from 66 to 270 ms (median=133 ms) and the delay from EHM onset to gaze shift onset averaged 183+/-108 ms (n=240). Their occurrence did not depend on visual target eccentricity in the studied range (7-35 degrees ), but influenced the metrics and dynamics of the ensuing gaze shifts (gain and velocity reduced). We also found in the two tested cats that low intensity microstimulation of the superior colliculus deeper layers elicited a head movement preceding the gaze shift. Altogether, these results suggest that the presentation of a visual target can elicit a head movement without triggering a saccadic eye/head gaze shift. The visuomotor pathways triggering these early head movements can involve the deep superior colliculus.

Cerebellar contribution to the spatial encoding of orienting gaze shifts in the head-free cat.

1. Cerebellar saccadic dysmetria may result from a disturbance in the processes that ensure correct execution of gaze displacement. Alternatively, an impairment in the preparatory processes that lead to the specification of the movement goal may also produce this deficit. 2. We report here on a pharmacologically induced dysmetria that suggests a cerebellar contribution to the neural processes encoding the location of the goal for orienting gaze shifts. 3. Shifts of gaze (eye-in-space) were recorded in the head-free cat after the GABA agonist muscimol was unilaterally injected into the caudal part of the fastigial nucleus. 4. Gaze saccades towards the inactivated side were hypermetric. These ipsiversive movements overshot the target by a constant error, regardless of target eccentricity and initial gaze position. 5. Gaze saccades directed away from the inactivated side undershot the target. The degree of hypometria increased when the amplitude of the required movement increased. 6. These results suggest a different contribution of the caudal fastigial nucleus to the accuracy of visually triggered gaze shifts, depending on the direction of the impending saccade. The systematic error of ipsiversive movements and the inappropriate movements evoked by presenting a target at the same physical location as gaze reveal that fastigial inactivation interfered with the processes that encode the location of a visual target.

Changes in initiation of orienting gaze shifts after muscimol inactivation of the caudal fastigial nucleus in the cat.

1. The production of a goal-directed saccadic gaze shift involves the specification of movement amplitude and direction, and the decision to trigger the movement. Behavioural and neurophysiological data suggest that these two functions involve separate processes which may interact. 2. The medio-posterior cerebellar areas are classically assigned a major contribution to the control of saccade metrics, and previous cerebellar lesion studies have revealed marked dysmetria of visually triggered gaze shifts. In contrast, these studies did not provide evidence for a cerebellar role in saccadic initiation. 3. In the present study, we investigated in the head-unrestrained cat the deficits in both the initiation and the metrics control of saccadic gaze shifts following pharmacological inactivation of the caudal part of the fastigial nucleus (cFN). 4. After cFN inactivation, latencies for contraversive gaze shifts increased to about 137 +/- 28% of normal, and latencies for ipsiversive gaze shifts decreased to about 84 +/- 8% of normal. Similar changes in head movement latency were observed, such that the temporal coupling between eye and head components remained largely unaffected. 5. Contraversive gaze shifts were more hypometric as their latency increased. In contrast, the degree of hypermetria in ipsiversive gaze shifts was unrelated to latency. 6. These results suggest a functional role of the medio-posterior cerebellum in gaze shift initiation and in storing information about the target location and/or the desired gaze shift amplitude.

Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. I. Gaze dysmetria.

The cerebellar control of orienting behavior toward visual targets was studied in the head-unrestrained cat by analyzing the deficits of saccadic gaze shifts after unilateral injection of muscimol in the caudal part of the fastigial nucleus (cFN). Gaze shifts are rendered strongly inaccurate by muscimol cFN inactivation. The characteristics of gaze dysmetria are specific to the direction of the movement with respect to the inactivated cFN. Gaze shifts directed toward the injected side are hypermetric. Irrespective of their starting position, all these ipsiversive gaze shifts overshoot the target by a constant horizontal error (or bias) to terminate at a "shifted goal" location. In particular, when gaze is directed initially at the future target's location, a response with an amplitude corresponding to the bias moves gaze away from the actual target. Additionally, when gaze is initially in between the target and this shifted goal location, the response again is directed toward the latter. This deficit of ipsiversive gaze shifts is characterized by a consistent increase in the y intercept of the relationship between horizontal gaze amplitude and horizontal retinal error. Slight increases in the slope sometimes are observed as well. Contraversive gaze shifts are markedly hypometric and, in contrast to ipsiversive responses, they do not converge onto a shifted goal but rather underestimate target eccentricity in a proportional way. This is reflected by a decrease in the slope of the relationship between horizontal gaze amplitude and horizontal retinal error, with, for some experiments, a moderate change in the y-intercept value. The same deficits are observed in a different setup, which permits the control of initial gaze position. Correction saccades rarely are observed when visual feedback is eliminated on initiation of the primary orienting response; instead, they occur frequently when the target remains visible. Like the primary contraversive saccades, they are hypometric and the ever-decreasing series of three to five correction saccades reduces the gaze fixation error but often does not completely eliminate it. We measured the position of gaze after the final correction saccade and found that fixation of a visible target is still shifted toward the inactivated cFN by 4.9 +/- 2.4 degrees. This fixation offset is correlated to, but on average 54% smaller than, the hypermetric bias of ipsiversive responses measured in the same experiments. In conclusion, the cFN contributes to the control of saccadic shifts of the visual axis toward a visual target. The hypometria of contraversive gaze shifts suggests a cFN role in adjusting a gain in the translation of retinal signals into gaze motor commands. On the basis of the convergence of ipsiversive gaze shifts onto a shifted goal, the straightness of gaze trajectory during these responses and the production of misdirected or inappropriately initiated responses toward this shifted goal, we propose that the cFN influences the processes that specify the goal of ipsiversive gaze shifts.

On-line compensation of gaze shifts perturbed by micro-stimulation of the superior colliculus in the cat with unrestrained head.

Prior studies have led to the gaze feedback hypothesis, which states that quick orienting movements of the visual axis (gaze shifts) are controlled by a feedback system. We have previously provided evidence for this hypothesis by extending the original study of Mays and Sparks (1980) to the cat with unrestrained head (Pélisson et al. 1989). We showed that cats compensated for a stimulation-induced perturbation of initial gaze position by generating, in the dark, an accurate gaze shift towards the remembered location of a flashed target. In the present study, we investigate goal-directed gaze shifts perturbed "in flight" by a brief stimulation of the superior colliculus. The microstimulation parameters were tuned such that significant perturbations were induced without halting the movement. The ambient light was turned off at the onset of the gaze shift, suppressing any visual feedback. We observed that, following stimulation offset, the gaze shift showed temporal and spatial changes in its trajectory to compensate for the transient perturbation. Such compensations, which occurred "on-line" before gaze shift termination, involved both eye and head movements and had dynamic characteristics resembling those of unperturbed saccadic gaze shifts. These on-line compensations maintained gaze accuracy when the stimulation was applied during the early phase of large and medium (about 60 and 40 degrees) movements. These results are compatible with the notion of a gaze feedback loop providing a dynamic gaze error signal.

Contribution of the rostral fastigial nucleus to the control of orienting gaze shifts in the head-unrestrained cat.

The implication of the caudal part of the fastigial nucleus (cFN) in the control of saccadic shifts of the visual axis is now well established. In contrast a possible involvement of the rostral part of the fastigial nuceus (rFN) remains unknown. In the current study we investigated in the head-unrestrained cat the contribution of the rFN to the control of visually triggered saccadic gaze shifts by measuring the deficits after unilateral muscimol injection in the rFN. A typical gaze dysmetria was observed: gaze saccades directed toward the inactivated side were hypermetric, whereas those with an opposite direction were hypometric. For both movement directions, gaze dysmetria was proportional to target retinal eccentricity and could be described as a modified gain in the translation of visual signals into eye and head motor commands. Correction saccades were triggered when the target remained visible and reduced the gaze fixation error to 2.7 +/- 1.3 degrees (mean +/- SD) on average. The hypermetria of ipsiversive gaze shifts resulted predominantly from a hypermetric response of the eyes, whereas the hypometria of contraversive gaze shifts resulted from hypometric responses of both eye and head. However, even in this latter case, the eye saccade was more affected than the motion of the head. As a consequence, for both directions of gaze shift the relative contributions of the eye and head to the overall gaze displacement were altered by muscimol injection. This was revealed by a decreased contribution of the head for ipsiversive gaze shifts and an increased head contribution for contraversive movements. These modifications were associated with slight changes in the delay between eye and head movement onsets. Inactivation of the rFN also affected the initiation of eye and head movements. Indeed, the latency of ipsiversive gaze and head movements decreased to 88 and 92% of normal, respectively, whereas the latency of contraversive ones increased to 149 and 145%. The deficits induced by rFN inactivation were then compared with those obtained after muscimol injection in the cFN of the same animals. Several deficits differed according to the site of injection within the fastigial nucleus (tonic orbital eye rotation, hypermetria of ipsiversive gaze shifts and fixation offset, relationship between dysmetria and latency of contraversive gaze shifts, postural deficit). In conclusion, the present study demonstrates that the rFN is involved in the initiation and the control of combined eye-head gaze shifts. In addition our findings support a functional distinction between the rFN and cFN for the control of orienting gaze shifts. This distinction is discussed with respect to the segregated fastigiofugal projections arising from the rFN and cFN.

Compensation for gaze perturbation during inactivation of the caudal fastigial nucleus in the head-unrestrained cat.

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.

Orienting gaze shifts during muscimol inactivation of caudal fastigial nucleus in the cat. II. Dynamics and eye-head coupling.

We have shown in the companion paper that muscimol injection in the caudal part of the fastigial nucleus (cFN) consistently leads to dysmetria of visually triggered gaze shifts that depends on movement direction. Based on the observations of a constant error and misdirected movements toward the inactivated side, we have proposed that the cFN contributes to the specification of the goal of the impending ipsiversive gaze shift. To test this hypothesis and also to better define the nature of the hypometria that affects contraversive gaze shifts, we report in this paper on various aspects of movement dynamics and of eye/head coordination patterns. Unilateral muscimol injection in cFN leads to a slight modification in the dynamics of both ipsiversive and contraversive gaze shifts (average velocity decrease = 55 degrees/s). This slowing in gaze displacements results from changes in both eye and head. In some experiments, a larger gaze velocity decrease is observed for ipsiversive gaze shifts as compared with contraversive ones, and this change is restricted to the deceleration phase. For two particular experiments testing the effect of visual feedback, we have observed a dramatic decrease in the velocity of ipsiversive gaze shifts after the animal had received visual information about its inaccurate gaze responses; but virtually no change in hypermetria was noted. These observations suggest that there is no obvious causal relationship between changes in dynamics and in accuracy of gaze shifts after muscimol injection in the cFN. Eye and head both contribute to the dysmetria of gaze. Indeed, muscimol injection leads to parallel changes in amplitude of both ocular and cephalic components. As a global result, the relative contribution of eye and head to the amplitude of ipsiversive gaze shifts remains statistically indistinguishable from that of control responses, and a small (1.6 degrees) increase in the head contribution to contraversive gaze shifts is found. The delay between eye and head movement onsets is increased by 7.3 +/- 7.4 ms for contraversive and decreased by 8.3 +/- 10.1 ms for ipsiversive gaze shifts, corresponding respectively to an increased or decreased lead time of head movement initiation. The modest changes in gaze dynamics, the absence of a link between eventual dynamics changes and dysmetria, and a similar pattern of eye-head coordination to that of control responses, altogether are compatible with the hypothesis that the hypermetria of ipsiversive gaze shifts results from an impaired specification of the metrics of the impending gaze shift. Regarding contraversive gaze shifts, the weak changes in head contribution do not seem to reflect a pathological coordination between eye and head but would rather result from the tonic deviations of gaze and head toward the inactivated side. Hence, our data suggest that the hypometria of contraversive gaze shifts also might result largely from an alteration of processes that specify the goal rather than the on-going trajectory, of saccadic gaze shifts.

Altered visuo-motor behavior during inactivation of the caudal fastigial nucleus in the cat.

It is known that the medio-posterior cerebellar lobules VI/VII of the vermis and caudal part of the fastigial nucleus (cFN) are involved in the control of saccadic displacements of the visual axis in space (gaze). We have recently shown in the head-unrestrained cat that inactivation of the cFN severely impairs the accuracy of orienting gaze shifts toward visual targets by altering the amplitude of both eye and head components. In the present paper, we report additional data that indicate that the deficits induced by cFN inactivation are not restricted to saccadic gaze shifts but extend to the forward reaching movement of the whole body toward a visual target. Indeed, the path followed by the animal walking toward a visible food target was systematically curved toward the inactivated side. This deficit could largely be accounted for by an angular bias in the heading direction used by the animal to reach the target. These data suggest that pharmacological inactivation of the cFN leads to a general deficit in spatial orientation.

Eye saccade dynamics during paradoxical sleep in the cat.

Cat eye movements were recorded during wakefulness and paradoxical sleep with the technique of the scleral search coil in a magnetic field. During waking, eye movements consisted of a succession of saccades and fixation phases. During paradoxical sleep, the pattern of eye movements displayed drifts of variable velocity and direction and short fixation phases, upon which saccades superimposed. These saccades displayed a repetitive, stereotyped, asymmetrical pattern. The maximum velocity/amplitude relationships, i.e. the main sequences, were determined for spontaneous and visually induced saccades of waking and for the following types of saccades during paradoxical sleep: (i) isolated saccades accompanied by ponto-geniculo-occipital (PGO) waves, (ii) isolated saccades accompanied by eye movement potentials (EMP), and (iii) saccades in bursts accompanied by PGO waves. The slope of the main sequence relationship of any type of paradoxical sleep saccade (from 21.7 degrees/s/degree for isolated saccades to 35.6 degrees/s/degree for saccades in bursts) was higher than that of any type of waking saccade (11.2 degrees/s/degree for spontaneous saccades to 14.7 degrees/s/degree for visually elicited ones). Furthermore, during paradoxical sleep, saccades in bursts were faster than isolated ones. This demonstrates that different neurophysiological mechanisms subserve the generation of waking saccades, paradoxical sleep isolated saccades and paradoxical sleep saccades in bursts, or that the oculomotor system is in a different state of excitation during these different sets of saccades. These findings throw new light on the functioning of the oculomotor system during paradoxical sleep and are discussed in terms of the functional significance of paradoxical sleep saccades and PGO waves.