Jean-Louis Vercher

Oculo-manual tracking of visual targets: control learning, coordination control and coordination model.

SummaryThe processes which develop to coordinate eye and hand movements in response to motion of a visual target were studied in young children and adults. We have shown that functional maturation of the coordination control between eye and hand takes place as a result of training. We observed, in the trained child and in the adult, that when the hand is used either as a target or to track a visual target, the dynamic characteristics of the smooth pursuit system are markedly improved: the eye to target delay is decreased from 150 ms in eye alone tracking to 30 ms, and smooth pursuit maximum velocity is increased by 100%. Coordination signals between arm and eye motor systems may be responsible for smooth pursuit eye movements which occur during self-tracking of hand or finger in darkness. These signals may also account for the higher velocity smooth pursuit eye movements and the shortened tracking delay when the hand is used as a target, as well as for the synkinetic eye-arm motions observed at the early stage of oculo-manual tracking training in children. We propose a model to describe the interaction which develops between two systems involved in the execution of a common sensorimotor task. The model applies to the visuo-oculo-manual tracking system, but it may be generalized to other coordinated systems. According to our definition, coordination control results from the reciprocal transfer of sensory and motor information between two or more systems involved in the execution of single, goal-directed or conjugate actions. This control, originating in one or more highly specialized structures of the central nervous system, combines with the control processes normally operating in each system. Our model relies on two essential notions which describe the dynamic and static aspects of coordination control: timing and mutual coupling.

EYE-HEAD-HAND COORDINATION IN POINTING AT VISUAL TARGETS - SPATIAL AND TEMPORAL ANALYSIS

This study investigated whether the execution of an accurate pointing response depends on a prior saccade orientation towards the target, independent of the vision of the limb. A comparison was made between the accuracy of sequential responses (in which the starting position of the hand is known and the eye centred on the target prior to the onset of the hand pointing movement) and synergetic responses (where both hand and gaze motions are simultaneously initiated on the basis of unique peripheral retinal information). The experiments were conducted in visual closed-loop (hand visible during the pointing movement) and in visual openloop conditions (vision of hand interrupted as the hand started to move). The latter condition eliminated the possibility of a direct visual evaluation of the error between hand and target during pointing. Three main observations were derived from the present work: (a) the timing of coordinated eye-head-hand pointing at visual targets can be modified, depending on the executed task, without a deterioration in the accuracy of hand pointing; (b) mechanical constraints or instructions such as preventing eye, head or trunk motion, which limit the redundancy of degrees of freedom, lead to a decrease in accuracy; (c) the synergetic movement of eye, head and hand for pointing at a visible target is not trivially the superposition of eye and head shifts added to hand pointing. Indeed, the strategy of such a coordinated action can modify the kinematics of the head in order to make the movements of both head and hand terminate at approximately the same time. The main conclusion is that eye-head coordination is carried out optimally by a parallel processing in which both gaze and hand motor responses are initiated on the basis of a poorly defined retinal signal. The accuracy in hand pointing is not conditioned by head movement per se and does not depend on the relative timing of eye, head and hand movements (synergetic vs sequential responses). However, a decrease in the accuracy of hand pointing was observed in the synergetic condition, when target fixation was not stabilised before the target was extinguished. This suggests that when the orienting saccade reaches the target before hand movement onset, visual updating of the hand motor control signal may occur. A rapid processing of this final input allows a sharper redefinition of the hand landing point.

Cerebellar involvement in the coordination control of the oculo-manual tracking system: effects of cerebellar dentate nucleus lesion

SummaryWhen the hand of the observer is used as a visual target, oculomotor performance evaluated in terms of tracking accuracy, delay and maximal ocular velocity is higher than when the subject tracks a visual target presented on a screen. The coordination control exerted by the motor system of the arm on the oculomotor system has two sources: the transfer of kinaesthetic information originating in the arm which increases the mutual coupling between the arm and the eyes and information from the arm movement efferent copy which synchronizes the motor activities of both subsystems (Gauthier et al. 1988; Gauthier and Mussa-Ivaldi 1988). We investigated the involvement of the cerebellum in coordination control during a visuo-oculo-manual tracking task. Experiments were conducted on baboons trained to track visual targets with the eyes and/or the hand. The role of the cerebellum was determined by comparing tracking performance defined in terms of delay, accuracy (position or velocity tracking errors) and maximal velocity, before and after lesioning the cerebellar dentate nucleus. Results showed that in the intact animal, ocular tracking was more saccadic when the monkey followed an external target than when it moved the target with its hand. After lesioning, eye-alone tracking of a visual target as well as eye-and-hand-tracking with the hand contralateral to the lesion was little if at all affected. Conversely, ocular tracking of the hand ipsilateral to the lesion side became more saccadic and the correlation between eye and hand movement decreased considerably while the delay between target and eyes increased. In normal animals, the delay between the eyes and the hand was close to zero, and maximal smooth pursuit velocity was around 100 degrees per second with close to unity gain; in eye-alone tracking the delay and maximal smooth pursuit velocity were 200 ms and 50 deg per second, respectively. After lesioning, delay and maximum velocity were respecttively around 210 ms and 40 deg per second, that is close to the values measured in eye-alone tracking. Thus, after dentate lesioning, the oculomotor system was unable to use information from the motor system of the arm to enhance its performance. We conclude that the cerebellum is involved in the “coordination control” between the oculomotor and manual motor systems in visuo-oculo-manual tracking tasks.

Oculo-manual coordination control: ocular and manual tracking of visual targets with delayed visual feedback of the hand motion

SummaryThe aim of this study was to examine coordination control in eye and hand tracking of visual targets. We studied eye tracking of a self-moved target, and simultaneous eye and hand tracking of an external visual target moving horizontally on a screen. Predictive features of eye-hand coordination control were studied by introducing a delay (0 to 450 ms) between the Subjects (Ss) hand motion and the motion of the hand-driven target on the screen. In self-moved target tracking with artificial delay, the eyes started to move in response to arm movement while the visual target was still motionless, that is before any retinal slip had been produced. The signal likely to trigger smooth pursuit in that condition must be derived from non-visual information. Candidates are efference copy and afferent signals from arm motion. When tracking an external target with the eyes and the hand, in a condition where a delay was introduced in the visual feedback loop of the hand, the Ss anticipated with the arm the movement of the target in order to compensate the delay. After a short tracking period, Ss were able to track with a low lag, or eventually to create a lead between the hand and the target. This was observed if the delay was less than 250–300 ms. For larger delays, the hand lagged the target by 250–300 ms. Ss did not completely compensate the delay and did not, on the average, correct for sudden changes in movement of the target (at the direction reversal of the trajectory). Conversely, in the whole range of studied delays (0–450 ms), the eyes were always in phase with the visual target (except during the first part of the first cycle of the movement, as seen previously). These findings are discussed in relation to a scheme in which both predictive (dynamic nature of the motion) and coordination (eye and hand movement system interactive signals) controls are included.

Mechanisms of short-term saccadic adaptation.

A number of processes have been identified that adaptively modify oculomotor control components. The adaptive process studied here can be reliably produced over a short period of time by a visual stimulus that forces postsaccadic error. This short-term adaptive process, usually termed parametric adaptation, consists of a change in response amplitude that develops progressively over 50 to 100 training stimuli. The resulting compensation is proportional to, but substantially less than, the error induced by the training stimuli. Both increases and decreases in response amplitude can be evoked by an appropriately timed and directed movement of the stimulus target, which forces postsaccadic error. Results show that a single type of training stimulus can influence movements over a broad spatial region, provided these movements are in the same direction as the training stimulus. Experiments that map the range of modification suggest that the increasing adaptive modification operates by remapping final position, whereas the decreasing adaptive modification is achieved through an overall reduction of gain. Training stimuli that attempt to evoke both increases and decreases in the same region show a net modification equivalent to the algebraic addition of individual adaptive processes.

Oculo-manual coordination control: respective role of visual and non-visual information in ocular tracking of self-moved targets

We evaluated the role of visual and non-visual information in the control of smooth pursuit movements during tracking of a self-moved target. Previous works have shown that self-moved target tracking is characterised by shorter smooth pursuit latency and higher maximal velocity than eye-alone tracking. In fact, when a subject tracks a visual target controlled by his own arm, eye movement and arm movement are closely synchronised. In the present study, we showed that, in a condition where the direction of motion of a self-moved visual target was opposite to that of the arm (same amplitude, same velocity, but opposite direction of movement), the resulting smooth pursuit eye movements occurred with low latency, and continued for about 140 ms in the direction of the arm movement rather than in the direction of the actual visual target movement. After 140 ms, the eye movement direction reversed through a combination of smooth pursuit and saccades. Subsequently, while arm and visual target still moved in opposite directions, smooth pursuit occurred in pace with the visual target motion. Subjects were also submitted to a series of 60 tracking trials, for which the arm-to-target motion relationship was systematically reversed. Under these conditions subjects were able to initiate early smooth pursuit in the actual direction of the visual target. Overall, these results confirm that non-visual information produced by the arm motor system can trigger and control smooth pursuit. They also demonstrate the plasticity of the neuronal network handling eye-arm coordination control.

Visual vestibular interaction: vestibulo-ocular reflex suppression with head-fixed target fixation.

SummaryIn order to maintain clear vision, the images on the retina must remain reasonably stable. Head movements are generally dealt with successfully by counterrotation of the eyes induced by the combined actions of the vestibulo-ocular reflex (VOR) and the opto-kinetic reflex. We have studied how, in humans, the VOR gain (VORG) is modulated to provide appropriate eye movements in two situations: 1. fixation of a stationary object of the visual space while the head moves. This requires a visuo-vestibulo-ocular reaction to induce eye movements opposite in direction, and equal in velocity to head movements, and 2. fixation of an object moving with the head. Here, the visuo-vestibulo-ocular reaction should be totally suppressed. These two situations were compared to a basic condition in which, to induce “pure” VOR, the subjects (Ss) in darkness were not allowed a visual target. Eye movements were recorded in seated Ss during constant amplitude sinusoidal and pulse-like passive rotations applied around the vertical axis. Subjects were in total darkness (DARK condition) and performing mental arithmetic. Alternatively, they were provided with a small target, either stationary with respect to earth (earth-fixed target: EFT), or moving with them (chairfixed-target: CFT). The sinusoidal rotation experiment was used as baseline for the ensuing experiments and yielded control data in agreement with the literature. In particular, rotation in the dark showed a VORG of 0.6. With, for example, 0.8 s passive pulse rotations, typical responses in all three visual conditions were rigorously identical during the first 150 to 180 ms. They showed a delay of about 16 ms of the eye behind the head with no significant difference between passive whole-body and passive head-alone rotations. In all conditions, once the eyes had started to move, a rapid increase in eye velocity was observed during 75 to 80 ms, after which, the average VORG was 0.9 ± 0.15. During the following 50 to 100 ms, the gain remained around 0.9 in all three conditions. Beyond 180 ms, the VORG remained around 0.9 in DARK, increased slowly towards 1 or decreased towards zero in the EFT and CFT conditions, respectively. The time-course of these later events suggests that visual tracking mechanisms came into play to reduce retinal slip through smooth pursuit. Sinusoidal rotations, extensively used in VOR studies, do not seem to be a satisfactory stimulus to rapidly and precisely characterize VOR function, particularly in pathological cases. Our data suggest that rapid transient rotations are more appropriate.

The role of ocular muscle proprioception during modifications in smooth pursuit output

The output of the smooth pursuit (SP) system can be increased by adding a portion of the recorded eye motion onto target motion, producing a situation analogous to that occurring with weakened ocular muscles. This change is most likely the result of alterations in the signals that code eye and target motion. We have assessed the contribution of one such signal, that arising from ocular proprioception, to the modification process during monocular SP by preventing the motion of the non-viewing eye with a suction scleral lens. The large increases normally observed for SP velocity following the modification period were substantially reduced under these conditions. Similar alterations were also observed in a manual tracking task. These results demonstrate that ocular proprioceptive signals serve to stabilize the output of the SP system following perturbations, via the recoding of eye and target motion.

INTERNAL REPRESENTATION OF GAZE DIRECTION WITH AND WITHOUT RETINAL INPUTS IN MAN

The contribution of retinal and extraretinal signals to the coding of eye position in the head was studied in human subjects (Ss). Horizontal saccades were produced in darkness. For some trials, before returning gaze direction to the starting position, a visual signal briefly stimulated the foveal retina. Results showed that this retinal input helped Ss to perceive gaze orientation more accurately after the saccade suggesting that the internal representation of eye position was improved when both extraretinal and retinal signals were available.

Egocentric visual target position and velocity coding: Role of ocular muscle proprioception

Limited knowledge is available regarding the processes by which the brain codes the velocity of visual targets with respect to the observer. Two models have been previously proposed to describe the visual target localization mechanism. Both assume that the necessary information is derived from the coding of the position of the eye in the orbit, either through a copy of the muscular activation (out flow model) or through eye muscle proprioception (in flow model). Eye velocity coding might be derived from velocity sensitive ocular muscle proprioceptors or from position coding signals through differentiation. We used techniques based on manual pointing and manual tracking of visual target, combined with passive deviation of one covered eye, to demonstrate that ocular muscle proprioception is involved in (i) eye-in-head position coding, hence in target localization function; (ii) long-term maintenance of ocular alignment (phoria); and (iii) sensing of visual target velocity with respect to the head. These observations support other data now available, describing the processes by which the brain codes position and velocity of visual targets. Such findings might interest engineers in the field of robotics who are facing the problem of providing robots with the ability to sense object position and velocity in order to create an internal model of their working environment.