Anticipation of physical causality guides eye movements

Causality is a unique feature of human perception. We present here a behavioral investigation of the influence of physical causality during visual pursuit of object collisions. Pursuit and saccadic eye movements of human subjects were recorded during ocular pursuit of two concurrently launched targets, one that moved according to the laws of Newtonian mechanics (the causal target) and the other one that moved in a physically implausible direction (the non-causal target). We found that anticipation of collision evoked early smooth pursuit decelerations. Saccades to non-causal targets were hypermetric and had latencies longer than saccades to causal targets. In conclusion, before and after a collision of two moving objects the oculomotor system implicitly predicts upcoming physically plausible target trajectories

Individual Differences in Impulsivity Predict Anticipatory Eye Movements

Impulsivity is the tendency to act without forethought. It is a personality trait commonly used in the diagnosis of many psychiatric diseases. In clinical practice, impulsivity is estimated using written questionnaires. However, answers to questions might be subject to personal biases and misinterpretations. In order to alleviate this problem, eye movements could be used to study differences in decision processes related to impulsivity. Therefore, we investigated correlations between impulsivity scores obtained with a questionnaire in healthy subjects and characteristics of their anticipatory eye movements in a simple smooth pursuit task. Healthy subjects were asked to answer the UPPS questionnaire (Urgency Premeditation Perseverance and Sensation seeking Impulsive Behavior scale), which distinguishes four independent dimensions of impulsivity: Urgency, lack of Premeditation, lack of Perseverance, and Sensation seeking. The same subjects took part in an oculomotor task that consisted of pursuing a target that moved in a predictable direction. This task reliably evoked anticipatory saccades and smooth eye movements. We found that eye movement characteristics such as latency and velocity were significantly correlated with UPPS scores. The specific correlations between distinct UPPS factors and oculomotor anticipation parameters support the validity of the UPPS construct and corroborate neurobiological explanations for impulsivity. We suggest that the oculomotor approach of impulsivity put forth in the present study could help bridge the gap between psychiatry and physiology

Processing of retinal and extraretinal signals for memory guided saccades during smooth pursuit

of retinal and extraretinal signals for memory-guided saccades during smooth pursuit. J Neurophysiol 93: 1510–1522, 2005. First published October 13, 2004; doi:10.1152/jn.00543.2004. It is an essential feature for the visual system to keep track of self-motion to maintain space constancy. Therefore the saccadic system uses extraretinal information about previous saccades to update the internal representation of memorized targets, an ability that has been identified in behavioral and electrophysiological studies. However, a smooth eye movement induced in the latency period of a memory-guided saccade yielded contradictory results. Indeed some studies described spatially accurate saccades, whereas others reported retinal coding of saccades. Today, it is still unclear how the saccadic system keeps track of smooth eye movements in the absence of vision. Here, we developed an original two-dimensional behavioral paradigm to further investigate how smooth eye displacements could be compensated to ensur

An integrative approach of the oculomotor system

Classically, the oculomotor system is divided into different subsystems each devoted to the control of a particular type of orienting movement, saccadic or smooth. However, this subdivision does not allow the study of higher order properties of the oculomotor system that emerge from the interaction of its parts. Therefore, the first aim of this thesis was to study new properties emerging from the integration of the saccadic and smooth pursuit subsystems (chapters II, III and IV). Similarly, the integration of retinal (position and velocity) and extra-retinal information (expectation, anticipation) was studied (chapters V,VI, VII, VIII). In the last part of this thesis, the important consequences that this integrative approach of the oculomotor system could have in the understanding of pathologies like Parkinson’s disease will be suggested (Perspectives).Thèse d'agrégation de l'enseignement supérieur (neurophysiologie) -- UCL, 200

The oculomotor signature of expected surprise

Expected surprise, defined as the anticipation of uncertainty associated with the occurrence of a future event, plays a major role in gaze shifting and spatial attention. In the present study, we analyzed its impact on oculomotor behavior. We hypothesized that the occurrence of anticipatory saccades could decrease with increasing expected surprise and that its influence on visually-guided responses could be different given the presence of sensory information and perhaps competitive attentional effects. This hypothesis was tested in humans using a saccadic reaction time task in which a cue indicated the future stimulus position. In the 'no expected surprise' condition, the visual target could appear only at one previously cued location. In other conditions, more likely future positions were cued with increasing expected surprise. Anticipation was more frequent and pupil size was larger in the 'no expected surprise' condition compared with all other conditions, probably due to increased arousal. The latency of visually-guided saccades increased linearly with the logarithm of surprise (following Hick's law) but their maximum velocity repeated the arousal-related pattern. Therefore, expected surprise affects anticipatory and visually-guided responses differently. Moreover, these observations suggest a causal chain linking surprise, attention and saccades that could be disrupted in attentional or impulse control disorders

Shared brainstem pathways for saccades and smooth-pursuit eye movements

A long-standing belief holds that the saccadic and smooth-pursuit eye movement systems are composed of largely separate premotor circuits, at least in the brainstem. One crucial prediction predicated on this belief is that the tonic discharge of omnipause neurons (OPNs), which are thought to be part of only the saccadic system, should not be modulated during pursuit eye movements. This report shows that the discharge of OPNs, in contradiction, is modulated downward during pursuit movements. In contrast to their behavior during saccades, where they pause completely for the duration of the movement, the downward modulation during pursuit did not totally silence OPNs. The depth of the downward modulation was correlated with the speed of the ongoing pursuit movement Another type of cell, which we have named saccade/pursuit neurons, was recorded in the paramedian pontine reticular formation near the location of OPNs. This subpopulation of burst cells discharged a cascade of spikes for saccades in a preferred direction. They also displayed a lower-frequency sustained discharge of spikes for the duration of pursuit in the same preferred direction. These data suggest a new type of combined model for the organization of the brainstem saccade/pursuit system. In this new combined model, the OPNs form a common inhibitory mechanism for both types of movements, and the saccade/pursuit neurons participate in the eye-velocity modulation of OPN discharge or membrane polarization during either type of movement

Supplementary eye fields stimulation facilitates anticipatory pursuit

Anticipatory movements are motor responses occurring before likely sensory events in contrast to reflexive actions. Anticipatory movements are necessary to compensate for delays present in sensory and motor systems. Smooth pursuit eye movements are often used as a paradigmatic example for the study of anticipation. However, the neural control of anticipatory pursuit is unknown. A previous study suggested that the supplementary eye fields (SEFs) could play a role in the guidance of smooth pursuit to predictable target motion. In this study, we favored anticipatory responses in monkeys by making the parameters of target motion highly predictable and electrically stimulated the SEF before and during this behavior. Stimulation sites were restricted to regions of the SEF where saccades could not be evoked at the same low currents. We found that electrical microstimulation in the SEF increased the velocity of anticipatory pursuit movements and decreased their latency. These effects will be referred to as anticipatory pursuit facilitation. The degree of facilitation was the largest if the stimulation train was delivered near the end of the fixation period, before the moment when anticipatory pursuit usually begins. No anticipatory smooth eye movements could be evoked during fixation without an expectation of target motion. These results suggest that the SEF pursuit area might be involved in the process of guiding anticipatory pursuit

Facilitation of smooth pursuit initiation by electrical stimulation in the supplementary eye fields

The role of the supplementary eye fields (SEF) during smooth pursuit was investigated with electrical microstimulation. We found that stimulation in the SEF increased the acceleration and velocity of the eyes in the direction of target motion during smooth pursuit initiation but not during sustained pursuit. The increase in eye velocity during initiation will be referred to as pursuit facilitation and was observed at sites where saccades could not be evoked with the same stimulation parameters. On average, electrical stimulation increased eye velocity by approximately 20%. At most sites, the threshold for a significant facilitation was 50 microA with a stimulation frequency of 300 Hz. Facilitation of pursuit initiation depended on the timing of stimulation trains. The effect was most pronounced if the stimulation was delivered before smooth pursuit initiation. On average, eye velocity in stimulation trials increased linearly as a function of eye velocity in control trials, and this function had a slope greater than one, suggesting a multiplicative influence of the stimulation. Stimulation during a fixation task did not evoke smooth eye movements. The latency of catch-up saccades was increased during facilitation, but their accuracy was not affected. Saccades toward stationary targets were not affected by the stimulation. The results are further evidence that the SEF plays a role in smooth pursuit in addition to its known role in saccade planning and suggest that this role may be to control the gain of smooth pursuit during initiation. The covariance between pursuit facilitation and the timing of the catch-up saccade as a result of stimulation suggests that these different eye movements systems are coordinated to achieve a common goal

Stopping smooth pursuit.

If a visual object of interest suddenly starts to move, we will try to follow it with a smooth movement of the eyes. This smooth pursuit response aims to reduce image motion on the retina that could blur visual perception. In recent years, our knowledge of the neural control of smooth pursuit initiation has sharply increased. However, stopping smooth pursuit eye movements is less well understood and will be discussed in this paper. The most straightforward way to study smooth pursuit stopping is by interrupting image motion on the retina. This causes eye velocity to decay exponentially towards zero. However, smooth pursuit stopping is not a passive response, as shown by behavioural and electrophysiological evidence. Moreover, smooth pursuit stopping is particularly influenced by active prediction of the upcoming end of the target. Here, we suggest that a particular class of inhibitory neurons of the brainstem, the omnipause neurons, could play a central role in pursuit stopping. Furthermore, the role of supplementary eye fields of the frontal cortex in smooth pursuit stopping is also discussed.This article is part of the themed issue 'Movement suppression: brain mechanisms for stopping and stillness'