Laurent Madelain

Pursuit of the ineffable: perceptual and motor reversals during the tracking of apparent motion

Pursuit can be guided by perceived rather than physical motion, but the temporal relationship between motion perception and pursuit is unknown. We used an apparent motion stimulus consisting of a horizontal row of evenly spaced Kanizsa illusory squares (1.44 deg2): the illusory contours appeared at the midpoints of the illusory squares presented in the previous frame, producing bi-directional apparent motion of the illusory contours (21.5 deg/s) that could be reversed at will. We measured eye movements in five subjects asked to (1) track the motion of the illusory squares, and (2) reverse the perceived direction while continuing to track the squares. We measured the timing of the voluntary perceptual reversals and compared this to the time course of the reversal in tracking direction. We found that subjects could smoothly track the apparent motion of illusory squares and also produce saccade-free reversals in pursuit velocity. The time course of these motor reversals closely followed the measurements of the perceptual reversal and, on average, the perceptual reversals preceded the pursuit reversals by 53 ms, a delay shorter than when the perceptual reversal was visually guided. Smooth pursuit and the perception of motion direction were in temporal register and highly correlated, suggesting that pursuit can provide a real-time readout for the state of motion perception.

Spatial deployment of attention influences both saccadic and pursuit tracking

We examined the effects of changing spatial aspects of attention during oculomotor tracking. Human subjects were instructed to make a discrimination on either the small (0.8 degrees ) central or the large (8 degrees ) peripheral part of a compound stimulus (two counter-rotating concentric rings) while the stimulus either translated across the screen or was stationary. During this period, a transient perturbation with either step or ramp movement profile occurred. For perturbations leading to a change in position larger than the small ring, saccades occurred more frequently and had much shorter latencies (by 135 ms) when attention was directed to the small ring than when attention was directed to the large ring. These latency differences were sufficiently great that from a single saccade one can identify the attentional instruction with 94% accuracy. However, with target steps as small as the small ring, saccade latencies differed less. For pursuit, ramp perturbations caused larger changes in eye velocity with little change in latency when attention was directed to the small ring. Finally, when only the motion of the non-attended ring was perturbed, most subjects showed stronger saccadic responses to perturbations of the small than the large ring, and stronger pursuit responses to perturbations of the large than the small ring. By fitting the saccade latency distributions with the Reddi and Carpenter LATER model, we found that our subjects apparently employed at least two distinct strategies for changing latency when attending large vs. small. We propose that the timing of the saccade decision process depends on both the size of the attended object and the magnitude of the perturbation.

Saccade adaptation as a model of flexible and general motor learning.

The rapid point-to-point movements of the eyes called saccades are the most commonly made movement by humans, yet differ from nearly every other type of motor output in that they are completed too quickly to be adjusted during their execution by visual feedback. Saccadic accuracy remains quite high over a lifetime despite inevitable changes to the physical structures controlling the eyes, indicating that the oculomotor system actively monitors and adjusts motor commands to achieve consistent behavioral production. Indeed, it seems that beyond the ability to compensate for slow, age-related bodily changes, saccades can be modified following traumatic injury or pathology that affects their production, or in response to more short-term systematic alterations to post-saccadic visual feedback in a laboratory setting. These forms of plasticity rely on the visual detection of accuracy errors by a unified set of mechanisms that support the process known as saccade adaptation. Saccade adaptation has been mostly studied as a phenomenon in its own right, outside of motor learning in general. Here, we highlight the commonalities between eye and arm movement adaptation by reviewing the literature across these fields wherever there are compelling overlapping theories or data. Recent exciting findings are challenging previous interpretations of the underlying mechanisms of saccade adaptation with the incorporation of concepts including prediction, reinforcement and contextual learning. We review the emerging ideas and evidence with particular emphasis on the important contributions made by Josh Wallman in this sphere over the past 15 years.

REINFORCING SACCADIC AMPLITUDE VARIABILITY

Saccadic endpoint variability is often viewed as the outcome of neural noise occurring during sensorimotor processing. However, part of this variability might result from operant learning. We tested this hypothesis by reinforcing dispersions of saccadic amplitude distributions, while maintaining constant their medians. In a first experiment we reinforced the least frequent saccadic amplitudes to increase variability, and then reinforced the central part of the amplitude distributions to reduce variability. The target was placed at a constant distance from the fovea after the saccade to maintain the postsaccadic visual signal constant and an auditory reinforcement was delivered depending on saccadic amplitude. The second experiment tested the effects of the contingency. We reinforced high levels of variability in 4 participants, whereas 4 other participants were assigned to a yoked control group. On average, saccadic amplitude standard deviations were doubled while the medians remained mostly unchanged in the experimental participants in both experiments, and variability returned to baseline level when low variability was reinforced. In the control group no consistent changes in amplitude distributions were observed. These results, showing that variability can be reinforced, challenge the idea of a stochastic neural noise. We instead propose that selection processes constrain saccadic amplitude distributions.

Saccade adaptation is unhampered by distractors.

Saccade adaptation has been extensively studied using a paradigm in which a target is displaced during the saccade, inducing an adjustment in saccade amplitude or direction. These changes in saccade amplitude are widely considered to be controlled by the post-saccadic position of the target relative to the fovea. However, because such experiments generally employ only a single target on an otherwise blank screen, the question remains whether the same adaptation could occur if both the target and a similar distractor were present when the saccade landed. To investigate this issue, three experiments were conducted, in which the post-saccadic locations of the target and distractor were varied. Results showed that decreased amplitude adaptation, increased amplitude adaptation, and recovery from adaptation were controlled by the post-saccadic position of the target rather than the distractor. These results imply that target selection is critical to saccade adaptation.

Saccade adaptation goes for the goal.

The oculomotor system maintains saccade accuracy by adjusting saccades that are consistently inaccurate. Four experiments were performed to determine the relative contribution of background and target postsaccadic displacement. Unlike typical saccade adaptation experiments, we used natural image scenes and masked target and background displacements during the saccade to exclude motion signals from allowing detection of the displacements. We found that the background had no effect on saccade gain while the target drove gain changes. Only when the target was blanked after the saccade did we observe some adaptation in the direction of the background displacement. We conclude that target selection is critical to saccade adaptation, and operates effectively against natural image backgrounds.

Operant conditioning of the visual smooth pursuit in young infants

Smooth pursuit is a complex behaviour which is not considered as totally functional at birth. The lack of maturation of the visuo-motor systems is generally invoked to explain this phenomenon. However, if this oculomotor response is an operant behaviour, an alternate explanation may be found in the absence of previous confrontation with the environmental contingencies. A first group of young infants were placed in situations in which their oculomotor responses could produce an auditory stimulus. In such situations, young infants are able to improve their pursuit. Music was randomly delivered to a second group. No music was delivered to a third group. For the last two groups no augmentation of the proportion of slow movements was observed. Our main conclusion is that visual tracking has the properties of an operant behaviour and may be enhanced at birth. These results will be discussed within the frameworks of the behavioural discrepancy and of the maturationist hypotheses of the ocular motor control.

Influence of near threshold visual distractors on perceptual detection and reaching movements.

Providing evidence against a dissociation between conscious vision for perception and unconscious vision for action, recent studies have suggested that perceptual and motor decisions are based on a unique signal but distinct decisional thresholds. The aim of the present study was to provide a direct test of this assumption in a perceptual-motor dual task involving arm movements. In 300 trials, 10 participants performed speeded pointing movements toward a highly visible target located at 10° from the fixation point and ± 45° from the body midline. The target was preceded by one or two close to threshold distractor(s) (80 ms stimulus onset asynchrony) presented ± 30° according to the target location. After each pointing movement, participants judged whether the distractor was present or not on either side of the target. Results showed a robust reaction time facilitation effect and a deviation toward the distractor when the distractor was both present and consciously perceived (Hit). A small reaction time facilitation was also observed when two distractors were physically present but undetected (double-miss)--this facilitation being highly correlated with the physical contrast of the distractors. These results are compatible with the theory proposing that perceptual and motor decisions are based on a common signal but emerge from a contrast dependent fixed threshold for motor responses and a variable context dependent criterion for perceptual responses. This paper thus extends to arm movement control previous findings related to oculomotor control.

Eye tracking a self-moved target with complex hand-target dynamics

Previous work has shown that the ability to track with the eye a moving target is substantially improved when the target is self-moved by the subjects hand compared with when being externally moved. Here, we explored a situation in which the mapping between hand movement and target motion was perturbed by simulating an elastic relationship between the hand and target. Our objective was to determine whether the predictive mechanisms driving eye-hand coordination could be updated to accommodate this complex hand-target dynamics. To fully appreciate the behavioral effects of this perturbation, we compared eye tracking performance when self-moving a target with a rigid mapping (simple) and a spring mapping as well as when the subject tracked target trajectories that he/she had previously generated when using the rigid or spring mapping. Concerning the rigid mapping, our results confirmed that smooth pursuit was more accurate when the target was self-moved than externally moved. In contrast, with the spring mapping, eye tracking had initially similar low spatial accuracy (though shorter temporal lag) in the self versus externally moved conditions. However, within ∼5 min of practice, smooth pursuit improved in the self-moved spring condition, up to a level similar to the self-moved rigid condition. Subsequently, when the mapping unexpectedly switched from spring to rigid, the eye initially followed the expected target trajectory and not the real one, thereby suggesting that subjects used an internal representation of the new hand-target dynamics. Overall, these results emphasize the stunning adaptability of smooth pursuit when self-maneuvering objects with complex dynamics.

Reinforcing saccadic amplitude variability in a visual search task

Human observers often adopt rigid scanning strategies in visual search tasks, even though this may lead to suboptimal performance. Here we ask whether specific levels of saccadic amplitude variability may be induced in a visual search task using reinforcement learning. We designed a new gaze-contingent visual foraging task in which finding a target among distractors was made contingent upon specific saccadic amplitudes. When saccades of rare amplitudes led to displaying the target, the U values (measuring uncertainty) increased by 54.89% on average. They decreased by 41.21% when reinforcing frequent amplitudes. In a noncontingent control group no consistent change in variability occurred. A second experiment revealed that this learning transferred to conventional visual search trials. These results provide experimental support for the importance of reinforcement learning for saccadic amplitude variability in visual search.