Different time scales of motion integration for anticipatory smooth pursuit and perceptual adaptation

Abstract

When repeatedly exposed to moving stimuli, the oculomotor system elicits anticipatory smooth pursuit (ASP) eye movements, even before the stimulus moves. ASP is affected oppositely to perceptual speed judgments of repetitive moving stimuli: After a sequence of fast stimuli, ASP velocity increases, whereas perceived speed decreases. These two effects--perceptual adaptation and oculomotor priming--could result from adapting a single common internal speed representation that is used for perceptual comparisons and for generating ASP. Here we test this hypothesis by assessing the temporal dependence of both effects on stimulus history. Observers performed speed discriminations on moving random dot stimuli, either while pursuing the movement or maintaining steady fixation. In both cases, responses showed perceptual adaptation: Stimuli preceded by fast speeds were perceived as slower, and vice versa. To evaluate oculomotor priming, we analyzed ASP velocity as a function of average stimulus speed in preceding trials and found strong positive dependencies. Interestingly, maximal priming occurred over short stimulus histories (∼two trials), whereas adaptation was maximal over longer histories (∼15 trials). The temporal dissociation of adaptation and priming suggests different underlying mechanisms. It may be that perceptual adaptation integrates over a relatively long period to robustly calibrate the operating range of the motion system, thereby avoiding interference from transient changes in stimulus speed. On the other hand, the oculomotor system may rapidly prime anticipatory velocity to efficiently match it to that of the pursuit target.

Humans adapt their anticipatory eye movements to the volatility of visual motion properties

“…In contrast, we have not addressed the question of whether and how statistical learning affects visual motion perception throughout our model-generated volatile sequences. In an empirical context similar to ours, Maus et al [10] have recently shown that perceptual adaptation for speed estimation occurs concurrently to priming-based anticipatory pursuit throughout a sequence of motion tracking trials with randomly varying speed. They actually found a robust repulsive adaptation effect, with perceptual judgements biased in favor of faster percepts after seeing stimuli that were slower and vice-versa.…”

“…Note that both these history lengths can be considered short in comparison to the several hundreds of trials that are commonly used in psychophysics and sensorimotor adaptation studies and that, similar to the present study, the inferred characteristic times are even shorter for the buildup of anticipatory eye movements. However, it is also important to note that in the study by Maus et al [10], the generative model underlying the random sequence of motion trials was different and much simpler than in the present study: In particular the role of environmental volatility was not directly addressed there. This makes a direct comparison between their results and ours difficult beyond a qualitative level.…”

“…These typically highlight sequential effects at the time scale of several seconds to minutes or even hours in the case of the adaptation to a persistent sensorimotor relation. Indeed, stimulus history of sensory events influences how the current stimulus is perceived [3][4][5][6][7] and acted upon [8][9][10][11]. Two qualitatively opposite effects of the stimulus history have been described: negative (adaptation), and positive (priming-like) effects.…”

“…Experience-based anticipatory pursuit behavior is remarkable in different aspects. First, its buildup is relatively fast, such that only a few trials are sufficient to observe the effects of specific regularities in the properties of visual motion, such as speed, timing or direction [10,44,46]. Second, it is a robust phenomenon, which has been observed on a large population of human participants and even in non-human primates (for a recent review see [47]).…”

Humans adapt their anticipatory eye movements to the volatility of visual motion properties

“…As shown in this sample screenshot, this was performed by moving a mouse cursor (black triangle) on a continuous rating scale between "Left", to "Unsure" and finally "Right". specific regularities in the properties of visual motion, such as speed, timing or direction [10,44,46]. Second, it is a robust phenomenon, which has been observed on a large population of human participants and even in non-human primates (for a recent review see [47]).…”