Images that move rapidly across the retina of the human eye blur because the retina has sluggish temporal dynamics. Voluntary smooth pursuit eye movements are modeled as matching object velocity to minimize retinal motion and prevent retinal blurring. However, "catch-up" saccades that are ubiquitous during pursuit interrupt it and disrupt clear vision. But catch-up saccades may not be a common feature of ocular pursuit, because their existence has been documented with a small moving spot, the classic pursuit stimulus, which is a weak motion stimulus that may poorly emulate larger pursuit objects. We found that spot pursuit does not generalize to that of larger objects. Observers pursued a spot or a larger virtual object with or without a superimposed spot target. Single-spot targets produced lower pursuit acceleration than larger objects. Critically, more saccadic intrusions occurred when stimuli had a central dot, even when position and velocity errors were equated, suggesting that catch-up saccades result from pursuing a single, small object or a feature on a large one. To determine what differentiates a large object from a small one, we progressively shrank the featureless virtual object and found that catch-up saccade frequency was highest when it fit in the fovea. The results suggest that pursuit of a small target or an object feature recruits a saccade mechanism that does not compensate for a weak motion signal; rather, the target compels foveation. Furthermore, catch-up saccades are likely generated by neural circuitry typically used to foveate small objects or features.
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.
Currently, there are no quantitative studies of smooth pursuit, a behavior attributed to the fovea, in individuals with macular degeneration (MD). We hypothesize that pursuit in MD patients depends on the relative positions of the scotoma and target trajectory. We tested this hypothesis with a scanning laser ophthalmoscope (SLO), which allows for direct visualization of the target on the damaged retina. Monocular microperimetry and eye movements were assessed in eleven individuals with differing degrees of MD. Observers were asked to visually track a 1.7° target that moved in one of eight radial directions at 5°/s–6°/s. Consistent with our hypothesis, pursuit metrics depended on whether the target moved into or out of scotoma. Pursuit gains decreased with increasing scotoma extent in the target's heading direction (p = 0.017). Latencies were higher when the scotoma was present along the target trajectory (in either starting or heading directions, p < 0.001). Furthermore, an analysis of retinal position shows that targets fell on the fixational locus nearly 50% of the time. The results suggest that MD patients are capable of smooth pursuit eye movements, but are limited by target trajectory and scotoma characteristics.
When confronted with a complex moving stimulus, the brain can integrate local element velocities to obtain a single motion signal, or segregate the elements to maintain awareness of their identities. The integrated motion signal can drive smooth-pursuit eye movements (Heinen and Watamaniuk, 1998), whereas the segregated signal guides attentive tracking of individual elements in multiple-object tracking tasks (MOT; Pylyshyn and Storm, 1988). It is evident that these processes can occur simultaneously, because we can effortlessly pursue ambulating creatures while inspecting disjoint moving features, such as arms and legs, but the underlying mechanism is unknown. Here, we provide evidence that separate neural circuits perform the mathematically opposed operations of integration and segregation, by demonstrating with a dual-task paradigm that the two processes do not share attentional resources. Human observers attentively tracked a subset of target elements composing a small MOT stimulus, while pursuing it ocularly as it translated across a computer display. Integration of the multidot stimulus yielded optimal pursuit. Importantly, performing MOT while pursuing the stimulus did not degrade performance on either task compared with when each was performed alone, indicating that they did not share attention. A control experiment showed that pursuit was not driven by integration of only the nontargets, leaving the MOT targets free for segregation. Nor was a predictive strategy used to pursue the stimulus, because sudden changes in its global velocity were accurately followed. The results suggest that separate neural mechanisms can simultaneously segregate and integrate the same motion signals.
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