Lawful tracking of visual motion in humans, macaques, and marmosets in a naturalistic, continuous, and untrained behavioral context.

Much study of the visual system has focused on how humans and monkeys integrate moving stimuli over space and time. Such assessments of spatiotemporal integration provide fundamental grounding for the interpretation of neurophysiological data, as well as how the resulting neural signals support perceptual decisions and behavior. However, the insights supported by classical characterizations of integration performed in humans and rhesus monkeys are potentially limited with respect to both generality and detail: Standard tasks require extensive amounts of training, involve abstract stimulus-response mappings, and depend on combining data across many trials and/or sessions. It is thus of concern that the integration observed in classical tasks involves the recruitment of brain circuits that might not normally subsume natural behaviors, and that quantitative analyses have limited power for characterizing single-trial or single-session processes. Here we bridge these gaps by showing that three primate species (humans, macaques, and marmosets) track the focus of expansion of an optic flow field continuously and without substantial training. This flow-tracking behavior was volitional and reflected substantial temporal integration. Most strikingly, gaze patterns exhibited lawful and nuanced dependencies on random perturbations in the stimulus, such that repetitions of identical flow movies elicited remarkably similar eye movements over long and continuous time periods. These results demonstrate the generality of spatiotemporal integration in natural vision, and offer a means for studying integration outside of artificial tasks while maintaining lawful and highly reliable behavior.

Look where you go: Characterizing eye movements toward optic flow.

When we move through our environment, objects in the visual scene create optic flow patterns on the retina. Even though optic flow is ubiquitous in everyday life, it is not well understood how our eyes naturally respond to it. In small groups of human and non-human primates, optic flow triggers intuitive, uninstructed eye movements to the focus of expansion of the pattern (Knöll, Pillow, & Huk, 2018). Here, we investigate whether such intuitive oculomotor responses to optic flow are generalizable to a larger group of human observers and how eye movements are affected by motion signal strength and task instructions. Observers (N = 43) viewed expanding or contracting optic flow constructed by a cloud of moving dots radiating from or converging toward a focus of expansion that could randomly shift. Results show that 84% of observers tracked the focus of expansion with their eyes without being explicitly instructed to track. Intuitive tracking was tuned to motion signal strength: Saccades landed closer to the focus of expansion, and smooth tracking was more accurate when dot contrast, motion coherence, and translational speed were high. Under explicit tracking instruction, the eyes aligned with the focus of expansion more closely than without instruction. Our results highlight the sensitivity of intuitive eye movements as indicators of visual motion processing in dynamic contexts.

Spatial localization during open-loop smooth pursuit.

Introduction: Numerous previous studies have shown that eye movements induce errors in the localization of briefly flashed stimuli. Remarkably, the error pattern is indicative of the underlying eye movement and the exact experimental condition. For smooth pursuit eye movements (SPEM) and the slow phase of the optokinetic nystagmus (OKN), perceived stimulus locations are shifted in the direction of the ongoing eye movement, with a hemifield asymmetry observed only during SPEM. During the slow phases of the optokinetic afternystagmus (OKAN), however, the error pattern can be described as a perceptual expansion of space. Different from SPEM and OKN, the OKAN is an open-loop eye movement. Methods: Visually guided smooth pursuit can be transformed into an open-loop eye movement by briefly blanking the pursuit target (gap). Here, we examined flash localization during open-loop pursuit and asked, whether localization is also prone to errors and whether these are similar to those found during SPEM or during OKAN. Human subjects tracked a pursuit target. In half of the trials, the target was extinguished for 300 ms (gap) during the steady-state, inducing open-loop pursuit. Flashes were presented during this gap or during steady-state (closed-loop) pursuit. Results: In both conditions, perceived flash locations were shifted in the direction of the eye movement. The overall error pattern was very similar with error size being slightly smaller in the gap condition. The differences between errors in the open- and closed-loop conditions were largest in the central visual field and smallest in the periphery. Discussion: We discuss the findings in light of the neural substrates driving the different forms of eye movements.

Spatiotemporal profile of peri-saccadic contrast sensitivity.

Sensitivity to luminance contrast is reduced just before and during saccades (saccadic suppression), whereas sensitivity to color contrast is unimpaired peri-saccadically and enhanced post-saccadically. The exact spatiotemporal map of these perceptual effects is as yet unknown. Here, we measured detection thresholds for briefly flashed Gaussian blobs modulated in either luminance or chromatic contrast, displayed at a range of eccentricities. Sensitivity to luminance contrast was reduced peri-saccadically by a scaling factor, which was almost constant across retinal space. Saccadic suppression followed a similar time course across all tested eccentricities and was maximal shortly after the saccade onset. Sensitivity to chromatic contrast was enhanced post-saccadically at all tested locations. The enhancement was not specifically linked to the execution of saccades, as it was also observed following a displacement of retinal images comparable to that caused by a saccade. We conclude that luminance and chromatic contrast sensitivities are subject to distinct modulations at the time of saccades, resulting from independent neural processes.

Binocular Mechanisms of 3D Motion Processing.

The visual system must recover important properties of the external environment if its host is to survive. Because the retinae are effectively two-dimensional but the world is three-dimensional (3D), the patterns of stimulation both within and across the eyes must be used to infer the distal stimulus-the environment-in all three dimensions. Moreover, animals and elements in the environment move, which means the input contains rich temporal information. Here, in addition to reviewing the literature, we discuss how and why prior work has focused on purported isolated systems (e.g., stereopsis) or cues (e.g., horizontal disparity) that do not necessarily map elegantly on to the computations and complex patterns of stimulation that arise when visual systems operate within the real world. We thus also introduce the binoptic flow field (BFF) as a description of the 3D motion information available in realistic environments, which can foster the use of ecologically valid yet well-controlled stimuli. Further, it can help clarify how future studies can more directly focus on the computations and stimulus properties the visual system might use to support perception and behavior in a dynamic 3D world.

Spatio-temporal topography of saccadic overestimation of time.

Rapid eye movements (saccades) induce visual misperceptions. A number of studies in recent years have investigated the spatio-temporal profiles of effects like saccadic suppression or perisaccadic mislocalization and revealed substantial functional similarities. Saccade induced chronostasis describes the subjective overestimation of stimulus duration when the stimulus onset falls within a saccade. In this study we aimed to functionally characterize saccade induced chronostasis in greater detail. Specifically we tested if chronostasis is influenced by or functionally related to saccadic suppression. In a first set of experiments, we measured the perceived duration of visual stimuli presented at different spatial positions as a function of presentation time relative to the saccade. We further compared perceived duration during saccades for isoluminant and luminant stimuli. Finally, we investigated whether or not saccade induced chronostasis is dependent on the execution of a saccade itself. We show that chronostasis occurs across the visual field with a clear spatio-temporal tuning. Furthermore, we report chronostasis during simulated saccades, indicating that spurious retinal motion induced by the saccade is a prime origin of the phenomenon.

Spatial perception during pursuit initiation.

Spatial perception is modulated by eye movements. During smooth pursuit, perceived locations are shifted in the direction of the eye movement. During active fixation, visual space is perceptually compressed towards the fovea. In our present study, we were interested to determine the time course of spatial localization during pursuit initiation, i.e. the transition period from fixation to steady-state pursuit. Human observers had to localize briefly flashed targets around the time of pursuit initiation. Our data clearly show that pursuit-like mislocalization starts well before the onset of the eye movement. Our results point towards corollary-discharge as neural source for the observed perceptual effect.

Localisation of auditory targets during optokinetic nystagmus.

Previous studies have shown that the perceived location of visual stimuli briefly flashed during smooth pursuit, saccades, or optokinetic nystagmus (OKN) is not veridical. We investigated whether these mislocalisations can also be observed for brief auditory stimuli presented during OKN. Experiments were carried out in a lightproof sound-attenuated chamber. Participants performed eye movements elicited by visual stimuli. An auditory target (white noise) was presented for 5 ms. Our data clearly indicate that auditory targets are mislocalised during reflexive eye movements. OKN induces a shift of perceived location in the direction of the slow eye movement and is modulated in the temporal vicinity of the fast phase. The mislocalisation is stronger for look- as compared to stare-nystagmus. The size and temporal pattern of the observed mislocalisation are different from that found for visual targets. This suggests that different neural mechanisms are at play to integrate oculomotor signals and information on the spatial location of visual as well as auditory stimuli.