Eye Movements: Early visual processing

Talk Session: Sunday, May 19, 2024, 5:15 – 7:15 pm, Talk Room 2

Talk 1, 5:15 pm

Investigating the relationship between human foveal anatomy and fixation behavior across different visual tasks

Benjamin Moon1 (), Ashley M. Clark1, Krishnamachari Prahalad1, Austin Roorda2, Pavan Tiruveedhula2, Wolf Harmening3, Aleksandr Gutnikov3, Samantha K. Jenks1, Sanjana Kapisthalam1, Michele Rucci1, Jannick P. Rolland1, Martina Poletti1; 1University of Rochester, 2University of California, Berkeley, 3University of Bonn

When looking at fine details, normally sighted observers center stimuli on a specific location in the foveola, the preferred retinal locus. This locus is slightly offset from the point of peak cone density and has been reported to remain consistent between tasks. However, differences in fixational oculomotor behavior are known to occur across tasks, which may lead to fine changes in the average stimulus position on the retina. Here we examined the distribution of the retinal positions of the fixated stimulus in different tasks in relation to cone density across the foveola. Using an adaptive optics scanning laser ophthalmoscope for simultaneous stimulus delivery and retinal imaging, we investigated oculomotor behavior of subjects (N=8) in three different tasks: fixation on a blinking square, a moving Maltese Cross, and a high-acuity Snellen task. Stimulus size was the same across tasks. We then quantified the difference between the average stimulus position on the retina across the tasks with respect to the location where cones are most densely packed. Peak cone densities across subjects varied from 13,847 to 20,897 cones per square degree, and the stimuli remained within the region where cone density was above 70% of the peak density in all conditions. This region spanned on average 0.23 degrees squared. Yet, differences across tasks were present. We found that the stimulus positions in the Snellen task spanned an area that was more than 50% larger on average when compared to either fixation task (p<0.05). Further, we found a small consistent shift (1.5+/-1.1 arcmin, p<0.033) toward the location of peak cone density in the Snellen task compared to the blinking square fixation. Although the mechanism responsible for the observed shift remains unclear, it raises interesting questions, as it does not yield a significant difference in the Nyquist sampling frequency.

Acknowledgements: Supported by NIH grants EY029788, EY018363, EY001319, and EY023591 and German Research Foundation grants Ha5323/6-1 and Ha5323/8-1

Talk 2, 5:30 pm

Minimal retinal slip is sufficient for peak visual acuity in the fovea

Veronika Lukyanova1, Julius Ameln1, Aleksandr Gutnikov1, Jenny Lorén Witten1, Bilge Sayim2, Wolf Harmening1; 1Department of Ophthalmology, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany, 2Sciences Cognitives et Sciences Affectives (SCALab), CNRS, UMR 9193, University of Lille, Lille, France

Humans can resolve visual targets beyond the Nyquist limit of photoreceptor sampling, likely because fixational eye movements (FEM) induce optimal retinal signals. The retinal space covered by a visual stimulus and hence the number of photoreceptors involved in a visual task grows with time, as FEM continuously move the retina across the image. Here, we determined the minimum amount of retinal slip required for achieving maximum visual performance in two visual acuity tasks. Using adaptive optics scanning laser ophthalmoscopy-based microstimulation, Tumbling-E and Two-dot stimuli were displayed in the foveola of two experienced and two naive participants. Therefore, resolution and positional acuity were measured and the cone photoreceptors used in the task were made visible. The amount of naturally occurring retinal slip was manipulated by varying stimulus duration (2-600 ms) and by additionally restricting it in one of the viewing conditions using real-time retinal stabilization. As expected, slip amplitudes increased linearly with increasing stimulus duration in all participants, at individual rates. Drift velocity and the covered area varied across participants, both linked to the individuals’ cone density. Across participants, we found maximum acuity between 0.9 and 1.13 of the cone Nyquist limit for resolution and between 0.26 and 0.57 for positional stimuli. Surprisingly, this was achieved after very short presentation times (80 ms), after which thresholds did not improve significantly. Within 80 ms, drift amplitudes ranged from 0.8 - 1.6 arcmin, equivalent to an absolute retinal slip of 1.5 - 2.4 cone diameters, depending on the participant. On average, resolution thresholds were unaffected by retinal stabilization. During short stimulus durations, positional acuity was better when presented retinally stabilized. These results demonstrate that the human visual system can extract spatial information during time frames that do not allow extended motion paths, and that natural motion is not required to reach maximum performance.

Acknowledgements: Wolf M. Harmening: German Research Foundation, Ha 5323/8-1. Bilge Sayim: Agence Nationale de la Recherche, ANR-19-FRAL-000.

Talk 3, 5:45 pm

Eccentricity, but not color contrast, influences microsaccadic prevention of visual fading

Max Levinson1, Christopher C. Pack1, Sylvain Baillet1; 1McGill University

When the eyes remain still for an extended period of time, visual boundaries can appear to fade. This illusory phenomenon is traditionally attributed to slow neuronal adaptation to stable retinal input. Microsaccades – small, mostly involuntary ocular movements during gaze fixation – counteract fading, but it is unclear exactly how. They might simply refresh the retinal image to reverse adaptation or introduce a unique visual resampling signal that interacts with adapting neural populations. To better understand boundary fading both in itself and as a probe of microsaccade function, we investigated why a stronger boundary, determined by isoluminant color contrast and eccentricity (distance from the visual field center), takes longer to fade. A stronger boundary could either create a more robust cortical signal requiring greater adaptation, and/or enhance the preventive effect of microsaccades. To test these two possibilities we recorded microsaccades during a perceptual filling-in task. Human participants fixated centrally until they experienced illusory merging of two isoluminant colored surfaces, separated by a circular ring boundary, due to perceptual boundary fading. We fit linear mixed models of trial-wise fading time to color contrast, boundary eccentricity, and fixational eye movement dynamics. While both color contrast and eccentricity altered fading time, they did so differently. Higher color contrast extended overall fading time but did not influence the efficacy of individual microsaccades. Conversely, lower eccentricity prolonged fading exclusively via eye movements. These findings demonstrate that stimulus properties can differently influence slow adaptation and microsaccadic counteraction. We propose that microsaccades prevent visual fading via transient boundary stimulation that scales with cortical magnification but is invariant to boundary contrast.

Talk 4, 6:00 pm

How the unstable eye sees a stable and moving world: Redux

Josephine D'Angelo1 (), Pavan Tiruveedhula1, Raymond J. Weber2, David W. Arathorn2, Austin Roorda1; 1University of California, Berkeley, 2Electrical & Computer Engineering, College of Engineering, Montana State University

Despite incessant retinal image motion, humans reliably perceive stable and moving objects in the world. In 2013, Arathorn et al. found that the direction of stimulus motion with respect to fixational eye motion impacts the amount of motion perceived: Subjects perceived motion when stimuli moved in the same direction as eye movements and perceived little to no motion when images moved directly opposite the direction of eye motion, surprisingly even under conditions where that motion was amplified. This suggests that the visual system computes its direction of motion and perceptually renders anything moving in a direction opposite to that eye motion as stable. We asked: How is the direction of eye motion determined? Is world-fixed retinal image background content needed to compute the direction of motion or are non-visual cues (eg. efferent copy) sufficient? We explored this question using an adaptive optics scanning laser ophthalmoscope which performs high resolution eye tracking and delivers retina-contingent stimuli. We quantified perceived motion using a method of adjustment where the subject compared a stimulus moving contingent to the retina and a stimulus moving on a random walk. The subject adjusted the diffusion constant of the random walk stimulus until the perceived motion of both stimuli looked equal. Experiments were done with retinal image background content and with all visual content removed. In the presence of retinal image background content, the perceived motion of stimuli moving with a 2.5X exaggerated retinal slip was suppressed; however, in conditions with no visual content we found that a higher magnitude of motion was perceived. Our results suggest that the presence of retinal image background content provides the primary signal for the visual system to compute its direction of motion, contradicting the intuition that the same content would provide a frame of reference to see that motion.

Acknowledgements: NIH BRP R01EY023591; NIH T32 EY007043

Talk 5, 6:15 pm

Sound activates a dormant visual-motor pathway bypassing primary visual cortex

Tatiana Malevich1,2,3 (), Yue Yu1,2,3, Matthias P. Baumann1,2,3, Tong Zhang1,2,3, Ziad M. Hafed1,2,3; 1Hertie Institute for Clinical Brain Research, Tuebingen, Germany, 2Werner Reichardt Centre for Integrative Neuroscience, Tuebingen, Germany, 3University of Tuebingen

Like in other species, the primate visual system contains an anatomical retinal projection bypassing the geniculostriate pathway and innervating the midbrain. However, unlike in some of these species, the functional significance of this alternative visual pathway remains unknown: increasing evidence suggests that it may be completely dormant. We first tested this by performing focal, reversible inactivation of the primary visual cortex (V1) and investigating a short-latency oculomotor reflex believed to rely on subcortical eye-movement control circuits. This reflex, called saccadic inhibition (recently reviewed by Buonocore and Hafed, 2023), is characterized by a short-latency inhibition of saccade generation by visual stimuli, as well as by a concomitant saccade direction biasing, first towards and then away from stimulus location. When we created a localized cortical scotoma, saccadic inhibition was completely abolished for stimuli in the blind field, confirming the geniculostriate pathway’s dominance. Superior colliculus visual responses were also eliminated. However, why does the alternative visual pathway, directly targeting oculomotor control circuits, exist at all? We hypothesized that this pathway might still be functional, albeit in a gated manner. During V1 inactivation, we paired a visual onset with a sound pulse (50 ms; 1 KHz; suprathreshold) that was completely uninformative about the visual stimulus’ location. Saccadic inhibition was partially restored, and it was different to when the sound pulse occurred alone. Most importantly, there was a re-emergence of saccade direction biasing towards the visual stimulus location, even though the sound was not spatially informative. Guessed visually-guided saccades towards a target presented in the blind field were also mildly more accurate with the uninformative sound. These results demonstrate that multi-sensory information can activate an otherwise dormant visual-motor pathway. These results also highlight the importance of multi-species comparisons of hierarchical sensory-motor processes, and they especially inform models of active sensory-guided behavior invoking parallel processing streams.

Talk 6, 6:30 pm

Temporal dynamics of serial dependence in ocular tracking

Bao Hong1,3 (), Jing Chen2,3, Li Li2,3; 1East China Normal University, Shanghai, China, 2New York University Shanghai, Shanghai, China, 3NYU-ECNU Institute of Brain and Cognitive Science at New York University Shanghai, Shanghai, China

An outstanding question regarding serial dependence is the level at which it operates—some argue for its direct influence on perception, while others posit that serial dependence only impacts post-perceptual processes. Here we examined when serial dependence appears and disappears to address this issue. We developed an ocular tracking task consisting of distinct temporal phases of tracking (retinal-motion-driven pursuit initiation vs. extraretinal-signal-supported steady-state tracking), coupled with high-resolution eye movement recordings, to provide an ideal testing paradigm for this purpose. Participants (N=16) tracked the step-ramp motion of a target spot (diameter: 0.64º; speed: 16º/s; direction: randomly drawn from the full 360° circle at the step size of 12°). We performed model-dependent analyses to measure the extent to which pursuit directions through the course of the current trial were affected by the previous target moving direction, with positive values indicating attraction and serial dependence and negative values indicating repulsion and adaptation. We observed a strong serial dependence at pursuit initiation that quickly declined over time, followed by a low-amplitude adaptation that remained stable throughout steady-state tracking. This result shows that serial dependence happens before adaptation in ocular tracking, providing evidence that serial dependence influences perception. We also found a strong correlation (r=0.88) between the strength of serial dependence and pursuit direction noise. Using a Bayesian observer model constrained by efficient coding, we further found that the temporal dynamics of serial dependence can be predicted by pursuit direction noise over time. This supports our proposal that the visual system may strike a balance between utilizing the temporal continuity of the physical environment (through serial dependence) and optimizing sensitivity to subtle changes in the environment (through adaptation), and this balance is regulated by sensory noise.

Acknowledgements: Supported by research grants from the National Natural Science Foundation of China (32071041, 32161133009); China Ministry of Education (ECNU 111 Project, Base B1601); the major grant seed fund and the boost fund from NYU Shanghai

Talk 7, 6:45 pm

Identifying the neural origins of pupil constrictions in response to isoluminant stimuli using contrast adaptation

Vasilii Marshev1 (), Haley Frey2, Jan Brascamp1; 1MSU, 2UC Berkeley

The events causing transient pupil constriction stretch beyond increased illumination. For example, changes in stimulus structure (orientation, color, motion) can cause constriction even if net illumination stays the same. Two explanations for this have been proposed: some argue that altered cortical feature-based responses cause constriction via their input to pupil control nuclei, others argue that local increases in retinal receptor drive a pupil light reflex even if net illuminance does not increase. We tested the two theories using orientation-specific adaptation, which is thought to have a cortical origin. Accordingly, reduced pupil constrictions following orientation-specific adaptation would support a cortical origin of these constrictions. Subjects’ pupil size was recorded while oblique test gratings were presented following presentation of a sliding high-contrast (100%) adapter grating. A test grating’s orientation could be either parallel or orthogonal to that of the adapter that preceded it. In Experiment 1, low-contrast test gratings, with a net luminance equal to that of the background, caused a constriction, but this response was the same for parallel and orthogonal gratings, even though perceptual judgments confirmed the presence of orientation-specific adaptation. In Experiment 2, test contrast was increased to produce more robust constrictions. Still, no orientation-specific modulation was observed. In Experiment 3 we used a test grating in which no pixel had a higher luminance than the background, thus minimizing the possibility of local increases in retinal receptor drive to light reflex. We again observed a transient pupil constriction but no orientation-specific modulation. While our results confirm that the pupil can constrict in response to stimuli that involve no global (Experiments 1-2) or even local (Experiment 3) luminance increases, they do not support the idea that these constrictions reflect altered cortical feature-based responses.

Talk 8, 7:00 pm

Effects of Pupil Size as Manipulated through ipRGC Activation on Visual Processing

Sebastiaan Mathôt1 (), Hermine Berberyan2, Philipp Büchel1, Veera Ruuskanen1, Ana Vilotjević1, Wouter Kruijne1; 1Department of Psychology, University of Groningen, The Netherlands, 2PwC, Amsterdam, The Netherlands

The size of the eyes’ pupils determines how much light enters the eye and also how well this light is focused. Through this route, pupil size shapes the earliest stages of visual processing. Yet causal effects of pupil size on vision are poorly understood and rarely studied. Here we introduce a new way to manipulate pupil size, which relies on activation of intrinsically photosensitive retinal ganglion cells (ipRGCs) to induce sustained pupil constriction. We report the effects of both experimentally induced and spontaneous changes in pupil size on visual processing as measured through EEG, and compare these to the effects of stimulus intensity and covert visual attention, because previous studies have shown that these factors all have comparable effects on some common measures of early visual processing. Using a mix of neural-network decoding, ERP analyses, and time-frequency analyses, we find that induced pupil size, spontaneous pupil size, stimulus intensity, and covert visual attention all affect EEG responses, mainly over occipital and parietal electrodes, but—crucially—that they do so in qualitatively different ways. Induced and spontaneous pupil-size changes mainly modulate activity patterns (but not overall power or intertrial coherence) in the high-frequency beta range; this may reflect an effect of pupil size on oculomotor activity and/ or visual processing. In addition, spontaneous (but not induced) pupil size tends to correlate positively with intertrial coherence in the alpha band; this may reflect a non-causal relationship, mediated by arousal. Taken together, our findings suggest that pupil size has qualitatively different effects on visual processing from stimulus intensity and covert visual attention. This suggests that pupil size strongly affects visual processing, and provides concrete starting points for further study of this important yet understudied earliest stage of visual processing.