Mehmet N. Agaoglu

Non-retinotopic Feature Processing in the Absence of Retinotopic Spatial Layout and the Construction of Perceptual Space from Motion

The spatial representation of a visual scene in the early visual system is well known. The optics of the eye map the three-dimensional environment onto two-dimensional images on the retina. These retinotopic representations are preserved in the early visual system. Retinotopic representations and processing are among the most prevalent concepts in visual neuroscience. However, it has long been known that a retinotopic representation of the stimulus is neither sufficient nor necessary for perception. Saccadic Stimulus Presentation Paradigm and the Ternus-Pikler displays have been used to investigate non-retinotopic processes with and without eye movements, respectively. However, neither of these paradigms eliminates the retinotopic representation of the spatial layout of the stimulus. Here, we investigated how stimulus features are processed in the absence of a retinotopic layout and in the presence of retinotopic conflict. We used anorthoscopic viewing (slit viewing) and pitted a retinotopic feature-processing hypothesis against a non-retinotopic feature-processing hypothesis. Our results support the predictions of the non-retinotopic feature-processing hypothesis and demonstrate the ability of the visual system to operate non-retinotopically at a fine feature processing level in the absence of a retinotopic spatial layout. Our results suggest that perceptual space is actively constructed from the perceptual dimension of motion. The implications of these findings for normal ecological viewing conditions are discussed.

Spatial Patterns of Fixation-Switch Behavior in Strabismic Monkeys

PURPOSE Patients with strabismus perceptually suppress information from one eye to avoid double vision. Mechanisms of visual suppression likely lead to fixation-switch behavior wherein the subject acquires targets with a specific eye depending on target location in space. The purpose of this study was to investigate spatial patterns of fixation-switch behavior in strabismic monkeys. METHODS Eye movements were acquired in three exotropic and one esotropic monkey in a binocular viewing saccade task. Spatial patterns of fixation were analyzed by calculating incidence of using either eye to fixate targets presented at various gaze locations. RESULTS Broadly, spatial fixation patterns and fixation-switch behavior followed expectations if a portion of the temporal retina was suppressed in exotropia and a portion of the nasal retina was suppressed in esotropia. Fixation-switch occurred for horizontal target locations that were approximately greater than halfway between the lines of sight of the foveating and strabismic eyes. Surprisingly, the border between right eye and left eye fixation zones was not sharply defined and there was a significant extent (>10°) over which the monkeys could acquire a target with either eye. CONCLUSIONS We propose that spatial fixation patterns in strabismus can be accounted for in a decision framework wherein the oculomotor system has access to retinal error information from each eye and the brain chooses between them to prepare a saccade. For target locations approximately midway between the two foveae, strength of retinal error representations from each eye is almost equal, leading to trial-to-trial variability in choice of fixating eye.

Motion Information via the Nonfixating Eye Can Drive Optokinetic Nystagmus in Strabismus.

PURPOSE Strabismic patients can perceptually suppress information from one eye to avoid double vision. However, evidence from prior studies shows that some parts of the visual field of the deviated eye are not suppressed. Our goal here was to investigate whether motion information available only to the deviated eye can be utilized by the oculomotor system to drive eye movements. METHODS Binocular eye movements were acquired in two exotropic monkeys in a dichoptic viewing task in which the fixating eye viewed a stationary spot and the deviated eye viewed a 10° × 10° stationary patch that contained a drifting grating stimulus moving at 10°/s to the right or left for 20 seconds. Spatial location and contrast of the grating were systematically varied in subsequent trials. For each trial, mean slow-phase velocity of the optokinetic nystagmus (OKN) elicited by grating motion was calculated. RESULTS We found that OKN responses can be elicited by a motion stimulus presented to the foveal region of the deviated eye. Optokinetic nystagmus magnitude varied depending on which eye was viewing the drifting grating and correlated well with fixation preference and fixation stability (indicators of amblyopia). The magnitude of OKN increased for increased relative contrast of the motion stimulus compared to the fixation spot. CONCLUSIONS Our results show that motion information available only to the deviated eye can drive optokinetic eye movements. We conclude that the brain has access to visual information from portions of the deviated eye (including the fovea) in strabismus that it can use to drive eye movements.

The effective reference frame in perceptual judgments of motion direction

The retinotopic projection of stimulus motion depends both on the motion of the stimulus and the movements of the observer. In this study, we aimed to quantify the contributions of endogenous (retinotopic) and exogenous (spatiotopic and motion-based) reference frames on judgments of motion direction. We used a variant of the induced motion paradigm and we created different experimental conditions in which the predictions of each reference frame were different. Finally, assuming additive contributions from different reference frames, we used a linear model to account for the data. Our results suggest that the effective reference frame for motion perception emerges from an amalgamation of motion-based, retinotopic and spatiotopic reference frames. In determining the percept, the influence of relative motion, defined by a motion-based reference frame, dominates those of retinotopic and spatiotopic motions within a finite region. We interpret these findings within the context of the Reference Frame Metric Field (RFMF) theory, which states that local motion vectors might have perceptual reference-frame fields associated with them, and interactions between these fields determine the selection of the effective reference frame.

Field-like interactions between motion-based reference frames

A reference frame is required to specify how motion is perceived. For example, the motion of part of an object is usually perceived relative to the motion of the object itself. Johansson (Psychological Research, 38, 379–393, 1976) proposed that the perceptual system carries out a vector decomposition, which rewsults in common and relative motion percepts. Because vector decomposition is an ill-posed problem, several studies have introduced constraints by means of which the number of solutions can be substantially reduced. Here, we have adopted an alternative approach and studied how, rather than why, a subset of solutions is selected by the visual system. We propose that each retinotopic motion vector creates a reference-frame field in the retinotopic space, and that the fields created by different motion vectors interact in order to determine a motion vector that will serve as the reference frame at a given point and time in space. To test this theory, we performed a set of psychophysical experiments. The field-like influence of motion-based reference frames was manifested by increased nonspatiotopic percepts of the backward motion of a target square with decreasing distance from a drifting grating. We then sought to determine whether these field-like effects of motion-based reference frames can also be extended to stationary landmarks. The results suggest that reference-field interactions occur only between motion-generated fields. Finally, we investigated whether and how different reference fields interact with each other, and found that different reference-field interactions are nonlinear and depend on how the motion vectors are grouped. These findings are discussed from the perspective of the reference-frame metric field (RFMF) theory, according to which perceptual grouping operations play a central and essential role in determining the prevailing reference frames.

Motion-based nearest vector metric for reference frame selection in the perception of motion.

We investigated how the visual system selects a reference frame for the perception of motion. Two concentric arcs underwent circular motion around the center of the display, where observers fixated. The outer (target) arcs angular velocity profile was modulated by a sine wave midflight whereas the inner (reference) arc moved at a constant angular speed. The task was to report whether the target reversed its direction of motion at any point during its motion. We investigated the effects of spatial and figural factors by systematically varying the radial and angular distances between the arcs, and their relative sizes. We found that the effectiveness of the reference frame decreases with increasing radial- and angular-distance measures. Drastic changes in the relative sizes of the arcs did not influence motion reversal thresholds, suggesting no influence of stimulus form on perceived motion. We also investigated the effect of common velocity by introducing velocity fluctuations to the reference arc as well. We found no effect of whether or not a reference frame has a constant motion. We examined several form- and motion-based metrics, which could potentially unify our findings. We found that a motion-based nearest vector metric can fully account for all the data reported here. These findings suggest that the selection of reference frames for motion processing does not result from a winner-take-all process, but instead, can be explained by a field whose strength decreases with the distance between the nearest motion vectors regardless of the form of the moving objects.

Interaction between stimulus contrast and pre-saccadic crowding

Objects that are briefly flashed around the time of saccades are mislocalized. Previously, robust interactions between saccadic perceptual distortions and stimulus contrast have been reported. It is also known that crowding depends on the contrast of the target and flankers. Here, we investigated how stimulus contrast and crowding interact with pre-saccadic perception. We asked observers to report the orientation of a tilted Gabor presented in the periphery, with or without four flanking vertically oriented Gabors. Observers performed the task either following a saccade or while maintaining fixation. Contrasts of the target and flankers were independently set to either high or low, with equal probability. In both the fixation and saccade conditions, the flanked conditions resulted in worse discrimination performance—the crowding effect. In the unflanked saccade trials, performance significantly decreased with target-to-saccade onset for low-contrast targets but not for high-contrast targets. In the presence of flankers, impending saccades reduced performance only for low-contrast, but not for high-contrast flankers. Interestingly, average performance in the fixation and saccade conditions was mostly similar in all contrast conditions. Moreover, the magnitude of crowding was influenced by saccades only when the target had high contrast and the flankers had low contrasts. Overall, our results are consistent with modulation of perisaccadic spatial localization by contrast and saccadic suppression, but at odds with a recent report of pre-saccadic release of crowding.

Suboptimal eye movements for seeing fine details

Human eyes are never stable, even during attempts of maintaining gaze on a visual target. Considering transient response characteristics of retinal ganglion cells, a certain amount of motion of the eyes is required to efficiently encode information and to prevent neural adaptation. However, excessive motion of the eyes leads to insufficient exposure to the stimuli, which creates blur and reduces visual acuity. Normal miniature eye movements fall in between these extremes, but it is unclear if they are optimally tuned for seeing fine spatial details. We used a state-of-the-art retinal imaging technique with eye tracking to address this question. We sought to determine the optimal gain (stimulus/eye motion ratio) that corresponds to maximum performance in an orientation-discrimination task performed at the fovea. We found that miniature eye movements are tuned but may not be optimal for seeing fine spatial details.

Neural Plasticity Following Surgical Correction of Strabismus in Monkeys

Purpose Although widely practiced, surgical treatment of strabismus has varying levels of success and permanence. In this study we investigated adaptive responses within the brain and the extraocular muscles (EOM) that occur following surgery and therefore determine long-term success of the treatment. Methods Single cell responses were collected from cells in the oculomotor and abducens nuclei before and after two monkeys (M1, M2) with exotropia (divergent strabismus) underwent a strabismus correction surgery that involved weakening of the lateral rectus (LR) and strengthening of the medial rectus (MR) muscle of one eye. Eye movement and neuronal data were collected for up to 10 months after surgery during a monocular viewing smooth-pursuit task. These data were fit with a first-order equation and resulting coefficients were used to estimate the population neuronal drive (ND) to each EOM of both eyes. Results Surgery resulted in a ∼70% reduction in strabismus angle in both animals that reverted toward presurgical misalignment by approximately 6 months after treatment. In the first month after surgery, the ND to the treated MR reduced in one animal and ND to the LR increased in the other animal, both indicating active neural plasticity that reduced the effectiveness of the treatment. Adaptive changes in ND to the untreated eye were also identified. Conclusions Active neural and muscle plasticity corresponding to both the treated and the untreated eye determines longitudinal success following surgical correction of strabismus. Outcome of surgical treatment could be improved by identifying ways to enhance “positive” adaptation and limit “negative” adaptation.

Comparison of Naso-temporal Asymmetry During Monocular Smooth Pursuit, Optokinetic Nystagmus, and Ocular Following Response in Strabismic Monkeys

ABSTRACT Purpose: Under monocular viewing conditions, humans and monkeys with infantile strabismus exhibit asymmetric naso-temporal (N-T) responses to motion stimuli. The goal of this study was to compare and contrast these N-T asymmetries during 3 visually mediated eye tracking tasks—optokinetic nystagmus (OKN), smooth pursuit (SP) response, and ocular following responses (OFR). Methods: Two adult strabismic monkeys were tested under monocular viewing conditions during OKN, SP, or OFR stimulation. OKN stimulus was unidirectional motion of a 30°x30° random dot pattern at 20°, 40°, or 80°/s for 1 minute. OFR stimulus was brief (200 ms) unidirectional motion of a 38°x28°whitenoise at 20°, 40°, or 80°/s. SP stimulus consisted of foveal step-ramp target motion at 10°, 20°, or 40°/s. Results: Mean nasalward steady state gain (0.87±0.16) was larger than temporalward gain (0.67±0.19) during monocular OKN (P<0.001). In monocular OFR, the asymmetry is manifested as a difference in OFR velocity gain (nasalward: 0.33±0.19, temporalward: 0.22±0.12; P=0.007). During monocular SP, mean nasal gain (0.97±0.2) was larger than temporal gain (0.66±0.14; P<0.001) and the mean nasalward acceleration during pursuit initiation (156±61°/s2) was larger than temporalward acceleration (118±77°/s2; P=0.04). Comparison of N-T asymmetry ratio across the 3 conditions using ANOVA showed no significant difference. Conclusions: N-T asymmetries are identified in all 3 visual tracking paradigms in both monkeys with either eye viewing. Our data are consistent with the current hypothesis for the mechanism for N-T asymmetry that invokes an imbalance in cortical drive to brainstem circuits.