Collective plasticity of binocular interactions in the adult visual system.

Binocular visual plasticity can be initiated via either bottom-up or top-down mechanisms, but it is unknown if these two forms of adult plasticity can be independently combined. In seven participants with normal binocular vision, sensory eye dominance was assessed using a binocular rivalry task, before and after a period of monocular deprivation and with and without selective attention directed towards one eye. On each trial, participants reported the dominant monocular target and the inter-ocular contrast difference between the stimuli was systematically altered to obtain estimates of ocular dominance. We found that both monocular light- and pattern-deprivation shifted dominance in favour of the deprived eye. However, this shift was completely counteracted if the non-deprived eye's stimulus was selectively attended. These results reveal that shifts in ocular dominance, driven by bottom-up and top-down selection, appear to act independently to regulate the relative contrast gain between the two eyes.

Eye movements in visual impairment.

This Special Issue describes the impact of visual impairment on visuomotor function. It includes contributions that examine gaze control in conditions associated with abnormal visual development such as amblyopia, dyslexia and neurofibromatosis as well as disorders associated with field loss later in life, such as macular degeneration and stroke. Specifically, the papers address both gaze holding (fixation), and gaze-following behavior (single saccades, sequences of saccades and smooth-pursuit) that characterize active vision in daily life and evaluate the influence of both pathological and simulated field loss. Several papers address the challenges to reading and visual search; describing how the patterns of eye movements in these real-world tasks adapt to visual impairment and highlighting how they could serve as diagnostic markers of visuomotor function.

The effects of simulated hemianopia on eye movements during text reading.

Vision loss is a common, devastating complication of cerebral strokes. In some cases the complete contra-lesional visual field is affected, leading to problems with routine tasks and, notably, the ability to read. Although visual information crucial for reading is imaged on the foveal region, readers often extract useful parafoveal information from the next word or two in the text. In hemianopic field loss, parafoveal processing is compromised, shrinking the visual span and resulting in slower reading speeds. Recent approaches to rehabilitation using perceptual training have been able to demonstrate some recovery of useful visual capacity. As gains in visual sensitivity were most pronounced at the border of the scotoma, it may be possible to use training to restore some of the lost visual span for reading. As restitutive approaches often involve prolonged training sessions, it would be beneficial to know how much recovery is required to restore reading ability. To address this issue, we employed a gaze-contingent paradigm using a low-pass filter to blur one side of the text, functionally simulating a visual field defect. The degree of blurring acts as a proxy for visual function recovery that could arise from restitutive strategies, and allows us to evaluate and quantify the degree of visual recovery required to support normal reading fluency in patients. Because reading ability changes with age, we recruited a group of younger participants, and another with older participants who are closer in age to risk groups for ischaemic strokes. Our results show that changes in patterns of eye movement observed in hemianopic loss can be captured using this simulated reading environment. This opens up the possibility of using participants with normal visual function to help identify the most promising strategies for ameliorating hemianopic loss, before translation to patient groups.

The spatial properties of adaptation-induced distance compression.

Exposure to a dynamic texture reduces the perceived separation between objects, altering the mapping between physical relations in the environment and their neural representations. Here we investigated the spatial tuning and spatial frame of reference of this aftereffect to understand the stage(s) of processing where adaptation-induced changes occur. In Experiment 1, we measured apparent separation at different positions relative to the adapted area, revealing a strong but tightly tuned compression effect. We next tested the spatial frame of reference of the effect, either by introducing a gaze shift between adaptation and test phase (Experiment 2) or by decoupling the spatial selectivity of adaptation in retinotopic and world-centered coordinates (Experiment 3). Results across the two experiments indicated that both retinotopic and world-centered adaptation effects can occur independently. Spatial attention to the location of the adaptor alone could not account for the world-centered transfer we observed, and retinotopic adaptation did not transfer to world-centered coordinates after a saccade (Experiment 4). Finally, we found that aftereffects in different reference frames have a similar, narrow spatial tuning profile (Experiment 5). Together, our results suggest that the neural representation of local separation resides early in the visual cortex, but it can also be modulated by activity in higher visual areas.

Disruption of Positional Encoding at Small Separations in the Amblyopic Periphery.

Purpose: Positional judgments in amblyopia are impaired more at the center of the visual field than in the periphery. However, the effects of visual field position frequently are confounded with stimulus separation. The purpose of this experiment was to parse the effects of stimulus separation and eccentricity on the positional deficit in amblyopia. Methods: Subjects adjusted the positions of stimuli of varying separations on isoeccentric arcs. The task was simultaneous bisection and alignment of broadband, high-contrast, uncrowded targets with reference to central fixation. Ten strabismic amblyopes and five normally sighted controls performed the task dichoptically; a subset of amblyopes performed the task monocularly with the amblyopic eye. Spread (inverse of precision) and bias were measured at multiple visual field locations comprising two to three separation \(\times\) four eccentricity conditions in each visual field quadrant. Results: In normal controls, both spread and bias increased with eccentricity, and spread (but not bias) increased linearly with separation until 7° eccentricity. Strabismic amblyopes showed a different profile: spread and bias were higher at small separations at all eccentricities, such that performance showed a quadratic trend against separation. Thus, at each eccentricity, the difference in performance between groups was largest at the smallest separation. Conclusions: These results are consistent with disruptions in Weber mechanisms of positional encoding in strabismic amblyopia, and indicate that binocular stimulation by proximal targets produces a loss of spatial precision well beyond the fovea.

Learning to silence saccadic suppression.

Perceptual stability is facilitated by a decrease in visual sensitivity during rapid eye movements, called saccadic suppression. While a large body of evidence demonstrates that saccadic programming is plastic, little is known about whether the perceptual consequences of saccades can be modified. Here, we demonstrate that saccadic suppression is attenuated during learning on a standard visual detection-in-noise task, to the point that it is effectively silenced. Across a period of 7 days, 44 participants were trained to detect brief, low-contrast stimuli embedded within dynamic noise, while eye position was tracked. Although instructed to fixate, participants regularly made small fixational saccades. Data were accumulated over a large number of trials, allowing us to assess changes in performance as a function of the temporal proximity of stimuli and saccades. This analysis revealed that improvements in sensitivity over the training period were accompanied by a systematic change in the impact of saccades on performance-robust saccadic suppression on day 1 declined gradually over subsequent days until its magnitude became indistinguishable from zero. This silencing of suppression was not explained by learning-related changes in saccade characteristics and generalized to an untrained retinal location and stimulus orientation. Suppression was restored when learned stimulus timing was perturbed, consistent with the operation of a mechanism that temporarily reduces or eliminates saccadic suppression, but only when it is behaviorally advantageous to do so. Our results indicate that learning can circumvent saccadic suppression to improve performance, without compromising its functional benefits in other viewing contexts.

Impact of microsaccades on visual shape processing.

Sensitivity to subtle changes in the shape of visual objects has been attributed to the existence of global pooling mechanisms that integrate local form information across space. Although global pooling is typically demonstrated under steady fixation, other work suggests prolonged fixation can lead to a collapse of global structure. Here, we ask whether small ballistic eye movements that naturally occur during periods of fixation affect the global processing of radial frequency (RF) patterns-closed contours created by sinusoidally modulating the radius of a circle. Observers were asked to discriminate the shapes of circular patterns and RF-modulated patterns while fixational eye movements were recorded binocularly at 500 Hz. Microsaccades were detected using a velocity-based algorithm, allowing trials to be sorted according to the relative timing of stimulus and microsaccade onset. Results revealed clear perisaccadic changes in shape discrimination thresholds. Performance was impaired when microsaccades occurred close to stimulus onset, but facilitated when they occurred shortly afterward. In contrast, global integration of shape was unaffected by the timing of microsaccades. These findings suggest that microsaccades alter the discrimination sensitivity to briefly presented shapes but do not disrupt the spatial pooling of local form signals.NEW & NOTEWORTHY Microsaccades cause rapid displacement of visual images during fixation and dramatically alter the perception of basic image features. However, their effect on more complex aspects of visual processing is not well understood. Here, we demonstrate a dissociation in the impact of microsaccades on shape perception. Although overall shape discrimination performance is modulated around the time of microsaccades, the pooling efficiency of global mechanisms that combine local form information across space remains unaffected.

Linking Multi-Modal MRI to Clinical Measures of Visual Field Loss After Stroke.

Loss of vision across large parts of the visual field is a common and devastating complication of cerebral strokes. In the clinic, this loss is quantified by measuring the sensitivity threshold across the field of vision using static perimetry. These methods rely on the ability of the patient to report the presence of lights in particular locations. While perimetry provides important information about the intactness of the visual field, the approach has some shortcomings. For example, it cannot distinguish where in the visual pathway the key processing deficit is located. In contrast, brain imaging can provide important information about anatomy, connectivity, and function of the visual pathway following stroke. In particular, functional magnetic resonance imaging (fMRI) and analysis of population receptive fields (pRF) can reveal mismatches between clinical perimetry and maps of cortical areas that still respond to visual stimuli after stroke. Here, we demonstrate how information from different brain imaging modalities-visual field maps derived from fMRI, lesion definitions from anatomical scans, and white matter tracts from diffusion weighted MRI data-provides a more complete picture of vision loss. For any given location in the visual field, the combination of anatomical and functional information can help identify whether vision loss is due to absence of gray matter tissue or likely due to white matter disconnection from other cortical areas. We present a combined imaging acquisition and visual stimulus protocol, together with a description of the analysis methodology, and apply it to datasets from four stroke survivors with homonymous field loss (two with hemianopia, two with quadrantanopia). For researchers trying to understand recovery of vision after stroke and clinicians seeking to stratify patients into different treatment pathways, this approach combines multiple, convergent sources of data to characterize the extent of the stroke damage. We show that such an approach gives a more comprehensive measure of residual visual capacity-in two particular respects: which locations in the visual field should be targeted and what kind of visual attributes are most suited for rehabilitation.

Does physical exercise and congruent visual stimulation enhance perceptual learning?

PURPOSE: There is currently great interest in methods that can modulate brain plasticity, both in terms of understanding the basic mechanisms, and in the remedial application to situations of sensory loss. Recent work has focussed on how different manipulations might be combined to produce new settings that reveal synergistic actions. Here we ask whether a prominent example of adult visual plasticity, called perceptual learning, is modified by other environmental factors, such as visual stimulation and physical exercise. METHODS: We quantified the magnitude, rate and transfer of perceptual learning using a peripheral Vernier alignment task, in two groups of subjects matched for a range of baseline factors (e.g. age, starting Vernier threshold, baseline fitness). We trained subjects for 5 days on a Vernier alignment task. In one group, we introduced an exercise protocol with congruent visual stimulation. The control group received the same visual stimulation, but did not exercise prior to measurement of Vernier thresholds. RESULTS: Although the task generated large amounts of learning (~40%) and some transfer to untrained conditions in both groups, there were no specific benefits associated with either the addition of an exercise schedule or congruent visual stimulation. CONCLUSION: In adults, short periods of physical exercise and visual stimulation do not enhance perceptual learning.

Publisher Correction: Temporal rate is not a distinct perceptual metric.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

The Effect of Perceptual Learning on Face Recognition in Individuals with Central Vision Loss.

Purpose: To examine whether perceptual learning can improve face discrimination and recognition in older adults with central vision loss. Methods: Ten participants with age-related macular degeneration (ARMD) received 5 days of training on a face discrimination task (mean age, 78 ± 10 years). We measured the magnitude of improvements (i.e., a reduction in threshold size at which faces were able to be discriminated) and whether they generalized to an untrained face recognition task. Measurements of visual acuity, fixation stability, and preferred retinal locus were taken before and after training to contextualize learning-related effects. The performance of the ARMD training group was compared to nine untrained age-matched controls (8 = ARMD, 1 = juvenile macular degeneration; mean age, 77 ± 10 years). Results: Perceptual learning on the face discrimination task reduced the threshold size for face discrimination performance in the trained group, with a mean change (SD) of -32.7% (+15.9%). The threshold for performance on the face recognition task was also reduced, with a mean change (SD) of -22.4% (+2.31%). These changes were independent of changes in visual acuity, fixation stability, or preferred retinal locus. Untrained participants showed no statistically significant reduction in threshold size for face discrimination, with a mean change (SD) of -8.3% (+10.1%), or face recognition, with a mean change (SD) of +2.36% (-5.12%). Conclusions: This study shows that face discrimination and recognition can be reliably improved in ARMD using perceptual learning. The benefits point to considerable perceptual plasticity in higher-level cortical areas involved in face-processing. This novel finding highlights that a key visual difficulty in those suffering from ARMD is readily amenable to rehabilitation.

Temporal rate is not a distinct perceptual metric.

Sensory adaptation experiments have revealed the existence of 'rate after-effects' - adapting to a relatively fast rate makes an intermediate test rate feel slow, and adapting to a slow rate makes the same moderate test rate feel fast. The present work aims to deconstruct the concept of rate and clarify how exactly the brain processes a regular sequence of sensory signals. We ask whether rate forms a distinct perceptual metric, or whether it is simply the perceptual aggregate of the intervals between its component signals. Subjects were exposed to auditory or visual temporal rates (a 'slow' rate of 1.5 Hz and a 'fast' rate of 6 Hz), before being tested with single unfilled intervals of varying durations. Results show adapting to a given rate strongly influences the perceived duration of a single empty interval. This effect is robust across both interval reproduction and duration discrimination judgments. These findings challenge our understanding of rate perception. Specifically, they suggest that contrary to some previous assertions, the perception of sequence rate is strongly influenced by the perception of the sequence's component duration intervals.

Temporal modulation improves dynamic peripheral acuity.

Macular degeneration and related visual disorders greatly limit foveal function, resulting in reliance on the peripheral retina for tasks requiring fine spatial vision. Here we investigate stimulus manipulations intended to maximize peripheral acuity for dynamic targets. Acuity was measured using a single interval orientation discrimination task at 10° eccentricity. Two types of image motion were investigated along with two different forms of temporal manipulation. Smooth object motion was generated by translating targets along an isoeccentric path at a constant speed (0-20°/s). Ocular motion was simulated by jittering target location using previously recorded fixational eye movement data, amplified by a variable gain factor (0-8). In one stimulus manipulation, the sequence was temporally subsampled by displaying the target on an evenly spaced subset of video frames. In the other, the contrast polarity of the stimulus was reversed at a variable rate. We found that threshold under object motion was improved at all speeds by reversing contrast polarity, while temporal subsampling improved resolution at high speeds but impaired performance at low speeds. With simulated ocular motion, thresholds were consistently improved by contrast polarity reversal, but impaired by temporal subsampling. We find that contrast polarity reversal and temporal subsampling produce differential effects on peripheral acuity. Applying contrast polarity reversal may offer a relatively simple image manipulation that could enhance visual performance in individuals with central vision loss.

Estimation of Contrast Sensitivity From Fixational Eye Movements.

Purpose: Even during steady fixation, people make small eye movements such as microsaccades, whose rate is altered by presentation of salient stimuli. Our goal was to develop a practical method for objectively and robustly estimating contrast sensitivity from microsaccade rates in a diverse population. Methods: Participants, recruited to cover a range of contrast sensitivities, were visually normal (n = 19), amblyopic (n = 10), or had cataract (n = 9). Monocular contrast sensitivity was estimated behaviorally while binocular eye movements were recorded during interleaved passive trials. A probabilistic inference approach was used to establish the likelihood of observed microsaccade rates given the presence or absence of a salient stimulus. Contrast sensitivity was estimated from a function fitted to the scaled log-likelihood ratio of the observed microsaccades in the presence or absence of a salient stimulus across a range of contrasts. Results: Microsaccade rate signature shapes were heterogeneous; nevertheless, estimates of contrast sensitivity could be obtained in all participants. Microsaccade-estimated contrast sensitivity was unbiased compared to behavioral estimates (1.2% mean), with which they were strongly correlated (Spearman's ρ 0.74, P < 0.001, median absolute difference 7.6%). Measurement precision of microsaccade-based contrast sensitivity estimates was worse than that of behavioral estimates, requiring more than 20 times as many presentations to equate precision. Conclusions: Microsaccade rate signatures are heterogeneous in shape when measured across populations with a broad range of contrast sensitivities. Contrast sensitivity can be robustly estimated from rate signatures by probabilistic inference, but more stimulus presentations are currently required to achieve similarly precise estimates to behavioral techniques.

Orientation Tuning and Contrast Dependence of Continuous Flash Suppression in Amblyopia and Normal Vision.

Purpose: Suppression in amblyopia may be an unequal form of normal interocular suppression or a distinct pathophysiology. To explore this issue, we examined the orientation tuning and contrast dependence of continuous flash suppression (CFS) in adults with amblyopia and visually normal controls. Methods: Nine patients (mean age, 26.9 ± SD 4.7 years) and 11 controls (mean age, 24.8 ± SD 5.3 years) participated. In the CFS paradigm, spatially one-dimensional noise refreshing at 10 Hz was displayed in one eye to induce suppression of the other eye, and suppression strength was measured by using a grating contrast increment detection task. In experiment 1, noise contrast was fixed and the orientation difference between the noise and the grating was varied. In experiment 2, noise and grating orientations were identical and noise contrast was varied. Results: Suppression patterns varied in both groups. In experiment 1, controls showed consistently orientation-tuned CFS (mean half-height bandwidth, 35.8° ± SD 21.5°) with near-equal strength between eyes. Five of nine patients with amblyopia exhibited orientation-independent CFS. Eight patients had markedly unequal suppression between eyes. Experiment 2 found that increasing the noise contrast to the amblyopic eye may produce suppression of the fellow eye, but suppression remained unequal between eyes. Conclusions: Our data revealed that orientation specificity in CFS was very broad or absent in some patients with amblyopia, which could not be predicted by clinical measures. Suppression was unbalanced across the entire contrast range for most patients. This suggests that abnormal early visual experience disrupts the development of interocular suppression mechanisms.

Selective modulation of visual sensitivity during fixation.

During periods of steady fixation, we make small-amplitude ocular movements, termed microsaccades, at a rate of 1-2 every second. Early studies provided evidence that visual sensitivity is reduced during microsaccades-akin to the well-established suppression associated with larger saccades. However, the results of more recent work suggest that microsaccades may alter retinal input in a manner that enhances visual sensitivity to some stimuli. Here we parametrically varied the spatial frequency of a stimulus during a detection task and tracked contrast sensitivity as a function of time relative to microsaccades. Our data reveal two distinct modulations of sensitivity: suppression during the eye movement itself and facilitation after the eye has stopped moving. The magnitude of suppression and facilitation of visual sensitivity is related to the spatial content of the stimulus: suppression is greatest for low spatial frequencies, while sensitivity is enhanced most for stimuli of 1-2 cycles/°, spatial frequencies at which we are already most sensitive in the absence of eye movements. We present a model in which the tuning of suppression and facilitation is explained by delayed lateral inhibition between spatial frequency channels. Our data show that eye movements actively modulate visual sensitivity even during fixation: the detectability of images at different spatial scales can be increased or decreased depending on when the image occurs relative to a microsaccade. NEW & NOTEWORTHY Given the frequency with which we make microsaccades during periods of fixation, it is vital that we understand how they affect visual processing. We demonstrate two selective modulations of contrast sensitivity that are time-locked to the occurrence of a microsaccade: suppression of low spatial frequencies during each eye movement and enhancement of higher spatial frequencies after the eye has stopped moving. These complementary changes may arise naturally because of sluggish gain control between spatial channels.

Rate after-effects fail to transfer cross-modally: Evidence for distributed sensory timing mechanisms.

Accurate time perception is critical for a number of human behaviours, such as understanding speech and the appreciation of music. However, it remains unresolved whether sensory time perception is mediated by a central timing component regulating all senses, or by a set of distributed mechanisms, each dedicated to a single sensory modality and operating in a largely independent manner. To address this issue, we conducted a range of unimodal and cross-modal rate adaptation experiments, in order to establish the degree of specificity of classical after-effects of sensory adaptation. Adapting to a fast rate of sensory stimulation typically makes a moderate rate appear slower (repulsive after-effect), and vice versa. A central timing hypothesis predicts general transfer of adaptation effects across modalities, whilst distributed mechanisms predict a high degree of sensory selectivity. Rate perception was quantified by a method of temporal reproduction across all combinations of visual, auditory and tactile senses. Robust repulsive after-effects were observed in all unimodal rate conditions, but were not observed for any cross-modal pairings. Our results show that sensory timing abilities are adaptable but, crucially, that this change is modality-specific - an outcome that is consistent with a distributed sensory timing hypothesis.

Position matching between the visual fields in strabismus.

The misalignment of visual input in strabismus disrupts positional judgments. We measured positional accuracy in the extrafoveal visual field (1°-7° eccentricity) of a large group of strabismic subjects and a normal control group to identify positional distortions associated with the direction of strabismus. Subjects performed a free localization task in which targets were matched in opposite hemifields whilst fixating on a central cross. The constant horizontal error of each response was taken as a measure of accuracy, in addition to radial and angular error. In monocular conditions, all stimuli were viewed by one eye; thus, the error reflected spatial bias. In dichoptic conditions, the targets were seen by separate eyes; thus, the error reflected the perceived stimulus shift produced by ocular misalignment in addition to spatial bias. In both viewing conditions, both groups showed reliable over- and underestimations of visual field position, here termed a compression of response coordinates. The normal group showed compression in the left periphery, regardless of eye of stimulation. The strabismic group showed a visual field-specific compression that was clearly associated with direction of strabismus. The variation in perceived shift of strabismic subjects was largely accounted for by the biases present in monocular viewing, suggesting that binocular correspondence was uniform in the tested region. The asymmetric strabismic compression could not be reproduced in normal subjects through prism viewing, and its presence across viewing conditions suggests a hemifield-specific change in spatial coding induced by long-standing ocular misalignment.

Motion-based super-resolution in the peripheral visual field.

Improvements in foveal acuity for moving targets have been interpreted as evidence for the ability of the visual system to combine information over space and time, in order to reconstruct the image at a higher resolution (super-resolution). Here, we directly test whether this occurs in the peripheral visual field and discuss its potential for improving functional capacity in ocular disease. The effect of motion on visual acuity was first compared under conditions in which performance was limited either by natural undersampling in the retinal periphery or by the presence of overlaid masks with opaque elements to simulate retinal loss. To equate the information content of moving and static sequences, we next manipulated the dynamic properties of the masks. Finally, we determined the dependence of motion-related improvements on the object of motion (target or mask) and its trajectory (smooth or jittered). Motion improved visual acuity for masked but not unmasked peripheral targets. Equating the information content of moving and static conditions removed some but not all of this benefit. Residual motion-related improvements were largest in conditions in which the target moved along a consistent and predictable path. Our results show that motion can improve peripheral acuity in situations in which performance is limited by abnormal undersampling. These findings are consistent with the operation of a super-resolution system and could have important implications for any pathology that alters the regular sampling properties of the retinal mosaic.