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.

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.

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.

Generalization of prior information for rapid Bayesian time estimation.

To enable effective interaction with the environment, the brain combines noisy sensory information with expectations based on prior experience. There is ample evidence showing that humans can learn statistical regularities in sensory input and exploit this knowledge to improve perceptual decisions and actions. However, fundamental questions remain regarding how priors are learned and how they generalize to different sensory and behavioral contexts. In principle, maintaining a large set of highly specific priors may be inefficient and restrict the speed at which expectations can be formed and updated in response to changes in the environment. However, priors formed by generalizing across varying contexts may not be accurate. Here, we exploit rapidly induced contextual biases in duration reproduction to reveal how these competing demands are resolved during the early stages of prior acquisition. We show that observers initially form a single prior by generalizing across duration distributions coupled with distinct sensory signals. In contrast, they form multiple priors if distributions are coupled with distinct motor outputs. Together, our findings suggest that rapid prior acquisition is facilitated by generalization across experiences of different sensory inputs but organized according to how that sensory information is acted on.

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.

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.

Visual crowding is unaffected by adaptation-induced spatial compression.

It has recently been shown that adapting to a densely textured stimulus alters the perception of visual space, such that the distance between two points subsequently presented in the adapted region appears reduced (Hisakata, Nishida, & Johnston, 2016). We asked whether this form of adaptation-induced spatial compression alters visual crowding. To address this question, we first adapted observers to a dynamic dot texture presented within an annular region surrounding the test location. Following adaptation, observers perceived a test array comprised of multiple oriented dot dipoles as spatially compressed, resulting in an overall reduction in perceived size. We then tested to what extent this spatial compression influences crowding by measuring orientation discrimination of a single dipole flanked by randomly oriented dipoles across a range of separations. Following adaptation, we found that the magnitude of crowding was predicted by the physical rather than perceptual separation between center and flanking dipoles. These findings contrast with previous studies in which crowding has been shown to increase when motion-induced position shifts act to reduce apparent separation (Dakin, Greenwood, Carlson, & Bex, 2011; Maus, Fischer, & Whitney, 2011).

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.

Encoding of rapid time-varying information is impaired in poor readers.

A characteristic set of eye movements and fixations are made during reading, so the position of words on the retinae is constantly being updated. Effective decoding of print requires this temporal stream of visual information to be segmented or parsed into its constituent units (e.g., letters or words). Poor readers' difficulties with word recognition could arise at the point of segmenting time-varying visual information, but the mechanisms underlying this process are little understood. Here, we used random-dot displays to explore the effects of reading ability on temporal segmentation. Thirty-eight adult readers viewed test stimuli that were temporally segmented by constraining either local motions or analogous form cues to oscillate back and fourth at each of a range of rates. Participants had to discriminate these segmented patterns from comparison stimuli containing the same motion and form cues but these were temporally intermingled. Results showed that the motion and form tasks could not be performed reliably when segment duration was shorter than a temporal resolution (acuity) limit. The acuity limits for both tasks were significantly and negatively correlated with reading scores. Importantly, the minimum segment duration needed to detect the temporally segmented stimuli was longer in relatively poor readers than relatively good readers. This demonstrates that adult poor readers have difficulty segmenting temporally changing visual input particularly at short segment durations. These results are consistent with evidence suggesting that precise encoding of rapid time-varying information is impaired in developmental dyslexia.

Object size determines the spatial spread of visual time.

A key question for temporal processing research is how the nervous system extracts event duration, despite a notable lack of neural structures dedicated to duration encoding. This is in stark contrast with the orderly arrangement of neurons tasked with spatial processing. In this study, we examine the linkage between the spatial and temporal domains. We use sensory adaptation techniques to generate after-effects where perceived duration is either compressed or expanded in the opposite direction to the adapting stimulus' duration. Our results indicate that these after-effects are broadly tuned, extending over an area approximately five times the size of the stimulus. This region is directly related to the size of the adapting stimulus-the larger the adapting stimulus the greater the spatial spread of the after-effect. We construct a simple model to test predictions based on overlapping adapted versus non-adapted neuronal populations and show that our effects cannot be explained by any single, fixed-scale neural filtering. Rather, our effects are best explained by a self-scaled mechanism underpinned by duration selective neurons that also pool spatial information across earlier stages of visual processing.

Why is the processing of global motion impaired in adults with developmental dyslexia?

Individuals with dyslexia are purported to have a selective dorsal stream impairment that manifests as a deficit in perceiving visual global motion relative to global form. However, the underlying nature of the visual deficit in readers with dyslexia remains unclear. It may be indicative of a difficulty with motion detection, temporal processing, or any task that necessitates integration of local visual information across multiple dimensions (i.e. both across space and over time). To disentangle these possibilities we administered four diagnostic global motion and global form tasks to a large sample of adult readers (N=106) to characterise their perceptual abilities. Two sets of analyses were conducted. First, to investigate if general reading ability is associated with performance on the visual tasks across the entire sample, a composite reading score was calculated and entered into a series of continuous regression analyses. Next, to investigate if the performance of readers with dyslexia differs from that of good readers on the visual tasks we identified a group of forty-three individuals for whom phonological decoding was specifically impaired, consistent with the dyslexic profile, and compared their performance with that of good readers who did not exhibit a phonemic deficit. Both analyses yielded a similar pattern of results. Consistent with previous research, coherence thresholds of poor readers were elevated on a random-dot global motion task and a spatially one-dimensional (1-D) global motion task, but no difference was found on a static global form task. However, our results extend those of previous studies by demonstrating that poor readers exhibited impaired performance on a temporally-defined global form task, a finding that is difficult to reconcile with the dorsal stream vulnerability hypothesis. This suggests that the visual deficit in developmental dyslexia does not reflect an impairment detecting motion per se. It is better characterised as a difficulty processing temporal information, which is exacerbated when local visual cues have to be integrated across multiple (>2) dimensions.

Fixational eye movements predict visual sensitivity.

During steady fixation, observers make small fixational saccades at a rate of around 1-2 per second. Presentation of a visual stimulus triggers a biphasic modulation in fixational saccade rate-an initial inhibition followed by a period of elevated rate and a subsequent return to baseline. Here we show that, during passive viewing, this rate signature is highly sensitive to small changes in stimulus contrast. By training a linear support vector machine to classify trials in which a stimulus is either present or absent, we directly compared the contrast sensitivity of fixational eye movements with individuals' psychophysical judgements. Classification accuracy closely matched psychophysical performance, and predicted individuals' threshold estimates with less bias and overall error than those obtained using specific features of the signature. Performance of the classifier was robust to changes in the training set (novel subjects and/or contrasts) and good prediction accuracy was obtained with a practicable number of trials. Our results indicate a tight coupling between the sensitivity of visual perceptual judgements and fixational eye control mechanisms. This raises the possibility that fixational saccades could provide a novel and objective means of estimating visual contrast sensitivity without the need for observers to make any explicit judgement.

Age-related changes in auditory and visual interactions in temporal rate perception.

We investigated how aging affects the integration of temporal rate for auditory flutter (amplitude modulation) presented with visual flicker. Since older adults were poorer at detecting auditory amplitude modulation, modulation depth was individually adjusted so that temporal rate was equally discriminable for 10 Hz flutter and flicker, thereby balancing the reliability of rate information available to each sensory modality. With age-related sensory differences normalized in this way, rate asynchrony skewed both auditory and visual rate judgments to the same extent in younger and older adults. Therefore, reliability-based weighting of temporal rate is preserved in older adults. Concurrent presentation of synchronous 10 Hz flicker and flutter improved temporal rate discrimination consistent with statistically optimal integration in younger but not older adults. In a control experiment, younger adults were presented with the same physical auditory stimulus as older adults. This time, rate asynchrony skewed perceived rate with greater auditory weighting rather than balanced integration. Taken together, our results indicate that integration of discrepant auditory and visual rates is not altered due to the healthy aging process once sensory deficits are accounted for, but that aging does abolish the minor improvement in discrimination performance seen in younger observers when concordant rates are integrated.

Characterizing the effects of multidirectional motion adaptation.

Recent sensory experience can alter our perception and change the response characteristics of sensory neurons. These effects of sensory adaptation are a ubiquitous property of perceptual systems and are believed to be of fundamental importance to sensory coding. Yet we know little about how adaptation to stimulus ensembles affects our perception of the environment as most psychophysical experiments employ adaptation protocols that focus on prolonged exposure to a single visual attribute. Here, we investigate how concurrent adaptation to multiple directions of motion affects perception of subsequently presented motion using the direction aftereffect. In different conditions, observers adapted to a stimulus ensemble comprised of dot directions sampled from different distributions or to bidirectional motion. Increasing the variance of normally distributed directions reduced the magnitude of the peak direction aftereffect and broadened its tuning profile. Sampling of asymmetric Gaussian and uniform distributions resulted in shifts of direction aftereffect tuning profiles consistent with changes in the perceived global direction of the adapting stimulus. Adding dots in a direction opposite or orthogonal to a unidirectional adapting stimulus led to a pronounced reduction in the direction aftereffect. A simple population-coding model, in which adaptation selectively alters the responsivity of direction-selective neurons, can accommodate the effects of multidirectional adaptation on the perceived direction of motion.

Body-part specificity for learning of multiple prior distributions in human coincidence timing.

During timing tasks, the brain learns the statistical distribution of target intervals and integrates this prior knowledge with sensory inputs to optimise task performance. Daily events can have different temporal statistics (e.g., fastball/slowball in baseball batting), making it important to learn and retain multiple priors. However, the rules governing this process are not yet understood. Here, we demonstrate that the learning of multiple prior distributions in a coincidence timing task is characterised by body-part specificity. In our experiments, two prior distributions (short and long intervals) were imposed on participants. When using only one body part for timing responses, regardless of the priors, participants learned a single prior by generalising over the two distributions. However, when the two priors were assigned to different body parts, participants concurrently learned the two independent priors. Moreover, body-part specific prior acquisition was faster when the priors were assigned to anatomically distant body parts (e.g., hand/foot) than when they were assigned to close body parts (e.g., index/middle fingers). This suggests that the body-part specific learning of priors is organised according to somatotopy.

Perceptual learning reconfigures the effects of visual adaptation.

Our sensory experiences over a range of different timescales shape our perception of the environment. Two particularly striking short-term forms of plasticity with manifestly different time courses and perceptual consequences are those caused by visual adaptation and perceptual learning. Although conventionally treated as distinct forms of experience-dependent plasticity, their neural mechanisms and perceptual consequences have become increasingly blurred, raising the possibility that they might interact. To optimize our chances of finding a functionally meaningful interaction between learning and adaptation, we examined in humans the perceptual consequences of learning a fine discrimination task while adapting the neurons that carry most information for performing this task. Learning improved discriminative accuracy to a level that ultimately surpassed that in an unadapted state. This remarkable improvement came at a price: adapting directions that before learning had little effect elevated discrimination thresholds afterward. The improvements in discriminative accuracy grew quickly and surpassed unadapted levels within the first few training sessions, whereas the deterioration in discriminative accuracy had a different time course. This learned reconfiguration of adapted discriminative accuracy occurred without a concomitant change to the characteristic perceptual biases induced by adaptation, suggesting that the system was still in an adapted state. Our results point to a functionally meaningful push-pull interaction between learning and adaptation in which a gain in sensitivity in one adapted state is balanced by a loss of sensitivity in other adapted states.

A neural hierarchy for illusions of time: duration adaptation precedes multisensory integration.

Perceived time is inherently malleable. For example, adaptation to relatively long or short sensory events leads to a repulsive aftereffect such that subsequent events appear to be contracted or expanded (duration adaptation). Perceived visual duration can also be distorted via concurrent presentation of discrepant auditory durations (multisensory integration). The neural loci of both distortions remain unknown. In the current study we use a psychophysical approach to establish their relative positioning within the sensory processing hierarchy. We show that audiovisual integration induces marked distortions of perceived visual duration. We proceed to use these distorted durations as visual adapting stimuli yet find subsequent visual duration aftereffects to be consistent with physical rather than perceived visual duration. Conversely, the concurrent presentation of adapted auditory durations with nonadapted visual durations results in multisensory integration patterns consistent with perceived, rather than physical, auditory duration. These results demonstrate that recent sensory history modifies human duration perception prior to the combination of temporal information across sensory modalities and provides support for adaptation mechanisms mediated by duration selective neurons situated in early areas of the visual and auditory nervous system (Aubie, Sayegh, & Faure, 2012; Duysens, Schaafsma, & Orban, 1996; Leary, Edwards, & Rose, 2008).

Duration channels mediate human time perception.

The task of deciding how long sensory events seem to last is one that the human nervous system appears to perform rapidly and, for sub-second intervals, seemingly without conscious effort. That these estimates can be performed within and between multiple sensory and motor domains suggest time perception forms one of the core, fundamental processes of our perception of the world around us. Given this significance, the current paucity in our understanding of how this process operates is surprising. One candidate mechanism for duration perception posits that duration may be mediated via a system of duration-selective 'channels', which are differentially activated depending on the match between afferent duration information and the channels' 'preferred' duration. However, this model awaits experimental validation. In the current study, we use the technique of sensory adaptation, and we present data that are well described by banks of duration channels that are limited in their bandwidth, sensory-specific, and appear to operate at a relatively early stage of visual and auditory sensory processing. Our results suggest that many of the computational principles the nervous system applies to coding visual spatial and auditory spectral information are common to its processing of temporal extent.

Audiovisual time perception is spatially specific.

Our sensory systems face a daily barrage of auditory and visual signals whose arrival times form a wide range of audiovisual asynchronies. These temporal relationships constitute an important metric for the nervous system when surmising which signals originate from common external events. Internal consistency is known to be aided by sensory adaptation: repeated exposure to consistent asynchrony brings perceived arrival times closer to simultaneity. However, given the diverse nature of our audiovisual environment, functionally useful adaptation would need to be constrained to signals that were generated together. In the current study, we investigate the role of two potential constraining factors: spatial and contextual correspondence. By employing an experimental design that allows independent control of both factors, we show that observers are able to simultaneously adapt to two opposing temporal relationships, provided they are segregated in space. No such recalibration was observed when spatial segregation was replaced by contextual stimulus features (in this case, pitch and spatial frequency). These effects provide support for dedicated asynchrony mechanisms that interact with spatially selective mechanisms early in visual and auditory sensory pathways.

Size-induced distortions in perceptual maps of visual space.

In order to interact with our environment, the human brain constructs maps of visual space. The orderly mapping of external space across the retinal surface, termed retinotopy, is maintained at subsequent levels of visual cortical processing and underpins our capacity to make precise and reliable judgments about the relative location of objects around us. While these maps, at least in the visual system, support high precision judgments about the relative location of objects, they are prone to significant perceptual distortion. Here, we ask observers to estimate the separation of two visual stimuli--a spatial interval discrimination task. We show that large stimulus sizes require much greater separation in order to be perceived as having the same separation as small stimulus sizes. The relationship is linear, task independent, and unrelated to the perceived position of object edges. We also show that this type of spatial distortion is not restricted to the object itself but can also be revealed by changing the spatial scale of the background, while object size remains constant. These results indicate that fundamental spatial properties, such as retinal image size or the scale at which an object is analyzed, exert a marked influence on spatial coding.