Vision Research

The dynamic range of contrast-encoding in the early visual system has been investigated at both single-neuron and population levels in animals using oriented stimuli such as gratings and Gabor patches. However, contrast-encoding of unoriented stimuli such as Gaussians has been less explored, even though such stimuli can evoke a large population response. In studies that employ Gaussians, contrast response functions (CRFs) of neurons and neural populations in primary visual cortex are typically characterized across a limited range of Weber contrasts up to 100%, which may not adequately reflect the statistics of contrast in natural scenes. Indeed, our analysis shows that locations with contrasts far exceeding 100% Weber contrast are ubiquitous in natural scenes. Thus, our current understanding of contrast encoding remains incomplete in the context of natural environments. Here, we measured spiking activities of individual neurons using electrophysiology and population responses using calcium imaging in V1 of fixating macaques while Gaussian stimuli were presented over a wide range of Weber contrasts, up to 900%. Both the average spiking response and the average population response continued to increase robustly above 100% Weber contrast. Only a small minority of neurons saturate below 100% Weber contrast. These results demonstrate that the dynamic range of contrast-encoding in V1 is broader than previously assumed and aligns more closely with the statistics of contrast in natural scenes. Significance StatementThe dynamic range of contrast-encoding in V1 has typically been characterized using only a limited range of contrasts, often excluding the high contrasts commonly found in natural scenes. We measured contrast response functions of individual neurons and neural populations in V1 across a much wider range of contrasts. We found that the responses of the majority of neurons, as well as the overall population, increased robustly up to extremely high contrasts. These findings suggest that the dynamic range of contrast encoding in V1 extends well beyond the commonly tested range.

The critical flicker fusion (CFF) threshold is a psychophysical measure used to quantify the temporal resolution of the visual system and is known to vary across individuals. However, it is unclear if this measure is stimulus-specific, or if it may represent a more fundamental processing rate for visual perception in general. Here, we assess if individual variation in CFF is predictive of two features of visual processing that are dependent on temporal perception: the attentional blink and global motion sensitivity. In a non-clinical sample of 84 individuals, flicker fusion thresholds were predictive of the magnitude of the attentional blink. In contrast, we found no link between flicker fusion and global motion sensitivity in a sample of 79 individuals. Our results suggest that CFF reflects a visual processing rate that impacts other, more complex perceptual tasks.

Filling-in occurs during the perceptual disappearance of a blank figure presented on a textured background. Current models of perceptual filling-in are based on a two-stage model where the figure boundary weakens after a period of adaptation, followed by the spreading of the background representation into the region representing the figure. This suggests a competition between figure boundary and background representations whereby filling-in is facilitated by a weaker boundary representation and a stronger background representation. Here, we test this interpretation, by using the oblique effect and surround-modulation suppression, which are functional properties of early visual cortex that modulate the expected strengths of the responses to the background texture and to the figure boundary. In a sample of N=58 participants, we found more filling-in with background textures of cardinal compared to oblique orientations (earlier onset time, with more and longer episodes of filling-in per trial), in line with a known, stronger neuronal response for cardinal than for oblique orientation in early visual cortex. We found more filling-in when the main axis of the rectangular figure was iso-oriented rather than cross-oriented with the background texture (more and longer episodes of filling-in per trial, but no change in onset time), in line with a lower response to oriented stimuli when surrounded by iso-oriented flankers compared to cross-oriented flankers. Overall, our results support the two-stage model and suggest the involvement of early visual cortical areas characterized by the oblique effect and orientation- tuned surround-suppression.

Recurrent processing involves feedforward, feedback and lateral connections and is thought to allow efficient visual processing. Anatomical and behavioral studies in humans have suggested that feedback connections mature later in development than feedforward connections and thus were proposed to depend to a larger degree on experience. In order to isolate feedforward from feedback activity and to investigate the role of early visual experience, we assessed seven individuals with reversed congenital cataracts and nine sighted controls using an "occlusion paradigm" with 7T magnetic resonance imaging (Smith & Muckli, 2010): Grayscale images of scenes were presented with the lower right quadrant covered by a white rectangle. We examined whether information about category (beaches, buildings, highways) and individual scenes could be extracted from early visual region vertices (V1 - V3) associated with the occluded quadrant of the visual field, in the absence of bottom-up visual input. This was achieved by decoding individual category or scene context utilizing a linear support vector machine. In addition, bidirectional information flow was assessed using connective field modeling. While both groups showed successful decoding of scene and category from vertices receiving bottom-up visual input, the accuracy was higher in normally sighted individuals than in individuals with reversed congenital cataracts. When bottom-up input was removed, decoding of categories remained successful in both groups, but decoding of individual scenes was only possible in normally sighted control individuals. Connective field modeling results indicated a less precise alignment of feedforward and feedback processing during visual stimulation in individuals with reversed congenital cataracts. These findings suggest that early visual experience is crucial for the refinement of feedback activity which in turn is crucial for well-tuned feedforward processing.

In previous studies by the author on binocular vision with the asymmetric eye (AE), which models a healthy human eye with misaligned optical components, the results were primarily presented in the Rodrigues vector (RV) framework and supported by simulations and 3D visualizations in GeoGebras dynamic geometry environment. In this paper, the novel geometric kinematics of the human eye, that is, the eye with misaligned optics, and simplified assumptions about the eye rotations (the eyes translational movements are disregarded), are developed within the framework of rigid-body rotations. The originality of the analysis lies in a precise geometric decomposition of a full rotation of the eyes posture into a torsion-free rotation (the geodesic part) and a torsional rotation (the non-geodesic extension of the geodesic part). This decomposition is extended to the corresponding decomposition of the angular velocity. A novel derivation of the eyes angular velocity from the RV formulation of the eye kinematics is proposed.

Visual response strength in the primate superior colliculus (SC) has recently been shown to inversely correlate with trial-by-trial saccadic reaction time in a much stronger way than visual response strength in the primary visual cortex (V1). However, for any given visual stimulus onset, populations of neurons in each brain area are concurrently activated, leaving open the question of how V1 visual response strength can predict trial-by-trial saccadic reaction time when multiple simultaneously recorded neurons are taken into account. Using a classic visually-guided saccade task, here we assessed the quality of predicting trial-by-trial saccadic reaction time from the visual response strengths of 1 to 10 simultaneously recorded neurons in each brain area. For each session, we modeled saccadic reaction time as a weighted linear combination of the visual response strengths of N simultaneously recorded neurons. Consistent with the prior work, the visual response strength of a single SC neuron was better than that of a single V1 neuron at predicting reaction time. By adding more simultaneously recorded neurons, the prediction got much better in the SC, but not in V1.Only for 100% contrast dark stimuli (darker in luminance than the surrounding gray background) did V1 show an increase in prediction quality with more simultaneously recorded neurons. This increase, which was still substantially weaker than in the SC, could reflect the preference of V1 neurons for dark contrasts. These results suggest that despite qualitative similarities between SC and V1 visual responses, SC visual responses are functionally reformatted from their V1 counterparts. SignificanceThe superior colliculus (SC) is an important sensory-motor structure for controlling eye movements, and it receives a significant portion of its inputs directly from the primary visual cortex (V1). Despite this, SC visual responses are much better correlated with trial-by-trial variability in saccadic eye movement timing than V1 visual responses, and this effect is strongly amplified when considering simultaneously recorded neurons. Thus, SC and V1 visual responses serve fundamentally different functions from a motor perspective.

Visual signals from the two eyes merge gradually as they pass through the primary visual cortex (V1). Here we use a computational model of Macaque V1 to study the first stage of this integration along the magnocellular pathway, in layer 4C, aiming to infer neuroanatomical origins of binocular response. It is known that neurons in layer 4C are predominantly monocular, though some do exhibit varying degrees of binocularity. We find (1) the emergence of narrow binocular strips along borders of ocular dominance columns (ODC), a finding that aligns with experiments; (2) most consistent with data is when 10 - 30% of interactions near ODC boundaries are cross-columnar; and (3) feedback from layer 6 is largely monocular. These results were obtained through systematic hypothesis testing using a multiscale model that is orders of magnitude faster than its biologically-detailed predecessors. We propose that multiscale modeling can be an effective tool for bridging anatomy and function.

Mental rotation in 3D is a key cognitive skill involving dynamic spatial transformations, for which pronounced individual differences have been documented. Here we ask whether individual differences in 3D abilities can be explained by analogous differences in 2D abilities. 3D mental-rotation was assessed by the Vandenberg & Kruse Mental Rotation Test (3D-MRT) and examined for association with performance and underlying electrocortical mechanisms during a 2D letter rotation task. Participants (N=40) first completed the MRT and then performed a computerized 2-D letter rotation task in which they had to identify whether letters were oriented in a standard or a mirrored direction (parity judgment) when rotated at 0{degrees}, 60{degrees}, 120{degrees}, and 180{degrees} while EEG was recorded. Reaction times (RTs) and error rates increased with angular disparity. The angular disparity effect on RT was smaller for mirrored letters. Low, relative to high, 3D-MRT scoring participants showed more pronounced accuracy declines at higher rotation angles. An EEG Event Related Potential (ERP) known as the Rotation-Related Negativity (RRN) became more pronounced with increasing angular disparity. High 3D-MRT scores were associated with a stronger RRN response at central-parietal sites. In addition, the ERP-P3b wave was more pronounced at central-parietal sites for low 3D-MRT scorers, independent of angular disparity. It is concluded that 3D rotational ability is positively associated with 2D mental rotation performance, and more strongly with enhanced recruitment of neural visual-spatial cortical representations than with enhanced recruitment of more general cognitive resources.

Choice probability (CP) quantifies the trial-by-trial covariation between a sensory neurons response and perceptual reports. Despite extensive interest in CP as a window into how perception is linked to the activity of sensory neurons, the usefulness of CP remains debated. On one hand, reported CP magnitudes vary widely across seemingly equivalent studies, questioning its utility as a metric. On the other hand, the absence of clear patterns in CP variability has made it difficult to use it to adjudicate between competing models of visual perception. Here, we performed a meta-analysis of 150 CP estimates from 59 macaque neurophysiology studies to identify factors that systematically influence CP. We confirmed the positive relationship between CP and neuronal sensitivity both across and within individual studies. When controlled for sensitivity, we found remarkable consistency in CP across varying tasks and brain regions with two notable exceptions. First, CPs were higher in tasks involving bistable percepts, reinforcing the link between CP magnitude and subjective perception. Second, CPs were smaller in area V1, supporting prior suggestions about V1s special role in visual processing. We further found a significant effect of stimulus duration on CP, providing evidence against strictly feedforward models and favoring models with substantial feedback and recurrent processing. Finally, we offer recommendations for future studies to enhance the cross-study comparability and theoretical utility of choice signals as the field transitions to large-scale population recordings. More broadly, our findings demonstrate the benefits of meta-studies that expose patterns across many different tasks and animals - yielding insights that complement large-scale population recordings.

Human object recognition is robust to challenging conditions, such as when ones view of an object is fragmented due to an occluding foreground object. In comparison, deep neural networks (DNNs) are typically more susceptible to occlusion, suggesting that human vision relies on distinct mechanisms. Here, we investigated the role of visual diet in the emergence of these mechanisms by asking whether human-like robustness might arise in DNNs when trained with image datasets that better reflect the properties of occlusion in natural vision. We trained convolutional and transformer DNNs to classify clear images only, images augmented with artificial occluders (i.e., geometric shapes) or natural occluders (objects segmented from photographs). We then evaluated DNN occlusion robustness and compared their performance profiles with 30 human participants. We found that DNNs trained with artificial occluders remained vulnerable to natural occlusion and exhibited less human-like performance than those trained with natural occlusion. Our findings suggest that human robustness to visual occlusion arises from learning to disentangle natural objects from each other rather than simply learning to recognize objects from partial views. They also imply that commonly used forms of artificial occlusion are unsuitable for the evaluation or promotion of robustness to real-world occlusion in DNNs.

Saccades made during memory maintenance prioritize memory for the saccade target, but it is unclear if this benefit is specific to a location or extends across memorized objects. In three experiments, we examined whether saccadic selection spreads to other locations within the same object. In Experiment 1, we asked observers to remember three oriented Gabors presented either within contour-defined objects or without object structure. A subsequent movement cue prompted observers to move their eyes to the indicated location. We then probed memory for stimuli at locations equidistant from the saccade target, in either the same or a different object. Memory was best for stimuli at locations congruent with the saccade target, and consistently weaker for other stimuli presented in the same or a different object than the saccade target. In Experiment 2, we created more complex objects by adding more object features to the stimulus. Again, memory performance was best for stimuli congruent with the saccade target location, whereas memory in incongruent trials was worse and similar for stimuli in the same and different object as the saccade target. In Experiment 3, we tested if saccadic selection is present and propagates within the object in a change detection task. Again, memory performance (i.e., change detection) was best at the saccade target location. However, this memory benefit also spread to other locations within the same object. Our results imply that saccadic selection in visual working memory is primarily space-based but can also spread towards locations within the object where a saccade was directed.

Zebrafish (Danio rerio) are an important vertebrate model for vision and neuroscience research. In the larval stages, the aquatic species begins to elicit the optomotor response (OMR) to stabilize themselves in water -- a behaviour that may be exploited in the laboratory to measure visual acuity. However, up to now, the measurement of the OMR in juvenile and adult zebrafish has been limited due to their behavioural complexity. Here, we optimize a protocol to assay zebrafish aged between 4 and 9 weeks-post-fertilization, by displaying sinusoidal gratings parallel to the zebrafish eye to elicit a robust OMR. We assessed the visual spatial-frequency tuning function of an environmentally induced myopia model to confirm the sensitivity and robustness of the protocol. Additionally, we show the OMR is sensitive to the contrast and temporal resolution of the sinusoidal gratings. Furthermore, we found that the time between stimulus presentations impact the spatial-frequency tuning function likely as time is required for zebrafish to return to baseline swimming after eliciting the OMR. Finally, we found that the OMR after ten versus twenty seconds of stimulus onset appears comparable; indicating that robust OMR responses in zebrafish can be elicited through relatively short stimulus presentations. Through the experiments conducted, we present an optimized protocol specific to zebrafish. The protocol may be used to follow the progression or treatment efficacy of progressive neurological disorders including specific visual disorders and higher brain functions with visual endophenotypes. Ultimately, this protocol allows for high-throughput robust measures of visual and neural function in zebrafish.

Whether and how various visual sensory areas contribute to the perceived location of visual stimuli remains unknown. To test the role of neurons in extrastriate area V4 in generating alterations in spatial perception during saccadic eye movements (saccades), we examined perisaccadic mislocalization--the perceptual phenomenon in which visual stimuli appearing around the time of a saccade are perceived at a different position than their actual location. We designed and implemented a combined behavioral and electrophysiological framework in non-human primates to directly relate trial-by-trial spatial perception reports during saccades to neuronal firing rates in V4 populations. We measured monkeys perception of stimulus location behaviorally and found perisaccadic mislocalization opposite to the saccade direction. We also quantified population responses by computing the center of mass of firing rate activity across probe locations for V4 neurons with receptive fields close to the saccade target. While perisaccadic neuronal responses showed shifts toward the saccade target, these shifts did not systematically vary with the magnitude of perceptual mislocalization across trials. In conclusion, receptive field shifts based on the perisaccadic firing rate of V4 neurons are not sufficient to account for the magnitude of perceptual mislocalization in each trial, suggesting that more complex neural representation of perisaccadic visual information may be critical for linking extrastriate neural activity to saccade-induced perception.

Mounting evidence suggests that recurrent processes in the visual system play a critical role during challenging recognition tasks. Backward masking techniques have traditionally been used as a non-invasive method for studying recurrent processes: A mask follows the target image, presumably disrupting ongoing processes. However, these techniques have the limitation that they do not allow the identification of the stage of the visual system at which critical recurrent processes are taking place. Here, leveraging advances in texture synthesis via deep networks, and the approximate correspondence between stages of the visual system and layers of deep networks, we develop a novel psychophysics paradigm where masks with textures targeting different stages of the visual system follow the presentation of challenging images. In a series of experiments, we present objects to human subjects either for a short duration or in unusual poses, followed by a textured mask either designed to only target the early visual system, or the entire visual system. We find that both texture types equally affect recognition abilities, suggesting that recurrent processes in or towards early stages of the visual system are already recruited for these recognition tasks.

Inhibition of return (IOR) refers to the slowing of response times (RTs) for stimuli presented at previously inspected locations relative to novel locations. However, the exact processing stage(s) at which IOR occurs, and its nature across different response modalities, remain debated. By reanalyzing RT data from a target-target IOR paradigm with a single noisy accumulator model, we tested whether IOR could occur at sensory or attentional stages of processing, or at later stages of decision and action selection. We considered IOR under two conditions: manual and saccadic responses. The within-trial Gaussian noise parameter best explained both manual and saccadic IOR, suggesting that in both modalities, IOR may result from a more fluctuating accumulation of evidence for repeated locations. These results support the hypothesis that target-target IOR may primarily involve attentional-level mechanisms. Significance statementWe respond more slowly to a stimulus that is presented within a short interval in the same location ("inhibition of return"), a bias thought to promote efficient visual exploration. Using evidence-accumulation modeling of manual and eye-movement reaction times from two previous studies, we found that the key change linked to inhibition of return is greater within-trial variability (noise) in evidence accumulation, not a higher decision threshold. Understanding which processing stage is affected can help connect behavioral effects to the brain networks that support attention and orienting.

During active vision, the brain must coordinate where to move the eyes with predictions about upcoming sensory input. Before each saccade, perception is enhanced at the upcoming fixation location, but whether this enhancement depends on expectations about target features remains unknown. Here, participants prepared a saccade to a cued location while reporting the presence and orientation of a brief visual target that appeared either at the saccade goal or at the opposite location. Feature expectation was manipulated across blocks by varying the probability of the two target orientations. Perceptual sensitivity (d') increased when targets were presented at the saccade goal, consistent with presaccadic enhancement, and was also higher for less expected features. However, these effects were independent: feature probability did not alter the magnitude of presaccadic enhancement. Moreover, presaccadic enhancement increased near saccade onset, whereas the advantage for less expected features weakened as movement onset approached. Saccade latency revealed a contrasting pattern. Visual targets presented at the saccade goal delayed movement initiation. This delay depended on feature probability, with longer latencies for unexpected than for expected features only when saccades were directed towards the target. This location-specific effect persisted after accounting for perceptual report, and the latency cost for unexpected features was reproduced in a follow-up experiment. Together, these findings show that feature probability enhanced sensitivity to unexpected information independently of presaccadic enhancement, while selectively delaying saccade initiation towards targets with unexpected features. This dissociation suggests that feature expectation modulates perception and action through functionally distinct forms of visual processing.

Human recognition of objects as animate or inanimate is fast and accurate. However, this task may be challenging for objects with animal-like properties (e.g., presence of eyes/face), albeit being inanimate (e.g., a cow-mug). Lookalike objects provide an opportunity to examine how visual perception resolves categorical ambiguities and whether it exhibits an intrinsic bias to see animacy. During electroencephalography (EEG), we presented healthy humans with images of objects at a regular, rapid frequency (6 Hz), where every five exemplars of a standard category (animate or inanimate), an exemplar of the other oddball category was shown (1.2 Hz). In some conditions, oddball-stimuli were replaced by lookalikes. Periodic visual stimulation should give rise to a distinctive EEG response at 6 Hz. Moreover, if the oddball category elicits a different neural response than the standard category, a distinct response should be observed at 1.2 Hz. This categorization response was found for animate-oddballs among inanimate objects, and vice versa. It was also found for lookalike-oddballs presented among animate or inanimate objects, but it was significantly higher in the first case, implying that lookalike objects were perceived as more similar to inanimate than animate objects. The degree of animal resemblance modulated the amplitude of neural response to lookalikes, without however changing the category boundary. These results--also replicated in an artificial model of human vision--demonstrate that animal resemblance of objects is registered in visual perception, but it does not alter the critical ability to distinguish between what is truly alive and what is not.

Perception is typically biased towards prior expectations. In some cases, however, it seems repelled away from expectations, such that percepts appear less like what is expected. Even more intriguingly, separate studies have recently reported that predictions derived from gravity may shape perception in opposing ways. Specifically, gravity causes unsupported objects to accelerate downwards, leading to two predictions; that objects will move downwards (location prior) and at an increasing speed (acceleration prior). There is evidence that perceptual judgements are attracted towards location priors yet repelled from acceleration ones. Here we examine these effects in the same paradigm to determine whether they result from different types of stimuli and judgement, or more interestingly, might result from opposite influences of common predictive mechanisms influencing perception. We first replicate previous reports of a systematic bias to report upward moving objects as more accelerating than downward moving objects: effectively a repulsion from acceleration priors. We then show that the effect applies both at the level of retinal space and due to contextual cues concerning gravitational direction. Finally, we find that participants errors in a location reproduction task are similarly consistent with a repulsion from acceleration priors and, simultaneously, with an attraction towards location priors. We conclude by considering the ways in which these concurrent attractive and repulsive biases may reflect mechanisms optimising fast, accurate, and informative experiences in our ever-changing sensory world, therefore optimising the interface between perception and learning. Public Significance StatementIn a series of behavioural experiments, we show that expectations about how objects move due to gravity concurrently attract perception towards the prediction that objects move downwards, and repel perception away from the prediction that they do so at an increasing rate. These opposing influences inform current theories of perceptual processing, which explain how expectations may generate percepts that are fast, veridical, and informative.

PurposeAlthough electroretinography (ERG) is vital for evaluating retinal function, conventional corneal electrodes slide or detach in animals. This study aimed to investigate the effectiveness of a novel approach to ERG recording using a metal eyelid speculum for both active and reference electrodes in conjunction with a skin electrode-based ERG device. MethodsWe tested a stainless-steel eyelid speculum as both active and reference electrodes with a skin-electrode ERG system (HE-2000vet) in six healthy Japanese White rabbits. Dark-adapted rod and maximal responses and light-adapted cone and 30 Hz flicker ERGs were recorded in three weekly sessions. ResultsReproducible waveforms with identifiable a- and b-waves were obtained in every eye; rod b-waves reached 50-90 {micro}V and cone b-waves 40-55 {micro}V. Intraclass correlation coefficients revealed substantial interocular agreement and moderate-to-substantial inter-session reproducibility for b-wave amplitude and implicit time, whereas a-wave metrics were less reliable owing to lower amplitudes. The advantages of speculum electrode over corneal electrodes are that it requires no fur shaving, maintains stable contact regardless of globe orientation, and allows real-time observation. ConclusionsThis study demonstrated that an eyelid-speculum electrode is a practical, non-invasive alternative for veterinary and experimental ERG recordings, producing signal quality sufficient for longitudinal and interocular analyses while avoiding cosmetic and technical drawbacks of conventional methods.

Categorisation is often treated as a form of compression: a high-dimensional stimulus space is reduced to a smaller set of behaviourally or cognitively useful classes. However, compression alone does not determine whether a category map is useful. The present manuscript develops an information-theoretic framework for evaluating categorisation in terms of both category complexity and target-relevant information preservation. Across a set of synthetic demonstrations, alternative category maps over the same stimulus space are shown to preserve different target variables, including identity, action, nuisance, and hierarchical category structure. The framework is then extended to learned visual representations by analysing layer-derived category maps from a pretrained ResNet-50 network applied to CIFAR-10 images. Two scenarios are compared: a clean-only object run and a pooled nuisance run containing clean, blurred, pixelated, and noise-perturbed images. The results show that category maps can have substantial entropy while preserving information about a variable that is not aligned with the specified target, and that the value of a categorisation depends on the target variable to be preserved. The manuscript argues that categorisation should therefore be evaluated not only by compression or separability, but by the information retained about a specified cognitive, behavioural, or computational target.