When You Do Not Get the Whole Picture: Scene Perception After Occipital Cortex Lesions.

Background: Occipital cortex lesions (OCLs) typically result in visual field defects (VFDs) contralateral to the damage. VFDs are usually mapped with perimetry involving the detection of point targets. This, however, ignores the important role of integration of visual information across locations in many tasks of everyday life. Here, we ask whether standard perimetry can fully characterize the consequences of OCLs. We compare performance on a rapid scene discrimination task of OCL participants and healthy observers with simulated VFDs. While the healthy observers will only suffer the loss of part of the visual scene, the damage in the OCL participants may further compromise global visual processing. Methods: VFDs were mapped with Humphrey perimetry, and participants performed two rapid scene discrimination tasks. In healthy participants, the VFDs were simulated with hemi- and quadrant occlusions. Additionally, the GIST model, a computational model of scene recognition, was used to make individual predictions based on the VFDs. Results: The GIST model was able to predict the performance of controls regarding the effects of the local occlusion. Using the individual predictions of the GIST model, we can determine that the variability between the OCL participants is much larger than the extent of the VFD could account for. The OCL participants can further be categorized as performing worse, the same, or better as their VFD would predict. Conclusions: While in healthy observers the extent of the simulated occlusion accounts for their performance loss, the OCL participants' performance is not fully determined by the extent or shape of their VFD as measured with Humphrey perimetry. While some OCL participants are indeed only limited by the local occlusion of the scene, for others, the lesions compromised the visual network in a more global and disruptive way. Yet one outperformed a healthy observer, suggesting a possible adaptation to the VFD. Preliminary analysis of neuroimaging data suggests that damage to the lateral geniculate nucleus and corpus callosum might be associated with the larger disruption of rapid scene discrimination. We believe our approach offers a useful behavioral tool for investigating why similar VFDs can produce widely differing limitations in everyday life.

Functional connectivity of the Precuneus reflects effectiveness of visual restitution training in chronic hemianopia.

Visual field defects in chronic hemianopia can improve through visual restitution training, yet not all patients benefit equally from this long and exhaustive procedure. Here, we asked if resting-state functional connectivity prior to visual restitution could predict training success. In two training sessions of eight weeks each, 20 patients with chronic hemianopia performed a visual discrimination task by directing spatial selective attention towards stimuli presented in either hemifield, while suppressing eye movements. We examined two effects: a sensitivity change in the attended (trained) minus the unattended (control) hemifield (i.e., a training-specific improvement), and an overall improvement (i.e., a total change in sensitivity after both sessions). We then identified five visual resting-state networks and evaluated their functional connectivity in relation to both training effects. We found that the functional connectivity strength between the anterior Precuneus and the Occipital Pole Network was positively related to the attention modulated (i.e., training-specific) improvement. No such relationship was found for the overall improvement or for the other visual networks of interest. Our finding suggests that the anterior Precuneus plays a role in attention-modulated visual field improvements. The resting-state functional connectivity between the anterior Precuneus and the Occipital Pole Network may thus serve as an imaging-based biomarker that quantifies a patient's potential capacity to direct spatial attention. This may help to identify hemianopia patients that are most likely to benefit from visual restitution training.

Useful Field of View Performance in the Intact Visual Field of Hemianopia Patients.

Purpose: Postchiasmatic brain damage commonly results in an area of reduced visual sensitivity or blindness in the contralesional hemifield. Previous studies have shown that the ipsilesional visual field can be impaired too. Here, we examine whether assessing visual functioning of the "intact" ipsilesional visual field can be useful to understand difficulties experienced by patients with visual field defects. Methods: We compared the performance of 14 patients on a customized version of the useful field of view test that presents stimuli in both hemifields but only assesses functioning of their intact visual half-field (iUFOV) with that of equivalent hemifield assessments in 17 age-matched healthy control participants. In addition, we mapped visual field sensitivity with the Humphrey Field Analyzer. Last, we used an adapted version of the National Eye Institute Visual Quality of Life-25 to measure their experienced visual quality of life. Results: We found that patients performed worse on the second and third iUFOV subtests, but not on the first subtest. Furthermore, patients scored significantly worse on almost every subscale, except ocular pain. Summed iUFOV scores (assessing the intact hemifield only) and Humphrey field analyzer scores (assessing both hemifields combined) showed almost similar correlations with the subscale scores of the adapted National Eye Institute Visual Quality of Life-25. Conclusions: The iUFOV test is sensitive to deficits in the visual field that are not picked up by traditional perimetry. We therefore believe this task is of interest for patients with postchiasmatic brain lesions and should be investigated further.

Eccentricity scale independence for scene perception in the first tens of milliseconds.

Visual processing of scenes in the first tens of milliseconds relies on global image summary statistics rather than localized processing. Although natural scenes typically involve our entire visual field, scenes are usually presented experimentally at limited eccentricity. Receptive-field size increases with foveal eccentricity while increasingly pooling activity from local receptive fields. Here, we asked to what extent an observer's performance on a scene-gist perception task depends on the contents of the scene as well as on the eccentricity of the scene. We manipulated the scene content by applying window and scotoma masks. In addition, we changed presentation eccentricity independent of image content by upscaling and downscaling the scenes. We find that discrimination is strongly affected when the scene is presented with a window of 5°, showing only the central part rather than the whole scene. Performance is, however, eccentricity scale independent provided that the same scene content is presented and a comparable area of the surface of primary visual cortex is activated. We furthermore show that this eccentricity scale independence holds for shorter presentation times, down to 17 ms in some scene-discrimination tasks, but not for the naturalness-discrimination task.

Human V2A: A map of the peripheral visual hemifield with functional connections to scene-selective cortex.

Humans can recognize a scene in the blink of an eye. This gist-based visual scene perception is thought to be underpinned by specialized visual processing emphasizing the visual periphery at a cortical locus relatively low in the visual processing hierarchy. Using wide-field retinotopic mapping and population receptive field (pRF) modeling, we identified a new visual hemifield map anterior of area V2d and inferior to area V6, which we propose to call area V2A. Based on its location relative to other visual areas, V2A may correspond to area 23V described in nonhuman primates. The pRF analysis revealed unique receptive field properties for V2A: a large (FWHM ∼23°) and constant receptive field size across the central ∼70° of the visual field. Resting-state fMRI connectivity analysis further suggests that V2A is ideally suited to quickly feed the scene-processing network with information that is not biased towards the center of the visual field. Our findings not only indicate a likely cortical locus for the initial stages of gist-based visual scene perception, but also suggest a reappraisal of the organization of human dorsomedial occipital cortex with a strip of separate hemifield representations anterior to the early visual areas (V1, V2d, and V3d).

Useful field of view test performance throughout adulthood in subjects without ocular disorders.

Previous research has shown an age-related decline in Useful Field of View (UFOV) test performance, which measures the duration required to extract relevant information from a scene in three subtasks. However, these results are mostly based on data that may have been confounded by (age-related) ocular diseases. We examined UFOV performance in subjects aged 19.5 to 70.3 years to investigate how UFOV performance changes throughout adulthood. All subjects underwent a thorough ophthalmological examination to exclude ocular disorders. We also examined some elementary visual functions, i.e., near and far visual acuity, crowding and contrast sensitivity. We investigated whether these functions were related to age and whether they could explain a possible age-related decline in UFOV performance. The subjects (n = 41) performed very well on almost every measure and reached far better UFOV and visual acuity scores than those reported by other studies that relied on self-reported absence of ocular pathology. We did not find significant relationships between age and any of the elementary visual functions or the first two UFOV subtasks (R2UFOV1 = 0.03, p = 0.25; R2UFOV2 = 0.07, p = 0.10). However, we found an age-related decline in performance on the third UFOV subtask (R2UFOV3 = 0.36, p < 0.001), which was unrelated to performance on the elementary visual function tasks. Our results show that performance on the first two UFOV subtasks as well as central elementary visual functions may remain high in the absence of obvious ophthalmological pathology.

Improvement in activities of daily living after visual training in patients with homonymous visual field defects using Goal Attainment Scaling.

BACKGROUND: Stroke is the most common cause of homonymous visual field defects (HVFDs). Yet, there is no standard protocol for composing a rehabilitation program. OBJECTIVE: In this study we assess ADL gain of visual training for vision restoration in HVFD patients by means of Goal Attainment Scaling. METHODS: Thirty-five patients trained two predefined regions of the visual field successively at home. In each region we compared the effects of both training rounds, one of which was thus 'directed' and the other 'undirected'. Visual fields were measured with Humphrey and Goldmann perimetry. QoL was assessed with three stroke-related questionnaires and ADL with Goal Attainment Scaling (GAS). RESULTS: Visual training improved the visual field for both Goldmann (ECSG = 5.82±0.94 mm; p = <0.001; n = 31) and Humphrey (0.79±0.20 dB; p = <0.001; n = 28) perimetry. All standardized stroke questionnaires were significantly improved after training (p < 0.039; n = 29), but showed no significant relation with either type of field improvement (p > 0.359). About 75% of the patients improved on their (personalized) GAS score. Interestingly, after both training rounds the GAS score increased in proportion to the extent of visual field improvement, for Goldmann border shift (p = 0.042; r = 0.38; n = 29) but not for Humphrey sensitivity increase (p = 0.337; r = 0.192; n = 28). Multiple regression revealed that GAS score was linearly related to the directed training component for Humphrey perimetry, but not for undirected training. CONCLUSION: Together these data suggest that (1) visual training aimed at vision restoration leads to visual field improvement and (2) the extent of visual field improvement is linearly related to the improvement of personal activities of daily living as evaluated by means of GAS. In conclusion, a personalized evaluation to assess treatment success showed the clinical significance of a visual training for vision restoration.

A meta-analysis of perceptual and cognitive functions involved in useful-field-of-view test performance.

The useful-field-of-view (UFOV) test measures the amount of information someone can extract from a visual scene in one glance. Its scores show relatively strong relationships with everyday activities. The UFOV test consists of three computer tests, suggested to measure processing speed and central vision, divided attention, and selective attention. However, other functions seem to be involved as well. In order to investigate the contribution of these suggested and other perceptual and cognitive functions, we performed a meta-analysis of 116 Pearson's correlation coefficients between UFOV scores and other test scores reported in 18 peer-reviewed articles. We divided these correlations into nine domains: attention, executive functioning, general cognition, memory, spatial ability, visual closure, contrast sensitivity, visual processing speed, and visual acuity. A multivariate mixed-effects model analysis revealed that each domain correlated significantly with each of the UFOV subtest scores. These correlations were stronger for Subtests 2 and 3 than for Subtest 1. Furthermore, some domains were more strongly correlated to the UFOV than others across subtests. We did not find interaction effects between subtest and domain, indicating that none of the UFOV subtests is more selectively sensitive to a particular domain than the others. Thus, none of the three UFOV subtests seem to measure one clear construct. Instead, a range of visual and cognitive functions is involved. Perhaps this is the reason for the UFOV's high ecological validity, as it involves many functions at once, making it harder to compensate if one of them fails.

Segregation of Spontaneous and Training Induced Recovery from Visual Field Defects in Subacute Stroke Patients.

Whether rehabilitation after stroke profits from an early start is difficult to establish as the contributions of spontaneous recovery and treatment are difficult to tease apart. Here, we use a novel training design to dissociate these components for visual rehabilitation of subacute stroke patients with visual field defects such as hemianopia. Visual discrimination training was started within 6 weeks after stroke in 17 patients. Spontaneous and training-induced recoveries were distinguished by training one-half of the defect for 8 weeks, while monitoring spontaneous recovery in the other (control) half of the defect. Next, trained and control regions were swapped, and training continued for another 8 weeks. The same paradigm was also applied to seven chronic patients for whom spontaneous recovery can be excluded and changes in the control half of the defect point to a spillover effect of training. In both groups, field stability was assessed during a no-intervention period. Defect reduction was significantly greater in the trained part of the defect than in the simultaneously untrained part of the defect irrespective of training onset (p = 0.001). In subacute patients, training contributed about twice as much to their defect reduction as the spontaneous recovery. Goal Attainment Scores were significantly and positively correlated with the total defect reduction (p = 0.01), percentage increase reading speed was significantly and positively correlated with the defect reduction induced by training (epoch 1: p = 0.0044; epoch 2: p = 0.023). Visual training adds significantly to the spontaneous recovery of visual field defects, both during training in the early and the chronic stroke phase. However, field recovery as a result of training in this subacute phase was as large as in the chronic phase. This suggests that patients benefited primarily of early onset training by gaining access to a larger visual field sooner.

Visual Rehabilitation in Chronic Cerebral Blindness: A Randomized Controlled Crossover Study.

The treatment of patients suffering from cerebral blindness following stroke is a topic of much recent interest. Several types of treatment are under investigation, such as substitution with prisms and compensation training of saccades. A third approach, aimed at vision restitution is controversial, as a proper controlled study design is missing. In the current study, 27 chronic stroke patients with homonymous visual field defects were trained at home with a visual training device. We used a discrimination task for two types of stimuli: a static point stimulus and a new optic flow-discontinuity stimulus. Using a randomized controlled crossover design, each patient received two successive training rounds, one with high contrast stimuli in their affected hemifield (test) and one round with low-contrast stimuli in their intact hemifield (control). Goldmann and Humphrey perimetry were performed at the start of the study and following each training round. In addition, reading performance was measured. Goldmann perimetry revealed a statistically significant reduction of the visual field defect after the test training, but not after the control training or after no intervention. For both training rounds combined, Humphrey perimetry revealed that the effect of a directed training (sensitivity change in trained hemifield) exceeded that of an undirected training (sensitivity change in untrained hemifield). The interaction between trained and tested hemifield was just above the threshold of significance (p = 0.058). Interestingly, reduction of the field defect assessed by Goldmann perimetry increases with the difference between defect size as measured by Humphrey and Goldmann perimetry prior to training. Moreover, improvement of visual sensitivity measured by Humphrey perimetry increases with the fraction of non-responsive elements (i.e., more relative field loss) in Humphrey perimetry prior to training. Reading speed revealed a significant improvement after training. Our findings demonstrate that our training can result in reduction of the visual field. Improved reading performance after defect training further supports the significance of our training for improvement in daily life activities.

Dissociation of retinal and headcentric disparity signals in dorsal human cortex.

Recent fMRI studies have shown fusion of visual motion and disparity signals for shape perception (Ban et al., 2012), and unmasking camouflaged surfaces (Rokers et al., 2009), but no such interaction is known for typical dorsal motion pathway tasks, like grasping and navigation. Here, we investigate human speed perception of forward motion and its representation in the human motion network. We observe strong interaction in medial (V3ab, V6) and lateral motion areas (MT(+)), which differ significantly. Whereas the retinal disparity dominates the binocular contribution to the BOLD activity in the anterior part of area MT(+), headcentric disparity modulation of the BOLD response dominates in area V3ab and V6. This suggests that medial motion areas not only represent rotational speed of the head (Arnoldussen et al., 2011), but also translational speed of the head relative to the scene. Interestingly, a strong response to vergence eye movements was found in area V1, which showed a dependency on visual direction, just like vertical-size disparity. This is the first report of a vertical-size disparity correlate in human striate cortex.

Differential responses in dorsal visual cortex to motion and disparity depth cues.

We investigated how interactions between monocular motion parallax and binocular cues to depth vary in human motion areas for wide-field visual motion stimuli (110 × 100°). We used fMRI with an extensive 2 × 3 × 2 factorial blocked design in which we combined two types of self-motion (translational motion and translational + rotational motion), with three categories of motion inflicted by the degree of noise (self-motion, distorted self-motion, and multiple object-motion), and two different view modes of the flow patterns (stereo and synoptic viewing). Interactions between disparity and motion category revealed distinct contributions to self- and object-motion processing in 3D. For cortical areas V6 and CSv, but not the anterior part of MT(+) with bilateral visual responsiveness (MT(+)/b), we found a disparity-dependent effect of rotational flow and noise: When self-motion perception was degraded by adding rotational flow and moderate levels of noise, the BOLD responses were reduced compared with translational self-motion alone, but this reduction was cancelled by adding stereo information which also rescued the subject's self-motion percept. At high noise levels, when the self-motion percept gave way to a swarm of moving objects, the BOLD signal strongly increased compared to self-motion in areas MT(+)/b and V6, but only for stereo in the latter. BOLD response did not increase for either view mode in CSv. These different response patterns indicate different contributions of areas V6, MT(+)/b, and CSv to the processing of self-motion perception and the processing of multiple independent motions.

Saccade target selection relies on feedback competitive signal integration.

It is often assumed that decision making involves neural competition, accumulation of evidence "scores" over time, and commitment to a particular alternative once its scores reach a critical decision threshold first. So far, however, neither the first-to-threshold rule nor the nature of competition (feedforward or feedback inhibition) has been revealed by experiments. Here, we presented two simultaneously flashed targets that reversed their intensity difference during each presentation and instructed human subjects to make a saccade toward the brightest target. All subjects preferentially chose the target that was brightest during the first stimulus phase. Unless this first phase lasted only 40 ms, this primacy effect persisted even if the second, reversed-intensity phase lasted longer. This effect did not result from premature commitment to the initially dominant target, because a strong target imbalance in the opposite direction later drove nearly all responses toward that location. Moreover, there was a nonmonotonic relation between target imbalance and primacy: increasing the target imbalance beyond 40 cd/m(2) caused an attenuation of primacy. These are the hallmarks of hysteresis, predicted by models in which target representations compete through strong feedback. Reaction times were independent of the choice probability. This dissociation suggests that target selection and movement initiation are distinct phenomena.

Speed and direction response profiles of neurons in macaque MT and MST show modest constraint line tuning.

Several models of heading detection during smooth pursuit rely on the assumption of local constraint line tuning to exist in large scale motion detection templates. A motion detector that exhibits pure constraint line tuning responds maximally to any 2D-velocity in the set of vectors that can be decomposed into the central, or classic, preferred velocity (the shortest vector that still yields the maximum response) and any vector orthogonal to that. To test this assumption, we measured the firing rates of isolated middle temporal (MT) and medial superior temporal (MST) neurons to random dot stimuli moving in a range of directions and speeds. We found that as a function of 2D velocity, the pooled responses were best fit with a 2D Gaussian profile with a factor of elongation, orthogonal to the central preferred velocity, of roughly 1.5 for MST and 1.7 for MT. This means that MT and MST cells are more sharply tuned for speed than they are for direction; and that they indeed show some level of constraint line tuning. However, we argue that the observed elongation is insufficient to achieve behavioral heading discrimination accuracy on the order of 1-2 degrees as reported before.

Adjacent visual representations of self-motion in different reference frames.

Recent investigations indicate that retinal motion is not directly available for perception when moving around [Souman JL, et al. (2010) J Vis 10:14], possibly pointing to suppression of retinal speed sensitivity in motion areas. Here, we investigated the distribution of retinocentric and head-centric representations of self-rotation in human lower-tier visual motion areas. Functional MRI responses were measured to a set of visual self-motion stimuli with different levels of simulated gaze and simulated head rotation. A parametric generalized linear model analysis of the blood oxygen level-dependent responses revealed subregions of accessory V3 area, V6(+) area, middle temporal area, and medial superior temporal area that were specifically modulated by the speed of the rotational flow relative to the eye and head. Pursuit signals, which link the two reference frames, were also identified in these areas. To our knowledge, these results are the first demonstration of multiple visual representations of self-motion in these areas. The existence of such adjacent representations points to early transformations of the reference frame for visual self-motion signals and a topography by visual reference frame in lower-order motion-sensitive areas. This suggests that visual decisions for action and perception may take into account retinal and head-centric motion signals according to task requirements.

Distance estimation is influenced by encoding conditions.

BACKGROUND: It is well established that foveating a behaviorally relevant part of the visual field improves localization performance as compared to the situation where the gaze is directed elsewhere. Reduced localization performance in the peripheral encoding conditions has been attributed to an eccentricity-dependent increase in positional uncertainty. It is not known, however, whether and how the foveal and peripheral encoding conditions can influence spatial interval estimation. In this study we compare observers' estimates of a distance between two co-planar dots in the condition where they foveate the two sample dots and where they fixate a central dot while viewing the sample dots peripherally. METHODOLOGY/PRINCIPAL FINDINGS: Observers were required to reproduce, after a short delay, a distance between two sample dots based on a stationary reference dot and a movable mouse pointer. When both sample dots are foveated, we find that the distance estimation error is small but consistently increases with the dots-separation size. In comparison, distance judgment in peripheral encoding condition is significantly overestimated for smaller separations and becomes similar to the performance in foveal trials for distances from 10 to 16 degrees. CONCLUSIONS/SIGNIFICANCE: Although we find improved accuracy of distance estimation in the foveal condition, the fact that the difference is related to the reduction of the estimation bias present in the peripheral condition, challenges the simple account of reducing the eccentricity-dependent positional uncertainty. Contrary to this, we present evidence for an explanation in terms of neuronal populations activated by the two sample dots and their inhibitory interactions under different visual encoding conditions. We support our claims with simulations that take into account receptive fields size differences between the two encoding conditions.

Occlusion-related lateral connections stabilize kinetic depth stimuli through perceptual coupling.

Local sensory information is often ambiguous forcing the brain to integrate spatiotemporally separated information for stable conscious perception. Lateral connections between clusters of similarly tuned neurons in the visual cortex are a potential neural substrate for the coupling of spatially separated visual information. Ecological optics suggests that perceptual coupling of visual information is particularly beneficial in occlusion situations. Here we present a novel neural network model and a series of human psychophysical experiments that can together explain the perceptual coupling of kinetic depth stimuli with activity-driven lateral information sharing in the far depth plane. Our most striking finding is the perceptual coupling of an ambiguous kinetic depth cylinder with a coaxially presented and disparity defined cylinder backside, while a similar frontside fails to evoke coupling. Altogether, our findings are consistent with the idea that clusters of similarly tuned far depth neurons share spatially separated motion information in order to resolve local perceptual ambiguities. The classification of far depth in the facilitation mechanism results from a combination of absolute and relative depth that suggests a functional role of these lateral connections in the perception of partially occluded objects.

The role of motion capture in an illusory transformation of optic flow fields.

In the optic flow illusion, the focus of an expanding optic flow field appears shifted when uniform flow is transparently superimposed. The shift is in the direction of the uniform flow, or "inducer." Current explanations relate the transformation of the expanding optic flow field to perceptual subtraction of the inducer signal. Alternatively, the shift might result from motion capture acting on the perceived focus position. To test this alternative, we replaced expanding target flow with contracting or rotating flow. Current explanations predict focus shifts in expanding and contracting flows that are opposite but of equal magnitude and parallel to the inducer. In rotary flow, the current explanations predict shifts that are perpendicular to the inducer. In contrast, we report larger shift for expansion than for contraction and a component of shift parallel to the inducer for rotary flow. The magnitude of this novel component of shift depended on the target flow speed, the inducer flow speed, and the presentation duration. These results support the idea that motion capture contributes substantially to the optic flow illusion.

Multi-timescale perceptual history resolves visual ambiguity.

When visual input is inconclusive, does previous experience aid the visual system in attaining an accurate perceptual interpretation? Prolonged viewing of a visually ambiguous stimulus causes perception to alternate between conflicting interpretations. When viewed intermittently, however, ambiguous stimuli tend to evoke the same percept on many consecutive presentations. This perceptual stabilization has been suggested to reflect persistence of the most recent percept throughout the blank that separates two presentations. Here we show that the memory trace that causes stabilization reflects not just the latest percept, but perception during a much longer period. That is, the choice between competing percepts at stimulus reappearance is determined by an elaborate history of prior perception. Specifically, we demonstrate a seconds-long influence of the latest percept, as well as a more persistent influence based on the relative proportion of dominance during a preceding period of at least one minute. In case short-term perceptual history and long-term perceptual history are opposed (because perception has recently switched after prolonged stabilization), the long-term influence recovers after the effect of the latest percept has worn off, indicating independence between time scales. We accommodate these results by adding two positive adaptation terms, one with a short time constant and one with a long time constant, to a standard model of perceptual switching.

Flash suppression and flash facilitation in binocular rivalry.

We show that previewing one half image of a binocular rivalry pair can cause it to gain initial dominance when the other half is added, a novel phenomenon we term flash facilitation. This is the converse of a known effect called flash suppression, where the previewed image becomes suppressed upon rivalrous presentation. The exact effect of previewing an image depends on both the duration and the contrast of the prior stimulus. Brief, low-contrast prior stimuli facilitate, whereas long, high-contrast ones suppress. These effects have both an eye-based component and a pattern-based component. Our results suggest that, instead of reflecting two unrelated mechanisms, both facilitation and suppression are manifestations of a single process that occurs progressively during presentation of the prior stimulus. The distinction between the two phenomena would then lie in the extent to which the process has developed during prior stimulation. This view is consistent with a neural model previously proposed to account for perceptual stabilization of ambiguous stimuli, suggesting a relation between perceptual stabilization and the present phenomena.