Retinotopic connectivity maps of human visual cortex with unconstrained eye movements.

Human visual cortex contains topographic visual field maps whose organization can be revealed with retinotopic mapping. Unfortunately, constraints posed by standard mapping hinder its use in patients, atypical subject groups, and individuals at either end of the lifespan. This severely limits the conclusions we can draw about visual processing in such individuals. Here, we present a novel data-driven method to estimate connective fields, resulting in fine-grained maps of the functional connectivity between brain areas. We find that inhibitory connectivity fields accompany, and often surround facilitatory fields. The visual field extent of these inhibitory subfields falls off with cortical magnification. We further show that our method is robust to large eye movements and myopic defocus. Importantly, freed from the controlled stimulus conditions in standard mapping experiments, using entertaining stimuli and unconstrained eye movements our approach can generate retinotopic maps, including the periphery visual field hitherto only possible to map with special stimulus displays. Generally, our results show that the connective field method can gain knowledge about retinotopic architecture of visual cortex in patients and participants where this is at best difficult and confounded, if not impossible, with current methods.

Visual stress responses to static images are associated with symptoms of Persistent Postural Perceptual Dizziness (PPPD).

BACKGROUND: Images that deviate from natural scene statistics in terms of spatial frequency and orientation content can produce visual stress (also known as visual discomfort), especially for migraine sufferers. These images appear to over-activate the visual cortex. OBJECTIVE: To connect the literature on visual discomfort with a common chronic condition presenting in neuro-otology clinics known as persistent postural perceptual dizziness (PPPD). Patients experience dizziness when walking through highly cluttered environments or when watching moving stimuli. This is thought to arise from maladaptive interaction between vestibular and visual signals for balance. METHODS: We measured visual discomfort to stationary images in patients with PPPD (N = 30) and symptoms of PPPD in a large general population cohort (N = 1858) using the Visual Vertigo Analogue Scale (VVAS) and the Situational Characteristics Questionnaire (SCQ). RESULTS: We found that patients with PPPD, and individuals in the general population with more PPPD symptoms, report heightened visual discomfort to stationary images that deviate from natural spectra (patient comparison, F (1, 1865) = 29, p < 0.001; general population correlations, VVAS, rs (1387) = 0.46, p < 0.001; SCQ, rs (1387) = 0.39, p < 0.001). These findings were not explained by co-morbid migraine. Indeed, PPPD symptoms showed a significantly stronger relationship with visual discomfort than did migraine (VVAS, zH = 8.81, p < 0.001; SCQ, zH = 6.29, p < 0.001). CONCLUSIONS: We speculate that atypical visual processing -perhaps due to a visual cortex more prone to over-activation -may predispose individuals to PPPD, possibly helping to explain why some patients with vestibular conditions develop PPPD and some do not.

Further Evidence That People Rely on Egocentric Information to Guide a Cursor to a Visible Target.

Everyday movements are guided by objects' positions relative to other items in the scene (allocentric information) as well as by objects' positions relative to oneself (egocentric information). Allocentric information can guide movements to the remembered positions of hidden objects, but is it also used when the object remains visible? To stimulate the use of allocentric information, the position of the participant's finger controlled the velocity of a cursor that they used to intercept moving targets, so there was no one-to-one mapping between egocentric positions of the hand and cursor. We evaluated whether participants relied on allocentric information by shifting all task-relevant items simultaneously leaving their allocentric relationships unchanged. If participants rely on allocentric information they should not respond to this perturbation. However, they did. They responded in accordance with their responses to each item shifting independently, supporting the idea that fast guidance of ongoing movements primarily relies on egocentric information.

Detection of scene-relative object movement and optic flow parsing across the adult lifespan.

Moving around safely relies critically on our ability to detect object movement. This is made difficult because retinal motion can arise from object movement or our own movement. Here we investigate ability to detect scene-relative object movement using a neural mechanism called optic flow parsing. This mechanism acts to subtract retinal motion caused by self-movement. Because older observers exhibit marked changes in visual motion processing, we consider performance across a broad age range (N = 30, range: 20-76 years). In Experiment 1 we measured thresholds for reliably discriminating the scene-relative movement direction of a probe presented among three-dimensional objects moving onscreen to simulate observer movement. Performance in this task did not correlate with age, suggesting that ability to detect scene-relative object movement from retinal information is preserved in ageing. In Experiment 2 we investigated changes in the underlying optic flow parsing mechanism that supports this ability, using a well-established task that measures the magnitude of globally subtracted optic flow. We found strong evidence for a positive correlation between age and global flow subtraction. These data suggest that the ability to identify object movement during self-movement from visual information is preserved in ageing, but that there are changes in the flow parsing mechanism that underpins this ability. We suggest that these changes reflect compensatory processing required to counteract other impairments in the ageing visual system.

Persistent postural perceptual dizziness is on a spectrum in the general population.

OBJECTIVE: To examine the idea that symptoms of persistent postural perceptual dizziness (PPPD) are more common than previously assumed and lie on a spectrum in the general population, thus challenging current theories that PPPD is only a consequence of a vestibular insult. METHODS: We collected 2 common clinical questionnaires of PPPD (Visual Vertigo Analogue Scale [VVAS] and Situational Characteristics Questionnaire [SCQ]) in 4 cohorts: community research volunteers (n = 1941 for VVAS, n = 1,474 for SCQ); paid online participants (n = 190 for VVAS, n = 125 for SCQ); students (n = 204, VVAS only); and patients diagnosed with PPPD (n = 25). RESULTS: We found that around 9%, 4%, and 11%, respectively, of the 3 nonclinical cohorts scored above the 25th percentile patient score on 1 PPPD measure (VVAS) and 49% and 54% scored above the 25th percentile patient score on the other measure (SCQ). Scores correlated negatively with age (counter to expectation). As expected, scores correlated with migraine in 2 populations, but this only explained a small part of the variance, suggesting that migraine is not the major factor underlying the spectrum of PPPD symptoms in the general population. CONCLUSION: We found high levels of PPPD symptoms in nonclinical populations, suggesting that PPPD is a spectrum that preexists in the population, rather than only being a consequence of vestibular insult. Atypical visuo-vestibular processing predisposes some individuals to visually induced dizziness, which is then exacerbated should vestibular insult (or more generalized insult) occur.

The role of time perception in temporal binding: Impaired temporal resolution in causal sequences.

Causality affects our perception of time; events that appear as causally related are perceived as closer together in time than unrelated events. This effect is known as temporal binding. One potential explanation of this effect is that causality slows an "internal clock" that is used in interval estimation. To explore this hypothesis, we first examined participants' perceived duration of a range of intervals between a causal action and an effect, or between two unrelated events. If (apparent) causality slows the internal clock, then plotting perceived duration against actual duration should reveal a shallower slope in the causality condition (a relative compression of perceived time). This pattern was found. We then examined an interesting corollary: that a slower rate during causal sequences would result in reduced temporal acuity. This is what we found: Duration discrimination thresholds were higher for causal compared to non-causal sequences. These results are compatible with a clock-slowing account of temporal binding. Implications for sensory recalibration accounts of binding are discussed.

The predictability of a target's motion influences gaze, head, and hand movements when trying to intercept it.

Does the predictability of a target's movement and of the interception location influence how the target is intercepted? In a first experiment, we manipulated the predictability of the interception location. A target moved along a haphazardly curved path, and subjects attempted to tap on it when it entered a hitting zone. The hitting zone was either a large ring surrounding the target's starting position (ring condition) or a small disk that became visible before the target appeared (disk condition). The interception location gradually became apparent in the ring condition, whereas it was immediately apparent in the disk condition. In the ring condition, subjects pursued the target with their gaze. Their heads and hands gradually moved in the direction of the future tap position. In the disk condition, subjects immediately directed their gaze toward the hitting zone by moving both their eyes and heads. They also moved their hands to the future tap position sooner than in the ring condition. In a second and third experiment, we made the target's movement more predictable. Although this made the targets easier to pursue, subjects now shifted their gaze to the hitting zone soon after the target appeared in the ring condition. In the disk condition, they still usually shifted their gaze to the hitting zone at the beginning of the trial. Together, the experiments show that predictability of the interception location is more important than predictability of target movement in determining how we move to intercept targets. NEW & NOTEWORTHY We show that if people are required to intercept a target at a known location, they direct their gaze to the interception point as soon as they can rather than pursuing the target with their eyes for as long as possible. The predictability of the interception location rather than the predictability of the path to that location largely determines how the eyes, head, and hand move.

Lateral visual occlusion does not change walking trajectories.

Difficulties with walking are often reported following brain damage that causes a lateralized loss of awareness on one side. Whether lateralized loss of awareness has a direct causal impact on walking is unknown. A review of the literature on visually guided walking suggests several reasons why a lateralized loss of visual awareness might be expected to lead to difficulties walking. Here, we isolated and examined the effect of lateralized vision loss on walking behavior in real and virtual environments. Healthy young participants walked to a target placed within a real room, in a virtual corridor, or on a virtual ground plane. In the ground-plane condition, the scene either was empty or contained three obstacles. We reduced vision on one side by occluding one eye (Experiment 1 and 2) or removing one hemifield, defined relative to either the head or trunk (Experiment 2), through use of eye patching (Experiment 1) and a virtual-reality system (Experiment 2). Visual-field restrictions did not induce significant deviations in walking paths in any of the occlusion conditions or any of the environments. The results provide further insight into the visual information that guides walking in humans, and suggest that lateralized vision loss on its own is not the primary cause of walking difficulties.

Ability to identify scene-relative object movement is not limited by, or yoked to, ability to perceive heading.

During locomotion humans can judge where they are heading relative to the scene and the movement of objects within the scene. Both judgments rely on identifying global components of optic flow. What is the relationship between the perception of heading, and the identification of object movement during self-movement? Do they rely on a shared mechanism? One way to address these questions is to compare performance on the two tasks. We designed stimuli that allowed direct comparison of the precision of heading and object movement judgments. Across a series of experiments, we found the precision was typically higher when judging scene-relative object movement than when judging heading. We also found that manipulations of the content of the visual scene can change the relative precision of the two judgments. These results demonstrate that the ability to judge scene-relative object movement during self-movement is not limited by, or yoked to, the ability to judge the direction of self-movement.

The Primary Role of Flow Processing in the Identification of Scene-Relative Object Movement.

Retinal image motion could be due to the movement of the observer through space or an object relative to the scene. Optic flow, form, and change of position cues all provide information that could be used to separate out retinal motion due to object movement from retinal motion due to observer movement. In Experiment 1, we used a minimal display to examine the contribution of optic flow and form cues. Human participants indicated the direction of movement of a probe object presented against a background of radially moving pairs of dots. By independently controlling the orientation of each dot pair, we were able to put flow cues to self-movement direction (the point from which all the motion radiated) and form cues to self-movement direction (the point toward which all the dot pairs were oriented) in conflict. We found that only flow cues influenced perceived probe movement. In Experiment 2, we switched to a rich stereo display composed of 3D objects to examine the contribution of flow and position cues. We moved the scene objects to simulate a lateral translation and counter-rotation of gaze. By changing the polarity of the scene objects (from light to dark and vice versa) between frames, we placed flow cues to self-movement direction in opposition to change of position cues. We found that again flow cues dominated the perceived probe movement relative to the scene. Together, these experiments indicate the neural network that processes optic flow has a primary role in the identification of scene-relative object movement.SIGNIFICANCE STATEMENT Motion of an object in the retinal image indicates relative movement between the observer and the object, but it does not indicate its cause: movement of an object in the scene; movement of the observer; or both. To isolate retinal motion due to movement of a scene object, the brain must parse out the retinal motion due to movement of the eye ("flow parsing"). Optic flow, form, and position cues all have potential roles in this process. We pitted the cues against each other and assessed their influence. We found that flow parsing relies on optic flow alone. These results indicate the primary role of the neural network that processes optic flow in the identification of scene-relative object movement.

Peripheral Visual Cues Contribute to the Perception of Object Movement During Self-Movement.

Safe movement through the environment requires us to monitor our surroundings for moving objects or people. However, identification of moving objects in the scene is complicated by self-movement, which adds motion across the retina. To identify world-relative object movement, the brain thus has to 'compensate for' or 'parse out' the components of retinal motion that are due to self-movement. We have previously demonstrated that retinal cues arising from central vision contribute to solving this problem. Here, we investigate the contribution of peripheral vision, commonly thought to provide strong cues to self-movement. Stationary participants viewed a large field of view display, with radial flow patterns presented in the periphery, and judged the trajectory of a centrally presented probe. Across two experiments, we demonstrate and quantify the contribution of peripheral optic flow to flow parsing during forward and backward movement.

Spared ability to perceive direction of locomotor heading and scene-relative object movement despite inability to perceive relative motion.

BACKGROUND: All contemporary models of perception of locomotor heading from optic flow (the characteristic patterns of retinal motion that result from self-movement) begin with relative motion. Therefore it would be expected that an impairment on perception of relative motion should impact on the ability to judge heading and other 3D motion tasks. MATERIAL AND METHODS: We report two patients with occipital lobe lesions whom we tested on a battery of motion tasks. Patients were impaired on all tests that involved relative motion in plane (motion discontinuity, form from differences in motion direction or speed). Despite this they retained the ability to judge their direction of heading relative to a target. A potential confound is that observers can derive information about heading from scale changes bypassing the need to use optic flow. Therefore we ran further experiments in which we isolated optic flow and scale change. RESULTS: Patients' performance was in normal ranges on both tests. The finding that ability to perceive heading can be retained despite an impairment on ability to judge relative motion questions the assumption that heading perception proceeds from initial processing of relative motion. Furthermore, on a collision detection task, SS and SR's performance was significantly better for simulated forward movement of the observer in the 3D scene, than for the static observer. This suggests that in spite of severe deficits on relative motion in the frontoparlel (xy) plane, information from self-motion helped identification objects moving along an intercept 3D relative motion trajectory. CONCLUSIONS: This result suggests a potential use of a flow parsing strategy to detect in a 3D world the trajectory of moving objects when the observer is moving forward. These results have implications for developing rehabilitation strategies for deficits in visually guided navigation.

Are perceptuo-motor decisions really more optimal than cognitive decisions?

Human high-level cognitive decisions appear sub-optimal (Kahneman, Slovic, & Tversky, 1982; Kahneman & Tversky, 1979). Paradoxically, perceptuo-motor decisions appear optimal, or nearly optimal (Trommershäuser, Maloney, & Landy, 2008). Here, we highlight limitations to the comparison of performance between and within domains. These limitations are illustrated by means of two perceptuo-motor decision-making experiments. The results indicate that participants did not optimize fundamental performance-related factors (precision and time usage), even though standard analyses may have classed participants as 'optimal'. Moreover, simulations and comparisons across our studies demonstrate that optimality depends on task difficulty. Thus, it seems that a standard model of perceptuo-motor decision-making fails to provide an absolute standard of performance. Importantly, this appears to be a limitation of optimal models of human behaviour in general. This, in conjunction with non-trivial evaluative- and methodological differences, suggests that verdicts favouring perceptuo-motor, or perceptual, systems over higher-level cognitive systems in terms of level of performance are premature.

Perceptuo-motor, cognitive, and description-based decision-making seem equally good.

Classical studies suggest that high-level cognitive decisions (e.g., choosing between financial options) are suboptimal. In contrast, low-level decisions (e.g., choosing where to put your feet on a rocky ridge) appear near-optimal: the perception-cognition gap. Moreover, in classical tasks, people appear to put too much weight on unlikely events. In contrast, when people can learn through experience, they appear to put too little weight on unlikely events: the description-experience gap. We eliminated confounding factors and, contrary to what is commonly believed, found results suggesting that (i) the perception-cognition gap is illusory and due to differences in the way performance is assessed; (ii) the description-experience gap arises from the assumption that objective probabilities match subjective ones; (iii) people's ability to make decisions is better than the classical literature suggests; and (iv) differences between decision-makers are more important for predicting peoples' choices than differences between choice tasks.

Flow parsing and heading perception show similar dependence on quality and quantity of optic flow.

Here we examine the relationship between the perception of heading and flow parsing. In a companion study we have investigated the pattern of dependence of human heading estimation on the quantity (amount of dots per frame) and quality (amount of directional noise) of motion information in an optic flow field. In the present study we investigated whether the flow parsing mechanism, which is thought to aid in the assessment of scene-relative object movement during observer movement, exhibits a similar pattern of dependence on these stimulus manipulations. Finding that the pattern of flow parsing effects was similar to that observed for heading thresholds would provide some evidence that these two complementary roles for optic flow processing are reliant on the same, or similar, neural computation. We found that the pattern of flow parsing effects observed does indeed display a striking similarity to the heading thresholds. As with judgements of heading, there is a critical value of around 25 dots per frame; below this value flow parsing effects rapidly deteriorate and above this value flow parsing effects are stable [see Warren et al. (1988) for similar results for heading]. Also, as with judgements of heading, when there were 50 or more dots there was a systematic effect of noise on the magnitude of the flow parsing effect. These results are discussed in the context of different possible schemes of flow processing to support both heading and flow parsing mechanisms.

Heading recovery from optic flow: comparing performance of humans and computational models.

Human observers can perceive their direction of heading with a precision of about a degree. Several computational models of the processes underpinning the perception of heading have been proposed. In the present study we set out to assess which of four candidate models best captured human performance; the four models we selected reflected key differences in terms of approach and methods to modelling optic flow processing to recover movement parameters. We first generated a performance profile for human observers by measuring how performance changed as we systematically manipulated both the quantity (number of dots in the stimulus per frame) and quality (amount of 2D directional noise) of the flow field information. We then generated comparable performance profiles for the four candidate models. Models varied markedly in terms of both their performance and similarity to human data. To formally assess the match between the models and human performance we regressed the output of each of the four models against human performance data. We were able to rule out two models that produced very different performance profiles to human observers. The remaining two shared some similarities with human performance profiles in terms of the magnitude and pattern of thresholds. However none of the models tested could capture all aspect of the human data.

Does optic flow parsing depend on prior estimation of heading?

We have recently suggested that neural flow parsing mechanisms act to subtract global optic flow consistent with observer movement to aid in detecting and assessing scene-relative object movement. Here, we examine whether flow parsing can occur independently from heading estimation. To address this question we used stimuli comprising two superimposed optic flow fields comprising limited lifetime dots (one planar and one radial). This stimulus gives rise to the so-called optic flow illusion (OFI) in which perceived heading is biased in the direction of the planar flow field. Observers were asked to report the perceived direction of motion of a probe object placed in the OFI stimulus. If flow parsing depends upon a prior estimate of heading then the perceived trajectory should reflect global subtraction of a field consistent with the heading experienced under the OFI. In Experiment 1 we tested this prediction directly, finding instead that the perceived trajectory was biased markedly in the direction opposite to that predicted under the OFI. In Experiment 2 we demonstrate that the results of Experiment 1 are consistent with a positively weighted vector sum of the effects seen when viewing the probe together with individual radial and planar flow fields. These results suggest that flow parsing is not necessarily dependent on prior estimation of heading direction. We discuss the implications of this finding for our understanding of the mechanisms of flow parsing.

Knowing when to move on: cognitive and perceptual decisions in time.

We investigated people's ability to decide how much time to spend on the task at hand. To make such decisions well, one must take into account, among other things, the cost of failing and how one's task performance changes as a function of time. We first investigated timing decisions when the underlying task was perceptual. Decisions were highly efficient and suggested that people can make good use of perceptual knowledge and abstract reward information. Previous studies have found that perceptual decisions are generally optimal, but that cognitive decisions are generally suboptimal--a perception-cognition gap. Does a similar gap exist for timing decisions? We compared timing decisions for a perceptual task with timing decisions for more cognitive tasks. Performance was highly similar across the tasks, which suggests that knowledge can be acquired, and used to make timing decisions, in an equally efficient way regardless of whether that knowledge is derived through perceptual or cognitive experience.

How we perceive the trajectory of an approaching object.

Various equations that describe how observers could recover the trajectory of an approaching object have been put forward. Many are relatively complex formulations that recover the veridical trajectory by scaling retinal cues, such as looming and changing disparity. However, these equations do not seem to describe human perception as observers typically misjudge trajectory angles. Thus, we examine whether a simpler formulation--one that does not predict veridical judgments-may better explain performance. We test the hypothesis that perceived trajectory is based on a speed ratio: the ratio of lateral angular speed to the sum of looming and changing disparity signals. To discriminate between this and alternative proposals, we examined the effect of object size on trajectory perception: The speed ratio hypothesis predicts that perceived trajectory will become less eccentric with increasing object size, while the alternatives predict that perceived trajectory will be independent of object size. Observers performed a trajectory judgment task in which they compared the trajectory direction of two approaching objects, of the same or different size, seen in separate intervals. We estimated perceptually parallel trajectories from their responses. In Experiment 1, objects differed in horizontal and vertical size, and in Experiment 2, they differed only in vertical size. In both experiments, observers' data showed a clear effect of object size and were close to predictions of the speed ratio hypothesis. We conclude that the alternate proposals we tested were not supported and that the speed ratio account is a sufficient account of the data.

The role of discrepant retinal motion during walking in the realignment of egocentric space.

Visually guided action relies on accurate perception of egocentric direction. Unfortunately, perceived direction easily becomes misaligned. How is this problem overcome? One theory (R. Held & S. J. Freedman, 1963) is that during self-movement the observer uses the relationship between anticipated and experienced sensory feedback as a source of information to maintain alignment. However, data supporting this theory is equivocal, and recent evidence appears contradictory. We reexamined the issue. We injected an error into perceived visual direction and then assessed realignment after a period of walking toward a target. We manipulated the sensory information available (presence of retinal motion, Experiment 1; presence of peripheral motion, Experiment 2) and found that as the amount of retinal motion was reduced (Experiments 1 and 2), realignment of perceived visual direction decreased. When we then (Experiment 3) removed the discrepancy between anticipated and experienced retinal motion, no realignment was observed. Our results provide evidence that a discrepancy between anticipated and experienced sensory feedback is an important source of information for the alignment of egocentric space, with retinal motion having a particular role in driving a realignment of perceived visual direction.