Attentional heterogeneity in social anxiety disorder: Evidence from Hidden Markov Models.

There is some evidence for heterogeneity in attentional processes among individuals with social anxiety. However, there is limited work considering how attentional processes may differ as a mechanism in a naturalistic task-based context (e.g., public speaking). In this secondary analysis we tested attentional heterogeneity among individuals diagnosed with social anxiety disorder (N = 21) in the context of a virtual reality exposure treatment study. Participants completed a public speaking challenge in an immersive 360°-video virtual reality environment with eye tracking at pre-treatment, post-treatment, and at 1-week follow-up. Using a Hidden Markov Model (HMM) approach with clustering we tested whether there were distinct profiles of attention pre-treatment and whether there were changes following the intervention. As a secondary aim we tested whether the distinct attentional profiles at pre-treatment predicted differential treatment outcomes. We found two distinct attentional profiles pre-treatment that we characterized as audience-focused and audience-avoidant. However, by the 1-week follow-up the two profiles were no longer meaningfully different. We found a meaningful difference between HMM groups for fear of public speaking at post-treatment b = -8.54, 95% Highest Density Interval (HDI) [-16.00, -0.90], Bayes Factor (BF) = 8.31 but not at one-week follow-up b = -5.83, 95% HDI [-13.25, 1.81], BF = 2.28. These findings provide support for heterogeneity in attentional processes among socially anxious individuals, but our findings indicate that this may change following treatment. Moreover, our results offer preliminary mechanistic evidence that patterns of avoidance may be specifically related to poorer treatment outcomes for virtual reality exposure therapy.

Integrating Gaze, image analysis, and body tracking: Foothold selection during locomotion.

Relatively little is known about the way vision is use to guide locomo-tion in the natural world. What visual features are used to choose paths in natural complex terrain? How do walkers trade off different costs such as getting to the goal, minimizing energy, and satisfying stability constraints? To answer these questions, it is necessary to monitor not only the eyes and the body, but also to represent the three dimensional structure of the terrain. We used photogrammetry techniques to do this, and found substantial regularities in the choice of paths. Walkers avoid paths that involve changes in height and choose more circuitous and flatter paths. This stable tradeoff is related to the walker's leg length and reflects both energetic and stability constraints. Gaze data and path choices suggest that subjects take into account the terrain approximately 5 steps ahead, and so are planning routes as well as particular footplants. Such planning ahead allows the minimization of energetic costs. Thus locomotor behavior in natural environments is controlled by decision mechanisms that attempt to optimize for multiple factors in the context of well-calibrated sensory and motor internal models.

Retinal motion statistics during natural locomotion.

Walking through an environment generates retinal motion, which humans rely on to perform a variety of visual tasks. Retinal motion patterns are determined by an interconnected set of factors, including gaze location, gaze stabilization, the structure of the environment, and the walker's goals. The characteristics of these motion signals have important consequences for neural organization and behavior. However, to date, there are no empirical in situ measurements of how combined eye and body movements interact with real 3D environments to shape the statistics of retinal motion signals. Here, we collect measurements of the eyes, the body, and the 3D environment during locomotion. We describe properties of the resulting retinal motion patterns. We explain how these patterns are shaped by gaze location in the world, as well as by behavior, and how they may provide a template for the way motion sensitivity and receptive field properties vary across the visual field.

Attention guidance augmentation of virtual reality exposure therapy for social anxiety disorder: a pilot randomized controlled trial.

Biased attention to social threats has been implicated in social anxiety disorder. Modifying visual attention during exposure therapy offers a direct test of this mechanism. We developed and tested a brief virtual reality exposure therapy (VRET) protocol using 360°-video and eye tracking. Participants (N = 21) were randomized to either standard VRET or VRET + attention guidance training (AGT). Multilevel Bayesian models were used to test (1) whether there was an effect of condition over time and (2) whether post-treatment changes in gaze patterns mediated the effect of condition at follow-up. There was a large overall effect of the intervention on symptoms of social anxiety, as well as an effect of the AGT augmentation on changes in visual attention to audience members. There was weak evidence against an effect of condition on fear of public speaking and weak evidence supporting a mediation effect, however these estimates were strongly influenced by model priors. Taken together, our findings suggest that attention can be modified within and during VRET and that modification of visual gaze avoidance may be casually linked to reductions in social anxiety. Replication with a larger sample size is needed.

Retinal optic flow during natural locomotion.

We examine the structure of the visual motion projected on the retina during natural locomotion in real world environments. Bipedal gait generates a complex, rhythmic pattern of head translation and rotation in space, so without gaze stabilization mechanisms such as the vestibular-ocular-reflex (VOR) a walker's visually specified heading would vary dramatically throughout the gait cycle. The act of fixation on stable points in the environment nulls image motion at the fovea, resulting in stable patterns of outflow on the retinae centered on the point of fixation. These outflowing patterns retain a higher order structure that is informative about the stabilized trajectory of the eye through space. We measure this structure by applying the curl and divergence operations on the retinal flow velocity vector fields and found features that may be valuable for the control of locomotion. In particular, the sign and magnitude of foveal curl in retinal flow specifies the body's trajectory relative to the gaze point, while the point of maximum divergence in the retinal flow field specifies the walker's instantaneous overground velocity/momentum vector in retinotopic coordinates. Assuming that walkers can determine the body position relative to gaze direction, these time-varying retinotopic cues for the body's momentum could provide a visual control signal for locomotion over complex terrain. In contrast, the temporal variation of the eye-movement-free, head-centered flow fields is large enough to be problematic for use in steering towards a goal. Consideration of optic flow in the context of real-world locomotion therefore suggests a re-evaluation of the role of optic flow in the control of action during natural behavior.

Selective visual attention during public speaking in an immersive context.

It has recently become feasible to study selective visual attention to social cues in increasingly ecologically valid ways. In this secondary analysis, we examined gaze behavior in response to the actions of others in a social context. Participants (N = 84) were asked to give a 5-minute speech to a five-member audience that had been filmed in 360° video, displayed in a virtual reality headset containing a built-in eye tracker. Audience members were coached to make movements that would indicate interest or lack of interest (e.g., nodding vs. looking away). The goal of this paper was to analyze whether these actions influenced the speaker's gaze. We found that participants showed reliable evidence of gaze towards audience member actions in general, and towards audience member actions involving their phone specifically (compared with other actions like looking away or leaning back). However, there were no differences in gaze towards actions reflecting interest (like nodding) compared with actions reflecting lack of interest (like looking away). Participants were more likely to look away from audience member actions as well, but there were no specific actions that elicited looking away more or less. Taken together, these findings suggest that the actions of audience members are broadly influential in motivating gaze behaviors in a realistic, contextually embedded (public speaking) setting. Further research is needed to examine the ways in which these findings can be elucidated in more controlled laboratory environments as well as in the real world.

Binocular vision and the control of foot placement during walking in natural terrain.

Coordination between visual and motor processes is critical for the selection of stable footholds when walking in uneven terrains. While recent work (Matthis et al. in Curr Biol 8(28):1224-1233, 2018) demonstrates a tight link between gaze (visual) and gait (motor), it remains unclear which aspects of visual information play a role in this visuomotor control loop, and how the loss of this information affects that relationship. Here we examine the role of binocular information in the visuomotor control of walking over complex terrain. We recorded eye and body movements while normally-sighted participants walked over terrains of varying difficulty, with intact vision or with vision in one eye blurred to disrupt binocular vision. Gaze strategy was highly sensitive to the complexity of the terrain, with more fixations dedicated to foothold selection as the terrain became more difficult. The primary effect of increased sensory uncertainty due to disrupted binocular vision was a small bias in gaze towards closer footholds, indicating greater pressure on the visuomotor control process. Participants with binocular vision losses due to developmental disorders (i.e., amblyopia, strabismus), who have had the opportunity to develop alternative strategies, also biased their gaze towards closer footholds. Across all participants, we observed a relationship between an individual's typical level of binocular visual function and the degree to which gaze is shifted toward the body. Thus the gaze-gait relationship is sensitive to the level of sensory uncertainty, and deficits in binocular visual function (whether transient or long-standing) have systematic effects on gaze strategy in complex terrains. We conclude that binocular vision provides useful information for locating footholds during locomotion. Furthermore, we have demonstrated that combined eye/body tracking in natural environments can be used to provide a more detailed understanding of the impact of a type of vision loss on the visuomotor control process of walking, a vital everyday task.

Avoidance of social threat: Evidence from eye movements during a public speaking challenge using 360°- video.

Social anxiety (SA) is thought to be maintained in part by avoidance of social threat, which exacerbates fear of negative evaluation. Yet, relatively little research has been conducted to evaluate the connection between social anxiety and attentional processes in realistic contexts. The current pilot study examined patterns of attention (eye movements) in a commonly feared social context - public speaking. Participants (N = 84) with a range of social anxiety symptoms gave an impromptu five-minute speech in an immersive 360°-video environment, while wearing a virtual reality headset equipped with eye-tracking hardware. We found evidence for the expected interaction between fear of public speaking and social threat (uninterested vs. interested audience members). Consistent with prediction, participants with greater fear of public speaking looked fewer times at uninterested members of the audience (high social threat) compared to interested members of the audience (low social threat) b = 0.418, p = 0.046, 95% CI [0.008, 0.829]. Analyses of attentional indices over the course of the speech revealed that the interaction between fear of public speaking and gaze on audience members was only significant in the first three-minutes. Our results provide support for theoretical models implicating avoidance of social threat as a maintaining factor in social anxiety. Future research is needed to test whether guided attentional training targeting in vivo attentional avoidance may improve clinical outcomes for those presenting with social anxiety.

Human Gaze Assisted Artificial Intelligence: A Review.

Human gaze reveals a wealth of information about internal cognitive state. Thus, gaze-related research has significantly increased in computer vision, natural language processing, decision learning, and robotics in recent years. We provide a high-level overview of the research efforts in these fields, including collecting human gaze data sets, modeling gaze behaviors, and utilizing gaze information in various applications, with the goal of enhancing communication between these research areas. We discuss future challenges and potential applications that work towards a common goal of human-centered artificial intelligence.

Atari-HEAD: Atari Human Eye-Tracking and Demonstration Dataset.

Large-scale public datasets have been shown to benefit research in multiple areas of modern artificial intelligence. For decision-making research that requires human data, high-quality datasets serve as important benchmarks to facilitate the development of new methods by providing a common reproducible standard. Many human decision-making tasks require visual attention to obtain high levels of performance. Therefore, measuring eye movements can provide a rich source of information about the strategies that humans use to solve decision-making tasks. Here, we provide a large-scale, high-quality dataset of human actions with simultaneously recorded eye movements while humans play Atari video games. The dataset consists of 117 hours of gameplay data from a diverse set of 20 games, with 8 million action demonstrations and 328 million gaze samples. We introduce a novel form of gameplay, in which the human plays in a semi-frame-by-frame manner. This leads to near-optimal game decisions and game scores that are comparable or better than known human records. We demonstrate the usefulness of the dataset through two simple applications: predicting human gaze and imitating human demonstrated actions. The quality of the data leads to promising results in both tasks. Moreover, using a learned human gaze model to inform imitation learning leads to an 115% increase in game performance. We interpret these results as highlighting the importance of incorporating human visual attention in models of decision making and demonstrating the value of the current dataset to the research community. We hope that the scale and quality of this dataset can provide more opportunities to researchers in the areas of visual attention, imitation learning, and reinforcement learning.

Introduction to special issue on "Prediction in Perception and Action".

The wide diversity of articles in this issue reveals an explosion of evidence for the mechanisms of prediction in the visual system. When thought of as visual priors, predictive mechanisms can be seen as tightly interwoven with incoming sensory data. Prediction is thus a fundamental and essential aspect not only of visual perception but of the actions that are guided by perception.

Modeling sensory-motor decisions in natural behavior.

Although a standard reinforcement learning model can capture many aspects of reward-seeking behaviors, it may not be practical for modeling human natural behaviors because of the richness of dynamic environments and limitations in cognitive resources. We propose a modular reinforcement learning model that addresses these factors. Based on this model, a modular inverse reinforcement learning algorithm is developed to estimate both the rewards and discount factors from human behavioral data, which allows predictions of human navigation behaviors in virtual reality with high accuracy across different subjects and with different tasks. Complex human navigation trajectories in novel environments can be reproduced by an artificial agent that is based on the modular model. This model provides a strategy for estimating the subjective value of actions and how they influence sensory-motor decisions in natural behavior.

Control of gaze in natural environments: effects of rewards and costs, uncertainty and memory in target selection.

The development of better eye and body tracking systems, and more flexible virtual environments have allowed more systematic exploration of natural vision and contributed a number of insights. In natural visually guided behaviour, humans make continuous sequences of sensory-motor decisions to satisfy current goals, and the role of vision is to provide the relevant information in order to achieve those goals. This paper reviews the factors that control gaze in natural visually guided actions such as locomotion, including the rewards and costs associated with the immediate behavioural goals, uncertainty about the state of the world and prior knowledge of the environment. These general features of human gaze control may inform the development of artificial systems.

Davida Teller Award Lecture 2017: What can be learned from natural behavior?

The essentially active nature of vision has long been acknowledged but has been difficult to investigate because of limitations in the available instrumentation, both for measuring eye and body movements and for presenting realistic stimuli in the context of active behavior. These limitations have been substantially reduced in recent years, opening up a wider range of contexts where experimental control is possible. Given this, it is important to examine just what the benefits are for exploring natural vision, with its attendant disadvantages. Work over the last two decades provides insights into these benefits. Natural behavior turns out to be a rich domain for investigation, as it is remarkably stable and opens up new questions, and the behavioral context helps specify the momentary visual computations and their temporal evolution.

Contributions of monocular and binocular cues to distance discrimination in natural scenes.

Little is known about distance discrimination in real scenes, especially at long distances. This is not surprising given the logistical difficulties of making such measurements. To circumvent these difficulties, we collected 81 stereo images of outdoor scenes, together with precisely registered range images that provided the ground-truth distance at each pixel location. We then presented the stereo images in the correct viewing geometry and measured the ability of human subjects to discriminate the distance between locations in the scene, as a function of absolute distance (3 m to 30 m) and the angular spacing between the locations being compared (2°, 5°, and 10°). Measurements were made for binocular and monocular viewing. Thresholds for binocular viewing were quite small at all distances (Weber fractions less than 1% at 2° spacing and less than 4% at 10° spacing). Thresholds for monocular viewing were higher than those for binocular viewing out to distances of 15-20 m, beyond which they were the same. Using standard cue-combination analysis, we also estimated what the thresholds would be based on binocular-stereo cues alone. With two exceptions, we show that the entire pattern of results is consistent with what one would expect from classical studies of binocular disparity thresholds and separation/size discrimination thresholds measured with simple laboratory stimuli. The first exception is some deviation from the expected pattern at close distances (especially for monocular viewing). The second exception is that thresholds in natural scenes are lower, presumably because of the rich figural cues contained in natural images.

Gaze and the Control of Foot Placement When Walking in Natural Terrain.

Human locomotion through natural environments requires precise coordination between the biomechanics of the bipedal gait cycle and the eye movements that gather the information needed to guide foot placement. However, little is known about how the visual and locomotor systems work together to support movement through the world. We developed a system to simultaneously record gaze and full-body kinematics during locomotion over different outdoor terrains. We found that not only do walkers tune their gaze behavior to the specific information needed to traverse paths of varying complexity but that they do so while maintaining a constant temporal look-ahead window across all terrains. This strategy allows walkers to use gaze to tailor their energetically optimal preferred gait cycle to the upcoming path in order to balance between the drive to move efficiently and the need to place the feet in stable locations. Eye movements and locomotion are intimately linked in a way that reflects the integration of energetic costs, environmental uncertainty, and momentary informational demands of the locomotor task. Thus, the relationship between gaze and gait reveals the structure of the sensorimotor decisions that support successful performance in the face of the varying demands of the natural world. VIDEO ABSTRACT.

Memory shapes visual search strategies in large-scale environments.

Search is a central visual function. Most of what is known about search derives from experiments where subjects view 2D displays on computer monitors. In the natural world, however, search involves movement of the body in large-scale spatial contexts, and it is unclear how this might affect search strategies. In this experiment, we explore the nature of memory representations developed when searching in an immersive virtual environment. By manipulating target location, we demonstrate that search depends on episodic spatial memory as well as learnt spatial priors. Subjects rapidly learned the large-scale structure of the space, with shorter paths and less head rotation to find targets. These results suggest that spatial memory of the global structure allows a search strategy that involves efficient attention allocation based on the relevance of scene regions. Thus spatial memory may allow less energetically costly search strategies.

Vision and Action.

Investigation of natural behavior has contributed a number of insights to our understanding of visual guidance of actions by highlighting the importance of behavioral goals and focusing attention on how vision and action play out in time. In this context, humans make continuous sequences of sensory-motor decisions to satisfy current behavioral goals, and the role of vision is to provide the relevant information for making good decisions in order to achieve those goals. This conceptualization of visually guided actions as a sequence of sensory-motor decisions has been formalized within the framework of statistical decision theory, which structures the problem and provides the context for much recent progress in vision and action. Components of a good decision include the task, which defines the behavioral goals, the rewards and costs associated with those goals, uncertainty about the state of the world, and prior knowledge.

Control of gaze while walking: Task structure, reward, and uncertainty.

While it is universally acknowledged that both bottom up and top down factors contribute to allocation of gaze, we currently have limited understanding of how top-down factors determine gaze choices in the context of ongoing natural behavior. One purely top-down model by Sprague, Ballard, and Robinson (2007) suggests that natural behaviors can be understood in terms of simple component behaviors, or modules, that are executed according to their reward value, with gaze targets chosen in order to reduce uncertainty about the particular world state needed to execute those behaviors. We explore the plausibility of the central claims of this approach in the context of a task where subjects walk through a virtual environment performing interceptions, avoidance, and path following. Many aspects of both walking direction choices and gaze allocation are consistent with this approach. Subjects use gaze to reduce uncertainty for task-relevant information that is used to inform action choices. Notably the addition of motion to peripheral objects did not affect fixations when the objects were irrelevant to the task, suggesting that stimulus saliency was not a major factor in gaze allocation. The modular approach of independent component behaviors is consistent with the main aspects of performance, but there were a number of deviations suggesting that modules interact. Thus the model forms a useful, but incomplete, starting point for understanding top-down factors in active behavior.