Visual motion processing and human tracking behavior

The accurate visual tracking of a moving object is a human fundamental skill that allows to reduce the relative slip and instability of the object's image on the retina, thus granting a stable, high-quality vision. In order to optimize tracking performance across time, a quick estimate of the object's global motion properties needs to be fed to the oculomotor system and dynamically updated. Concurrently, performance can be greatly improved in terms of latency and accuracy by taking into account predictive cues, especially under variable conditions of visibility and in presence of ambiguous retinal information. Here, we review several recent studies focusing on the integration of retinal and extra-retinal information for the control of human smooth pursuit.By dynamically probing the tracking performance with well established paradigms in the visual perception and oculomotor literature we provide the basis to test theoretical hypotheses within the framework of dynamic probabilistic inference. We will in particular present the applications of these results in light of state-of-the-art computer vision algorithms

Goal-Directed Behavior under Variational Predictive Coding: Dynamic Organization of Visual Attention and Working Memory

Mental simulation is a critical cognitive function for goal-directed behavior because it is essential for assessing actions and their consequences. When a self-generated or externally specified goal is given, a sequence of actions that is most likely to attain that goal is selected among other candidates via mental simulation. Therefore, better mental simulation leads to better goal-directed action planning. However, developing a mental simulation model is challenging because it requires knowledge of self and the environment. The current paper studies how adequate goal-directed action plans of robots can be mentally generated by dynamically organizing top-down visual attention and visual working memory. For this purpose, we propose a neural network model based on variational Bayes predictive coding, where goal-directed action planning is formulated by Bayesian inference of latent intentional space. Our experimental results showed that cognitively meaningful competencies, such as autonomous top-down attention to the robot end effector (its hand) as well as dynamic organization of occlusion-free visual working memory, emerged. Furthermore, our analysis of comparative experiments indicated that introduction of visual working memory and the inference mechanism using variational Bayes predictive coding significantly improve the performance in planning adequate goal-directed actions

Target Selection by Frontal Cortex During Coordinated Saccadic and Smooth Pursuit Eye Movement

Oculomotor tracking of moving objects is an important component of visually based cognition and planning. Such tracking is achieved by a combination of saccades and smooth pursuit eye movements. In particular, the saccadic and smooth pursuit systems interact to often choose the same target, and to maximize its visibility through time. How do multiple brain regions interact, including frontal cortical areas, to decide the choice of a target among several competing moving stimuli? How is target selection information that is created by a bias (e.g., electrical stimulation) transferred from one movement system to another? These saccade-pursuit interactions are clarified by a new computational neural model, which describes interactions among motion processing areas MT, MST, FPA, DLPN; saccade specification, selection, and planning areas LIP, FEF, SNr, SC; the saccadic generator in the brain stem; and the cerebellum. Model simulations explain a broad range of neuroanatomical and neurophysiological data. These results are in contrast with the simplest parallel model with no interactions between saccades and pursuit than common-target selection and recruitment of shared motoneurons. Actual tracking episodes in primates reveal multiple systematic deviations from predictions of the simplest parallel model, which are explained by the current model.National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624

Recurrent cerebellar architecture solves the motor-error problem

Current views of cerebellar function have been heavily influenced by the models of Marr and Albus, who suggested that the climbing fibre input to the cerebellum acts as a teaching signal for motor learning. It is commonly assumed that this teaching signal must be motor error (the difference between actual and correct motor command), but this approach requires complex neural structures to estimate unobservable motor error from its observed sensory consequences. We have proposed elsewhere a recurrent decorrelation control architecture in which Marr-Albus models learn without requiring motor error. Here, we prove convergence for this architecture and demonstrate important advantages for the modular control of systems with multiple degrees of freedom. These results are illustrated by modelling adaptive plant compensation for the three-dimensional vestibular ocular reflex. This provides a functional role for recurrent cerebellar connectivity, which may be a generic anatomical feature of projections between regions of cerebral and cerebellar cortex

Gaze control modelling and robotic implementation

Although we have the impression that we can process the entire visual field in a single fixation, in reality we would be unable to fully process the information outside of foveal vision if we were unable to move our eyes. Because of acuity limitations in the retina, eye movements are necessary for processing the details of the array. Our ability to discriminate fine detail drops off markedly outside of the fovea in the parafovea (extending out to about 5 degrees on either side of fixation) and in the periphery (everything beyond the parafovea). While we are reading or searching a visual array for a target or simply looking at a new scene, our eyes move every 200-350 ms. These eye movements serve to move the fovea (the high resolution part of the retina encompassing 2 degrees at the centre of the visual field) to an area of interest in order to process it in greater detail. During the actual eye movement (or saccade), vision is suppressed and new information is acquired only during the fixation (the period of time when the eyes remain relatively still). While it is true that we can move our attention independently of where the eyes are fixated, it does not seem to be the case in everyday viewing. The separation between attention and fixation is often attained in very simple tasks; however, in tasks like reading, visual search, and scene perception, covert attention and overt attention (the exact eye location) are tightly linked. Because eye movements are essentially motor movements, it takes time to plan and execute a saccade. In addition, the end-point is pre-selected before the beginning of the movement. There is considerable evidence that the nature of the task influences eye movements. Depending on the task, there is considerable variability both in terms of fixation durations and saccade lengths. It is possible to outline five separate movement systems that put the fovea on a target and keep it there. Each of these movement systems shares the same effector pathway—the three bilateral groups of oculomotor neurons in the brain stem. These five systems include three that keep the fovea on a visual target in the environment and two that stabilize the eye during head movement. Saccadic eye movements shift the fovea rapidly to a visual target in the periphery. Smooth pursuit movements keep the image of a moving target on the fovea. Vergence movements move the eyes in opposite directions so that the image is positioned on both foveae. Vestibulo-ocular movements hold images still on the retina during brief head movements and are driven by signals from the vestibular system. Optokinetic movements hold images during sustained head rotation and are driven by visual stimuli. All eye movements but vergence movements are conjugate: each eye moves the same amount in the same direction. Vergence movements are disconjugate: The eyes move in different directions and sometimes by different amounts. Finally, there are times that the eye must stay still in the orbit so that it can examine a stationary object. Thus, a sixth system, the fixation system, holds the eye still during intent gaze. This requires active suppression of eye movement. Vision is most accurate when the eyes are still. When we look at an object of interest a neural system of fixation actively prevents the eyes from moving. The fixation system is not as active when we are doing something that does not require vision, for example, mental arithmetic. Our eyes explore the world in a series of active fixations connected by saccades. The purpose of the saccade is to move the eyes as quickly as possible. Saccades are highly stereotyped; they have a standard waveform with a single smooth increase and decrease of eye velocity. Saccades are extremely fast, occurring within a fraction of a second, at speeds up to 900°/s. Only the distance of the target from the fovea determines the velocity of a saccadic eye movement. We can change the amplitude and direction of our saccades voluntarily but we cannot change their velocities. Ordinarily there is no time for visual feedback to modify the course of the saccade; corrections to the direction of movement are made in successive saccades. Only fatigue, drugs, or pathological states can slow saccades. Accurate saccades can be made not only to visual targets but also to sounds, tactile stimuli, memories of locations in space, and even verbal commands (“look left”). The smooth pursuit system keeps the image of a moving target on the fovea by calculating how fast the target is moving and moving the eyes accordingly. The system requires a moving stimulus in order to calculate the proper eye velocity. Thus, a verbal command or an imagined stimulus cannot produce smooth pursuit. Smooth pursuit movements have a maximum velocity of about 100°/s, much slower than saccades. The saccadic and smooth pursuit systems have very different central control systems. A coherent integration of these different eye movements, together with the other movements, essentially corresponds to a gating-like effect on the brain areas controlled. The gaze control can be seen in a system that decides which action should be enabled and which should be inhibited and in another that improves the action performance when it is executed. It follows that the underlying guiding principle of the gaze control is the kind of stimuli that are presented to the system, by linking therefore the task that is going to be executed. This thesis aims at validating the strong relation between actions and gaze. In the first part a gaze controller has been studied and implemented in a robotic platform in order to understand the specific features of prediction and learning showed by the biological system. The eye movements integration opens the problem of the best action that should be selected when a new stimuli is presented. The action selection problem is solved by the basal ganglia brain structures that react to the different salience values of the environment. In the second part of this work the gaze behaviour has been studied during a locomotion task. The final objective is to show how the different tasks, such as the locomotion task, imply the salience values that drives the gaze

Neural Dynamics of Saccadic and Smooth Pursuit Eye Movement Coordination during Visual Tracking of Unpredictably Moving Targets

How does the brain use eye movements to track objects that move in unpredictable directions and speeds? Saccadic eye movements rapidly foveate peripheral visual or auditory targets and smooth pursuit eye movements keep the fovea pointed toward an attended moving target. Analyses of tracking data in monkeys and humans reveal systematic deviations from predictions of the simplest model of saccade-pursuit interactions, which would use no interactions other than common target selection and recruitment of shared motoneurons. Instead, saccadic and smooth pursuit movements cooperate to cancel errors of gaze position and velocity, and thus to maximize target visibility through time. How are these two systems coordinated to promote visual localization and identification of moving targets? How are saccades calibrated to correctly foveate a target despite its continued motion during the saccade? A neural model proposes answers to such questions. The modeled interactions encompass motion processing areas MT, MST, FPA, DLPN and NRTP; saccade planning and execution areas FEF and SC; the saccadic generator in the brain stem; and the cerebellum. Simulations illustrate the model’s ability to functionally explain and quantitatively simulate anatomical, neurophysiological and behavioral data about SAC-SPEM tracking.National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624

Visual attention deficits in schizophrenia can arise from inhibitory dysfunction in thalamus or cortex

Schizophrenia is associated with diverse cognitive deficits, including disorders of attention-related oculomotor behavior. At the structural level, schizophrenia is associated with abnormal inhibitory control in the circuit linking cortex and thalamus. We developed a spiking neural network model that demonstrates how dysfunctional inhibition can degrade attentive gaze control. Our model revealed that perturbations of two functionally distinct classes of cortical inhibitory neurons, or of the inhibitory thalamic reticular nucleus, disrupted processing vital for sustained attention to a stimulus, leading to distractibility. Because perturbation at each circuit node led to comparable but qualitatively distinct disruptions in attentive tracking or fixation, our findings support the search for new eye movement metrics that may index distinct underlying neural defects. Moreover, because the cortico-thalamic circuit is a common motif across sensory, association, and motor systems, the model and extensions can be broadly applied to study normal function and the neural bases of other cognitive deficits in schizophrenia.R01 MH057414 - NIMH NIH HHS; R01 MH101209 - NIMH NIH HHS; R01 NS024760 - NINDS NIH HHSPublished versio

Neural Dynamics of Saccadic and Smooth Pursuit Eye Movement Coordination during Visual Tracking of Unpredictably Moving Targets

How does the brain use eye movements to track objects that move in unpredictable directions and speeds? Saccadic eye movements rapidly foveate peripheral visual or auditory targets and smooth pursuit eye movements keep the fovea pointed toward an attended moving target. Analyses of tracking data in monkeys and humans reveal systematic deviations from predictions of the simplest model of saccade-pursuit interactions, which would use no interactions other than common target selection and recruitment of shared motoneurons. Instead, saccadic and smooth pursuit movements cooperate to cancel errors of gaze position and velocity, and thus to maximize target visibility through time. How are these two systems coordinated to promote visual localization and identification of moving targets? How are saccades calibrated to correctly foveate a target despite its continued motion during the saccade? A neural model proposes answers to such questions. The modeled interactions encompass motion processing areas MT, MST, FPA, DLPN and NRTP; saccade planning and execution areas FEF and SC; the saccadic generator in the brain stem; and the cerebellum. Simulations illustrate the model’s ability to functionally explain and quantitatively simulate anatomical, neurophysiological and behavioral data about SAC-SPEM tracking.National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624

Evidence of inverted-gravity driven variation in predictive sensorimotor function.

We move our eyes to place the fovea into the part of a viewed scene currently of interest. Recent evidence suggests that each human has signature patterns of eye movements like handwriting which depend on their sensitivity, allocation of attention and experience. Use of implicit knowledge of how earth's gravity influences object motion has been shown to aid dynamic perception. We used a projected ball tracking task with a plain background offering no context cues to probe the effect of acquired experience about physical laws of gravitation on performance differences of 44 participants under a simulated gravity and an atypical (upward) antigravity condition. Performance measured by the unsigned difference between instantaneous eye and stimulus positions (RMSE) was consistently worse in the antigravity condition. In the vertical RMSE, participants took about 200ms longer to improve to the best performance for antigravity compared to gravity trials. The antigravity condition produced a divergence of individual performance which was correlated with levels of questionnaire based quantified traits of schizotypy but not control traits. Grouping participants by high or low traits revealed a negative relationship between schizotypy traits level and both initiation and maintenance of tracking, a result consistent with trait related impoverished sensory prediction. The findings confirm for the first time that where cues enabling exact estimation of acceleration are unavailable, knowledge of gravity contributes to dynamic prediction improving motion processing. With acceleration expectations violated, we demonstrate that antigravity tracking could act as a multivariate diagnostic window into predictive brain function