Ocular Counter Rotation During Gaze Shifts

Abducens motor neurons (ABD) are known to receive oculomotor signals via the excitatory and inhibitory burst neurons (BN) as well as head velocity related signals via the vestibular nucleus (VN). If the oculomotor input to the ABD was the same, would there be a difference in the properties of the observed eye movement between head restrained (HR) and head unrestrained (HU) gaze shifts? To answer this question, the activity of 22 BN was recorded during HR and HU visual motor tasks performed by non human primates. A template matching algorithm was used to find a pair of trials (HR, HU) with matching BN activity. This guaranteed that the oculomotor input to the ABD was the same. Matched trials were found to have similar gaze amplitudes, but the peak eye velocity of HU movement was lower than HR movement. A time varying gain of the head velocity input was calculated as the ratio of the difference between the eye velocities over the head velocity. This yielded a gain that was high at the onset of the movement, decreased through out the gaze shift and plateau at one after gaze shift offset. Thus the head movement was highly inhibiting the eye movement at HU gaze onset which decreased throughout the gaze shift until it reached and remained at one at the end of the gaze shift. Finally a computer simulation was used to check if the difference in the eye velocities could be explained by VN inputs. The simulation modeled the difference in ABD firing rate (ÄABD) between HR and HU matched trials as the weighted sum of the difference in the firing rate of VN (ÄPVPc, ÄPVPi and ÄEHc) input. The BN input was not used in this model because for matched trials the input was the same, thus the difference was equal to zero. The simulation showed that the weight of EHc cells input was the highest, thus accounting for most of the difference in the ABD. This lead to the conclusion that EHc cells played a major role in reducing the eye velocity during head unrestrained gaze shifts

High-field fMRI reveals brain activation patterns underlying saccade execution in the human superior colliculus

Background The superior colliculus (SC) has been shown to play a crucial role in the initiation and coordination of eye- and head-movements. The knowledge about the function of this structure is mainly based on single-unit recordings in animals with relatively few neuroimaging studies investigating eye-movement related brain activity in humans. Methodology/Principal Findings The present study employed high-field (7 Tesla) functional magnetic resonance imaging (fMRI) to investigate SC responses during endogenously cued saccades in humans. In response to centrally presented instructional cues, subjects either performed saccades away from (centrifugal) or towards (centripetal) the center of straight gaze or maintained fixation at the center position. Compared to central fixation, the execution of saccades elicited hemodynamic activity within a network of cortical and subcortical areas that included the SC, lateral geniculate nucleus (LGN), occipital cortex, striatum, and the pulvinar. Conclusions/Significance Activity in the SC was enhanced contralateral to the direction of the saccade (i.e., greater activity in the right as compared to left SC during leftward saccades and vice versa) during both centrifugal and centripetal saccades, thereby demonstrating that the contralateral predominance for saccade execution that has been shown to exist in animals is also present in the human SC. In addition, centrifugal saccades elicited greater activity in the SC than did centripetal saccades, while also being accompanied by an enhanced deactivation within the prefrontal default-mode network. This pattern of brain activity might reflect the reduced processing effort required to move the eyes toward as compared to away from the center of straight gaze, a position that might serve as a spatial baseline in which the retinotopic and craniotopic reference frames are aligned

A Neural Model of Visually Guided Steering, Obstacle Avoidance, and Route Selection

A neural model is developed to explain how humans can approach a goal object on foot while steering around obstacles to avoid collisions in a cluttered environment. The model uses optic flow from a 3D virtual reality environment to determine the position of objects based on motion discontinuities, and computes heading direction, or the direction of self-motion, from global optic flow. The cortical representation of heading interacts with the representations of a goal and obstacles such that the goal acts as an attractor of heading, while obstacles act as repellers. In addition the model maintains fixation on the goal object by generating smooth pursuit eye movements. Eye rotations can distort the optic flow field, complicating heading perception, and the model uses extraretinal signals to correct for this distortion and accurately represent heading. The model explains how motion processing mechanisms in cortical areas MT, MST, and posterior parietal cortex can be used to guide steering. The model quantitatively simulates human psychophysical data about visually-guided steering, obstacle avoidance, and route selection.Air Force Office of Scientific Research (F4960-01-1-0397); National Geospatial-Intelligence Agency (NMA201-01-1-2016); National Science Foundation (SBE-0354378); Office of Naval Research (N00014-01-1-0624

Learning the Optimal Control of Coordinated Eye and Head Movements

Various optimality principles have been proposed to explain the characteristics of coordinated eye and head movements during visual orienting behavior. At the same time, researchers have suggested several neural models to underly the generation of saccades, but these do not include online learning as a mechanism of optimization. Here, we suggest an open-loop neural controller with a local adaptation mechanism that minimizes a proposed cost function. Simulations show that the characteristics of coordinated eye and head movements generated by this model match the experimental data in many aspects, including the relationship between amplitude, duration and peak velocity in head-restrained and the relative contribution of eye and head to the total gaze shift in head-free conditions. Our model is a first step towards bringing together an optimality principle and an incremental local learning mechanism into a unified control scheme for coordinated eye and head movements

Computational Study of Multisensory Gaze-Shift Planning

In response to appearance of multimodal events in the environment, we often make a gaze-shift in order to focus the attention and gather more information. Planning such a gaze-shift involves three stages: 1) to determine the spatial location for the gaze-shift, 2) to find out the time to initiate the gaze-shift, 3) to work out a coordinated eye-head motion to execute the gaze-shift. There have been a large number of experimental investigations to inquire the nature of multisensory and oculomotor information processing in any of these three levels separately. Here in this thesis, we approach this problem as a single executive program and propose computational models for them in a unified framework. The first spatial problem is viewed as inferring the cause of cross-modal stimuli, whether or not they originate from a common source (chapter 2). We propose an evidence-accumulation decision-making framework, and introduce a spatiotemporal similarity measure as the criterion to choose to integrate the multimodal information or not. The variability of report of sameness, observed in experiments, is replicated as functions of the spatial and temporal patterns of target presentations. To solve the second temporal problem, a model is built upon the first decision-making structure (chapter 3). We introduce an accumulative measure of confidence on the chosen causal structure, as the criterion for initiation of action. We propose that gaze-shift is implemented when this confidence measure reaches a threshold. The experimentally observed variability of reaction time is simulated as functions of spatiotemporal and reliability features of the cross-modal stimuli. The third motor problem is considered to be solved downstream of the two first networks (chapter 4). We propose a kinematic strategy that coordinates eye-in-head and head-on-shoulder movements, in both spatial and temporal dimensions, in order to shift the line of sight towards the inferred position of the goal. The variabilities in contributions of eyes and head movements to gaze-shift are modeled as functions of the retinal error and the initial orientations of eyes and head. The three models should be viewed as parts of a single executive program that integrates perceptual and motor processing across time and space

Implications of interrupted eye–head gaze shifts for resettable integrator reset.

Abstract The neural circuit responsible for saccadic eye movements is generally thought to resemble a closed loop controller. Several models of the saccadic system assume that the feedback signal of such a controller is an efference copy of "eye displacement", a neural estimate of the distance already travelled by the eyes, provided by the so-called "resettable integrator" (RI). The speed, with which the RI is reset, is thought to be fast or instantaneous by some authors and gradual by others. To examine this issue, psychophysicists have taken advantage of the target-distractor paradigm. Subjects engaged in it, are asked to look to only one of two stimuli (the "target") and not to a distractor presented in the diametrically opposite location and they often generate movement sequences in which a gaze shift towards the "distractor" is followed by a second gaze shift to the "target". The fact that the second movement is not systematically erroneous even when very short time intervals (about 5 ms) separate it from the first movement has been used to question the verisimilitude of gradual RI reset. To explore this matter we used a saccade-generating network that relies on a RI coupled to a head controller and a model of the rotational vestibulo-ocular reflex. An analysis of the activation functions of model units provides disproof by counterexample: "targets" can be accurately acquired even when the RI of the saccadic burst generator is not reset at all after the end of the first, interrupted eye-head gaze shift to the distractor and prior to the second, complete eye-head gaze shift to the "target"

Neural Representations for Sensory-Motor Control, III: Learning a Body-Centered Representation of 3-D Target Position

A neural model is described of how the brain may autonomously learn a body-centered representation of 3-D target position by combining information about retinal target position, eye position, and head position in real time. Such a body-centered spatial representation enables accurate movement commands to the limbs to be generated despite changes in the spatial relationships between the eyes, head, body, and limbs through time. The model learns a vector representation--otherwise known as a parcellated distributed representation--of target vergence with respect to the two eyes, and of the horizontal and vertical spherical angles of the target with respect to a cyclopean egocenter. Such a vergence-spherical representation has been reported in the caudal midbrain and medulla of the frog, as well as in psychophysical movement studies in humans. A head-centered vergence-spherical representation of foveated target position can be generated by two stages of opponent processing that combine corollary discharges of outflow movement signals to the two eyes. Sums and differences of opponent signals define angular and vergence coordinates, respectively. The head-centered representation interacts with a binocular visual representation of non-foveated target position to learn a visuomotor representation of both foveated and non-foveated target position that is capable of commanding yoked eye movementes. This head-centered vector representation also interacts with representations of neck movement commands to learn a body-centered estimate of target position that is capable of commanding coordinated arm movements. Learning occurs during head movements made while gaze remains fixed on a foveated target. An initial estimate is stored and a VOR-mediated gating signal prevents the stored estimate from being reset during a gaze-maintaining head movement. As the head moves, new estimates arc compared with the stored estimate to compute difference vectors which act as error signals that drive the learning process, as well as control the on-line merging of multimodal information.Air Force Office of Scientific Research (F49620-92-J-0499); National Science Foundation (IRI -87-16960, IRI-90-24877); Office of Naval Research (N00014-92-J-l309

A Neural Model of Visually Guided Steering, Obstacle Avoidance, and Route Selection

A neural model is developed to explain how humans can approach a goal object on foot while steering around obstacles to avoid collisions in a cluttered environment. The model uses optic flow from a 3D virtual reality environment to determine the position of objects based on motion discotinuities, and computes heading direction, or the direction of self-motion, from global optic flow. The cortical representation of heading interacts with the representations of a goal and obstacles such that the goal acts as an attractor of heading, while obstacles act as repellers. In addition the model maintains fixation on the goal object by generating smooth pursuit eye movements. Eye rotations can distort the optic flow field, complicating heading perception, and the model uses extraretinal signals to correct for this distortion and accurately represent heading. The model explains how motion processing mechanisms in cortical areas MT, MST, and VIP can be used to guide steering. The model quantitatively simulates human psychophysical data about visually-guided steering, obstacle avoidance, and route selection.Air Force Office of Scientific Research (F4960-01-1-0397); National Geospatial-Intelligence Agency (NMA201-01-1-2016); National Science Foundation (NSF SBE-0354378); Office of Naval Research (N00014-01-1-0624

High-Field fMRI Reveals Brain Activation Patterns Underlying Saccade Execution in the Human Superior Colliculus

BACKGROUND: The superior colliculus (SC) has been shown to play a crucial role in the initiation and coordination of eye- and head-movements. The knowledge about the function of this structure is mainly based on single-unit recordings in animals with relatively few neuroimaging studies investigating eye-movement related brain activity in humans. METHODOLOGY/PRINCIPAL FINDINGS: The present study employed high-field (7 Tesla) functional magnetic resonance imaging (fMRI) to investigate SC responses during endogenously cued saccades in humans. In response to centrally presented instructional cues, subjects either performed saccades away from (centrifugal) or towards (centripetal) the center of straight gaze or maintained fixation at the center position. Compared to central fixation, the execution of saccades elicited hemodynamic activity within a network of cortical and subcortical areas that included the SC, lateral geniculate nucleus (LGN), occipital cortex, striatum, and the pulvinar. CONCLUSIONS/SIGNIFICANCE: Activity in the SC was enhanced contralateral to the direction of the saccade (i.e., greater activity in the right as compared to left SC during leftward saccades and vice versa) during both centrifugal and centripetal saccades, thereby demonstrating that the contralateral predominance for saccade execution that has been shown to exist in animals is also present in the human SC. In addition, centrifugal saccades elicited greater activity in the SC than did centripetal saccades, while also being accompanied by an enhanced deactivation within the prefrontal default-mode network. This pattern of brain activity might reflect the reduced processing effort required to move the eyes toward as compared to away from the center of straight gaze, a position that might serve as a spatial baseline in which the retinotopic and craniotopic reference frames are aligned