Tutis Vilis

Geometric relations of eye position and velocity vectors during saccades.

Measurements of angular position and velocity vectors of the eye in three human and three monkey subjects showed that: (1) position vectors lie roughly in a single plane, in accordance with Listings law, between and during saccades; (2) primary position of the eye is often far from the centre of the oculomotor range. (3) saccades have nearly-fixed rotation axes, which tilt out of Listings plane in a systematic way depending on current eye position. Findings 1 and 3 show that saccadic control signals accurately reflect the properties of three-dimensional rotations, as predicted by a new quaternion model of the saccadic system; models that approximate rotational kinematics using vectorial addition and integration do not predict these findings.

COMPUTING THREE-DIMENSIONAL EYE POSITION QUATERNIONS AND EYE VELOCITY FROM SEARCH COIL SIGNALS

The four-component rotational operators called quaternions, which represent eye rotations in terms of their axes and angles, have several advantages over other representations of eye position (such as Fick coordinates): they provide easy computations, symmetry, a simple form for Listings law, and useful three-dimensional plots of eye movements. In this paper we present algorithms for computing eye position quaternions and eye angular velocity (not the derivative of position in three dimensions) from two search coils (not necessarily orthogonal) on one eye in two or three magnetic fields, and for locating primary position using quaternions. We show how differentiation of eye position signals yields poor estimates of all three components of eye velocity.

Generation of torsional and vertical eye position signals by the interstitial nucleus of cajal

The neural integrator, which converts eye velocity signals into position signals, is central to oculomotor theory. Similar integrators are probably necessary in any neural system that changes and maintains muscular tension. The integrator for horizontal eye position is in the pons, but the locations of the vertical and torsional integrators have not been clearly defined. Recording three-dimensional eye movements in alert monkeys during microstimulation and pharmacological inactivation of midbrain sites showed that the interstitial nucleus of Cajal generates both the torsional and vertical eye position signals. Up and down signals are linked with clockwise signals in the right brain and counterclockwise signals in the left brain. This three-dimensional coordinate system achieves orthogonality and bilateral symmetry without redundancy and optimizes energy efficiency for horizontal visual scanning.

Rotation of Listing's plane during vergence

When visually fixating targets on an isovergence surface, the position of each eye was constrained to a plane. Thus, Listings law holds during vergence. The planes were, however, rotated temporally with respect to those when viewing distant targets. The effect of this rotation was to produce a torsion which depended on eye elevation; extorsion of the two eyes for downward gaze and intorsion for upward gaze. The saccadic velocity command was relatively unaffected during vergence. Computer simulations suggest that the saccadic tonic command and the vergence command interact multiplicatively in three dimensions.

Inhibition and generation of saccades: Rapid event-related fMRI of prosaccades, antisaccades, and nogo trials

Flexible, adaptive behavior often requires the inhibition of automatic responses in favor of voluntary response generation. The antisaccade task requires active inhibition of the automatic saccade to a peripheral stimulus followed by generation of a voluntary antisaccade to the opposite location. Previous studies demonstrated greater functional magnetic resonance imaging (fMRI) activation for antisaccades than prosaccades in cortical saccade areas but did not distinguish the relative contributions of saccadic inhibition and generation. To address this question, we compared prosaccades, antisaccades, and nogo trials in a rapid event-related fMRI experiment with ten human subjects (6 female, 4 male). Trials were compound, containing a colored fixation point to cue trial type, followed by a 200-ms gap and then peripheral stimulus presentation and response. Required responses for prosaccade, antisaccade, and nogo trials, respectively, were to generate a saccade to the stimulus, look away from it, and inhibit the automatic saccade while maintaining central fixation. Frontal and supplementary eye fields, anterior cingulate cortex, intraparietal sulcus, and precuneus, exhibited surprisingly similar activation patterns for prosaccade and nogo responses, suggesting that BOLD signal in cortical saccade regions might predominantly reflect visual detection and attention processes rather than saccade generation or inhibition. These regions displayed greater activation for antisaccade responses versus prosaccade or nogo responses, possibly due to visuospatial remapping or increased attention levels in the antisaccade task. In right superior frontal sulcus, right supramarginal gyrus, and posterior cingulate sulcus, activation was greater for nogo compared to prosaccade responses, suggesting a role in active saccadic inhibition.

Arm movement performance during reversible basal ganglia lesions in the monkey

SummaryArm motor performance of eight Cebus monkeys was examined during reversible cooling in the ventral lateral region of the putamen and globus pallidus (primarily the external segment), where neurons discharging during arm movements have been found (DeLong 1972).When attempting to hold a handle stationary during basal ganglia cooling, all monkeys developed flexion at the wrist and some developed a slow flexion drift of the arm at the elbow. The prominence of wrist flexion emphasizes that the basal ganglia may normally influence distal musculature.During basal ganglia cooling an increase in segmental stretch reflexes (15–30 ms) was sometimes observed following arm perturbations, but no consistent increase occurred in the later EMG responses (30–95 ms) in contrast to results obtained in Parkinsonian patients (Tatton and Lee 1975).No major changes were observed in the time of onset of the earliest EMG activity in the agonist muscle in a simple reaction time elbow movement task during basal ganglia cooling.Basal ganglia lesions produced major disorders in both flexion and extension movements including slowing of movements and rebound of the arm towards its initial position after onset of movement. These disorders were accompanied by an increase in tonic activity of both flexors and extensors while holding and by increased levels of cocontraction of agonists and antagonists during attempted movements.It is suggested that this basal ganglia disorder is due to a failure to achieve the correct balance of activity between agonists and antagonists that is appropriate for a particular motor act.

The superior colliculus and spatiotemporal translation in the saccadic system

Abstract The superior colliculus (SC) plays an important part in generating saccadic eye movements, sending signals coding desired eye rotation to the brainstem. These signals must be translated from the topographic (spatial) representation used in the SC to the firing frequency (temporal) code used downstream. We show that a model of the saccadic system using the quaternion representation of eye rotations yields a spatiotemporal translation with all the experimentally observed properties: activation of a particular site in the SC generates a saccade of a particular amplitude and direction; activation of multiple sites evokes a vector average (weighted by activity levels) of the saccades coded by the individual sites; the intensity and temporal profile of activation determine saccade speed but not metrics. The feature of the model that is essential to these results is a particular sort of redundancy in the quaternion representation, coupled with multiplicative downstream handling of SC outputs.

Segregation and persistence of form in the lateral occipital complex

While the lateral occipital complex (LOC) has been shown to be implicated in object recognition, it is unclear whether this brain area is responsive to low-level stimulus-driven features or high-level representational processes. We used scrambled shape-from-motion displays to disambiguate the presence of contours from figure-ground segregation and to measure the strength of the binding process for shapes without contours. We found persisting brain activation in the LOC for scrambled displays after the motion stopped indicating that this brain area subserves and maintains figure-ground segregation processes, a low-level function in the object processing hierarchy. In our second experiment, we found that the figure-ground segregation process has some form of spatial constancy indicating top-down influences. The persisting activation after the motion stops suggests an intermediate role in object recognition processes for this brain area and might provide further evidence for the idea that the lateral occipital complex subserves mnemonic functions mediating between iconic and short-term memory.

Modularity and parallel processing in the oculomotor integrator

The neural signals that hold eye position originate in a brainstem structure called the neural integrator, so-called because it is thought to compute these position signals using a process equivalent to mathematical integration. Most previous experiments have assumed that the neural integrator reacts to damage like a sigle mathematical integrator: the eye is expected to drift towards a unique resting point at a simple exponential rate dependent on current eye position. Physiologically, this would require a neural network with uniformly distributed internal connections. However, Cannon et al. (1983) proposed a more robust modular internal configuration, with dense local connections and sparse remote connections, computationally equivalent to a parallel array of independent sub-integrators. Damage to some sub-integrators would not affect function in the others, so that part of the position signal would remain intact, and a more complex pattern of drift would result. We evaluated this parallel integrator hypothesis by recording three-dimensional eye positions in the light and dark from five alert monkeys with partial neural integrator failure. Our previous study showed that injection of the inhibitory γ aminobutyric acid agonist muscimol into the mesencephalic interstitial nucleus of Cajal (INC) causes almost complete failure of the integrators for vertical and torsional eye position after ∼ 30 min. This study examines the more modest initial effects. Several aspects of the initial vertical drift could not be accounted for by the single integrator scheme. First, the eye did not initially drift towards a single resting position; rapid but brief drift was observed towards multiple resting positions. With time after the muscimol injection, this range of stable eye positions progressively narrowed until it eventually approximated a single point. Second, the drift had multiple time constants. Third, multiple regression analysis revealed a significant correlation between drift rate and magnitude of the previous saccade, in addition to a correlation between drift rate and position. This saccade dependence enabled animals to stabilize gaze by making a series of saccades to the same target, each with less post-saccadic drift than its predecessor. These observations were predicted and explained by a model in which each of several parallel integrators generated a fraction of the eye-position command. Drift was simulated by setting the internal gain of some integrators at one (perfect integration), others at slightly less than one (imperfect integration), and the remainder at zero (no integration), as expected during partial damage to an anatomically modular network. These results support the previous suggestion that internal connections within the neural integrator network are restricted to local modules. The advantages of this modular configuration are a relative immunity to random local computational errors and partial conservation of function after damage. Similar computational advantages may be an important consequence of the modular patterns of connectivity observed throughout the brain.

Representation of Head-Centric Flow in the Human Motion Complex

Recent neuroimaging studies have identified putative homologs of macaque middle temporal area (area MT) and medial superior temporal area (area MST) in humans. Little is known about the integration of visual and nonvisual signals in human motion areas compared with monkeys. Through extra-retinal signals, the brain can factor out the components of visual flow on the retina that are induced by eye-in-head and head-in-space rotations and achieve a representation of flow relative to the head (head-centric flow) or body (body-centric flow). Here, we used functional magnetic resonance imaging to test whether extra-retinal eye-movement signals modulate responses to visual flow in the human MT+ complex. We distinguished between MT and MST and tested whether subdivisions of these areas may transform the retinal flow into head-centric flow. We report that interactions between eye-movement signals and visual flow are not evenly distributed across MT+. Pursuit hardly influenced the response of MT to flow, whereas the responses in MST to the same retinal stimuli were stronger during pursuit than during fixation. We also identified two subregions in which the flow-related responses were boosted significantly by pursuit, one overlapping part of MST. In addition, we found evidence of a metric relation between rotational flow relative to the head and fMRI signals in a subregion of MST. The latter findings provide an important advance over published single-cell recordings in monkey MST. A visual representation of the rotation of the head in the world derived from head-centric flow may supplement semicircular canals signals and is appropriate for cross-calibrating vestibular and visual signals.