Three-dimensional vestibular eye and head reflexes of the chameleon: characteristics of gain and phase and effects of eye position on orientation of ocular rotation axes during stimulation in yaw direction

We investigated gaze-stabilizing reflexes in the chameleon using the three-dimensional search-coil technique. Animals were rotated sinusoidally around an earth-vertical axis under head-fixed and head-free conditions, in the dark and in the light. Gain, phase and the influence of eye position on vestibulo-ocular reflex rotation axes were studied. During head-restrained stimulation in the dark, vestibulo-ocular reflex gaze gains were low (0.1-0.3) and phase lead decreased with increasing frequencies (from 100° at 0.04Hz to <30° at 1Hz). Gaze gains were larger during stimulation in the light (0.1-0.8) with a smaller phase lead (<30°) and were close to unity during the head-free conditions (around 0.6 in the dark, around 0.8 in the light) with small phase leads. These results confirm earlier findings that chameleons have a low vestibulo-ocular reflex gain during head-fixed conditions and stimulation in the dark and higher gains during head-free stimulation in the light. Vestibulo-ocular reflex eye rotation axes were roughly aligned with the head's rotation axis and did not systematically tilt when the animals were looking eccentrically, up- or downward (as predicted by Listing's Law). Therefore, vestibulo-ocular reflex responses in the chameleon follow a strategy, which optimally stabilizes the entire retinal images, a result previously found in non-human primate

Peaks and Troughs of Three-Dimensional Vestibulo-ocular Reflex in Humans

The three-dimensional vestibulo-ocular reflex (3D VOR) ideally generates compensatory ocular rotations not only with a magnitude equal and opposite to the head rotation but also about an axis that is collinear with the head rotation axis. Vestibulo-ocular responses only partially fulfill this ideal behavior. Because animal studies have shown that vestibular stimulation about particular axes may lead to suboptimal compensatory responses, we investigated in healthy subjects the peaks and troughs in 3D VOR stabilization in terms of gain and alignment of the 3D vestibulo-ocular response. Six healthy upright sitting subjects underwent whole body small amplitude sinusoidal and constant acceleration transients delivered by a six-degree-of-freedom motion platform. Subjects were oscillated about the vertical axis and about axes in the horizontal plane varying between roll and pitch at increments of 22.5° in azimuth. Transients were delivered in yaw, roll, and pitch and in the vertical canal planes. Eye movements were recorded in with 3D search coils. Eye coil signals were converted to rotation vectors, from which we calculated gain and misalignment. During horizontal axis stimulation, systematic deviations were found. In the light, misalignment of the 3D VOR had a maximum misalignment at about 45°. These deviations in misalignment can be explained by vector summation of the eye rotation components with a low gain for torsion and high gain for vertical. In the dark and in response to transients, gain of all components had lower values. Misalignment in darkness and for transients had different peaks and troughs than in the light: its minimum was during pitch axis stimulation and its maximum during roll axis stimulation. We show that the relatively large misalignment for roll in darkness is due to a horizontal eye movement component that is only present in darkness. In combination with the relatively low torsion gain, this horizontal component has a relative large effect on the alignment of the eye rotation axis with respect to the head rotation axis

The kinematics of far-near re-fixation saccades

We have analyzed the three-dimensional spatiotemporal characteristics of saccadic refixations between far and near targets in three behaviorally trained rhesus monkeys. The kinematics underlying these rapid eye movements can be accurately described by rotations of the eyes in four different planes, namely, first disconjugate rotations in the horizontal plane of regard converging the eyes toward the near target, followed by rotations in each eye's vertical direction plane, and finally, disconjugate rotations in a common frontoparallel plane. This compounded rotation of the eye was underlying an initially fast-rising variable torsion that typically overshot the final torsion, which the eyes attained at the time of target acquisition. The torsion consisted of a coarse, widely varying component of opposite polarity in the two eyes, which contained a more robust, much smaller modulation that sharply increased toward the end of saccades. The reorientation of the eyes in torsion depended on each eye's azimuth, elevation, and target distance. We conclude that refixation saccades are generated by motor commands that control ocular torsion in concert with the saccade generator, which operates in Donders-Listing kinematics underlying Listing's law

Three-dimensional ocular kinematics underlying binocular single vision

We have analyzed the binocular coordination of the eyes during far-to-near re-fixation saccades based on the evaluation of distance ratios and angular directions of the projected target images relative to the eyes' rotation centers. By defining the geometric point of binocular single vision, called Helmholtz point, we found that disparities during fixations of targets at near distances were limited in the subject's three-dimensional visual field to the vertical and forward directions. These disparities collapsed to simple vertical disparities in the projective binocular image plane. Subjects were able to perfectly fuse the vertically disparate target images with respect to the projected Helmholtz point of single binocular vision, independent of the particular location relative to the horizontal plane of regard. Target image fusion was achieved by binocular torsion combined with corrective modulations of the differential half-vergence angles of the eyes in the horizontal plane. Our findings support the notion that oculomotor control combines vergence in the horizontal plane of regard with active torsion in the frontal plane to achieve fusion of the dichoptic binocular target images

Temporal properties of optic flow responses in the ventral intraparietal area.

Item does not contain fulltextThe ventral intraparietal area (VIP) is located at the end of the dorsal stream. Its neurons are known to have receptive-field characteristics similar to those of MT and MST neurons, but little is known about the temporal characteristics of VIP cells' responses. How fast are directionally selective responses evoked in the ventral intraparietal area after viewing optic flow patterns, and what are the temporal properties of these neuronal responses? To examine these questions, we recorded the activity of 37 directionally selective ventral intraparietal area (VIP) neurons in two awake macaque monkeys in response to optic flow stimuli with presentation times ranging from 17 ms to 2000 ms. We found a minimum response latency of 45 ms, and a median latency of 152 ms. Of all neurons, 10% showed early response components only (response latency 150 ms and sustained activity in 500-2000 ms interval), and 35% both early and late response components. Early responses appeared to very brief stimulus presentations (33-ms duration), while the late responses required longer stimulus durations. The directional selectivity was independent of optic flow duration in all cells. These results suggest that only a subset of neurons in area VIP may contribute to the fast processing of optic flow, while showing that the temporal properties of VIP responses clearly differ from the temporal characteristics of neurons in areas MT and MST

Responses of neurons in area VIP to self-induced and external visual motion.

Item does not contain fulltextSingle-unit recordings were obtained from directionally tuned neurons in area VIP (ventral intraparietal) in two rhesus monkeys under conditions of external (passive) and self-induced (active) visual motion. A large majority of neurons showed significant differences in directional tuning for passive and active visual motion with regard to preferred direction and tuning width. The differences in preferred directions are homogeneously distributed between similar and opposite. Generally, VIP neurons are more broadly tuned to passive than to active visual motion. This is most striking for the group of cells with widely different preferred directions in active and passive conditions. Response amplitudes to passive and active visual motion are not different in general, but are slightly smaller for passive visual motion if the preferred directions differ widely. We conclude that VIP neurons can distinguish between passive and active visual motion