Conserved subcortical processing in visuo-vestibular gaze control

Gaze stabilization compensates for movements of the head or external environment to minimize image blurring. Multisensory information stabilizes the scene on the retina via the vestibulo-ocular (VOR) and optokinetic (OKR) reflexes. While the organization of neuronal circuits underlying VOR is well-described across vertebrates, less is known about the contribution and evolution of the OKR and the basic structures allowing visuo-vestibular integration. To analyze these neuronal pathways underlying visuo-vestibular integration, we developed a setup using a lamprey eye-brain-labyrinth preparation, which allowed coordinating electrophysiological recordings, vestibular stimulation with a moving platform, and visual stimulation via screens. Lampreys exhibit robust visuo-vestibular integration, with optokinetic information processed in the pretectum that can be downregulated from tectum. Visual and vestibular inputs are integrated at several subcortical levels. Additionally, saccades are present in the form of nystagmus. Thus, all basic components of the visuo-vestibular control of gaze were present already at the dawn of vertebrate evolution.Swedish Medical Research Council | Ref. VR-M-K2013-62X-03026Swedish Medical Research Council | Ref. VR-M-2015-02816Swedish Medical Research Council | Ref. VR-M-2018-02453Swedish Medical Research Council | Ref. VR-M-2019-01854Ministerio de Ciencia e Innovación | Ref. PID2020-113646GA-I00Ministerio de Ciencia e Innovación | Ref. RYC2018-024053 -IXunta de Galicia | Ref. ED431B 2021/04European Commission | Ref. EU/FP7, n. 316639European Commission | Ref. Horizon 2020, n. 720270European Commission | Ref. Horizon 2020, n. 785907European Commission | Ref. Horizon 2020, n. 945539Gösta Fraenckel Foundation for Medical Research | Ref. FS-2020:000

Ocular counter-rolling during head tilt

When tilting the head towards the shoulder there are numerous mechanisms influencing on the generation and maintenance of ocular counter-roll. Each of these mechanisms has its own temporal and spatial characteristics which influences on the counter-rolled eye position. We described a fast transient anti-compensatory torsion movement (torsion peak) as the first response to the head tilting which most certainly has its origin in the vestibular organ and the utricular maculae. Superimposed on this torsion peak we described nystagmus beats with the fast phase directed in the same direction as the head tilt movement suggesting a paralleled activation of the vertical semicircular canals. Synchronous with the torsion peak a fast vertical vergence eye movement was seen. The vertical vergence was always with left eye over right eye in the rightward head tilt and always with right eye over left eye the leftward head tilts, thus inducing a physiological skew deviation. The aetiology for this fast vertical vergence response is currently unknown but could probably be explained by a similar vestibular mechanism as for the torsion peak. A substantial amount of ocular counter-rolling (OCR) was a consistent finding in all subjects and test conditions during static head tilt. The OCR increased with head tilt but the relative compensation to the amount of head tilt decreased. For example, a 15° head tilt induced 3° OCR which corresponds to a gain of 0.20. A 30° head tilt induced an even larger OCR (5°) which corresponds to a gain of 0.16. A consistent finding was an OCR disconjugacy of the right and left eye which increased with head tilt. For instance, a rightward head tilt induced a larger ex-cyclo of the left eye than incyclo of the right eye leading to an ex-cyclovergence. The underlying mechanism might be the increased saccular impact in extreme head tilts. Sacculus has been suggested to induce disconjugate OCR while utriculus is thought to induce conjugate OCR. The static head tilt induced a vertical disconjugacy (i.e. vertical vergence) that increased with the head tilt. The direction of the eye position was however not consistent. Some subjects demonstrated a right eye over left eye position in the rightward head tilts while others demonstrated the opposite outcome. This might be explained by a difference in the ocular visual and torsional axes. To maintain binocularity the eyes are forced into vergence and depending on the position of the axes the direction of the vergence movement will differ. When holding the head in a tilted position the torsional position is found to drift. Initially this drift was directed away from the reference position thus increasing the amount of OCR. After a minute the drift was found to change direction and heading towards the reference position, thus decreasing the OCR. The OCR increasing drift might be explained by a decline in the leftward utricular discharge, induced by macula inertia during the initial interaural translation, in favour of the rightward utricular gravitational discharge. The OCR decreasing drift might be explained by an adaptation of the utricular maculae. Other possible explanations might be a leaky neural integrator or a vestibular memory loss which could induce the OCR decreasing drift found during a sustained head tilt

Torsional and vertical eye movements during head tilt dynamic characteristics. Invest Ophthalmol Vis Sci

PURPOSE. As the first response to a Bielschowsky head tilt test (BHTT), a fast transient torsional eye movement in the same direction as the head tilt has been shown with the threedimensional (3D)-video oculography (3D-VOG) technique, and this movement is paralleled by a transient vertical vergence shift inducing a physiological skew deviation. The purpose of the present study was to investigate these dynamic eye movements further in response to a BHTT paradigm with the magnetic search coil technique. METHODS. Ten healthy subjects performed a BHTT (15°, 30°, and 45°) toward each shoulder while (search coil) the monocular eye and head positions were recorded. The same head tilt paradigm was repeated in a second test while (3D-VOG) the binocular eye position was recorded. RESULTS. Subsequent to the initiation of the head tilt (latency, ϳ160 ms) a rapid torsional eye movement (mean peak velocity: 40 deg/s; mean amplitude: 4°) was seen in the same direction as the head movement, followed by a somewhat slower return movement. This torsion was synchronous with a vertical vergence eye movement (mean amplitude 3°). The vertical vergence was always with left eye over right eye in the rightward head tilt and in head straightening from the left shoulder. In the left head tilt and in the head straightening from the right shoulder, this movement was always with the right eye over the left eye. CONCLUSIONS. A torsional and vertical vergence back-and-forth eye movement induced by a BHTT was confirmed with the search coil technique. Utricular inertia due to an interaural head translation, combined with a stimulation of the vertical semicircular canals, seems to be a plausible explanation for these eye movements. (Invest Ophthalmol Vis Sci

Intensified visual clutter induces increased sympathetic signalling, poorer postural control, and faster torsional eye movements during visual rotation.

Many dizzy patients express a hypersensitivity to visual motion and clutter. This study aims to investigate how exposure to rotating visual clutter affects ocular torsion, vertical skewing, body-sway, the autonomic pupillary response, and the subjective feeling of discomfort to the stimulation. Sixteen healthy subjects were exposed to 20 seconds rotational visual stimulation (72 deg/s; 50 deg visual field). Visual stimuli were comprised of black lines on a white background, presented at low and high intensity levels of visual clutter, holding 19 lines and 38 lines respectively. Ocular torsion and vertical skewing were recorded using the Chronos Eye Tracker, which also measured pupil size as a reflection of the autonomic response. Postural control was evaluated by measuring body-sway area on the Wii Balance Board. Values were compared to data retrieved 20 seconds before and after the optokinetic stimulation, as subjects viewed the stationary visual scene. The high intensity stimulus resulted in significantly higher torsional velocities. Subjects who were exposed to low intensity first exhibited higher velocities for both intensities. Both pupil size and body sway increased for the higher intensity to both the moving and stationary visual scene, and were positively correlated to torsional velocity. In conclusion, exposure to visual clutter was reflected in the eye movement response, changes in postural control, and the autonomic response. This response may hold clinical utility when assessing patients suffering from visual motion hypersensitivity, while also providing some context as to why some healthy people feel discomfort in visually cluttered surroundings

Typical development of Motion perception and Form discrimination abilities in children

Visual functions have been widely investigated in patients with developmental disorders. This study aims to analyze the development of dorsal and ventral visual function in children with typical development, measured as motion and form discrimination abilities. A sample of 304 children (age: 4-12 years; 154 males) participated in the experiment. Non-verbal intelligence (Raven\u2019s matrices), visual acuity (Lea test), motion perception (motion coherence test-MCT) and form recognition (form coherence test-FCT) were assessed. The MCT consists of 150 white dots on a black background moving coherently at a constant velocity in one of the eight directions (signal) or in a Brownian manner (noise). The task was to recognize the direction of the signal dots. The FCT consists of white dots (signal) composing one of eight possible forms through spatial alignment of the dots, the noise was created by non-aligned dots distorting the form. The task was to recognize the form. Difficulty was increased by reducing the dot coherence (signal/noise) from 100% (no noise) to 36% in five levels. MANOVA showed a significant increment of motion and form perception accuracy with age, steeper for form as compared to motion recognition. Both functions are influenced by noise but motion discrimination seemed to be less affected. While noise had a stronger effect on the younger children in the FCT (worse performance with noise in the youngest) no such age effect was found in MCT. Motion and form perception are related to general intelligence at different ages as well as to the visual acuity. These results confirm the slowness in development of dorsal function as compared to ventral function. Visuo-spatial attention, general intelligence and visual acuity mediate the visual functionality development

The Effect of Luminance Condition on Form, Form-from-Motion and Motion Perception

This study investigated to what extent rod-dominated vision affects motion and form perception accuracy. Twenty-nine healthy subjects took part in the experiment. Form coherence (FC), form-from-motion (FFM) and motion coherence (MC) tests were assessed in low-light (rod-dominated vision) and high-light (cone-dominated vision) conditions. For each test we determined the accuracy by evaluating the correct detection obtained in five levels of coherence (corresponding to different signal-to-noise ratio). The results evidenced that motion, form and form-from-motion accuracy decreased in low-light condition. Furthermore, light condition effect was differently mediated by noise according to the type of task. The motion perception is affected only at high noise levels, while form discrimination was globally affected at all the levels, also in absence of noise, both for static (FC) and dynamic stimuli (FFM). We conclude that in rod-dominated vision form-from-motion perception is more defected than form and motion perception. We hypothesized that our results are due to the integration between M and P cells in FFM test increases the form perception accuracy in high-light condition but this advantage is completely lost during low-light condition, when the rods need to integrate information both from M and P cells

The influence of crystalline lens accommodation on post-saccadic oscillations in pupil-based eye trackers

It is well known that the crystalline lens (henceforth lens) can oscillate (or 'wobble') relative to the eyeball at the end of saccades. Recent research has proposed that such wobbling of the lens is a source of post-saccadic oscillations (PSOs) seen in data recorded by eye trackers that estimate gaze direction from the location of the pupil. Since the size of the lens wobbles increases with accommodative effort, one would predict a similar increase of PSO-amplitude in data recorded with a pupil based eye tracker. In four experiments, we investigated the role of lens accommodation on PSOs in a video-based eye tracker. In Experiment 1, we replicated previous results showing that PSO-amplitudes increase at near viewing distances (large vergence angles), when the lens is highly accommodated. In Experiment 2a, we manipulated the accommodative state of the lens pharmacologically using eye drops at a fixed viewing distance and found, in contrast to Experiment 1, no significant difference in PSO-amplitude related to the accommodative state of the lens. Finally, in Experiment 2b, the effect of vergence angle was investigated by comparing PSO-amplitudes at near and far while maintaining a fixed lens accommodation. Despite the pharmacologically fixed degree of accommodation, PSO-amplitudes were systematically larger in the near condition. In summary, PSOs cannot exhaustively be explained by lens wobbles. Possible confounds related to pupil size and eye-camera angle are investigated in Experiments 3 and 4, and alternative mechanisms behind PSOs are probed in the discussion