using-eye-tracking-to-assess-relative-importance-visual-vestibular

Using Eye-tracking to Assess the Relative Importance of Visual and Vestibular Input to Subcortical Motion Processing in the Roll Plane

The present protocol evaluates the relative impact of visual and vestibular inputs during roll plane rotations using optokinetic, vestibular, and combined ...

Karolinska Institutet

St Erik Eye Hospital

Eye movement evaluation constitutes the basis of diagnosis in dizzy patients. Through evaluating ocular torsion and vertical skewing during balance provoking stimulation, the aim of this study was to investigate the impact of vision on a typical vestibular eye movement response.

Vestibular Eye Movements Are Heavily Impacted by Visual Motion and Are Sensitive to Changes in Visual Intensities.

As animals forage for food and water or evade predators, they must rapidly decide what visual features in the environment deserve attention. In vertebrates, this visuomotor computation is implemented within the neural circuits of the optic tectum (superior colliculus in mammals). However, the mechanisms by which tectum decides whether to approach or evade remain unclear, and also which neural mechanisms underlie this behavioral choice. To address this problem, we used an eye-brain-spinal cord preparation to evaluate how the lamprey responds to visual inputs with distinct stimulus-dependent motor patterns. Using ventral root activity as a behavioral readout, we classified 2 main types of fictive motor responses: () a unilateral burst response corresponding to orientation of the head toward slowly expanding or moving stimuli, particularly within the anterior visual field, and () a unilateral or bilateral burst response triggering fictive avoidance in response to rapidly expanding looming stimuli or moving bars. A selective pharmacological blockade revealed that the brainstem-projecting neurons in the deep layer of the tectum in interaction with local inhibitory interneurons are responsible for selecting between these 2 visually triggered motor actions conveyed through downstream reticulospinal circuits. We suggest that these visual decision-making circuits had evolved in the common ancestor of vertebrates and have been conserved throughout vertebrate phylogeny.

The role of the optic tectum for visually evoked orienting and evasive movements.

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.

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

Antihistamines make up the first line of treatments against motion-sickness. Still, their efficacy and specific mechanism have come into question. The aim of this study was to investigate the effect of meclizine on motion-sensitivity.

The effects of meclizine on motion sickness revisited.

Acceleration plays a great impact on the vestibular system, but is attributed little influence over vision. This study aims to explore how visual and vestibular acceleration affect roll-plane oculomotor responses, including their addiative effect.

Visual and Vestibular Integration Express Summative Eye Movement Responses and Reveal Higher Visual Acceleration Sensitivity than Previously Described.

Vertical vergence is generally associated with one of three mechanisms: vestibular activation during a head tilt, induced by vertical visual disparity, or as a by-product of ocular torsion. However, vertical vergence can also be induced by seemingly unrelated visual conditions, such as optokinetic rotations. This study aims to investigate the effect of vision on this latter form of vertical vergence. Eight subjects (4m/4f) viewed a visual scene in head erect position in two different viewing conditions (monocular and binocular). The scene, containing white lines angled at 45° against a black background, was projected at an eye-screen distance of 2 m, and rotated 28° at an acceleration of 56°/s. Eye movements were recorded using a Chronos Eye-Tracker, and eye occlusions were carried out by placing an infrared-translucent cover in front of the left eye during monocular viewing. Results revealed vergence amplitudes during binocular viewing to be significantly lower than those seen for monocular conditions (p = 0.003), while torsion remained unaffected. This indicates that vertical vergence to optokinetic stimulation, though visually induced, is visually suppressed during binocular viewing. Considering that vertical vergence is generally viewed as a vestibular signal, the findings may reflect a visually induced activation of a vestibular pathway.

Optokinetic stimulation induces vertical vergence, possibly through a non-visual pathway.

Assessing visual attention and alertness is of great importance in visual and cognitive neuroscience, providing objective measures valuable for both researchers and clinicians. This study investigates how the optokinetic response differs between levels of visual attention in healthy adults while controlling for alertness.

Alertness and Visual Attention Impact Different Aspects of the Optokinetic Reflex.

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.

Conserved subcortical processing in visuo-vestibular gaze control.

Visually Induced Dizziness (VID) is a common post-concussion sequalae that remains poorly understood and difficult to quantify. The present study aims to identify biomarkers for VID in the form of gaze-stabilizing eye movements. Nine patients with post-commotio VID and nine age-matched healthy controls were recruited by physiotherapists at a local neurorehabilitation centre. Torsional and vergence eye movements were recorded while participants viewed a series of optokinetic rotations where the central- and peripheral regions moved coherently, incoherently, or semi-randomly. Results showed that vergence and torsional velocities were increased in VID patients, reflecting increased oculomotor gain to visual motion, and that responses correlated with symptom severity. Coherent stimulation produced fastest torsional slow-phases across all participants; when faced with confliction directional information, eye movements tended to follow the direction of the central visual field, albeit at slower velocities than during coherent motion, meaning that while torsion was sensitive to visual content of the entire visual field it expressed directional preference to the central stimulation. In conclusion, post-commotio VID was associated with faster slow-phases during optokinetic gaze-stabilization, with both vergence and torsion being correlated to symptom intensity. As torsional tracking remains inaccessible using commercial eye-trackers, vertical vergence may prove particularly accessible for clinical utility.

Concussed patients with visually induced dizziness exhibit increased ocular torsion and vertical vergence during optokinetic gaze-stabilization.

The present study aimed to construct and validate a Swedish translation (VVAS-S) of the Visual Vertigo Analogue Scale (VVAS).

Translation and validation of a Swedish version of the Visual Vertigo Analogue Scale.

This qualitative systematic review presents an overview of the state of the research relating to visual motion hypersensitivity (VMH) and offers a reference tool for future studies in the field. The study set out to identify and collate articles investigating risk groups with aberrant responses to visual motion as compared to healthy control groups, presenting evidence for risk factors associated with visual motion hypersensitivity. Data were synthesized into the state of the research and analyzed in the context of the clinical characteristics of each risk factor. Literature searches were performed on Medline Ovid, EMBASE, Web of Science, and Cinahl, identifying a total of 586 studies of which 54 were finally included. Original articles published between the dates of commencement for each database and 19th January 2021 were included. JBI critical appraisal tools were implemented for each corresponding article type. In total, the following number of studies was identified for each respective risk factor: age (n = 6), migraines (n = 8), concussions (n = 8), vestibular disorders (n = 13), psychiatric conditions (n = 5), and Parkinson's disease (n = 5). Several studies described VMH as the primary concern (n = 6), though these primarily included patients with vestibulopathies. There were considerable differences in the nomenclature employed to describe VMH, depending largely on the investigating group. An overview of investigated risk factors and their evaluation methods was presented in a Sankey diagram. Posturography was the most implemented methodology but due to diverse measurements meta-analyses were not possible. One may however note that while the easily implemented Vestibular Ocular Motor Screening (VOMS) was designed for concussed patients, it may prove useful for other risk groups.

Clinical characteristics of visual motion hypersensitivity: a systematic review.

Post-concussion syndrome (PCS) is commonly associated with dizziness and visual motion sensitivity. This case-control study set out to explore altered motion processing in PCS by measuring gaze stabilization as a reflection of the capacity of the brain to integrate motion, and it aimed to uncover mechanisms of injury where invasive subcortical recordings are not feasible.

A Proposed Mechanism for Visual Vertigo: Post-Concussion Patients Have Higher Gain From Visual Input Into Subcortical Gaze Stabilization.

Ocular torsion and vertical divergence reflect the brain's sensorimotor integration of motion through the vestibulo-ocular reflex (VOR) and the optokinetic reflex (OKR) to roll rotations. Torsion and vergence however express different response patterns depending on several motion variables, but research on their temporal dynamics remains limited. This study investigated the onset times of ocular torsion (OT) and vertical vergence (VV) during visual, vestibular, and visuovestibular motion, as well as their relative decay rates following prolonged optokinetic stimulations. Temporal characteristics were retrieved from three separate investigations where the level of visual clutter and acceleration were controlled. Video eye-tracking was used to retrieve the eye-movement parameters from a total of 41 healthy participants across all trials. Ocular torsion consistently initiated earlier than vertical vergence, particularly evident under intensified visual information density, and higher clutter levels were associated with more balanced decay rates. Additionally, stimulation modality and accelerations affected the onsets of both eye movements, with visuovestibular motion triggering earlier responses compared to vestibular motion, and increased accelerations leading to earlier onsets for both movements. The present study showed that joint visuovestibular responses produced more rapid onsets, indicating a synergetic sensorimotor process. It also showed that visual content acted as a fusional force during the decay period, and imposed greater influence over the torsional onset compared to vergence. Acceleration, by contrast, did not affect the temporal relationship between the two eye movements. Altogether, these findings provide insights into the sensorimotor integration of the vestibulo-ocular and optokinetic reflex arcs.

Temporal dynamics of ocular torsion and vertical vergence during visual, vestibular, and visuovestibular rotations.

The present study explored visually induced vertical vergence (VIVV) as non-specific motion processing response. Healthy participants (7 male, mean age 28.57 ± 2.30; 9 female, mean age 27.67 ± 3.65) were exposed to optokinetic stimuli in an HTC VIVE virtual reality headset while VIVV, pupil-size, and postural sway was recorded. The methodology was shown to produce VIVV in the roll plane at 30 deg/s. Subsequent trials consisted of 40 s optokinetic motion in yaw, pitch, and roll directions at 60 deg/s, and radial optic flow; optokinetic directions were inverted after 20 s of motion. Median VIVV amplitude changes were normalized to the clockwise roll rotation, analysed, and correlated with changes in pupil-size and body sway. VIVV, pupil-size, and body sway were all affected by changes in optokinetic direction. Post-hoc analyses showed significant VIVV responses during optokinetic yaw and pitch rotations, as well as during radial optic flow stimulations. VIVV magnitudes were universally correlated with pupil-size and body sway. In conclusion, VIVV was expressed in all tested dimensions and may consequently serve as a visual motion processing biomarker. Failing to support binocularity while responding to optokinetic directionality, VIVV may reflect an eye-movement response associated with increased postural instability and stress, similar to a dorsal light reflex.

Visually induced vertical vergence as a motion processing biomarker associated with postural instability.

The present study explored the presence of torsional gaze-stabilization to proprioceptive neck activation in humans. Thirteen healthy subjects (6 female, mean age 25) were exposed to passive body rotations while maintaining a head-fixed, gravitationally upright, position. Participants were seated in a mechanical sled, their heads placed in a chin rest embedded in a wooden beam while wearing an eye tracker attached to the beam using strong rubber bands to ensure head stability. The body was passively rotated underneath the head both in darkness and while viewing a projected visual scene. Static torsional gaze positions were compared between the baseline position prior to the stimulation, and immediately after the final body tilt had been reached. Results showed that passive neck flexion produced ocular torsion when combined with a visual background. The eyes exhibited rotations in the opposite direction of the neck's extension, matching a hypothetical head tilt in the same direction as the sled. This corresponded with a predicted head rotation aimed at straightening the head in relation to the body. No such response was seen during trials in darkness. Altogether, these findings suggest that proprioception may produce a predictive gaze-stabilizing response in humans.

Article	Year
Vestibular Eye Movements Are Heavily Impacted by Visual Motion and Are Sensitive to Changes in Visual Intensities. Investigative ophthalmology & visual science\| PubMed ID: 30897617	2019
The role of the optic tectum for visually evoked orienting and evasive movements. Proceedings of the National Academy of Sciences of the United States of America\| PubMed ID: 31296565	2019
Intensified visual clutter induces increased sympathetic signalling, poorer postural control, and faster torsional eye movements during visual rotation. PloS one\| PubMed ID: 31900468	2020
The effects of meclizine on motion sickness revisited. British journal of clinical pharmacology\| PubMed ID: 32077140	2020
Visual and Vestibular Integration Express Summative Eye Movement Responses and Reveal Higher Visual Acceleration Sensitivity than Previously Described. Investigative ophthalmology & visual science\| PubMed ID: 32392313	2020
Optokinetic stimulation induces vertical vergence, possibly through a non-visual pathway. Scientific reports\| PubMed ID: 32968160	2020
Alertness and Visual Attention Impact Different Aspects of the Optokinetic Reflex. Investigative ophthalmology & visual science\| PubMed ID: 34668924	2021
Conserved subcortical processing in visuo-vestibular gaze control. Nature communications\| PubMed ID: 35948549	2022
Concussed patients with visually induced dizziness exhibit increased ocular torsion and vertical vergence during optokinetic gaze-stabilization. Scientific reports\| PubMed ID: 36879031	2023
Translation and validation of a Swedish version of the Visual Vertigo Analogue Scale. Annals of medicine\| PubMed ID: 36896483	2023
Clinical characteristics of visual motion hypersensitivity: a systematic review. Experimental brain research\| PubMed ID: 37341755	2023
A Proposed Mechanism for Visual Vertigo: Post-Concussion Patients Have Higher Gain From Visual Input Into Subcortical Gaze Stabilization. Investigative ophthalmology & visual science\| PubMed ID: 38607620	2024
Temporal dynamics of ocular torsion and vertical vergence during visual, vestibular, and visuovestibular rotations. Experimental brain research\| PubMed ID: 38695940	2024
Visually induced vertical vergence as a motion processing biomarker associated with postural instability. Neuroscience\| PubMed ID: 39053671	2024
Human proprioceptive gaze stabilization during passive body rotations underneath a fixed head. Scientific reports\| PubMed ID: 39075206	2024

Tobias Wibble

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