Human proprioceptive gaze stabilization during passive body rotations underneath a fixed head.

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.

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

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.

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

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.

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

Purpose: 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. Methods: A total of 554 eye movements were analyzed in 10 PCS patients and nine healthy controls across 171 trials. Optokinetic and vestibulo-ocular reflexes were recorded using a head-mounted eye tracker while participants were exposed to visual, vestibular, and visuo-vestibular motion stimulations in the roll plane. Torsional and vergence eye movements were analyzed in terms of slow-phase velocities, gain, nystagmus frequency, and sensory-specific contributions toward gaze stabilization. Results: Participants expressed eye-movement responses consistent with expected gaze stabilization; slow phases were fastest for visuo-vestibular trials and slowest for visual stimulations (P < 0.001) and increased with stimulus acceleration (P < 0.001). Concussed patients demonstrated increased gain from visual input to gaze stabilization (P = 0.005), faster slow phases (P = 0.013), earlier nystagmus beats (P = 0.003), and higher relative visual influence over the gaze-stabilizing response (P = 0.001), presenting robust effect sizes despite the limited population size. Conclusions: The enhanced neural responsiveness to visual motion in PCS, combined with semi-intact visuo-vestibular integration, presented a subcortical hierarchy for altered gaze stabilization. Drawing on comparable animal trials, findings suggest that concussed patients may suffer from diffuse injuries to inhibiting pathways for optokinetic information, likely early in the visuo-vestibular hierarchy of sensorimotor integration. These findings offer context for common but elusive symptoms, presenting a neurological explanation for motion sensitivity and visual vertigo in PCS.

Clinical characteristics of visual motion hypersensitivity: a systematic review.

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.

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

PURPOSE: The present study aimed to construct and validate a Swedish translation (VVAS-S) of the Visual Vertigo Analogue Scale (VVAS). MATERIALS AND METHODS: The original English VVAS was translated into Swedish by the two authors and back-translated by an independent professional translator. Pilot-tests were performed on two healthy participants and five patients suffering from Visually Induced Dizziness (VID). The translation was deemed understandable by all subjects. Twenty-one patients with VID were recruited to complete the VVAS-S, once in-lab and once at home after 2-3 weeks. Cronbach's alpha, inter-item consistency and internal consistency were calculated. RESULTS: Test-retest values were reliably strong across all items. Cronbach's alpha was 0.843, which is considered to represent very-high reliability. The corrected-item total-correlation was above 0.3 for all items, meaning they were appropriately associated with one-another. Fourteen out of 36 inter-item correlation interactions were within the 0.2-0.4 range. CONCLUSIONS: The VVAS-S was found to be comparable to the original VVAS in terms of internal reliability. The translation was perceived as easy to implement by all participants and can be considered ready for clinical use in a Swedish-speaking setting. Item-specific correlations may be valuable for developing future vertigo questionnaires.Key messagesThe Swedish version of the Visual Vertigo Analogue Scale is a questionnaire suitable for evaluating visually induced dizziness in a Swedish population. This study found that the Swedish questionnaire was comparable to the original in terms of internal consistency. The Swedish Visual vertigo Analogue Scale can be found as an appendix to this article.

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

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.

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.

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

Purpose: 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. Methods: Twelve healthy subjects (8 men and 4 women; mean age = 33 ± 9.36) with intact gaze-stability, visual acuity, and binocularity were recruited. Subjects viewed a rotating visual scene provoking torsional optokinetic nystagmus (OKN) while wearing a video eye tracker in a seated head-fixed position. Tasks requiring focused, neutral, and divided visual attention were issued to each subject and the OKN was recorded. Pupil sizes were monitored as a proxy for alertness. Results: Pupil dilation was increased for both focused and divided visual attention. The number of nystagmus beats was highest for the focused condition and lowest for the divided attentional task. OKN gain was increased during both focused and divided attention. The distribution of nystagmus beats over time showed that only focused attention produced a reliable adaptation of the OKN. Conclusions: Results consequently indicate that OKN frequency is adaptive to a viewer's level of visual attention, whereas OKN gain is influenced by alertness levels. This pattern offers insight into the neural processes integrating visual input with reflexive motor responses. For example, it contextualizes why attention to visual stimuli can cause dizziness, as the OKN frequency reflects activity of the velocity storage mechanism. Additionally, the OKN could offer a possible venue for differentiating between visual attention and alertness during psychometric testing.

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

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°/s2. 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.

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

Purpose: 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. Methods: Seated in a mechanical sled, 13 healthy volunteers (7 men, 6 women; mean age 25 years) were exposed to a series of visual (VIS) optokinetic, vestibular (VES) whole-body, and combined (VIS + VES) rotations. This was carried out at two acceleration intensities. Subjects wore a video-based eye tracker, enabling analysis of torsional and skewing eye movement responses, which were used to evaluate the individual response to each trial. The tracker also contained accelerometers allowing head tracking. Results: Both ocular torsion and vertical skewing were sensitive to acceleration intensities for VES and VIS + VES. For VIS only, skewing exhibited such a response. An increased acceleration yielded a decreased torsion-skewing ratio for VIS, explained by the change in skewing, but remained unchanged for VES and VIS + VES. Torsion exhibited particularly reliable summative effect, yielding a relative contribution of 32% VIS and 75% VES during low acceleration, and 19% and 85%, respectively, during high acceleration. Conclusions: The change in the skewing response to different intensities indicates that the visual system is more sensitive to visual accelerations than previously described. Eye movements showed reliable summative effects, indicating a robust visual-vestibular integration that indicates their integrative priorities for each acceleration, with the visual system being more involved during low accelerations. Such objective quantifications could hold clinical utility when assessing sensory mismatch in vertiginous patients.

The effects of meclizine on motion sickness revisited.

AIMS: 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. METHODS: This study was carried out as a triple-blinded randomized trial involving 12 healthy subjects who were exposed to (i) vestibular (VES), (ii) visual (VIS) and (iii) visual-vestibular (VIS+VES) stimulations in the roll plane. Subjects were divided into 2 groups by stratified randomization, receiving either meclizine or a placebo. Stimulations were carried out before, and after, drug administration, presented at 2 intensity levels of 14 and 28°/s2 . Eye movements were tracked, and torsional slow-phase velocities, amplitudes and nystagmus beats were retrieved. Subjects initially graded for their motion-sickness susceptibility. RESULTS: Susceptibility had no effect on intervention outcome. Despite large variations, repeated ANOVAS showed that meclizine led to a relative increase in torsional velocity compared to placebo during vestibular stimulation for both intensities: 2.36 (7.65) from -0.01 (4.17) during low intensities, and 2.61 (6.67) from -3.49 (4.76) during high. The visual-vestibular stimuli yielded a decrease during low acceleration, -0.40 (3.87) from 3.75 (5.62), but increased during high, 3.88 (6.51) from -3.88 (8.55). CONCLUSIONS: Meclizine had an inhibitory effect on eye movement reflexes for low accelerations during VIS+VES trials. This indicates that meclizine may not primarily work through sensory-specific mechanisms, but rather on a more central level. Practically, meclizine shows promise in targeting motion-sickness evoked by everyday activities, but its use may be counterproductive in high-acceleration environments.

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.

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

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: (i) a unilateral burst response corresponding to orientation of the head toward slowly expanding or moving stimuli, particularly within the anterior visual field, and (ii) 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.

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

Purpose: 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. Methods: Twelve healthy subjects (six young, six old) were exposed to (1) vestibular (VES), (2) visual (VIS), and (3) visual-vestibular (VIS+VES) stimulation. These were carried out as whole-body roll (VES), optokinetic rolling of visual scenes (VIS), and a combination of both (VIS+VES). Visual scenes were presented at two intensity levels. Eye movement velocities were used to evaluate the relative impact of visual and vestibular stimulation. Results: Torsional velocities were lowest for VIS regardless of age. Velocities for the old group did not differ between VES and VIS+VES, whereas those for the young group were higher for VIS+VES. Regardless of age, amplified visual intensity resulted in an increased torsion-skewing ratio, seen as more degrees of torsion per degrees of skewing. The contributions of VIS and VES in proportion to VIS+VES were calculated as 0.18 (0.08) and 0.74 (0.14), respectively. Conclusions: Our findings demonstrate that vertical skewing is physiologically seen in combination with ocular torsion as a response to visual stimulation, with young subjects exhibiting a more dynamic response. The torsion-skewing ratio was sensitive to small changes in visual intensities, which may prove useful when evaluating visual motion sensitivity. The visual contribution to the vestibular eye movement response highlights the clinical importance of visual examinations when evaluating dizzy patients.