Method Article

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

DOI:

10.3791/68289

⸱

August 22nd, 2025

 , 
1Marianne Bernadotte Centrum, Department for Clinical Neuroscience, Karolinska Institutet, 2St Erik Eye Hospital

In This Article

Summary

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The methodology explored visual and vestibular contributions to gaze stabilization during optokinetic and whole-body rotations. Stimulations were carried out through visual, vestibular, and visuovestibular trials. Torsional eye-movement gain and nystagmus frequencies served as indicators for the subcortical relay of sensory-specific motion information towards the reflexive brainstem response for each trial.

Abstract

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The present protocol evaluates the relative impact of visual and vestibular inputs during roll plane rotations using optokinetic, vestibular, and combined visuovestibular stimulations. Subjects underwent isolated visual rotations, whole-body vestibular rotations in darkness, and visuovestibular stimulations combining static visual scenes with head rotations. Dynamic and static eye movement gains, absolute amplitudes, velocities, and accelerations were measured alongside perceptual responses. Trials included a baseline rest period before and after movement to stabilize oculomotor fixation. Precise eye- and head-tracking were achieved using the Chronos Eye-Tracking Device (C-ETD), which recorded ocular torsion and head movements across three translational and three rotational dimensions. Eye movements were analyzed for slow-phase velocities and nystagmus frequency, with data quality ensured by averaging torsional outputs from both eyes and excluding frames with artefacts. Real-time gaze alignment monitoring allowed trial repetition as needed, and post-hoc analysis excluded confounding movements. Optokinetic stimulation involved projected visual elements rotating around a fixation point, while vestibular trials employed motorized whole-body rotations in darkness. Visuovestibular trials combined both stimuli, creating relative retinal motion. Data synchronization between eye and head trackers ensured accurate frame-by-frame analysis recorded at 100 Hz. Sensory-specific contributions to gaze stabilization were quantified by comparing slow-phase velocities across trial types. Sensory-specific gains were indexed by dividing visual and vestibular responses by visuovestibular outcomes and validated through comparisons with summed individual responses. Results revealed robust sensory integration, with the relative contributions of visual and vestibular inputs quantified. This protocol offers a detailed framework for evaluating multisensory integration during roll plane rotations. The protocol may therefore serve to elucidate sensory deficits in motion processing, as well as present novel oculomotor biomarkers. It has previously been employed to evaluate how visual clutter and motion accelerations impact motion processing and has highlighted an increased reliance on visual input in concussed patients.

Introduction

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Motion processing is a fundamental and continuous neural process. In humans, we receive information primarily through our visual and vestibular sensory systems, reflecting external- and self-motion, respectively. These two systems employ complex neural networks across lower- and higher neural regions, but on their most basic level rely on basic subcortical pathways to produce reflexive responses that allow good postural control and gaze-stability1,2. Proprioception serves as the third sensory contributor to good postural control, and while it has been shown that somatosensation may guide gaze-stabilizing behaviors, its role in producing distinct eye movements is limited1,3.

Gaze-stabilization is generally achieved through two separate reflexive arcs, the optokinetic reflex (OKR), which leads the eye to follow a moving visual element, and the vestibulo-ocular reflex (VOR), which supports visual acuity by causing the eyes to move in the opposite direction of the head1. While distinct entities, these reflexive arcs also share several neural pathways, and in our habitual state, we naturally combine visual and vestibular input to create an impression of motion4.

There are several methods for assessing how vision and vestibular input are processed during this basic sensorimotor integration. Many feature balance tests, combining visual and vestibular input in different iterations5,6,7, while others employ eye tracking to assess the gaze-stabilizing response8,9. These two very different motor responses share key neural pathways, and we have, in recent studies, outlined robust correlations between gaze-stabilization and postural control10,11. With eye-tracking becoming increasingly available and relying entirely on non-voluntary motor commands, an argument may be made for their reflecting a more innate sensorimotor integration than the balance response.

A majority of studies make use of vertical or horizontal gaze stabilization when assessing the eye movement response12,13. The present protocol instead implements ocular torsion, the rotation of the eye around its visual axis, as a main indicator for gaze stabilization. Ocular torsion exhibits a more dynamic gain than gaze-stabilization caused by yaw- or pitch rotations, or translational movements14. Coupled with greater variability, this means that torsion is more readily influenced by motion parameters, such as visual clutter or acceleration, or medical conditions15,16,17,18. As torsion is outside the remit of voluntary oculomotor control it also serves a more direct indicator of basic sensorimotor integration, as a subject is only able to influence the response through their attention rather than any intended motor command19. Ocular torsion can be triggered by both visual and vestibular rotations in the roll plane20,21. The torsional OKR and VOR may therefore be used to assess how visual and vestibular motion information is handled during sensorimotor integration on its most basic level. By issuing isolated visual and vestibular stimulations and then comparing the responses to those observed during combined visuovestibular trials, one may deduce how each sensory system is influencing the eye movement response and consequently how the brain processes external- and self-motion in any particular setting. One may also investigate how various medical conditions featuring subjective motion processing deficits affect this basic capacity for visuovestibular integration. As gaze-stability has been shown to be directly correlated with postural stability10,11, sharing largely the same basic neural pathways22, the eye movement response may also indicate an individual's postural stability to various conditions without requiring pressure plate measurements. This may be of particular interest when evaluating patients with sensory reweighting, such as observed in post-concussion syndrome18.

The present protocol outlines a methodology for employing combinations of optokinetic and whole-body roll plane rotations to provoke torsional OKR and VOR responses. Using eye and head tracking to trace ocular torsion and vestibular input, the resulting data may then be used to deduce how each sensory modality compares in relation to one another. The goal of the protocol was to present a robust methodology for assessing sensory influences over gaze stabilization and the basic capacity for sensorimotor integration in humans and individuals suffering from sensory reweighing.

The present study evaluated the relative contribution to visual and vestibular motion processing during roll plane rotations. It involved exposing subjects to isolated optokinetic rotations, isolated vestibular whole-body rotations in darkness, and combined visuovestibular motion stimulations during which subjects are rotated while viewing a static visual scene (see Figure 1). This was done with healthy controls and individuals suffering from sensory reweighing, as indicated by a subjective hypersensitivity to visual motion, following a concussion. The main outcome parameters included the dynamic and static eye-movement gains during each stimulation, as well as absolute eye movement amplitudes, velocities, and accelerations. Each trial in the present protocol started with 20 s of the subject, or the visual scene, being kept at rest before the onset of the rotational movement. After reaching the predetermined amplitude, the scene or subject was kept at that rotational amplitude for another 20 s before the trial was terminated; it is recommended that stimulation is kept at rest for at least 10 s before and after each rotational movement to meet the minimum requirements for allowing stable oculomotor fixation and establishing a baseline. While the present protocol issued all stimulations in the counter-clockwise direction, note that directionality has been shown to have no effect on the torsional response15. No training or acclimatization was deemed necessary due to the reflexive nature of the outcome variables.

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Protocol

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All participants provided informed written consent prior to participation. The study was approved by the regional ethics review board (2018/1768-31/1) and carried out in accordance with the principles outlined in the Declaration of Helsinki. The protocol followed STROBE guidelines.

1. Participant selection

  1. Subject all participants to a comprehensive clinical assessment by a medical doctor and a neuropsychologist.
  2. Use the following exclusion criteria: ocular motor or gaze dysfunction, vestibular or somatosensory deficits, recent initiation of centrally acting medication (within 3 months), or any neurological or sensory disorder other than post-concussion syndrome (PCS).
  3. Assess ocular motility and stereoscopic vision (TNO ≤ 60 arcsec) and select all participants who can fuse visual stimuli in the experimental setup.
  4. Assess peripheral vestibular function using head impulse tests in all canal planes; screen central function for skew deviation. Test somatosensory input to balance using a foam-based Romberg's test with eyes closed. One patient was excluded due to poor binocular vision, and one control was excluded due to latent nystagmus in darkness.

2. Eye- and head-tracking

NOTE: The present protocol demands precise eye- and head-tracking during full-body rotations, reflecting optokinetic and vestibular motion parameters, respectively. For this reason, a head-mounted eye-tracking device is required, and the present protocol implemented the Chronos Eye-Tracking Device (C-ETD).

  1. Eye-tracking setup
    NOTE: The eye movement parameters used to evaluate the effects of visual and vestibular stimuli focus on dynamic changes in ocular torsion. Eye-tracking devices must record torsional movements, and to minimize errors, data should be collected from both nasal and temporal pupil sides and averaged. Binocular eye movements should be traced to identify issues like incorrect torsion or mask slippage, where the position of the cameras shifts due to the mask moving in relation to the eyes. Torsional analysis can then use data from one eye. The analysis involves slow-phase velocities and nystagmus beat frequency to evaluate oculomotor gain and quick-phase distributions. A 100 Hz sample rate is recommended as a minimum for reliable slow-phase analysis.
    1. Subject preparation: Ensure the subject is securely seated in the designated chair for all trials. Adjust the seating position for stability and comfort to minimize the risk for unwanted head movements or mask slippages.
    2. Eye-tracker placement: Place the head-mounted eye-tracker on the subject's head. Secure the head and eye-tracker using hook-and-loop straps or an equivalent method to minimize head movement.
    3. Camera alignment and calibration: Confirm that the cameras have an unobstructed view of the eyes throughout all movements. Ensure no noticeable mask slippage occurs during active head movements. Strap the subject to the chair and perform the eye-tracker calibration. Do not adjust the eye-tracker position after calibration.
  2. Head-tracking setup
    ​NOTE: The investigator must ensure proper head positioning for two reasons: to maintain immobility during optokinetic trials and to calculate the gain between head and eye rotations during vestibular and visuovestibular trials. The C-ETD head mount has accelerometers tracking head motion in six dimensions, with a minimum requirement to measure head position, velocity, and acceleration in the roll plane and horizontal translations. Head tilts can alter torsional eye movement, so head position in the horizontal dimension must be monitored to ensure no tilts. The accelerometer must track the subject's head movement, not its own, and the head mount must be securely fastened. The head-tracker frequency must be synchronized with the eye-tracker, with the head-tracker rate not falling below that of the eye-tracker.
    1. Determining the rotation point: Set the point of rotation around which the whole-body rotation will take placeby adjusting the rotation point of the mechanical sled. Ensure this point is positioned between the subject's eyes to adjust for height differences.
    2. Head-tracker installation: Secure the head-mounted tracker firmly to the subject's head.
    3. Cable management and synchronization: Ensure that the connection cable between the eye-tracker and head-tracker is positioned to avoid entanglement. Verify that the cable does not exert any force on the subject's head during stimulation.

3. Optokinetic stimulation

NOTE: During optokinetic stimulation, the subject sits in the same position as during the vestibular trials, at rest. The subject should be centered in front of the screen, with the line of sight aligned to the primary gaze position, ensuring forward-facing gaze in both horizontal and vertical dimensions. The central fixation point, a circle, provides directional motion cues during the active stimulation phase. Optokinetic elements, such as small circles, are evenly distributed across the screen, offering a clear contrast. The visual elements rotate around the fixation point at predetermined velocities or accelerations, reaching a set amplitude.

  1. Selecting the visual stimulation: Choose a high-contrast visual scene with scattered lines or dots centered around a fixation point. Position the fixation point directly in front of the subject's eyes in both vertical and horizontal dimensions. The center of rotation will subsequently be aligned with the subject's visual axis.
  2. Preparing the environment: Eliminate distracting light sources to ensure the visual scene is the only illumination. Use a screen large enough to encompass as much of the subject's visual field as possible.
  3. Subject instructions: Instruct the subject to maintain fixation on the central point throughout the trial. Inform the subject that the trial is starting before beginning any recordings.
  4. Trial execution: Start the eye- and head-tracking software. Present the static visual scene for 10 s before initiating motion.
  5. Motion stimulation: At 1-2 s before motion onset, instruct the subject to keep their eyes wide open. Initiate visual motion, rotating the scene to a fixed amplitude at a predetermined acceleration. In the present protocol, the optokinetic scene rotated at 7°/s², 14°/s², and 28°/s² to a maximum amplitude of 28° counterclockwise; these parameters were chosen to offer a nuanced distribution of visual and vestibular input to the eye movement response13,14.
  6. Post-stimulation evaluation: Maintain the static scene at the endpoint for 10 s if evaluating static eye position. Otherwise, terminate the trial immediately after motion cessation.

4. Vestibular stimulation

NOTE: Vestibular trials involved whole-body rotations in complete darkness to isolate head rotations in the roll plane while minimizing visual and proprioceptive input. The protocol used a custom-designed motorized sled powered by two independent belts, each driven by an AC brushless servo motor (400 V), allowing precise control over movement. The center of rotation was aligned with the glabella to accommodate height differences. Participants were instructed to fixate on an imagined reference point ahead while their heads were secured to minimize unintended movements. Accelerometer data from the C-ETD system was used to monitor head stability and ensure that movement parameters adhered to the protocol.

  1. Preparing the environment and subject: Ensure the room is completely dark to eliminate visual directional cues. Secure the subject in the mechanized sled, minimizing the risk of unintended head or body movements. Align the center of rotation with the subject's glabella to accommodate height differences.
  2. Subject instructions: Instruct the subject to visualize a central fixation point and maintain gaze on it throughout the trial. While small deviations are difficult to eliminate, this will help promote gaze stability during motion.
  3. Trial execution: Inform the subject that the trial is about to start. Start the eye- and head-tracking software, allowing 10 s to pass before initiating movement.
  4. Motion stimulation: At 1-2 s before movement onset, instruct the subject to keep their eyes wide open. Activate the mechanical sled to produce a head rotation matching the amplitude and acceleration of the optokinetic movement in step 3.5. Verify head stability using accelerometer data before and after each movement. Sudden head jerks will compromise oculomotor recordings at the affected timepoints
  5. Post-stimulation evaluation: Maintain the subject at the final rotated position for 10 s if evaluating static eye position. Otherwise, terminate the trial immediately after motion cessation.

5. Visuovestibular stimulation

NOTE: Visuovestibular stimulation combined whole-body rotations, as described for vestibular trials, with the static visual image from the optokinetic trials. This created a relative rotation of the visual field on the retina in the direction opposite the body rotation, integrating both optokinetic and vestibular motion inputs into a single cohesive stimulation.

  1. Combined stimulation setup: Seat the subject in the mechanical sled and present the visual scene following steps 3.1-3.3. The combined stimulus should create relative motion between vestibular and visual inputs.
  2. Trial execution: Repeat steps 4.3-4.5 to activate the whole-body rotation while the subject views the static visual scene. Ensure the visual stimulus is stationary in space, moving in the opposite direction of the subject's rotation. Synchronisation between optokinetic and vestibular stimulation is essential for accurate data collection.

6. Data analysis

NOTE: Ocular torsion was assessed using iris feature tracking with C-ETD software, including only data with a signal quality above 0.5. Two tracking lines on either side of the pupil were selected for each eye, and data from the eye with the highest number of frames above 0.5 in signal quality were averaged. The data were analyzed using OriginPro 2017, excluding nystagmus and head movement artefacts, with participants prompted to keep their eyes open one second before stimulation to minimize blink artefacts.

  1. Data collection and preparation
    1. Use eye-tracking software (e.g., C-ETD) to analyze eye-tracking videos and extract torsional, vertical, and horizontal eye movements.
    2. Configure and calibrate pupil tracking according to the eye-tracking system's guidelines. When assessing torsional responses by feature tracking, select two reference points on each side of the pupil for both eyes. These reference points should feature distinct topographical features that can be used for template matching. Run the eye-tracking analysis program to generate positional data over time and export all eye movement data into a separate file.
    3. In the exported file, filter the data using the signal quality index provided by the software. For C-ETD, retain only data with a signal quality > 0.5, or an equivalent quality threshold for other systems.
    4. Select the eye with the highest number of frames scoring > 0.5 in signal quality. Average torsion data across the best-quality tracking lines for the selected eye, ensuring representation from both sides of the pupil.
  2. Data visualization and quality control
    1. Digitize and synchronize input data from the eye-tracking system (eye movements, head position, and chair motion) before importing it into the analysis software.
    2. Visually inspect the data, including torsional, vertical, and horizontal eye positions over time, as well as head position in the roll plane, to verify a stable baseline and expected movement responses during each trial (see Figure 1 for representative eye movement responses). Identify any confounding eye movements in the horizontal or vertical direction.
  3. Exclude slow phases coinciding with unexpected eye or head movements to maintain data quality and fixation consistency. If such movements occurred during active motion stimulation, remove the data and consider repeating the trial.
    1. To analyze slow phases, manually trace each torsional slow phase to exclude confounding data. Calculate slow-phase velocity as the change in amplitude divided by the duration. Evaluate the timing of nystagmus beats (onset of quick phases) to analyze temporal distribution. Record the total number of nystagmus beats per trial. This may be done by counting the number of recorded quick phases for each trial and subject.
    2. Include all slow-phase traces from every trial and participant to ensure reliable, representative data and enhance statistical power.
  4. Quantifying sensory contributions
    1. Create a spreadsheet listing slow-phase velocities for visual, vestibular, and visuo-vestibular trials.
    2. Determine eye-stimulus gain by comparing each slow-phase acceleration with the corresponding stimulus acceleration, dividing the torsional acceleration by the optokinetic or head rotation acceleration for each trial.
    3. Assess sensory-specific contributions by dividing the mean slow-phase gain from visual and vestibular trials by that from visuo-vestibular trials to compute an index. Perform this on the averaged data for each subject and acceleration condition. For example, if visual and vestibular trials yield torsional accelerations of 3 deg/s2 and 7 deg/s2, respectively, and visuo-vestibular trials produce 10 deg/s2, the visual and vestibular contributions would be 30% and 70%, respectively.
    4. Validate this method by comparing visuo-vestibular slow-phase gain with the sum of visual and vestibular slow-phase gain across subjects and trials. For example, if optokinetic trials yield an average torsional velocity of 3 deg/s2 and vestibular trials 7 deg/s2, visuo-vestibular trials should approximate 10 deg/s2.
    5. Use a t-test to compare the sum of visual and vestibular gains with observed visuo-vestibular gain; a robust integration should show no significant difference.
    6. Organize the final dataset into a table containing slow-phase acceleration, torsional gain, nystagmus frequency, timestamps for individual nystagmus beats, and indexed values of relative visual and vestibular contributions. Structure data by subject, trial type (visual, vestibular, or visuo-vestibular), and motion acceleration.
    7. Conduct statistical analyses by separating variables into slow-phase acceleration, nystagmus frequency, nystagmus distribution over time, and sensory contribution indices. Consider factors such as subject, modality, and acceleration. It is recommended to employ a multifactorial analysis method, such as ANOVA, depending on data distribution.

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Results

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A total of 171 trials were conducted, in which all participants underwent visual, vestibular, and combined visuo-vestibular stimulations at three acceleration levels. Eye-tracking assessments were performed on all resulting nystagmus slow phases (n = 223 for nine control participants (seven females); n = 331 for 10 patients (three females)). Statistical analyses were based on the mean values obtained for each participant (n = 19), with data averaged across trials. Healthy controls and patients were matched in terms of ag...

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Discussion

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The present protocol offers a validated methodology for assessing subcortical motion processing through torsional gaze-stabilization, a reflex mediated by brainstem circuits23. By combining visual and vestibular stimulation, the method enables the evaluation of multisensory integration through ocular torsion responses. Prior implementations have demonstrated their sensitivity to acceleration-dependent vestibular contributions16, visual information density1...

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Disclosures

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The authors have no conflicts of interest to report.

Acknowledgements

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The present study was supported by the Promobilia Foundation (research grant A23126 to TW).

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Materials

List of materials used in this article
NameCompanyCatalog NumberComments
AC Brushless Servo Motors / Baldor BSM90C, 400 VBB Motors and Mechanical, Fort Smith, AK, USAUPC 781568378342Used to construct the mechanized sled
Chronos Eye tracking device (C-ETD)Chronos Vision GmbH, Berlin, GermanyNo longer availableNewer models are available from the company, offering higher recording rates.
OriginProOriginLab, Northampton, MA, USAOriginPro 17Used to visualise and analyse eye-, head-, and chair traces.
SPSS StatististicsIBM, Chicago, IL, USASPSS Statistics 28Used for the statistical analyses

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Tags

Visual InputRoll Plane RotationsOptokinetic StimulationVisuovestibular StimulationOculomotor BiomarkersNystagmus FrequencySensory Integration

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