measuring-influence-magnetic-vestibular-stimulation-on-nystagmus-self

Measuring the Influence of Magnetic Vestibular Stimulation on Nystagmus, Self-Motion Perception, and Cognitive Performance in a 7T MRT

Strong magnetic fields induce dizziness, vertigo, and nystagmus due to Lorentz forces acting on the cupula in the semi-circular canals, an effect called ...

University of California

Patients with acute vestibular disorders are often a diagnostic challenge for neurologists, especially when the evaluation must be conducted remotely. The clinical dilemma remains: Does the patient have a benign peripheral inner ear problem or a worrisome central vestibular disorder, such as a stroke? The use of a focused history and the virtual HINTS (head impulse test, nystagmus evaluation, and test of skew) examination are key steps towards correctly diagnosing and triaging the acute vertiginous patient. When looking for signs of vestibulo-ocular dysfunction, there are important technological and practical considerations for an effective clinical interpretation.

Opinion and Special Articles: Remote Evaluation of Acute Vertigo: Strategies and Technological Considerations.

Differentiating benign from dangerous causes of dizziness or vertigo presents a major diagnostic challenge for many clinicians. Bedside presentations of peripheral vestibular disorders and posterior fossa strokes are often indistinguishable other than by a few subtle vestibular eye movements. The most challenging of these to interpret is the head impulse test (HIT) of vestibulo-ocular reflex (VOR) function. There have been major advances in portable video-oculography (VOG) quantification of the video HIT (vHIT), but these specialized devices are not routinely available in most clinical settings. As a first step towards smartphone-based diagnosis of strokes in patients presenting vestibular symptoms, we sought proof of concept that we could use a smartphone application ("app") to accurately record the vHIT.

Proof of Concept for an "eyePhone" App to Measure Video Head Impulses.

Video-oculography (VOG) goggles have been integrated into the assessment of semicircular canal function in patients with vestibular disorders. However, a similar bedside VOG method for testing otolith function is lacking.

Evaluation of the Video Ocular Counter-Roll (vOCR) as a New Clinical Test of Otolith Function in Peripheral Vestibulopathy.

A woman, age 44, with a positive anti-YO paraneoplastic cerebellar syndrome and normal imaging developed an ocular motor disorder including periodic alternating nystagmus (PAN), gaze-evoked nystagmus (GEN) and rebound nystagmus (RN). During fixation there was typical PAN but changes in gaze position evoked complex, time-varying oscillations of GEN and RN. To unravel the pathophysiology of this unusual pattern of nystagmus, we developed a mathematical model of normal function of the circuits mediating the vestibular-ocular reflex and gaze-holding including their adaptive mechanisms. Simulations showed that all the findings of our patient could be explained by two, small, isolated changes in cerebellar circuits: reducing the time constant of the gaze-holding integrator, producing GEN and RN, and increasing the gain of the vestibular velocity-storage positive feedback loop, producing PAN. We conclude that the gaze- and time-varying pattern of nystagmus in our patient can be accounted for by superposition of one model that produces typical PAN and another model that produces typical GEN and RN, without requiring a new oscillator in the gaze-holding system or a more complex, nonlinear interaction between the two models. This analysis suggest a strategy for uncovering gaze-evoked and rebound nystagmus in the setting of a time-varying nystagmus such as PAN. Our results are also consistent with current ideas of compartmentalization of cerebellar functions for the control of the vestibular velocity-storage mechanism (nodulus and ventral uvula) and for holding horizontal gaze steady (the flocculus and tonsil).

Modeling the interaction among three cerebellar disorders of eye movements: periodic alternating, gaze-evoked and rebound nystagmus.

The primary sensory modality for probing spatial perception can vary among psychophysical paradigms. In the subjective visual vertical (SVV) task, the brain must account for the position of the eye within the orbit to generate an estimate of a visual line orientation, whereas in the subjective haptic vertical (SHV) task, the position of the hand is used to sense the orientation of a haptic bar. Here we investigated whether a hand sensory bias can affect SHV measurement. We measured SHV in 12 subjects (6 left-handed and 6 right-handed) with a forced-choice paradigm using their left and right hands separately. The SHV measurement was less accurate than the SVV measurements (-0.6 ± 0.7) and it was biased in the direction of the hand used in the task but was not affected by handedness; SHV left hand -6.8 ± 2.1° (left-handed -7.9 ± 3.6°, right-handed -5.8 ± 2.5°) and right hand 9.8 ± 1.5° (left-handed 7.4 ± 2.2°, right-handed 12.3 ± 1.8°). SHV measurement with the same hand was also affected by the haptic bar placement on the left or right side versus midline, showing a side effect (left vs midline -2.0 ± 1.3°, right vs midline 3.8 ± 1.7°). Midline SHV measures using the left and right hands were different, confirming a laterality effect (left hand -4.5 ± 1.7°, right hand 6.4 ± 2.0°). These results demonstrate a sensory bias in SHV measurement related to the effects of both hand-in-body (i.e., right vs left hand) and hand-in-space positions. Such modality-specific bias may result in disparity between SHV and SVV measurements, and therefore cannot be generalized to vertical or spatial perception.

Psychophysical Haptic Measurement of Vertical Perception: Elucidating a Hand Sensory Bias.

We present here neuro-otological tests using portable video-oculography (VOG) and strategies assisting physicians in the process of decision making beyond the classical 'HINTS' testing battery at the bedside.

Current concepts in acute vestibular syndrome and video-oculography.

We report a patient with spontaneous upbeat nystagmus (UBN) due to an ischemic lesion involving the paramedian tract (PMT) in the medulla. Eye movement recordings, using an infrared video-oculography (VOG) system, showed that the slow phase of the nystagmus was initially velocity-decreasing but gradually became velocity-increasing. Simulation of the nystagmus with a mathematical model supports a role for the PMT in relaying premotor signals for vertical gaze holding to the cerebellum. Our model shows that the disruption in cerebellar input from PMT can lead to the velocity-increasing waveform of the nystagmus, whereas the velocity-decreasing waveform could be related to a mismatch between the innervational commands to the ocular muscles (the pulse and step) needed to hold gaze steady.

Upbeat Nystagmus with an Unusual Velocity-Decreasing and Increasing Waveform: a Sign of Gaze-Holding Dysfunction in the Paramedian Tracts in the Medulla?

Introduction While the mechanism of posterior canal benign paroxysmal positional vertigo (BPPV) is widely accepted as canalolithiasis, the pathophysiology of horizontal canal BPPV remains controversial. We seek to analyze vestibular test results of patients with horizontal canal BPPV with ageotropic nystagmus (AHC) and geotropic nystagmus (GHC) in comparison to patients with posterior canal BPPV (PC) to better understand its pathophysiology. Methods In a retrospective chart review of adults with BPPV at a tertiary referral balance center, we reviewed the clinical characteristics and compared videonystagmography, caloric, rotary chair, subjective visual vertical (SVV)/ subjective visual horizontal (SVH), and vestibular evoked myogenic potential (VEMP) results between groups. Results We included 11 AHC and seven GHC patients and randomly selected 20 PC patients as the comparison group. All groups had a high rate of migraine and low rates of diabetes and head trauma, but no difference between groups. Ipsilateral caloric weakness was more prevalent in the GHC group compared to the PC group (p=0.02). One of two AHC patients and both GHC patients who had SVV/SVH testing had abnormal findings. The only AHC patient who had ocular VEMP testing had abnormal results. Additionally, we observed a significant downbeating component to nystagmus (4 deg/sec or greater) exclusively in the AHC group (5/10 patients, p=0.001). Conclusions Patients with AHC and GHC have unique vestibular testing results. In particular, only AHC patients showed a downbeating component to their nystagmus, which may suggest utricular dysfunction in the pathophysiology of AHC.

Vestibular Test Results in Patients With Horizontal Canal Benign Paroxysmal Positional Vertigo.

Smartphones have shown promise in the assessment of neuro-ophthalmologic and vestibular disorders. We have shown that the head impulse test results recorded using our application are comparable with measurements from clinical video-oculography (VOG) goggles. The smartphone uses ARKit's capability to acquire eye and head movement positions without the need of performing a calibration as in most eye-tracking devices. Here, we measure the accuracy and precision of the eye and head position recorded using our application.

Eye and Head Movement Recordings Using Smartphones for Telemedicine Applications: Measurements of Accuracy and Precision.

In this paper, we present a review of how the various aspects of any study using an eye tracker (such as the instrument, methodology, environment, participant, etc.) affect the quality of the recorded eye-tracking data and the obtained eye-movement and gaze measures. We take this review to represent the empirical foundation for reporting guidelines of any study involving an eye tracker. We compare this empirical foundation to five existing reporting guidelines and to a database of 207 published eye-tracking studies. We find that reporting guidelines vary substantially and do not match with actual reporting practices. We end by deriving a minimal, flexible reporting guideline based on empirical research (Section "An empirically based minimal reporting guideline").

Eye tracking: empirical foundations for a minimal reporting guideline.

The primary sensory modality for probing spatial orientation can vary among psychophysical tasks. In the subjective visual vertical (SVV) task, a visual stimulus is used to measure perceived vertical orientation, while a haptic stimulus is used in the subjective haptic vertical (SHV) task. Here we examined disparity in SHV and SVV task results and asked whether it could be related to biases in probing different spatial estimates by each task. Forty-two healthy volunteers (mean ± SD age, 25 ± 10 years; 19 females; 21 left handed) were recruited. The effect of a task to measure spatial orientation was calculated as the difference between SHV and SVV values, and with the head upright and tilted 20° laterally. There was a task bias regardless of head position related to hand use in the haptic task but not handedness (mean head upright ± SEM: left hand, -3.7 ± 1.1°; right hand, 7.9 ± 1.0°). When this task bias was subtracted out, there was a similar spatial bias using each hand in the SHV task that was also comparable to the SVV task (mean head with left tilt: left hand, 3.9 ± 0.7°; right hand, 4.4 ± 0.7°; SVV, 4.9 ± 0.7°; mean head with right tilt: left hand, -4.6 ± 0.9°; right hand, -4.6 ± 0.8°; SVV, -4.7 ± 1.0°). These findings show that the disparity in visual and haptic measures of spatial orientation is primarily related to a modality-specific bias, and once the effect of hand use is removed from the haptic measurements, the spatial bias becomes comparable to the visual task.

Measures of Spatial Orientation: Spatial Bias Analogs in Visual and Haptic Tasks.

Nystagmus identification and interpretation is challenging for non-experts who lack specific training in neuro-ophthalmology or neuro-otology. This challenge is magnified when the task is performed  telemedicine. Deep learning models have not been heavily studied in video-based eye movement detection.

aEYE: A deep learning system for video nystagmus detection.

Periodic alternating nystagmus (PAN) is a rare oscillatory ocular motor disorder. The effects of gravity on the dynamic behavior of PAN can be studied by monitoring the nystagmus while changing head orientation. Previous studies of patients with PAN reached different conclusions about the effect of changing the orientation of the head relative to gravity on the ongoing PAN, either no effect or a damping of the nystagmus within several minutes. What neuronal circuits could account for the difference in the effects of gravity among PAN patients? We modeled how the brain resolves the tilt-translation ambiguity in normal individuals and added an unstable, oscillatory vestibular system generating PAN. PAN was suppressed in our patient in ear-down positions, in a similar pattern to that of a previously reported patient. This effect was simulated by reducing the gain of the projection of the "rotation feedback" loop to the velocity-storage integrator to approximately 5% of its normal value. With normal "rotation feedback" PAN is expected to dissipate quickly as soon as the head is rotated away from upright position. Moreover, by disconnecting the rotation feedback completely (gain = zero) the model simulated PAN that was reported to be unaffected by gravity. Thus, understanding the effect of this single parameter, the gain of the rotation feedback, can explain the observed variability among our own and previous studies.

Modeling the effect of gravity on periodic alternating nystagmus.

When looking around a visual scene, humans make saccadic eye movements to fixate objects of interest. While the extraocular muscles can execute saccades in any direction, not all saccade directions are equally likely: saccades in horizontal and vertical directions are most prevalent. Here, we asked whether head orientation plays a role in determining saccade direction biases. Study participants ( = 14) viewed natural scenes and abstract fractals (radially symmetric patterns) through a virtual reality headset equipped with eye tracking. Participants' heads were stabilized and tilted at -30°, 0°, or 30° while viewing the images, which could also be tilted by -30°, 0°, and 30° relative to the head. To determine whether the biases in saccade direction changed with head tilt, we calculated polar histograms of saccade directions and cross-correlated pairs of histograms to find the angular displacement resulting in the maximum correlation. During free viewing of fractals, saccade biases largely followed the orientation of the head with an average displacement value of 24° when comparing head upright to head tilt in world-referenced coordinates (  = 17.63,  < 0.001). There was a systematic offset of 2.6° in saccade directions, likely reflecting ocular counter roll (OCR;   = 3.13,  = 0.008). When participants viewed an Earth upright natural scene during head tilt, we found that the orientation of the head still influenced saccade directions (  = 3.7,  = 0.001). These results suggest that nonvisual information about head orientation, such as that acquired by vestibular sensors, likely plays a role in saccade generation.

Head Orientation Influences Saccade Directions during Free Viewing.

The objective of the study is to develop deep learning models using synthetic fundus images to assess the direction (intorsion versus extorsion) and amount (physiologic versus pathologic) of static ocular torsion. Static ocular torsion assessment is an important clinical tool for classifying vertical ocular misalignment; however, current methods are time-intensive with steep learning curves for frontline providers.

Deep Learning Model for Static Ocular Torsion Detection Using Synthetically Generated Fundus Images.

Assessment of recovery following vestibular loss has been limited by the lack of bedside measures in clinical settings. Here, we used the video ocular counter-roll (vOCR) test to study otolith-ocular function and compensatory effect of neck proprioception in patients at different stages of vestibular loss.

Article	Year
Opinion and Special Articles: Remote Evaluation of Acute Vertigo: Strategies and Technological Considerations. Neurology\| PubMed ID: 33004609	2021
Proof of Concept for an "eyePhone" App to Measure Video Head Impulses. Digital biomarkers\| PubMed ID: 33615116	2021
Evaluation of the Video Ocular Counter-Roll (vOCR) as a New Clinical Test of Otolith Function in Peripheral Vestibulopathy. JAMA otolaryngology-- head & neck surgery\| PubMed ID: 33764386	2021
Modeling the interaction among three cerebellar disorders of eye movements: periodic alternating, gaze-evoked and rebound nystagmus. Journal of computational neuroscience\| PubMed ID: 34003422	2021
Psychophysical Haptic Measurement of Vertical Perception: Elucidating a Hand Sensory Bias. Neuroscience\| PubMed ID: 34848259	2022
Current concepts in acute vestibular syndrome and video-oculography. Current opinion in neurology\| PubMed ID: 34889806	2022
Upbeat Nystagmus with an Unusual Velocity-Decreasing and Increasing Waveform: a Sign of Gaze-Holding Dysfunction in the Paramedian Tracts in the Medulla? Cerebellum (London, England)\| PubMed ID: 35133635	2023
Vestibular Test Results in Patients With Horizontal Canal Benign Paroxysmal Positional Vertigo. Cureus\| PubMed ID: 35223244	2022
Eye and Head Movement Recordings Using Smartphones for Telemedicine Applications: Measurements of Accuracy and Precision. Frontiers in neurology\| PubMed ID: 35370913	2022
Eye tracking: empirical foundations for a minimal reporting guideline. Behavior research methods\| PubMed ID: 35384605	2023
Measures of Spatial Orientation: Spatial Bias Analogs in Visual and Haptic Tasks. eNeuro\| PubMed ID: 35944973	2022
aEYE: A deep learning system for video nystagmus detection. Frontiers in neurology\| PubMed ID: 36034311	2022
Modeling the effect of gravity on periodic alternating nystagmus. Journal of the neurological sciences\| PubMed ID: 36115220	2022
Head Orientation Influences Saccade Directions during Free Viewing. eNeuro\| PubMed ID: 36351820	2022
Deep Learning Model for Static Ocular Torsion Detection Using Synthetically Generated Fundus Images. Translational vision science & technology\| PubMed ID: 36630147	2023
Video Ocular Counter-Roll (vOCR): Otolith-Ocular Function and Compensatory Effect of the Neck Following Vestibular Loss. Otolaryngology--head and neck surgery : official journal of American Academy of Otolaryngology-Head and Neck Surgery\| PubMed ID: 36861848	2023

Jorge Otero-Millan

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