Treatment of Gravitational Pulling Sensation in Patients With Mal de Debarquement Syndrome (MdDS): A Model-Based Approach

Abstract

Perception of the spatial vertical is important for maintaining and stabilizing vertical posture during body motion. The velocity storage pathway of vestibulo-ocular reflex (VOR), which integrates vestibular, optokinetic, and proprioception in the vestibular nuclei vestibular-only (VO) neurons, has spatio-temporal properties that are defined by eigenvalues and eigenvectors of its system matrix. The yaw, pitch and roll eigenvectors are normally aligned with the spatial vertical and corresponding head axes. Misalignment of the roll eigenvector with the head axes was hypothesized to be an important contributor to the oscillating vertigo during MdDS. Based on this, a treatment protocol was developed using simultaneous horizontal opto-kinetic stimulation and head roll (OKS-VOR). This protocol was not effective in alleviating the MdDS pulling sensations. A model was developed, which shows how maladaptation of the yaw eigenvector relative to the head yaw, either forward, back, or side down, could be responsible for the pulling sensation that subjects experience. The model predicted the sometimes counter-intuitive OKS directions that would be most effective in re-adapting the yaw eigenvector to alleviate the pulling sensation in MdDS. Model predictions were consistent with the treatment of 50 patients with a gravitational pulling sensation as the dominant feature. Overall, pulling symptoms in 72% of patients were immediately alleviated after the treatment and lasted for 3 years after the treatment in 58% of patients. The treatment also alleviated the pulling sensation in patients where pulling was not the dominant feature. Thus, the OKS method has a long-lasting effect comparable to that of OKS-VOR readaptation. The study elucidates how the spatio-temporal organization of velocity storage stabilizes upright posture and how maladaptation of the yaw eigenvector generates MdDS pulling sensations. Thus, this study introduces a new way to treat gravitational pull which could be used alone or in combination with previously proposed VOR readaptation techniques.

Keywords: MdDS; bobbing; gravitational pull; orientation-vector; rocking; swaying; velocity storage; vestibular only (VO) neurons.

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Copyright © 2022 Yakushin, Raphan and Cho.

Figures

FIGURE 1

OKS stimulation used to induce horizontal (A) and vertical (B) optokinetic nystagmus. It should be noted that the chamber wall is cylindric and stripes in (A,B) are curved and wider at the periphery. See text for a detailed description of the stimulus.

FIGURE 2

Model of the postural control. (A) Inverted pendulum model. COM – center of mass, COP – center of pressure. (B) Model of sensory integration of visual, vestibular, and proprioceptive inputs [modified from Horak (2009)]. This model includes the low frequency postural adjustments contributed by velocity storage.

FIGURE 3

Gaze and body postural control contributed by the velocity storage integrator. G0 is the gain coupling matrix from the semicircular canals (SCC) to velocity storage. G2 is the gain matrix coupling the optokinetic velocity input to velocity storage. G4 is the gain coupling matrix from the proprioceptive velocity input to velocity storage. G1 and G3 are the direct pathway gain matrices from the semicircular canals and optokinetic input and are responsible for the rapid responses to head and optokinetic movement. There is also a rapid proprioceptive pathway (G5), but these are assumed not to play a role in the maladaptation leading to MdDS.

FIGURE 4

(A) Head coordinate frame used in this study. (B) Yaw, pitch and roll eigenvectors in normal non-adapted states and are aligned with the head axes. (C) Yaw, pitch and roll eigenvectors shifted from their normal orthogonal orientations due to maladaptation of the velocity storage system matrix. (D) Gain matrix of velocity storage in normal state, when yaw, pitch, and roll eigenvectors are aligned with the head axes. (E,F) Gain matrix of velocity storage with yaw eigenvector shifted forward (E) or sideways (F). (G) Gain matrix of velocity storage when all 3 eigenvectors are shifted from their normal (D) orientations. Insets in (D–G) on the right from gain matrices are a top view of the head. EV – eigenvector.

FIGURE 5

Summary of the model-based predicted treatment protocol for gravitational pulling sensation. EV- Eigenvector. (A) Sideview of the pulling back sensation. The Yaw EV is shifted forward so the head yaw is back relative to the EV. The vector representing this pulling back sensation is the cross product of Yaw Head with Yaw EV and according to a right-hand rule, this is a vector out of the left ear (circle with a dot). The OKS treatment is OKS up, which re-adapts the Yaw EV toward Yaw Head. The direction of rotation of OKS represented by a circle with an x, opposite to the maladapted vector rotation. (B) Sideview of the pulling forward sensation. The Yaw EV is maladapted back re the Yaw Head, inducing a forward pulling sensation. The vector for this rotation is into the left ear (circle with an x) and the OKS stimulus to readapt is down and represented by a vector out of the left ear. (C) Pull Left ear down. This occurs when the Yaw EV is rotated right. The appropriate treatment using horizontal OKS is toward the right, which because of the known cross-coupling of velocity storage would adapt the Yaw EV toward the Yaw Head. It should be noted that the model predicts that a more potent OKS stimulus to re-adapt this shift in the EV would be a counterclockwise roll OKS from the subject viewpoint, which would be a vector opposing the rotation of the Yaw EV relative to the Yaw Head. (D) Pull Right Ear down. This occurs when the Yaw EV is rotated left relative to the Yaw Head. The appropriate treatment using horizontal OKS is toward the left, which because of the known cross-coupling of velocity storage would adapt the Yaw EV toward the Yaw Head. In this instance, the model predicts that a more potent OKS stimulus to re-adapt this shift in the EV would be a clockwise roll OKS from the subject viewpoint, which would be a vector opposing the rotation of the Yaw EV relative to the Yaw Head. Front view. Gray rectangles – screens with OKS stimulus. The direction of OKS is indicated by arrows. The direction of the OKS vectors for side down pulling sensation is consistent with previously studied cross-coupling when the head is tilted side down.

FIGURE 6

The COP changes as a function of time (Static posturography). (A) Side-to-side (swaying) body oscillations. (B) Forward-back (rocking) body oscillations. Static posturography of a 52-year-old female with MdDS triggered immediately after a flight. Prior to treatment, the patient had no swaying (A, black trace) but reported strong backward gravitational pulling (B, black trace). The shaded areas in (A,B) are intervals when the patient had her eyes open. (C,D) Trajectory plots of COP before (C) and after (D) exposure of upward OKS at 5°/s for 1 min. After treatment, postural stability increased (A,B,D blue traces).

FIGURE 7

Static posturography of a 48-year-old female with MdDS triggered immediately after a cruise. Details of individual plots are described in Figure 6. The patient experienced a sensation of gravitational pulling to the left (A, black trace) and some rocking (B, black trace). When the eyes were closed, the patient’s body gradually drifted to the left. When the posture reached a certain deviation from upright, to gain stability patient quickly moved her body back to the upright position. This is different from body swaying when oscillation is sinusoidal and body deviations are symmetrical about upright. After exposure to OKS to the right at 5°/s for 2 min, the sensation of gravitational pulling to the left was reduced (C, blue traces). As a result, side-to-side body oscillations were no longer observed. Minimal forward-back body oscillations remained unchanged (D, blue traces). (D) Trajectory plots of COP before (C) and after (D) treatment. After treatment, postural stability increased (A,B,D blue traces).

FIGURE 8

Static posturography of a 71-year-old female with MdDS triggered immediately after a cruise. Details of individual plots are described in Figure 6. The patient reported a sensation of forward gravitational pulling. Body deviation side-to-side were minimal (A, black traces). When the patient closed her eyes, the body was gradually falling forward, but when deviation reached certain level, it was pulled back toward upright position (B, black trace). After exposure to downward OKS at 5°/s for 2 min, the swaying remained minimal (C, blue trace) and forward body deviation was reduced (D). Self-score of overall symptoms prior to treatment was 7/10, and after treatment was 4.5/10.

FIGURE 9

Static posturography of a 52-year-old female with MdDS of unknown origin (possibly swimming). Details of individual plots are described in Figure 6. The patient did not experience any swaying (A, black trace) but reported a sensation of rocking and backwards gravitational pulling (B, black trace). Forward-back motion was irregular but deviations forward and back were of similar amplitude. Thus, static posturography did not have a typical pattern of rocking or gravitational pull sensation forward or backward. After exposure to OKS to the right at 5°/s while rolling the head at 0.1 Hz for 3 min (treatment for rocking), swaying remained minimal (A, blue trace) but rocking became stronger and regular at 0.15 Hz (D, blue traces). The patient reported worsening of her symptoms. At the same time fore-aft oscillations became regular (C,D). The appropriate treatment should have been upward OKS for the pulling back sensation. This shows that inappropriate treatment, based on some “intuitive” notion and not model-based could have deleterious consequences.