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. 2017 Jan 30;8:23.
doi: 10.3389/fneur.2017.00023. eCollection 2017.

Inaccurate Saccades and Enhanced Vestibulo-Ocular Reflex Suppression During Combined Eye-Head Movements in Patients With Chronic Neck Pain: Possible Implications for Cervical Vertigo

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Free PMC article

Inaccurate Saccades and Enhanced Vestibulo-Ocular Reflex Suppression During Combined Eye-Head Movements in Patients With Chronic Neck Pain: Possible Implications for Cervical Vertigo

Janine L Johnston et al. Front Neurol. .
Free PMC article

Abstract

Background: The primate ocular motor system is designed to acquire peripheral targets of interest by coordinating visual, vestibular, and neck muscle activation signals. The vestibulo-ocular reflex (VOR) is greatly reduced at the onset of large eye-head (gaze) saccades and resumes before the end of the saccades to stabilize eye-in-orbit and ensure accurate target acquisition. Previous studies have relied on manipulating head movements in normal individuals to study VOR suppression and gaze kinematics. We sought to determine if reduced head-on-trunk movement alters VOR suppression and gaze accuracy similar to experiments involving normal subjects and if intentionally increasing head and neck movement affects these dynamics.

Methods: We measured head and gaze movements using magnetic search coil oculography in eight patients with cervical soft tissue disorders and seven healthy subjects. All participants made horizontal head-free saccades to acquire a laser dot target that stepped pseudorandomly 30-65° to either side of orbital mid-position, first using typical head and eye movements and again after being instructed to increase head amplitudes as much as possible.

Results: Compared to healthy subjects, patients made smaller head movements that contributed only 6% to total gaze saccade amplitudes. Head movements were also slowed, prolonged, and delayed. VOR suppression was increased and prolonged. Gaze saccades were inaccurate and delayed with long durations and decreased peak velocities.

Conclusion: In patients with chronic neck pain, the internal commands issued for combined eye-head movements have large enough amplitudes to create accurate gaze saccades; however, because of increased neck stiffness and viscosity, the head movements produced are smaller, slower, longer, and more delayed than they should be. VOR suppression is disproportionate to the size of the actual gaze saccades because sensory feedback signals from neck proprioceptors are non-veridical, likely due to prolonged coactivation of cervical muscles. The outcome of these changes in eye-head kinematics is head-on-trunk stability at the expense of gaze accuracy. In the absence of vestibular loss, the practical consequences may be dizziness (cervical vertigo) in the short term and imbalance and falls in the long term.

Keywords: VOR suppression; cervical vertigo; combined eye–head saccades; gaze kinematics; neck pain.

Figures

Figure 1
Figure 1
Eye movement amplitudes (gray circles) and head contribution amplitudes (black x’s) during combined eye–head (gaze) shifts of 45–65° amplitudes in (A) healthy subjects, (B) patients making typical head movements, and (C) patients making larger head movements. Dashed lines have slopes of 1. In healthy subjects (A), the head starts contributing to the gaze saccade earlier (about 25–30°), similar to when initial eye-in-orbit position is aligned with or in the same direction as the intended gaze saccade. Patients (B) make gaze shifts that are almost entirely composed of eye-in-orbit movements, with limited head contribution (6%) even for saccades greater than 50°. This is similar to when the initial eye position is deviated in a direction away from the direction of the intended saccades. When patients consciously increase gaze amplitudes (C), there is increasing head contribution (19%) and decreasing eye-in-orbit contribution to the gaze saccade, similar to control subjects making typical head movements (20%).
Figure 2
Figure 2
(A) Position tracings of a control subject making a 50° saccade with typical head movement. The vestibulo-ocular reflex (VOR) is active at the end of the gaze saccade and the eye-in-orbit counter-rotates to maintain target fixation. (B) Position tracings of a patient making a 60° saccade with typical head movement. The first gaze saccade is hypometric, and the VOR is suppressed allowing the gaze to move in the same direction as the head, followed by another saccade. Only when the target is acquired does the VOR become active. (C) Position tracings of the same patient making a 50° saccade with intentionally increased head movement amplitude. Similar to the healthy subject, the VOR is near unity at the end of the first saccade. T, target; G, gaze (eye-in-space); E, eye-in-orbit; H, head movement.
Figure 3
Figure 3
Peak head velocities for healthy subjects and patients during typical head movements (A) and larger head movements (B). For typical head movements, patients’ peak velocities are within normal range for comparably sized head movements (A) but are significantly slower when larger head movements are attempted (B). Circles are patient values. Dashed line is linear regression line for patients; solid line is linear regression line for control subjects with 95% confidence intervals (dotted lines).

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