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

Abstract

BackgroundThe 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.MethodsWe 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.ResultsCompared 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.ConclusionIn 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.

Symptoms in cervical vertigo

“…Recent studies have identified possible objective measures of neck contribution in those diagnosed with cervical vertigo. 17,30,31 When compared to healthy control subjects, Johnston et al found that a prolonged reduction in vestibular response to head movement (ie, VOR) when patients attempted to acquire visual targets with cervical soft tissue disorders and normal neuro-otologic examinations. 31 Their results suggest that neck limitations, due to pain or stiffness, manifest an exaggerated proprioceptive response and subsequent disproportionate VOR suppression, which translates into subjective symptoms of dizziness and imbalance.…”

Cervicothoracic Mechanical Impairment as Part of Complete Neurological Fall Risk Appraisal

“…In our population of patients with chronic soft-tissue rheumatic complaints, increased fall frequency and fear of falling occurred in patients who had reduced cervical mobility and increased mid-thoracic kyphoscoliosis. With chronic neck and upper back pain, horizontal head rotations become smaller, slower, longer, and more delayed over time, 11 as evidenced by negative correlations between head rotations and symptom duration in all faller cohorts. The consequence is head-on-trunk stability at the expense of gaze accuracy when making large unpredictable horizontal head-free gaze shifts.…”

“…10 Chronic cervical immobility prolongs VOR suppression during combined eye-head movements because coactivation of cervical muscles causes non-veridical sensory signals from neck proprioceptors. This in turn causes diminished gaze accuracy, 11 potentially impairing navigation through complex visual environments where it is essential to accurately redirect gaze to novel targets. We determined these abnormalities of saccade metrics and VOR suppression to be consistent and robust findings in patients with chronically restricted cervical mobility.…”

“…We hypothesized that these abnormalities would lead to imbalance and falls in this cohort of patients, who do not otherwise have quantitative evidence of vestibulopathy. 11 To date, there has been little written about fall risk in those with chronically restricted neck mobility. Gabell et al 12 examined 100 individuals aged 65-85 years and found that restricted neck movements increased the probability of falling twofold.…”

Disease Classification Based on Synthesis of Multiple Long Short-Term Memory Classifiers Corresponding to Eye Movement Features

“…The literature [31][32][33][34] showed how eye movement and nystagmus videos can be utilized in dizziness diagnosis. Theekapun Charoenpong et al [32] proposed a method to diagnose vertigo by measuring the eye movement velocity of nystagmus.…”