Gaze stabilization in chronic vestibular-loss and in cerebellar ataxia: Interactions of feedforward and sensory feedback mechanisms

Abstract

During gaze shifts, humans can use visual, vestibular, and proprioceptive feedback, as well as feedforward mechanisms, for stabilization against active and passive head movements. The contributions of feedforward and sensory feedback control, and the role of the cerebellum, are still under debate. To quantify these contributions, we increased the head moment of inertia in three groups (ten healthy, five chronic vestibular-loss and nine cerebellar-ataxia patients) while they performed large gaze shifts to flashed targets in darkness. This induces undesired head oscillations. Consequently, both active (desired) and passive (undesired) head movements had to be compensated for to stabilize gaze. All groups compensated for active and passive head movements, vestibular-loss patients less than the other groups (P < 0.001, passive/active compensatory gains: vestibular-loss 0.23 ± 0.09/0.43 ± 0.12, healthy 0.80 ± 0.17/0.83 ± 0.15, cerebellar-ataxia 0.68 ± 0.17/0.77 ± 0.30, mean ± SD). The compensation gain ratio against passive and active movements was smaller than one in vestibular-loss patients (0.54 ± 0.10, P = 0.001). Healthy and cerebellar-ataxia patients did not differ in active and passive compensation. In summary, vestibular-loss patients can better stabilize gaze against active than against passive head movements. Therefore, feedforward mechanisms substantially contribute to gaze stabilization. Proprioception alone is not sufficient (gain 0.2). Stabilization against active and passive head movements was not impaired in our cerebellar ataxia patients.

Unstable Gaze in Functional Dizziness: A Contribution to Understanding the Pathophysiology of Functional Disorders

“…During OSC epoch, both the healthy subject and the functional patient show intact gaze stabilization. input (Saǧlam and Lehnen, 2014). Together with the present results, by using the example of functional dizziness patients, we are one step closer in locating an erroneous site of perceptual dysregulation in functional disorders (Edwards et al, 2012;Van den Bergh et al, 2017;Henningsen et al, 2018;Pezzulo et al, 2019).…”

“…These findings demonstrate the significant role of both intact processing of vestibular feedback and expectation formation based on correct internal models, during eye–head gaze shifts. Their contribution over the course of the gaze shifts has been previously demonstrated within the same experimental paradigm, where patients with complete bilateral vestibular loss show gaze stabilization in the CR epoch despite missing sensory input ( Saǧlam and Lehnen, 2014 ). Together with the present results, by using the example of functional dizziness patients, we are one step closer in locating an erroneous site of perceptual dysregulation in functional disorders ( Edwards et al, 2012 ; Van den Bergh et al, 2017 ; Henningsen et al, 2018 ; Pezzulo et al, 2019 ).…”

“…using the same experimental design (Saǧlam and Lehnen, 2014): patients with complete bilateral vestibular loss show better gaze stabilization in the CR epoch than the OSC epoch, confirming the contribution of internal model and efference copy use in this stabilization epoch. Based on the "perceptual dysregulation" theory (Edwards et al, 2012;Van den Bergh et al, 2017;Henningsen et al, 2018;Pezzulo et al, 2019), during large eyehead gaze shifts, we expect functional dizziness patients to rely on incorrect internal models of their head, thus showing unstable gaze during the CR, but not the OSC epoch.…”

“…Therefore, for gaze stabilization, motor planning is used to expect the sensory consequences of the head movement (e.g., Shanidze et al, 2010;King and Shanidze, 2011). The contribution of motor planning information on gaze stabilization in the CR epoch of this experimental paradigm has been demonstrated previously in bilateral vestibular loss patients (Saǧlam and Lehnen, 2014). Due to ongoing active head motion here, VOR is still suppressed in the CR epoch, although suppression is likely to be attenuated toward the end of the active movement (e.g., Lefèvre et al, 1992).…”

“…Gaze gains were defined as the amount of compensatory eye movement in respect to head movement and were calculated as the slope of the linear regression between eye and head velocity profiles using the MATLAB built-in function robustfit (analogously to Saǧlam and Lehnen, 2014 ). Gaze gains were computed for two gaze stabilization epochs: the internally-driven CR epoch as part of the planned gaze shift, using internal expectations and sensory information for stabilization, and the sensory-driven OSC epoch for sensory-dependent gaze stabilization after gaze shift end.…”