Vestibular and cerebellar contribution to gaze optimality

Abstract

Patients with chronic bilateral vestibular loss have large gaze variability and experience disturbing oscillopsia, which impacts physical and social functioning, and quality of life. Gaze variability and oscillopsia in these patients are attributed to a deficient vestibulo-ocular reflex, i.e. impaired online feedback motor control. Here, we assessed whether the lack of vestibular input also affects feed-forward motor learning, i.e. the ability to choose optimal movement parameters that minimize variability during active movements such as combined eye-head gaze shifts. A failure to learn from practice and reshape feed-forward motor commands in response to sensory error signals to achieve appropriate movements has been proposed to explain dysmetric gaze shifts in patients with cerebellar ataxia. We, therefore, assessed the differential roles of both sensory vestibular information and the cerebellum in choosing optimal movement kinematics. We have previously shown that, in the course of several gaze shifts, healthy subjects adjust the motor command to minimize endpoint variability also when movements are experimentally altered by an increase in the head moment of inertia. Here, we increased the head inertia in five patients with chronic complete bilateral vestibular loss (aged 45.4±7.1 years, mean±standard deviation), nine patients with cerebellar ataxia (aged 56.7±12.6 years), and 10 healthy control subjects (aged 39.7±6.3 years) while they performed large (75° and 80°) horizontal gaze shifts towards briefly flashed targets in darkness and, using our previous optimal control model, compared their gaze shift parameters to the expected optimal movements with increased head inertia. Patients with chronic bilateral vestibular loss failed to update any of the gaze shift parameters to the new optimum with increased head inertia. Consequently, they displayed highly variable, suboptimal gaze shifts. Patients with cerebellar ataxia updated some movement parameters to serve the minimum variance optimality principle but inaccurately undershot the target leading to an average gaze error of 11.4±2.0°. Thus, vestibulopathy leads to gaze variability not only as a result of deficient online gaze control but also a failure in motor learning because of missing error signals. Patients with cerebellar ataxia in our setting can learn from practice-similar to recent findings in reaching movements-and reshape feed-forward motor commands to decrease variability. However, they compromise optimality with inaccurately short movements. The importance of vestibular information for motor learning implies that patients with incomplete bilateral vestibulopathy, and patients with cerebellar ataxia, should be advised to actively move their head whenever appropriate. This way, sensory error signals can be used to shape the motor command and optimize gaze shifts trial-by-trial.

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

“…Feedforward control of counter-rotations is in accordance with previous observations that counterrotations serve gaze optimality [25] by minimizing post-movement trial-to-trial gaze variability that is corrupted by signal dependent [8,9] and constant noise [30,31]. Large gaze shift without any counterrotation would be more variable than a movement with the same gaze trajectory realized naturally with a counter-rotation [25].…”

“…Other aspects of the gaze data e.g., eye and head movement durations, peak velocities, trial-to-trial gaze variability have been published elsewhere [25]. Figure 1A shows eye and head velocity profiles for a representative healthy subject, and a vestibularloss and a cerebellar-ataxia patient (patient 8, Table 1) when the head moment of inertia was increased.…”

“…Large gaze shift without any counterrotation would be more variable than a movement with the same gaze trajectory realized naturally with a counter-rotation [25].…”

Quantification of Head Movement Predictability and Implications for Suppression of Vestibular Input during Locomotion

“…There is evidence that the cerebellum could play a crucial role in predicting sensory consequences of movement (Cullen and Brooks, 2015). Recent findings in humans on gaze control during active head movements also underline the importance of efference copy signals in accordance with the optimal motor control framework (Saglam et al, 2014). …”

Cytochrome P450 26b1-mediated specification of vestibular striola and central zones is required for transient responses in linear acceleration

“…For example, squirrel monkeys show transient head tremor and postural instability after plugging one of the lateral semicircular canals 62 . Patients with chronic bilateral vestibular loss that exhibit gaze variability and oscillopsia also show pronounced head oscillations in response to weighted head mass, compared to healthy individuals 63 . This head tremor behavior is attributed to a failure of vestibular input that is normally required to maintain head stability 64,65 and ensure movement accuracy during active goal-directed behaviors 63,66 .…”