Compensatory and Orienting Eye Movements Induced By Off-Vertical Axis Rotation (OVAR) in Monkeys

Abstract

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15 degrees, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15-90 degrees, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7-0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABA(B) agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by approximately 90 degrees, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3 degrees /g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0 degrees /g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ~180 degrees relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.

Frequency-Dependent Spatiotemporal Tuning Properties of Non–Eye Movement Related Vestibular Neurons to Three-Dimensional Translations in Squirrel Monkeys

“…In addition, translations on the horizontal plane evoke a second type, though at a much lower sensitivity in normal animals, of eye movements that exhibits low-pass dynamics and is not sensitive to behavioral context (Angelaki and Hess 1996;Telford et al 1998). Existing evidence suggests that the evoked torsional/vertical eye movements to IA/NO translations are part of orienting ocular responses most prominent during changes of head orientation with respect to gravity, i.e., tilts (Kushiro et al 2002;Merfeld et al 2001). Since epithelial hair cells on otolith maculae are equally excited by inertial-or gravitation-driven shearing forces, the diminished orienting ocular responses to head translations on the horizontal plane and compensatory LVOR to tilts suggest that the animals' ability to distinguish translation versus tilt is an active neural process.…”

Processing of Angular Motion and Gravity Information Through an Internal Model

“…Many previous studies have tried to describe vestibular information processing in terms of more or less sophisticated cascades of linear and nonlinear filters. Although this kind of approach can perfectly describe a large class of experimental phenomena (Kushiro et al 2002;Raphan and Cohen 2002;Raphan and Sturm 1991), it cannot account for the considerable challenge that the brain is faced with by the noisy character of afferent information (Roddey et al 2000;Sadeghi et al 2007). The insight into the nature of vestibular signal processing that one can hope to reach by this kind of modeling is therefore rather limited.…”

“…In both these protocols, the sensory mismatch results in a rapid decrease of the vestibular or visual afterresponse, a phenomenon that has also been called dumping, characterized by a sharp shortening of the postrotatory time constant. A completely different type of protocol consists in rotating a subject at constant velocity about a tilted axis (Angelaki and Hess 1996b;Angelaki et al 2000, Harris 1988Kushiro et al 2002) (Fig. 1D).…”

Head tilt–translation combinations distinguished at the level of neurons

“…Angelaki et al 1999;Droulez and Darlot 1989;Glasauer 1993;Angelaki 2004, Holly 2000;Kushiro et al 2002;Merfeld et al 1993;Merfeld and Zupan 2002;Mergner and Glasauer 1999;Ormsby and Young 1977), where the neural mechanisms for the mathematical operations are not under study (except to a certain extent in Green and Angelaki (2004), as discussed in Sect. 1).…”