Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula

Spatial orientation of the angular vestibuloocular reflex (aVOR) was studied in rhesus monkeys after complete and partial ablation of the nodulus and ventral uvula. Horizontal, vertical, and torsional components of slow phases of nystagmus were analyzed to determine the axes of eye rotation, the time constants (Tcs) of velocity storage, and its orientation vectors. The gravito-inertial acceleration vector (GIA) was tilted relative to the head during optokinetic afternystagmus (OKAN), centrifugation, and reorientation of the head during postrotatory nystagmus. When the GIA was tilted relative to the head in normal animals, horizontal Tcs decreased, vertical and/or roll time constants (Tc(vert/roll)) lengthened according to the orientation of the GIA, and vertical and/or roll eye velocity components appeared (cross-coupling). This shifted the axis of eye rotation toward alignment with the tilted GIA. Horizontal and vertical/roll Tcs varied inversely, with T(chor) being longest and T(cvert/roll) shortest when monkeys were upright, and the reverse when stimuli were around the vertical or roll axes. Vertical or roll Tcs were longest when the axes of eye rotation were aligned with the spatial vertical, respectively. After complete nodulo-uvulectomy, T(chor) became longer, and periodic alternating nystagmus (PAN) developed in darkness. T(chor) could not be shortened in any of paradigms tested. In addition, yaw-to-vertical/roll cross-coupling was lost, and the axes of eye rotation remained fixed during nystagmus, regardless of the tilt of the GIA with respect to the head. After central portions of the nodulus and uvula were ablated, leaving lateral portions of the nodulus intact, yaw-to-vertical/roll cross-coupling and control of Tc(vert/roll) was lost or greatly reduced. However, control of Tchor was maintained, and T(chor) continued to vary as a function of the tilted GIA. Despite this, the eye velocity vector remained aligned with the head during yaw axis stimulation after partial nodulo-uvulectomy, regardless of GIA orientation to the head. The data were related to a three-dimensional model of the aVOR, which simulated the experimental results. The model provides a basis for understanding how the nodulus and uvula control processing within the vestibular nuclei responsible for spatial orientation of the aVOR. We conclude that the three-dimensional dynamics of the velocity storage system are determined in the nodulus and ventral uvula. We propose that the horizontal and vertical/roll Tcs are separately controlled in the nodulus and uvula with the dynamic characteristics of vertical/roll components modulated in central portions and the horizontal components laterally, presumably in a semicircular canal-based coordinate frame.