Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. An otolith-controlled transformation that depends on an intact cerebellar nodulus. Angelaki, Dora E., and Bernhard J. M. Hess. Dept. of Surgery (Otolaryngology), University of Mississippi Medical Center, Jackson MS, Dept. of Neurology, University Hospital Zurich, CH-8091, Switzerland.
APStracts 2:0042N, 1995.
SUMMARY AND CONCLUSIONS
1. We have recently studied the spatial representation of angular motion signals in rhesus monkeys by examining the orientation of postrotatory vestibulo-ocular responses when tilting head and body relative to gravity after constant velocity rotation about an earth-vertical axis. We have reported that low frequency angular motion signals in the vestibulo-ocular reflex (VOR) of rhesus monkeys are spatially transformed such that they remain invariant relative to gravity. The present study examines the properties of these inertial vestibular signals by employing similar stimulation conditions in animals with either selective semicircular canal plugging or selective lesions of the cerebellar lobule X (nodulus) and ventral lobule IX (uvula). 2. The spatial organization of postrotatory VOR was studied in two rhesus monkeys which had either the lateral or one of the vertical canal pairs inactivated by plugging. In both monkeys, the spatio-temporal characteristics of postrotatory velocity after rotation in the plane of an intact canal pair and tilting in the plane of the plugged canal pair was indistinguishable from those of intact animals: Postrotatory responses following tilts in the plane of the plugged canal pair were strongly damped, whereas an orthogonal response component was generated that rotated the eye velocity vector towards alignment with gravity. Thus, otolith information rather than transient semicircular canal signals that normally co-exist during tilts seem to provide the necessary cues for the central transformation of semicircular canal signals. 3. The three-dimensional VOR properties were studied in two animals whose cerebellar nodulus and ventral uvula were surgically ablated. Following these lesions, the temporal properties of the horizontal, vertical and torsional VOR during earth-vertical axis rotations were differentially affected. For horizontal VOR, the duration of postrotatory nystagmus was prolonged and the responses acquired strongly underdamped (i.e., oscillatory) properties. Similarly, sinusoidal responses were characterized by smaller phase leads after the lesion. For torsional VOR, the duration of postrotatory nystagmus was significantly shorter after the lesions, reaching post-lesion values of 3.6+/-1.7 s and 6.4+/-1.1 s compared to pre-lesion values of 22.4+/-4.5 s and 33.6+/-5.3 s for each animal. In addition, large phase leads characterized the torsional VOR during low frequency sinusoidal stimulation. The dynamic properties of the vertical VOR in the lesioned animals, on the other hand, was indistinguishable from controls. 4. The cerebellar lesions affected the spatial organization of the horizontal and vertical/torsional systems in a differential way. Inertial transformation of lateral canal activity was only partially affected. Head tilts during postrotatory horizontal VOR still induced generation of an orthogonal component in the appropriate direction, however, appropriate temporal tuning of the responses was lost. As a result, postrotatory eye velocity rotated towards alignment with gravity but systematically undershot the appropriate tilt angle. 5. Lesions of the nodulus and ventral uvula eliminated the ability of the vertical canal system to modify its dynamic characteristics as a function of head tilt. In contrast to the lateral canal system, however, this loss was also accompanied by a complete inability to reorient eye velocity relative to gravity. We conclude that neural processing of vestibular signals in the nodulus/ventral uvula is involved in maintaining an inertial coding of angular motion in the vertical canal system. 6. These experimental observations are simulated by a simple model in which semicircular canal activity is processed through an inertial center that reorients semicircular canal head velocity signals relative to gravity based on a combination of rotation and projection principles. One of the predictions of the inertial vestibular system is the previously unexplained generation of a steady-state compensatory nystagmus during constant velocity, earth-vertical axis rotation when the head is simultaneously sinusoidally oscillated about a nested orthogonal axis (e.g., pitch while rotating). In agreement with this, animals with lesions of the nodulus/ventral uvula were unable to generate this response. 7. We conclude that there exists a central vestibulo-motor system which utilizes both otolith and semicircular canal signals in order to detect absolute angular motion of the head in space. These results further suggest that the vestibulo-ocular velocity storage represents an oculomotor footprint of this system and could be simply regarded as an epiphenomenon associated with the particular experimental conditions when the VOR is tested in head and body-restrained subjects. 

Received 26 July 1994; accepted in final form 19 January 1995.
APS Manuscript Number J458-4.
Article publication pending J. Neurophysiol.
ISSN 1080-4757 Copyright 1995 The American Physiological Society.
Published in APStracts on  3 April 1995.