Exp Brain Res (1994) 102:45 56 9 Springer-Verlag 1994 Mingjia Dai 9 Leigh McGarvie - Inessa Kozlovskaya Theodore Raphan 9 Bernard Cohen Effects of spaceflight on ocular counterrolling and the spatial orientation of the vestibular system Received: 29 March 1994 / Accepted: 21 July 1994 Abstract We recorded the horizontal (yaw), vertical (pitch), and torsional (roll) eye movements of two rhesus monkeys with scleral search coils before and after the COSMOS Biosatellite 2229 Flight. The aim was to de- termine effects of adaptation to microgravity on the vestibulo-ocular reflex (VOR). The animals flew for 11 days. The first postflight tests were 22 h and 55 h after landing, and testing extended for 11 days after reentry. There were four significant effects of spaceflight on func- tions related to spatial orientation: (1) Compensatory ocular counterrolling (OCR) was reduced by about 70% for static and dynamic head tilts with regard to gravity. The reduction in OCR persisted in the two ani- mals throughout postflight testing. (2) The gain of the torsional component of the angular VOR (roll VOR) was decreased by 15% and 50% in the two animals over the same period. (3) An up-down asymmetry of nystag- mus, present in the two monkeys before flight was re- duced after exposure to microgravity. (4) The spatial orientation of velocity storage was shifted in the one monkey that could be tested soon after flight. Before flight, the yaw axis eigenvector of optokinetic afternys- tagmus was close to gravity when the animal was up- right or tilted. After flight, the yaw orientation vector was shifted toward the body yaw axis. By 7 days after M. Dai ([~]) - L. McGarvie . B. Cohen Department of Neurology, Box 1135, Mount Sinai School of Medicine, 1 East 100th Street, New York, NY 10029, USA; FAX no: 212-831-1610 B. Cohen Department of Physiology and Biophysics, Mount Sinai School of Medicine, New York, USA I. Kozlovskaya Institute of Biomedical Problems, Moscow, Russia T. Raphan Department of Computer and Information Science, Brooklyn College, CUNY, USA recovery, it had reverted to a gravitational orientation. We postulate that spaceflight causes changes in the vestibular system which reflect adaptation of spatial ori- entation from a gravitational to a body frame of refer- ence. These changes are likely to play a role in the pos- tural, locomotor, and gaze instability demonstrated on reentry after spaceflight. Key words Spaceflight - Otoliths Ocular counterrolling - Velocity storage - Monkey Introduction Adaptation to microgravity presents a unique set of challenges to the vestibular system. On earth, the otoliths are subject to a constant gravitoinertial acceler- ation (GIA) due to gravity. Tilting the head does not change the magnitude of the GIA, it only rotates it rela- tive to the head. Translation induces an additional ac- celeration component which effectively rotates the GIA vector and increases its magnitude. In space, the GIA component due to gravity is absent, and the otoliths only sense the linear acceleration associated with trans- lation. Consequently, the linear acceleration vector nev- er rotates relative to the head in space, but only changes its magnitude along the direction of movement. The semicircular canals which respond to angular accelera- tion function in microgravity as they did on earth. Since there is no otolith-induced compensatory tor- sion of the eyes (ocular counterrolling, OCR) in space, and since compensatory torsional eye movements due to head-on-body tilt are negligible in flight (Hofstetter- Degen et al. 1993), the demand for otolith-driven OCR is probably much reduced. It has been postulated that there is a reinterpretation of otolith input in micrograv- ity so that linear acceleration, sensed by otolith organs, is now interpreted primarily as translation (Reschke et al. 1984; Parker et al. 1985; Arrott and Young 1986; Young et al. 1986). In support of this, interaural linear acceleration after spaceflight produces predominantly