RAPID COMMUNICATION Oculomotor Control of Primary Eye Position Discriminates Between Translation and Tilt

Hess, Bernhard J. M. and Dora E. Angelaki. Oculomotor control tion of Listing’s plane is the state of ocular vergence (Mok of primary eye position discriminates between translation and tilt. et al. 1992). J. Neurophysiol. 81: 394–398, 1999. We have previously shown When the head dynamically rotates in space, for example, that fast phase axis orientation and primary eye position in rhesus during off-vertical axis rotations, it has been shown that monkeys are dynamically controlled by otolith signals during head vestibulo-ocular reflex (VOR) fast phase eye positions also rotations that involve a reorientation of the head relative to gravity. maintain a planar organization as do visually guided sacBecause of the inherent ambiguity associated with primary otolith cades with the head stationary. In this case, however, there afferent coding of linear accelerations during head translation and is a robust and consistent gravity-dependent shift and/or tilt tilts, a similar organization might also underlie the vestibulo-ocular of fast phase displacement planes (and thus primary posireflex (VOR) during translation. The ability of the oculomotor system to correctly distinguish translational accelerations from tion), yet through angles much greater than those observed gravity in the dynamic control of primary eye position has been in static tilt positions (Hess and Angelaki 1997a,b) . For investigated here by comparing the eye movements elicited by example, during rotation of the head about its yaw axis sinusoidal lateral and fore-aft oscillations (0.5 Hz{ 40 cm, equivain a tilted position, torsional and vertical primary position lent to { 0.4 g) with those during yaw rotations (1807 /s) about a modulate as a function of the component of gravity along vertically tilted axis (23.67) . We found a significant modulation the pitch and roll axis, respectively. of primary eye position as a function of linear acceleration (gravInformation regarding head orientation relative to gravity ity) during rotation but not during lateral and fore-aft translation. is presumably conveyed by primary otolith afferents that This modulation was enhanced during the initial phase of rotation detect linear accelerations. Because the gravitational and inwhen there was concomitant semicircular canal input. These findertial mass of the otoconia of the otolith organs are physiings suggest that control of primary eye position and fast phase axis orientation in the VOR are based on central vestibular mechacally identical, primary otolith afferents do not discriminate nisms that discriminate between gravity and translational head acbetween head tilt and translation (Fernández and Goldberg celeration. 1976; Loe et al. 1973). This fact raises the question whether it is gravity per se, i.e., instantaneous head orientation, or the resultant gravito-inertial acceleration, i.e., the total ouput I N T R O D U C T I O N of the otolith organs, that controls this remarkable gravityStatic head tilt relative to gravity induces compensatory dependent adjustment of the spatial orientation of saccade otolith-ocular reflexes. In the rabbit, these reflexes account and VOR fast phase axes. To address this question, we comfor up to Ç60% of the angle of head tilt (Baarsma and pared the modulation of VOR fast phase displacement planes Collewijn 1975). In frontal-eyed species, such as monkeys elicited during off-vertical axis rotation and linear translaor humans, the corresponding static otolith-ocular reflexes tion. Preliminary results have been published in abstract exhibit a much smaller gain of onlyÇ10%. In these species, form (Hess and Angelaki 1997c). the action of static otolith-ocular reflexes in different head tilted positions is best demonstrated by the effects on the