Spatial organization of linear vestibuloocular reflexes of the rat: responses during horizontal and vertical linear acceleration.

1. The spatial properties of linear vestibuloocular reflexes (LVOR) were studied in pigmented rats in response to sinusoidal linear acceleration on a sled. The orientation of the animal on the sled was altered in 15 degrees steps over the range of 360 degrees. Horizontal, vertical, and torsional components of eye movements were recorded with the magnetic field search coil technique in complete darkness. Conjugacy of the two eyes was studied in the horizontal movement plane. 2. Acceleration along the optic axis of one eye (approximately 50 degrees lateral) induced maximal vertical responses in the ipsilateral eye and, at the same time, maximal torsional responses in the contralateral eye. These vertical and torsional responses of the LVOR coincide with those obtained when the respective coplanar vertical semicircular canals are stimulated. Such a congruence suggests a common reference frame for LVOR and angular vestibuloocular reflexes (AVOR), with the result that direct combination of signals indicating apparent and real head tilt is facilitated. 3. Transformations of vertical and torsional responses into head coordinates (pitch and roll) show that these movements are compensatory in direction for any combination of apparent head tilt in pitch and roll planes. 4. Gain (rotation of the eye/apparent rotation of the gravity direction) was approximately 0.3 at 0.1 Hz and decreased to approximately 0.1 at 1.0 Hz. Vertical responses tended to have a larger gain than torsional responses. Phase lag relative to peak acceleration increased from about -9 degrees to about -47 degrees over the same frequency range. 5. Vertical linear acceleration evoked only vertical eye movements at a frequency of 1.0 Hz. 6. Horizontal responses of both eyes were symmetric or asymmetric in amplitude and in-phase (conjugate) or out-of-phase (disconjugate) with respect to each other, depending on the direction of linear acceleration. Translation in the transverse direction evoked conjugate compensatory horizontal responses. Forward-backward translation evoked movements of both eyes that were symmetric in amplitude, but 180 degrees out-of-phase. Translation along diagonal axes evoked almost no horizontal responses in the eye facing in the direction of linear motion but maximal horizontal responses in the eye facing away from the direction of linear motion. These disconjugate movements resulted in a modulation of the vergence angle of the eyes. 7. Disconjugate horizontal responses in darkness are best explained by the assumption that part of the visual consequences of a translational head displacement (i.e., change of viewing distance in light) is taken into account centrally.(ABSTRACT TRUNCATED AT 400 WORDS)