Functional and anatomic organization of three-dimensional eye movements in rabbit cerebellar flocculus

1. The three-dimensional, binocular eye movements evoked by electrical microstimulation of the cerebellar flocculus of alert, pigmented rabbits were recorded using the scleral search coil technique. The components of these eye movements were obtained in reference to an orthogonal coordinate system consisting of a vertical axis and two horizontal axes at 45 degrees and 135 degrees azimuth. The azimuth coordinate was taken to increase to both sides from the 0 degrees reference in the direction of the nose. 2. Eye movements were evoked most readily by stimulation (0.2-ms pulses at 200 Hz for 1 s, intensity < or = 20 microA) at loci in the deep granular layer and the white matter. They consisted of slow (5-20 deg/s) movements. The responses were either binocular, with the eye ipsilateral to the stimulated flocculus usually having the larger amplitude, or were monocular, in which case they were restricted to the ipsilateral eye. 3. The evoked responses were classified according to the combination of the largest measured component of rotation for the two eyes and its sense of rotation (clockwise, CW, or counterclockwise, CCW). Seventy-eight percent of the evoked eye movements could be placed in one of two classes. For one of these classes the largest response component was a short-latency abduction of the ipsilateral eye about its vertical axis (19%), whereas for the other class (59%), the largest response component was a short-latency CCW rotation of the ipsilateral (left) eye about its 135 degrees axis. This response was frequently (50%) accompanied by a smaller short-latency CW rotation of the contralateral (right) eye about its 45 degrees axis. 4. The two main classes of three-dimensional eye movements are associated differentially with anatomically distinguishable compartments that are revealed by acetylcholinesterase histochemistry. Of the five anatomically distinguishable compartments in the floccular white matter, three are predominant. The middle of these three compartments is associated with the vertical axis class of movements, whereas the two adjacent compartments are associated with the 135 degrees class of eye movements. The eye movement relation of the other two, smaller compartments, was not determined. 5. The spatial orientation of the rotation axes of the two main classes of evoked eye movements closely corresponds to that of the preferred axes of the visual climbing fiber input to the flocculus. This suggests that both are organized in a similar coordinate system.(ABSTRACT TRUNCATED AT 400 WORDS)