FUNCTIONAL AND ANATOMIC ORGANIZATION OF 3-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 rabb its were recorded using the scleral search coil technique. The compone nts of these eye movements were obtained in reference to an orthogonal coordinate system consisting of a vertical axis and two horizontal ax es at 45 degrees and 135 degrees azimuth. The azimuth coordinate was t aken to increase to both sides from the 0 degrees reference in the dir ection of the nose. 2. Eye movements were evoked most readily by stimu lation (0.2-ms pulses at 200 Hz for 1 s, intensity less than or equal to 20 mu A) at loci in the deep granular layer and the white matter. T hey consisted of slow (5-20 deg/s) movements. The responses were eithe r binocular, with the eye ipsilateral to the stimulated flocculus usua lly 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 compon ent of rotation for the two eyes and its sense of rotation (clockwise, CW, or counterclockwise, CCW). Seventy-eight percent of the evoked ey e movements could be placed in one of two classes. For one of these cl asses the largest response component was a short-latency abduction of the ipsilateral eye about its vertical axis (19%), whereas for the oth er class (59%), the largest response component was a short-latency CCW rotation of the ipsilateral(left) eye about its 135 degrees axis. Thi s response was frequently (50%) accompanied by a smaller short-latency CW rotation of the contralateral (right) eye about its 45 degrees axi s. 4. The two main classes of three-dimensional eye movements are asso ciated differentially with anatomically distinguishable compartments t hat are revealed by acetylcholinesterase histochemistry. Of the five a natomically distinguishable compartments in the floccular white matter , three are predominant. The middle of these three compartments is ass ociated with the vertical axis class of movements, whereas the two adj acent compartments are associated with the 135 degrees class of eye mo vements. The eye movement relation of the other two, smaller compartme nts, was not determined. 5. The spatial orientation of the rotation ax es of the two main classes of evoked eye movements closely corresponds to that of the preferred axes of the visual climbing fiber input to t he flocculus. This suggests that both are organized in a similar coord inate system. The spatial orientation of the axes of this coordinate s ystem also bears a close resemblance to that of the preferred axes of the semicircular canals. 6. The association of distinct classes of eye movements with the anatomically distinguishable compartments suggests that these compartments are the structural correlate of a coordinate system and that any particular eye rotation is synthesized from compon ents taken in this coordinate system.