The long-term objective is to better understand cerebellar function by investigating the neuronal signal processing underlying eye movements elicited by natural stimulation. The experiments will focus on the flocculus of the rabbit. The central theme is that signal processing in the flocculus entails mapping within and between intrinsic reference frames related to the geometry of the semicircular canals and the extraocular muscles, and that these reference frames have an anatomical counterpart in the modular organization of the cerebellum. The modular organization is seen in the cortex as anatomically distinguishable compartments containing physiologically distinct climbing fibers and their associated Purkinje cells. The modules are woven together by the parallel fibers, which traverse several modules. For the most part, the experimental method will be manipulation of extracellularly recorded Purkinje cell activity by presentation of natural visual, vestibular, and proprioceptive stimuli. The relative contribution of the ascending and parallel fiber segments of granule cell axons to generation of Purkinje cell simple spikes will be assessed by recording multi-unit granule cell activity and single unit Purkinje cell activity in the anesthetized rabbit in response to stimulation of extraocular proprioceptors. Distribution of this activity will be determined in relation to the floccular modules that differentially control particular extraocular muscles. If, as hypothesized, stretch of a particular eye muscle activates granule cells only in those modules that control that muscle, then the distribution of Purkinje cell activity across modules will provide a measure of the relative influence of the two parts of the granule cell axon. A similar study will be done using natural visual stimulation to investigate the generality of the findings. Two studies will provide a more unified view of climbing fiber function. In one study, extraocular proprioceptive stimulation will be used in the anesthetized rabbit to determine the conditions under which climbing fiber activation of Purkinje cells produces a short-lasting enhancement of simple spike modulation. In another study, pairs of floccular Purkinje cells will be recorded simultaneously in the awake rabbit to determine how the capacity of the inferior olive to discharge synchronously and rhythmically is influenced by eye movements evoked by natural visual and vestibular stimuli. In preparation for studying floccular participation in control of eye movements made in combination with head movements, contributions of neck muscle proprioceptors to signal processing will be investigated by recording from Purkinje cells in both the anesthetized and awake rabbit whose body can be rotated about a vertical axis while the head is stationary. One of the five floccular modules differs from the other four because its climbing fibers are not modulated by retinal image motion. The anatomy of the projections to the part of the inferior olive providing the climbing fibers to this module suggests that it may be related to voluntary gaze shifts. This hypothesis will be evaluated by recording from Purkinje cells in the awake rabbit allowed to move its head about the vertical axis to produce voluntary gaze shifts, which in the rabbit normally occur as combined eye/head movements.
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