Spatial organization of visual messages of the rabbit's cerebellar flocculus. II. Complex and simple spike responses of Purkinje cells

Abstract

1. Complex and simple spike responses of Purkinje cells were recorded in the flocculus of anesthetized, paralyzed rabbits during rotating full-field visual stimuli produced by a three-axis planetarium projector. 2. On the basis of the spatial properties of their complex spike responses, floccular Purkinje cells could be placed into three distinct classes called Vertical Axis, Anterior (45 degrees) Axis and Posterior (135 degrees) Axis. The first two classes occurred in both monocular and binocular forms; the third class was encountered only in binocular form. For the binocular response forms, stimulation through one eye, called the dominant eye, elicited a stronger modulation of the complex spike firing rate than did stimulation of the other eye. The approximate orientation of that axis about which full-field rotation elicited the deepest modulation (the preferred axis) when presented to the dominant eye served as the class label. These classes are the same as those determined qualitatively for inferior olive neurons in the previous paper (47). The present study provides a quantitative description of their spatial tuning. 3. For Vertical Axis cells, the dominant eye was ipsilateral with respect to the flocculus recording site. The preferred axis was vertical and null (no-response) axes were in the horizontal plane. For the binocular response form of Vertical Axis cells (less than 10% of this class), the direction preferences for the two eyes were synergistic with respect to rotation about the vertical axis. 4. The dominant eye for the Anterior (45 degrees) Axis cells was contralateral, with the preferred axis oriented in the horizontal plane at approximately 45 degrees contralateral azimuth. The modulation depth showed a close to cosine relation with the angle between the preferred axis and the stimulus rotation axis. The average orientation (n = 10) for the dominant eye preferred axis, determined by the best-fit sinusoid, was 47 degrees contralateral azimuth. The preferred axis orientation for the ipsilateral (nondominant) eye in the binocular response forms was between 45 and 90 degrees azimuth in the horizontal plane. A null axis for each eye was at approximately 90 degrees to the preferred axis. 5. The Posterior (135 degrees) Axis cells were encountered only in binocular response forms. The dominant eye was ipsilateral, with the preferred axis oriented at approximately 135 degrees ipsilateral azimuth close to the horizontal plane. The modulation depth showed a close to cosine relation with the angle between the preferred axis and the stimulus rotation axis.(ABSTRACT TRUNCATED AT 400 WORDS)

Intraburst and Interburst Signaling by Climbing Fibers

“…Excitatory and inhibitory phases of the CFR modulation of a VA cell was defined relative to counterclockwise and clockwise motions of the turntable, with the beginning of each phase corresponding to the beginning of the motion in each direction. As found previously (Graf et al, 1988), the complex spike activity of all VA Purkinje cells increased for retinal image motion in the temporal to nasal direction referenced to the eye ipsilateral to the recorded flocculus. A contrast ratio characterizing the modulation was defined as the difference in the number of CFRs between excitatory and inhibitory phases divided by the total number of CFRs during visual stimulation.…”

“…Similar measurements were also made for visual modulation of climbing fiber activity in floccular Purkinje cells that responded best to visual rotation about the vertical axis (VA) (Graf et al, 1988). Our goal was to examine the possibility that the number of spikes within the climbing fiber bursts carries a signal.…”

“…Single Purkinje cell activity was extracellularly identified by the presence of complex spikes. Purkinje cells in the flocculus that respond best to visual whole-field rotation about either the VA or the horizontal 45°-135°a xis were identified by slowly moving (ϳ1°/s) a large hand-held visual pattern (Graf et al, 1988). Penetration of a Purkinje cell by the microelectrode often resulted in a period of injury discharge, after which relatively large EPSPs attributable to the climbing fiber input could be recorded (Eccles et al, 1966;Armstrong and Rawson, 1979).…”

Brain Stem Pursuit Pathways: Dissociating Visual, Vestibular, and Proprioceptive Inputs During Combined Eye-Head Gaze Tracking

“…The role of the climbing fiber input is still unclear (reviewed in Simpson et al 1996), but many assume that it functions to modify the efficacy of the synapse between mossy fibers and Purkinje cell. Moreover there is evidence that in rabbit (Frens et al 2001;Graf et al 1988) and monkey (Kahlon and Lisberger 2000;Stone and Lisberger 1990b) complex spike trains encode performance errors (i.e., retinal slip).…”

Levels of Analysis of the Vestibulo-Ocular Reflex: A Postmodern Approach

“…Since yaw movement stimulates primarily the horizontal semicircular canal pair (Curthoys, Markham and Blanks, 1975), this approach implied that other canal pairs also had their own independent connections to the appropriate eye muscles. The idea of a set of three sub-systems defined by the semicircular canals within the skull underlying the generation of the VOR around any axis received support from the spatial tuning of sensory responses in various parts of the brain known to be involved in the neural interpretation of the VOR Simpson, Graf and Leonard, 1981;Graf, Simpson and Leonard, 1988;Oyster, Takahashi and Collewijn, 1972). Furthermore the direction of pull of the oculomotor muscles themselves also seem to be arranged in planes roughly aligning with the orientation of the semicircular canal planes .…”