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Long-term adaptive changes in primate vestibuloocular reflex. III. Electrophysiological observations in flocculus of normal monkeys.

1. The discharge characteristics of 1,239 single units recorded in the flocculus of alert monkeys were studied in relation to visual, vestibular, and oculomotor events in a variety of paradigms. Animals were trained to fixate small target lights and were required to perform various tracking tasks designed to facilitate the quantitative analysis of associated unit discharges. Units were subdivided into three major groups: granular layer input elements (GLIEs, 77 1 units), interneurons (tentatively classified as Golgi cells, 122 units), and Purkinje output cells (P-cells, 346 units). 2. The discharges of 94.2% of the GLIEs modulated in one or more of the paradigms and two major classes were defined: a) eye movement-only GLIEs (53.6%) modulated their discharge solely in relation to eye movements. Some altered their discharge only in relation to saccadic eye movements (saccadeonly units, y1 = 65), the majority of these being silent during fixation and discharging at high rates just before and during saccades in one or more directions. The remainder of the units in this class exhibited maintained discharges, which were influenced by steady eye positionthe rate increasing progressively as fixation shifted in the socalled on-directionand also showed additional modulation related to eye velocity during pursuit and/or vestibular stimulation (phasic-tonic units, y1 = 348); saccade-related discharges were various, but the most common pattern was the so-called burst-tonic. b) vestibular GLIEs (27.8%) modulated their discharge in relation to head velocity during horizontal chair oscillations as if receiving a vestibular input. The modulation of some of these units was solely determined by the chair movement (vestibular-only units, yt = 47), while others also altered their discharge in relation to saccadic eye movements, mostly by pausing (vestibularplus-saccade units, y2 = 70); yet others were further influenced by steady eye position and, in addition, by eye velocity during pursuit and/or vestibular stimulation (vestibular-plus-position units, y2 = 97). Other GLIEs discharged in relation to vergence/ accommodation (3.9%), visual inputs (2.7%), attempted head movements (5.2%), and blinks (1%). 3. Discharges of putative Golgi cells had unusually regular interspike intervals. Seventy-one of the 122 such cells modulated in one or more of the paradigms, most discharging in relation to eye movements but less clearly and vigorously than the corresponding GLIEs. Some produced only weak saccade-related bursts (~1 = 12), while others discharged tonically in relation to steady eye position (yt = 24) but only weakly and frequently exhibited nonlinear rate-position relationships. One-quarter of the cells (~2 = 32) discharged tonically in relation to eye movements, but showed marked decays in firing during prolonged eccentric fixation and displayed very distorted, though consistent, discharge frequency profiles during sinusoidal and triangle-waveform pursuit. 4. P-cell simple spike discharges often had unusually irregular interspike intervals; 93% modulated in one or more of the para-