DISCHARGE PATTERNS OF NEURONS IN THE PRETECTAL NUCLEUS OF THE OPTIC TRACT (NOT) IN THE BEHAVING PRIMATE

1. To determine the possible role of the primate pretectal nucleus of the optic tract (NOT) in the generation of optokinetic and smooth-pursuit eye movements, we recorded the activity of 155 single units in four behaving rhesus macaques. The monkeys were trained to fixate a stationary target spot during visual testing and to track a small moving spot in a variety of visual environments. 2. The majority (82%) of NOT neurons responded only to visual stimuli. Most units responded vigorously for large-field (70 x 50°) moving visual stimuli and responded less, if at all, during smooth-pursuit eye movements in the dark; many of these units had large receptive fields (>10 x 10°) that included the fovea. The remaining visual units responded more vigorously during smooth-pursuit eye movements in the dark than during movement of large-field visual stimuli; all but one had small receptive fields (<10 x 10°) that included the fovea. For all visual units that responded during smooth pursuit, extinction of the small moving target so briefly that pursuit continued caused the firing rates to drop to resting levels, confirming that the discharge was due to visual stimulation of receptive fields with foveal and perifoveal movement sensitivity and not to smooth-pursuit eye movements per se. 3. Eighteen percent of all NOT units ceased their tonic discharge in association with all saccades including the quick phases accompanying optokinetic or vestibular nystagmus. The pause in firing began after saccade onset, was unrelated to saccade duration and occurred even in complete darkness. 4. Most (90%) of the visual NOT units were direction selective. They exhibited an increase in firing above resting during horizontal (ipsilateral) background movement and/or during smooth pursuit of a moving spot and a decrease in firing during contralateral movement. 5. The firing rates of NOT units were highly dependent on stimulus velocity. All had velocity thresholds of <1°/s and exhibited a monotonic increase in firing rate with visual stimulus velocity over part (n = 90%) or all (n = 10%) of the tested range (i.e., 1-200°/s). Most NOT units exhibited velocity tuning with an average preferred velocity of 64°/s. Only a few units were tuned to slowly moving (<15°/s) visual stimuli. 6. NOT units evinced no modulation in firing rate during horizontal whole-body oscillation about a vertical axis in the dark. However, when the animal suppressed the vestibuloocular reflex (VOR) by fixating a visual target moving with it, the discharge rates of NOT units were modulated. A comparison of firing rate with the slip velocity that occurred 60-100 ms earlier showed that the modulation was due to movement of the target spot relative to the fovea during imperfect suppression of the VOR. 7. Trains of low-current (i.e., 10-80 μA) electrical stimuli delivered at sites where units preferred horizontal visual motion elicited nystagmic eye movements with an ipsilaterally directed slow phase. Nystagmus could not be elicited from pretectal sites that did not contain such units. 8. Because most NOT neurons prefer full-field stimuli and electrical stimulation in their midst elicits nystagmic eye movements that strongly resemble optokinetic nystagmus (OKN), it seems likely that the simian NOT, like that of the rabbit, constitutes the afferent limb of the horizontal OKN pathway.