VISUAL AND OCULOMOTOR FUNCTIONS OF MONKEY SUBTHALAMIC NUCLEUS

1. Single-unit recordings were obtained from the subthalamic nuclei of three monkeys trained to perform a series of visuooculomotor tasks. The monkeys were trained to fixate on a spot of light on the screen (fixation task). When the spot was turned off and a target spot came on, they were required to fixate on the target quickly by making a saccade. Visually guided saccades were elicited when the target came on without a time gap (saccade task). Memory-guided saccades were elicited by delivering a brief cue stimulus while the monkey was fixating; after a delay, the fixation spot was turned off and the monkey made a saccade to the remembered target (delayed saccade task). 2. Of 265 neurons tested, 95 showed spike activity that was related to some aspects of the visuooculomotor tasks, whereas 66 neurons responded to active or passive limb or body movements. The task-related activities were classified into the following categories: eye fixation-related, saccade-related, visual stimulus-related, target- and reward-related, and lever release-related. 3. Activity related to eye fixation (n = 22) consisted of a sustained spike discharge that occurred while the animal was fixating on a target light during the tasks. The activity increased after the animal started fixating on the target and abruptly ceased when the target went off. The activity was unrelated to eye position. It was not elicited during eye fixation outside the tasks. The activity decreased when the target spot was removed. 4. Activity related to saccades (n = 22) consisted of a phasic increase in spike frequency that was time locked with a saccade made during the tasks. The greatest increases occurred predominantly after saccade onset. This activity usually was unrelated to spontaneous saccades made outside the task. The changes in activity typically were optimal in one direction, generally toward the contralateral side. 5. Visual responses (n = 14) consisted of a phasic excitation in response to a visual probe stimulus or target. Response latencies usually were 70-120 ms. The receptive fields generally were centered in the contralateral hemifield, sometimes extending into the ipsilateral field. The receptive fields included the foveal region in seven neurons; most of these neurons responded best to parafoveal stimulation. Peripheral stimuli sometimes suppressed the activity of visually responsive neurons. 6. Activity related to target and reward (n = 29) consisted of sustained spike discharge that occurred only when the monkey could expect a reward by detecting the dimming of the light spot that he was fixating. This activity was present regardless of whether the monkey obtained the reward by releasing a lever or by just maintaining fixation on the target. Eye fixation on a light stimulus may not be prerequisite: sometimes it started even before the target point came on. 7. Among neurons exhibiting activity that was related to lever release during the task (n = 49), four different types of responses were recorded: excitation before lever release, excitation after lever release, inhibition before lever release, and a combination of excitation and inhibition. These neurons showed no change in activity in relation to limb movements made outside the tasks. 8. Neurons related to visuooculomotor tasks were located primarily in the ventral part of the subthalamic nucleus, whereas neurons responsive to skeletomotor movements were found predominantly in the dorsal part. 9. These results are considered in relation to the current view that the subthalamic nucleus sends excitatory signals to the substantia nigra pars reticulata, which in turn exerts tonic inhibition of saccadic burst cells in the superior colliculus. In contrast to the caudate-nigral connection, which would play a role in the initiation of saccades by a disinhibitory mechanism, the subthalamic nucleus might act to suppress eye movements. The suppressive mechanism would act to maintain eye position on an object of interest, prevent unwanted eye movements under specific circumstances, or recover eye fixation once a saccade is executed.