Minimal synaptic delay in the saccadic output pathway of the superior colliculus studied in awake monkey

Abstract

The synaptic organization of the saccade-related neuronal circuit between the superior colliculus (SC) and the brainstem saccade generator was examined in an awake monkey using a saccadic, midflight electrical-stimulation method. When microstimulation (50-100 microA, single pulse) was applied to the SC during a saccade, a small, conjugate contraversive eye movement was evoked with latencies much shorter than those obtained by conventional stimulation. Our results may be explained by the tonic inhibition of premotor burst neurons (BNs) by omnipause neurons that ceases during saccades to allow BNs to burst. Thus, during saccades, signals originating from the SC can be transmitted to motoneurons and seen in the saccade trajectory. Based on this hypothesis, we estimated the number of synapses intervening between the SC and motoneurons by applying midflight stimulation to the SC, the BN area, and the abducens nucleus. Eye position signals were electronically differentiated to produce eye velocity to aid in detecting small changes. The mean latencies of the stimulus-evoked eye movements were: 7.9 +/- 1.0 ms (SD; ipsilateral eye) and 7.8 +/- 0.9 ms (SD; contralateral eye) for SC stimulation; 4.8 +/- 0.5 ms (SD; ipsilateral eye) and 5.1 +/- 0.7 ms (SD; contralateral eye) for BN stimulation; and 3.6 +/- 0.4 ms (SD; ipsilateral eye) and 5.2 +/- 0.8 ms (SD; contralateral eye) for abducens nucleus stimulation. The time difference between SC- and BN-evoked eye movements (about 3 ms) was consistent with a disynaptic connection from the SC to the premotor BNs.