The onset and vector of orienting behaviors, such as saccades, are controlled by commands that descend from a population of neurons in deep layers of the superior colliculus (dSC). In this study, to characterize the role of the collicular local circuitry that generates the spatiotemporal pattern of command activity in the dSC neuronal population, responses evoked by single-pulse electrical stimulation in superficial layers of the superior colliculus (sSC) were analyzed by a 64-channel field potential recording system (planar electrode, 8 x 8 pattern; 150 microm interelectrode spacing) in slices obtained from 16- to 22-d-old mice. A negative field potential with short latency and short duration spatially restricted to the recording sites in sSC was evoked adjacent to the stimulation site. After bath application of 10 mum bicuculline, the same stimulus induced a large negative field response with long duration that spread from sSC to dSC. The dSC potential initially showed a positive response, presumably because of reversal of the negative potential that originated in sSC, and then a long negative response that spread horizontally as far as 1 mm. These responses disappeared after application of an NMDA receptor antagonist, 2-amino-5-phosphonovelarate, indicating that NMDA receptors have an important role in the generation of these responses. Simultaneous whole-cell patch-clamp recordings showed that the long-lasting negative field potentials corresponded to the depolarization accompanying burst spike activity of SC neurons. The present study revealed an extensive excitatory network in the dSC that may contribute to the generation of activity by a large population of neurons that discharge before a saccade.
