In vitro whole-cell patch-clamp methods were used to examine the contribution of one component of intracollicular circuitry, the superficial gray layer, to the generation of bursts of action potentials that occur in the intermediate layer and that command head and eye movements in vivo. Applying a single brief (0.5 ms) pulse of current to the superficial layer of rat collicular slices evoked prolonged bursts of excitatory postsynaptic currents (EPSCs) in the cells of the intermediate layer. The EPSCs were sufficient to elicit bursts of action potentials that lasted as long as 300 ms and resembled presaccadic command bursts. To examine the contribution of neurons within the superficial layer to the production of these bursts, we determined how superficial neurons respond to the same current pulses that evoke bursts in the intermediate layer. Recordings from 61 superficial layer cells revealed 19 neurons that produced multiple action potentials following stimulation. Nine of these 19 neurons were wide- and narrow-field vertical cells, which are known to project to the intermediate layer and could contribute to producing the EPSC bursts. The remaining cells (n = 42) did not generate trains of action potentials and 21 of these showed only subthreshold potential changes in response to the stimulus. Our results indicate that most superficial cells do not directly contribute to production of the EPSC bursts, but a small number do have the properties necessary to provide a prolonged excitatory drive to the premotor neurons.