The mammalian superior colliculus (SC) is a midbrain structure that integrates multimodal sensory inputs and computes commands to initiate rapid eye movements. SC neurons burst with the sudden onset of a visual stimulus, followed by persistent activity that may underlie shifts of attention and decision making. Experiments in vitro suggest that circuit reverberations play a role in the burst activity in the SC, but the origin of persistent activity is unclear. In the present study we characterized an afterdepolarization (ADP) that follows action potentials in slices of rat SC. Population responses seen with voltage-sensitive dye imaging consisted of rapid spikes followed immediately by a second distinct depolarization of lower amplitude and longer duration. Patch-clamp recordings showed qualitatively similar behavior: in nearly all neurons throughout the SC, rapid spikes were followed by an ADP. Ionic and pharmacological manipulations along with experiments with current and voltage steps indicated that the ADP of SC neurons arises from Na(+) current that either persists or resurges following Na(+) channel inactivation at the end of an action potential. Comparisons of pharmacological properties and frequency dependence revealed a clear parallel between patch-clamp recordings and voltage imaging experiments, indicating a common underlying membrane mechanism for the ADP in both single neurons and populations. The ADP can initiate repetitive spiking at intervals consistent with the frequency of persistent activity in the SC. These results indicate that SC neurons have intrinsic membrane properties that can contribute to electrical activity that underlies shifts of attention and decision making.

The mammalian superior colliculus (SC) is a laminar midbrain structure that translates visual signals into commands to shift the focus of attention and gaze. The SC plays an integral role in selecting targets and ultimately generating rapid eye movements to those targets. In all mammals studied to date, neurons in the SC are arranged topographically such that the location of visual stimuli and the endpoints of orienting movements form organized maps in superficial and deeper layers, respectively. The organization of these maps is thought to underlie attentional priority by assessing which regions of the visual field contain behaviorally relevant information. Using voltage imaging and patch-clamp recordings in parasagittal SC slices from the rat, we found the synaptic circuitry of the visuosensory map in the SC imposes a strong bias. Voltage imaging of responses to electrical stimulation revealed more spread in the caudal direction than the rostral direction. Pharmacological experiments demonstrated that this asymmetry arises from GABAA receptor activation rostral to the site of stimulation. Patch-clamp recordings confirmed this rostrally directed inhibitory circuit and showed that it is contained within the visuosensory layers of the SC. Stimulation of two sites showed that initial stimulation of a caudal site can take priority over subsequent stimulation of a rostral site. Taken together, our data indicate that the circuitry of the visuosensory SC is hard-wired to give higher priority to more peripheral targets, and this property is conferred by a uniquely structured, dedicated inhibitory circuit.