Abstract

Attention and target selection in the superior colliculus have been described as involving a winner-take-all (WTA) process in which the most salient stimulus suppresses the responses to other stimuli by as yet unknown anatomical connections. From recordings in the homologous structure in the pigeon, the optic tectum (TeO), we show that the WTA computation may be done in two compact, satellite structures comprising the nucleus isthmi pars parvocellularis (Ipc; parabigeminal in mammals) and pars magnocellularis (Imc), with the result fedback to TeO. The Ipc and the Imc nuclei are laminar structures reciprocally connected to TeO. Each Ipc neuron sends an axon to the same location of the tectum from which its visual inputs come, terminating in a cholinergic, columnar brush-like arborization. In contrast, Imc neurons make GABAergic, inhibitory, connections over most of Ipc and the tectum. Local visual stimulation triggers burst responses in Ipc neurons which can be recorded as large amplitude oscillatory bursts (OBs) at the homotopic locations in TeO. By recording burst responses in Ipc and tectal OBs in anaesthetized pigeons, we show that burst/OB responses evoked by visual stimulation of their receptive field can be totally suppressed by new stimuli (2 deg) presented in the visual field even at wide angular distances (80 deg). The suppressed burst responses at a given Ipc recording site are usually replaced by a high frequency oscillation of 500-600 Hz. Extracellular and intracellular recordings in Imc show that this high frequency activity corresponds to synchronized Imc neuronal firing triggered by the newly activated location and spread throughout Ipc by the Imc wide terminal fields. These results suggest that the isthmi-tectal network allows visual stimuli in one location to gain control of Ipc, the remainder being inhibited by Imc. This local Ipc activity may act, via the bursting paintbrush terminals in the tectum, as a focal beam of attention increasing the saliency of stimuli in the corresponding location in the visual field.