The aim of this study was to determine the functional importance of intrinsic connections within the hamster's superior colliculus (SC) in the development of the visual responses of neurons in the deep layers of this nucleus. We used localized injections of lidocaine to block action potentials of fibers that passed through the superficial layers and injections of CoCl2 to block synaptic transmission in these layers. We also determined the morphology of a number of the deep layer cells recorded in these experiments by intracellular injection of HRP. Injection of lidocaine into the superficial layers completely abolished the visual- and/or optic chiasm-evoked responses of all 40 deep layer cells tested. Thus, fibers that either pass through or synapse in the superficial layers are necessary for the visual responses of deep layer neurons. Injections of CoCl2 restricted to the superficial layers significantly reduced the visual responsivity of 86% of 92 deep layer neurons tested and abolished the visual responses of 68% of these cells. Superficial layer injections of CoCl2 were equally effective in reducing the responses of neurons with dendrites that ascended into the superficial layers (all seven cells tested and recovered) and those of cells with dendrites restricted to the deep layers (six of seven cells tested and recovered). Injections of CoCl2 into the deep layers, in the region of the cell being recorded, significantly reduced the visual responses of 59% of 37 cells and abolished the visual responses of 40% of the neurons tested. Deep CoCl2 injections abolished the visual responses of three of four cells with dendrites restricted to the deep layers and only one of four cells with dendrites that ascended into the superficial layers. These results indicate that descending interlaminar axons from visually responsive superficial layer cells may be responsible for the visual responsivity of most neurons in the deep SC layers of hamster. Also, some deep layer neurons in this species may receive effective visual input through their dendrites that ascend into the superficial layers, where they are likely to be contacted by retinal axons or axon collaterals of superficial layer cells.