Velocity response profiles of collicular neurons: parallel and convergent visual information channels

We have recorded from single neurons in the retinorecipient layers of the superior colliculus of the cat. We distinguished several functionally distinct groups of collicular neurons on the basis of their velocity response profiles to photic stimuli. The first group was constituted by cells responding only to photic stimuli moving at slow-to-moderate velocities across their receptive fields (presumably receiving strong excitatory W-type input but not, or only subthreshold, Y-type input). These cells were recorded throughout the stratum griseum superficiale and stratum opticum and constituted 50% of our sample. The second group of cells exhibited excitatory responses only at moderate and fast velocities (presumably receiving excitatory Y-type but not W-type input). These cells constituted only about 7% of the sample and were located principally in the lower stratum griseum superficiale. The third group of cells was constituted by cells excited over the entire range of velocities tested (1-2000 /s) and presumably received substantial excitatory input from both W- and Y-channels. These cells constituted almost 26% of our sample and were located in the lower stratum griseum superficiale, stratum opticum and the upper part of the stratum griseum intermediale. Overall, cells receiving excitatory Y-type input, i.e. the sum of group two and group three cells, constituted about a third of the sample and their excitatory discharge fields were significantly larger than those of cells receiving only W-type input. A fourth distinct group of collicular neurons was also constituted by cells responding over a wide range of stimulus velocities. These cells were excited by slowly moving stimuli, while fast-moving photic stimuli evoked purely suppressive responses. The excitatory discharge fields of these cells (presumably, indicating the spatial extent of the W-input) were located within much larger inhibitory fields, the extent of which presumably indicates the spatial extent of the Y-input. These low-velocity-excitatory/high-velocity-suppressive cells were recorded from the stratum griseum superficiale, stratum opticum and stratum griseum intermediale and constituted about 17% of the sample. The existence of low-velocity-excitatory/high-velocity-suppressive cells in the mammalian colliculus has not been previously reported. Low-velocity-excitatory/high-velocity-suppressive cells might play an important role in activating "fixation/orientation" and "saccade" premotor neurons recorded by others in the intermediate and deep collicular layers. Overall, in the majority (57%) of collicular neurons in our sample there was no indication of a convergence of W- and Y-information channels. However, in a substantial minority of collicular cells (about 43% of the sample) there was clear evidence of such convergence and about 40% of these (low-velocity-excitatory/high-velocity-suppressive cells) appear to receive excitatory input from the W-channel and inhibitory input from the Y-channel.