PHYSIOLOGICAL-PROPERTIES OF NEURONS IN THE OPTIC LAYER OF THE RATS SUPERIOR COLLICULUS

We made intracellular recordings from 74 neurons in the optic layer of the rat superior colliculus (SC). Resting membrane potentials were -6 2.3 +/- 6.2 (SD) mV, and input resistances were 37.9 +/- 10.1 M Omega. Optic layer neurons had large sodium spikes (74.2 +/- 12.3 mV) with a n overshoot of 12 mV and a half-amplitude duration of 0.75 +/- 0.2 ms. Each sodium spike was followed by two afterhyperpolarizations (AHPs), one of short duration and one of longer duration, which were mediated by tetraethylammonium (TEA)-sensitive (I-C) or apamin-sensitive (I-AH P) calcium-activated potassium currents, respectively. Sodium spikes w ere also followed by an afterdepolarization (ADP), which was only reve aled when the AHPs were blocked by TEA or apamin. In response to hyper polarizing current pulses, optic layer neurons showed an inward rectif ication mediated by H channels. At the break of the current pulse, the re was a rebound low-threshold spike (LTS) with a short duration of <2 5 ms. The LTS usually induced two sodium spikes (doublet). Most optic layer neurons (84%) behaved as intrinsically bursting cells. They resp onded to suprathreshold depolarization with an initial burst (or doubl et) followed by a train of regular single spikes. The remaining 16% of cells acted as chattering cells with high-frequency gamma (20-80 Hz) rhythmic burst firing within a narrow range of depolarized potentials. The interburst frequency was voltage dependent and also time dependen t, i.e., showed frequency adaptation. Unmasking the ADP with either TE A or apamin converted all of the tested intrinsically bursting cells i nto chattering cells, indicating that the ADP played a crucial role in the generation of rhythmic burst firing. Optic layer neurons receive direct retinal excitation mediated by both N-methyl-D-aspartate (NMDA) and non-NMDA receptors. Optic tract (OT) stimulation also led to gamm a-aminobutyric acid-A (GABA(A)) receptor-mediated inhibition, the main effect of which was to curtail the excitatory response to retinal inp uts by shunting the excitatory postsynaptic current. Intracellular sta ining with biocytin showed that the optic layer neurons that we record ed from were mostly either wide-field vertical neurons or other cells with predominately superficially projecting dendrites. These cells wer e similar to calbindin immunoreactive cells seen in the optic layer. T he characteristics of these optic layer neurons, such as prominent AHP s, strong shunting effect of inhibition, and short-lasting LTS, sugges t that they respond transiently to retinal inputs. This is consistent with a function for these cells as the first relay station in the extr ageniculate visual pathway.