Diverse inhibitory and excitatory mechanisms shape temporal tuning in transient OFF α ganglion cells in the rabbit retina

Key points: Neurons combine excitatory and inhibitory signals to perform computations. In the retina, interactions between excitation and inhibition enable neurons to detect specific visual features. We describe how several excitatory and inhibitory mechanisms work together to allow transient OFF α ganglion cells in the rabbit retina to respond selectively to high temporal frequencies and thus detect faster image motion. The weightings of these different mechanisms change with the contrast and spatiotemporal properties of the visual input, and thereby support temporal tuning in α cells over a range of visual conditions. The results help us understand how ganglion cells selectively integrate excitatory and inhibitory signals to extract specific information from the visual input. Abstract: The 20 to 30 types of ganglion cell in the mammalian retina represent parallel signalling pathways that convey different information to the brain. α ganglion cells are selective for high temporal frequencies in visual inputs, which makes them particularly sensitive to rapid motion. Although α ganglion cells have been studied in several species, the synaptic basis for their selective temporal tuning remains unclear. Here, we analyse excitatory synaptic inputs to transient OFF α ganglion cells (t-OFF α GCs) in the rabbit retina. We show that convergence of excitatory and inhibitory synaptic inputs within the bipolar cell terminals presynaptic to the t-OFF α GCs shifts the temporal tuning to higher temporal frequencies. GABAergic inhibition suppresses the excitatory input at low frequencies, but potentiates it at high frequencies. Crossover glycinergic inhibition and sodium channel activity in the presynaptic bipolar cells also potentiate high frequency excitatory inputs. We found differences in the spatial and temporal properties, and contrast sensitivities of these mechanisms. These differences in stimulus selectivity allow these mechanisms to generate bandpass temporal tuning of t-OFF α GCs over a range of visual conditions.