Synaptic circuitry mediating light-evoked signals in dark-adapted mouse retina

Abstract

Light-evoked excitatory cation current (Δ I C) and inhibitory chloride current (Δ I Cl) of rod and cone bipolar cells and AII amacrine cells (AIIACs) were recorded from slices of dark-adapted mouse retinas, and alpha ganglion cells were recorded from flatmounts of dark-adapted mouse retinas. The cell morphology was revealed by Lucifer yellow fluorescence with a confocal microscope. Δ I C of all rod depolarizing bipolar cells (DBC Rs) exhibited similar high sensitivity to 500 nm light, but two patterns of Δ I Cl were observed with slightly different axon morphologies. At least two types of cone depolarizing bipolar cells (DBC Cs) were identified: one with axon terminals ramified in 70–85% of IPL depth and DBC R-like Δ I C sensitivity, and the other with axon terminals ramified in 55–75% of IPL depth and much lower Δ I C sensitivity. The relative rod/cone inputs to DBCs and AIIACs were analyzed by comparing the Δ I C and Δ I Cl thresholds and dynamic ranges with the corresponding values of rods and cones. On average, the sensitivity of a DBC R to the 500 nm light is about 20 times higher than that of a rod. The sensitivity of an AIIAC is more than 1000 times higher than that of a rod, suggesting that AIIAC responses are pooled through a coupled network of about 40 AIIACs. Interactions of rod and cone signals in dark-adapted mouse retinas appear asymmetrical: rod signals spread into the cone system more efficiently than cone signals into the rod system. The mouse synaptic circuitry allows small rod signals to be highly amplified and effectively transmitted to the cone system via rod/cone and AIIAC/DBC C coupling. Three types of alpha ganglion cells (αGCs) were identified. (1) ONGCs exhibits no spike activity in darkness, increased spikes in light, sustained inward Δ I C, sustained outward Δ I Cl of varying amplitude, and large soma (20–25 μm in diameter) with an alpha-cell-like dendritic field about 180–350 μm stratifying near 70% of the IPL depth. (2) Transient OFFαGCs (tOFFαGCs) exhibit no spike activity in darkness, transient increased spikes at light offset, small sustained outward Δ I C in light, a large transient inward Δ I C at light offset, a sustained outward Δ I Cl, and a morphology similar to the ONαGCs except for that their dendrites stratified near 30% of the IPL depth. (3) Sustained OFFα GCs (sOFFαGCs) exhibit maintained spike activity of 5–10 Hz in darkness, sustained decrease of spikes in light, sustained outward Δ I C, sustained outward Δ I Cl, and a morphology similar to the tOFFαGCs. By comparing the response thresholds and dynamic ranges of αGCs with those of the pre-ganglion cells, our data suggest that the light responses of each type of αGCs are mediated by different sets of bipolar cells and amacrine cells.