Temporal Transformation of the Rod Single-Photon Response in the Retinal Circuitry

The temporal sensitivity of rod vision is higher than expected based on slow single-photon responses produced by phototransduction in rod outer segments. We sought to establish the retinal basis for the temporal speeding of rod responses and their dependence on phototransduction.

We made patch-clamp recordings of photocurrent and photovoltage from rods and rod bipolar cells (RBCs), and loose-patch and voltage-clamp recordings from ON α retinal ganglion cells, in three mouse strains: wild-type (WT), rhodopsin hemizygotes (Rh+/-), and GCAPs-/-.

Single-photon responses from the three strains differed in the kinetics of their waveforms: Rh+/- were more rapid than WT and GCAPs-/- considerably slower. RBCs in all three strains decayed much faster than their respective rod current responses, and much of this transformation was the prior result of conversion of rod photocurrent to photovoltage. Light responses were further accelerated at the bipolar-cell synapse and in the inner plexiform layer, with the remarkable result that ganglion-cell EPSPs and spike output both nearly overlap in waveform from all three strains despite large differences in rod photocurrents. These kinetic alterations were mostly affected by linear filters at each step in integration, with some contribution also from nonlinear interactions especially apparent in the GCAPs-/- retina.

The retina extracts principally the initial phase of single-photon responses through a series of high-pass, largely linear filters at each integration stage. Much of this transformation occurs in the rods themselves, but important contributions are also made at the rod-to-RBC synapse and within the inner plexiform layer.