The temporal resolution of the visual system progressively increases with light intensity. Under scotopic conditions, temporal resolution is relatively poor, and may be limited by both retinal and cortical processes. Rod photoresponses themselves are quite slow because of the slowly deactivating biochemical cascade needed for light transduction. Here, we have used a transgenic mouse line with faster than normal rod phototransduction deactivation (RGS9-overexpressors) to test whether rod signaling to second-order retinal neurons is rate-limited by phototransduction or by other mechanisms. We compared electrical responses of individual wild-type and RGS9-overexpressing (RGS9-ox) rods to steady illumination and found that RGS9-ox rods required 2-fold brighter light for comparable activation, owing to faster G-protein deactivation. When presented with flickering stimuli, RGS9-ox rods showed greater magnitude fluctuations around a given steady-state current amplitude. Likewise, in vivo electroretinography (ERG) and whole-cell recording from OFF-bipolar, rod bipolar, and horizontal cells of RGS9-ox mice displayed larger than normal magnitude flicker responses, demonstrating an improved ability to transmit frequency information across the rod synapse. Slow phototransduction recovery therefore limits synaptic transmission of increments and decrements of light intensity across the first retinal synapse in normal retinas, apparently sacrificing temporal responsiveness for greater overall sensitivity in ambient light.