Synaptic transfer of rod signals to horizontal and bipolar cells in the retina of the toad (Bufo marinus).

1. Simultaneous intracellular recordings of responses to light flashes were obtained from rod-horizontal cell and rod-hyperpolarizing bipolar cell pairs in isolated retinae of the toad. The gain and temporal filtering of synaptic transfer were characterized throughout the rods' range of light responses. 2. Paired rod-horizontal cell and rod-bipolar cell responses to dim flashes (less than 0.4 Rh*, where Rh* denotes effective photoisomerizations per rod per flash) exhibited nearly the same time course. Analysis of the onset of the horizontal cell responses revealed a temporal lag equivalent to a single stage of low-pass filtering (tau f = 75-200 ms). No filtering was discerned in the transfer of dim-flash responses from rods to bipolars. On average, horizontal cells were five times as sensitive (mV/Rh*) and hyperpolarizing bipolar cells 10.7 times as sensitive as their paired rods. 3. For brighter flashes, up to 1600 Rh*, the rising and return phases of bipolar responses appeared to be simple scaled versions of the rod responses. The scaling factor was equal to the ratio of flash sensitivities for dim flashes. Rod responses greater than about 2 mV produced a saturation of the bipolar cell response. 4. The return phases of the horizontal cell responses were kinetically similar, scaled versions of the rod responses for rod potentials less than about 5 mV. However, the rising phases lagged significantly behind those of the rod. The effective time constant of the lag increased proportionally with flash intensity. For the brighter flashes, the horizontal cell response peaked as much as a second after the rod response. 5. The linear scaling, minimal temporal filtering and saturation of the bipolar cell responses were satisfactorily reproduced by a model of synaptic transfer that assumed that the rate of transmitter release followed the rod voltage exponentially and that the postsynaptic conductance followed Michaelis-Menten saturation (Falk & Fatt, 1972). 6. The progressively longer lag in the horizontal cell responses to brighter flashes was satisfactorily simulated by a kinetically limited Falk and Fatt model which postulated that the effective electrical time constant of the horizontal cell membrane strongly depended on synaptic or voltage-modulated conductances. 7. Satisfactory model simulations of all postsynaptic responses required that an e-fold change in the release rate of transmitter from the rod be obtained with a 2 mV change in the rod potential.