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

Abstract

(,r = 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.

Synaptic transmission at retinal ribbon synapses

“…These studies of synaptic gain, however, do not establish an underlying linear mechanism because the predictions using models based either on linear or higher-order relations between Ca 2+ influx and transmitter release do not differ greatly for small signals. With larger light-evoked voltage excursions, the sigmoidal relationship between I Ca and rod membrane potential becomes increasingly evident (Attwell et al, 1987;Wu, 1988;Belgum and Copenhagen, 1988;Witkovsky et al, 1997). Fig.…”

“…Amphibian cones show a smaller gain reduction with strong hyperpolarization than do rods and thus cones communicate efficiently with second-order neurons over a larger range of light levels than rods (Attwell et al, 1987;Wu, 1988;Belgum and Copenhagen, 1988;Witkovsky et al, 1997). Like rods, however, synaptic output from cones appears to be linearly related to I Ca (Witkovsky et al, 2001).…”

Lateral Gain Control in the Outer Retina Leads to Potentiation of Center Responses of Retinal Neurons

“…This gain reduction strictly depends on the cone membrane potential and most likely arises from the voltage dependence of the L-type Ca channels of the cones (Thoreson et al, 2003;Heidelberger et al, 2005). Attwell et al (1987) and Belgum and Copenhagen (1988) have described a similar phenomenon for rods.…”

Properties and functional roles of hyperpolarization‐gated currents in guinea‐pig retinal rods

“…The main reason is that the transient peak generated by Ih activation in response to bright light stimuli is clipped by the rod synapse (Attwell et al 1987;Witkovsky et al 1997). In addition, no bandpass amplification has previously been reported for signals transmitted through the rod-horizontal and rodhyperpolarizing bipolar synapses (Belgum & Copenhagen, 1988), which has been considered to be an indication of no filtering at the first stage of synaptic transmission in the retina. In the above work, however, the contribution of the current to voltage conversion was not investigated.…”

“…According to our data, inner segment conductances are modelled as an LRC circuit and confer bandpass amplification to the voltage generated in response to outersegment current injection. After this stage of bandpass amplification, synaptic transmission from rods to secondorder neurones is modelled by a stage of low-pass filtering (Belgum & Copenhagen, 1988). Activation of Ih may affect synaptic transmission by letting the voltage, which controls transmitter release by the rod synapse, recover to its dark level in advance of the dark current.…”