Parallel cone bipolar pathways to a ganglion cell use different rates and amplitudes of quantal excitation

Abstract

The cone signal reaches the cat's On-β (X) ganglion cell via several parallel circuits (bipolar cell types b1, b2, and b3). These circuits might convey different regions of the cone's temporal bandwidth. To test this, I presented a step of light that elicited a transient depolarization followed by a sustained depolarization. The contribution of bipolar cells to these response components was isolated by blocking action potentials with tetrodotoxin and by blocking inhibitory synaptic potentials with bicuculline and strychnine. Stationary fluctuation analysis of the sustained depolarization gave the rate of quantal bombardment: ~5100 quanta sec-1 for small central cells and ~45,000 quanta sec-1 for large peripheral cells. Normalizing these rates for the vastly different numbers of bipolar synapses (150-370 per small cell vs 2000 per large cell), quantal rate was constant across the retina, ~22 quanta synapse-1 sec-1. Nonstationary fluctuation analysis gave the mean quantal EPSP amplitude: ~240 μV for the transient depolarization and 30 μV for the sustained depolarization. The b1 bipolar cell is known from noise analysis of the On-α ganglion cell to have a near-maximal sustained release of only approximately two quanta synapse-1 sec-1. This implies that the other bipolar types (b2 and b3) contribute many more quanta to the sustained depolarization (≥46 synapse-1 sec-1). Type b1 probably contributes large quanta to the transient depolarization. Thus, bipolar cell types b1 and b2/b3 apparently constitute parallel circuits that convey, respectively, high and low frequencies.