Static and dynamic membrane properties of large-terminal bipolar cells from goldfish retina: experimental test of a...

Capacitance measurements allow direct studies of exocytosis and endocytosis in single synaptic terminals isolated from bipolar neurons of goldfish retina. Extending the technique to intact bipolar cells, with their more complex morphology, requires information about the cells' electrotonic architecture. To this end, we developed a compartment model of bipolar neurons isolated from goldfish retina and tested the model experimentally. The isolated cells retained morphology similar to that of bipolar neurons in intact goldfish retina. In whole cell recordings, current relaxations in response to 10-mV hyperpolarizing voltage pulses decayed with a biexponential time course. This suggests that the cells may be described by a two-compartment equivalent circuit with compartments corresponding to the soma/dendrites (6-10 pF) and synaptic terminal (2-4 pF), linked by the axial resistance (30-60 M omega) of the axon. Four lines of evidence validate the equivalent circuit. 1) Similar estimates of somatic/dendritic and terminal capacitance were obtained whether the patch pipette was attached to the soma or to the synaptic terminal. 2) Estimates of the capacitance of the two compartments in intact cells were similar to estimates from somata and terminals that were isolated by cleavage of the connecting axon. 3) When current transients were generated from a more complete computer simulation of a bipolar neuron, analysis of the simulated transients with the use of the simple two-compartment model yielded capacitance estimates similar to those used to set up the simulation. 4) In isolated cells, the model gave estimates of depolarization-evoked increases in capacitance of the synaptic terminal that were quantitatively similar to those measured in terminals that were detached from the rest of the cell. Although in previous studies researchers have attempted to apply a similar equivalent circuit to more geometrically complex cells, morphological correlates of the equivalent-circuit compartments have been elusive. Our results demonstrate that in dissociated bipolar cells, precise morphological correlates can be assigned to the equivalent-circuit compartments. Additionally, the work shows that time-resolved capacitance measurements of synaptic transmitter release are possible in intact, isolated bipolar neurons and may also be feasible in intact tissue.