S. Mennerick et al., STATIC AND DYNAMIC MEMBRANE-PROPERTIES OF LARGE-TERMINAL BIPOLAR CELLS FROM GOLDFISH RETINA - EXPERIMENTAL TEST OF A COMPARTMENT MODEL, Journal of neurophysiology, 78(1), 1997, pp. 51-62
Capacitance measurements allow direct studies of exocytosis and endocy
tosis in single synaptic terminals isolated from bipolar neurons of go
ldfish retina. Extending the technique to intact bipolar cells, with t
heir more complex morphology, requires information about the cells' el
ectrotonic 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 tha
t of bipolar neurons in intact goldfish retina. In whole cell recordin
gs, current relaxations in response to 10-mV hyperpolarizing voltage p
ulses decayed with a biexponential time course. This suggests that the
cells may be described by a two-compartment equivalent circuit with c
ompartments 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) S
imilar estimates of somatic/dendritic and terminal capacitance were ob
tained whether the patch pipette was attached to the soma or to the sy
naptic terminal. 2) Estimates of the capacitance of the two compartmen
ts in intact cells were similar to estimates from somata and terminals
that were isolated by cleavage of the connecting axon. 3) When curren
t transients were generated from a more complete computer simulation o
r a bipolar neuron, analysis of the simulated transients with the use
of the simple two-compartment model yielded capacitance estimates simi
lar 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 me
asured in terminals that were detached from the rest of the cell. Alth
ough 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 mor
phological correlates cane assigned to the equivalent-circuit compartm
ents. Additionally, the work shows that time-resolved capacitance meas
urements of synaptic transmitter release are possible in intact, isola
ted bipolar neurons and may also be feasible in intact tissue.