Passive membrane properties and electrotonic signal processing in retinal rod bipolar cells

Abstract

Rod bipolar cells transmit visual signals from their dendrites, where they receive input from rod photoreceptors, to their axon terminals, where they synapse onto amacrine cells. Little is known, however, about the transmission and possible transformation of these signals. We have combined axon terminal recording in retinal slices, quantitative, light-microscopic morphological reconstruction and computer modelling to obtain detailed compartmental models of rat rod bipolar cells. Passive cable properties were estimated by directly fitting the current responses of the models evoked by voltage pulses to the physiologically recorded responses. At a holding potential of -60 mV, the average best-fit parameters were 1.1 microF cm(-2) for specific membrane capacitance (C(m)), 130 Omega cm for cytoplasmic resistivity (R(i)), and 24 kOmega cm(2) for specific membrane resistance (R(m)). The passive integration of excitatory and inhibitory synaptic inputs was examined by computer modelling with physiologically realistic synaptic conductance waveforms. For both transient and steady-state synaptic inhibition, the inhibitory effect was relatively insensitive to the location of the inhibition. For transient synaptic inhibition, the time window of effective inhibition depended critically on the relative timing of inhibition and excitation. The passive signal transmission between soma and axon terminal was examined by the electrotonic transform and quantified as the frequency-dependent voltage attenuation of sinusoidal voltage waveforms. For the range of parameters explored (axon diameter and length, R(i)), the lowest cutoff frequency observed was approximately 300 Hz, suggesting that realistic scotopic visual signals will be faithfully transmitted from soma to axon terminal, with minimal passive attenuation along the axon.