Reliability and Frequency Response of Excitatory Signals Transmitted to Different Types of Retinal Ganglion Cell

Abstract

The same visual stimulus evokes a different pattern of neural signals each time the stimulus is presented. Because this unreliability reduces visual performance, it is important to understand how it arises from neural circuitry. We asked whether different types of ganglion cell receive excitatory signals with different reliability and frequency content and, if so, how retinal circuitry contributes to these differences. If transmitter release is governed by Poisson statistics, the SNR of the postsynaptic currents (ratio of signal power to noise power) should grow linearly with quantal rate (qr), a prediction that we confirmed experimentally. Yet ganglion cells of the same type receive quanta at different rates. Thus to obtain a measure of reliability independent of quantal rate, we calculated the ratio SNR/qr, and found this measure to be type-specific. We also found type-specific differences in the frequency content of postsynaptic currents, although types whose dendrites branched at nearby levels of the inner plexiform layer (IPL) had similar frequency content. As a result, there was an orderly distribution of frequency response through the depth of the IPL, with alternating layers of broadband and high-pass signals. Different types of bipolar cell end at different depths of the IPL and provide excitatory synapses to ganglion cell dendrites there. Thus these findings indicate that a bipolar cell synapse conveys signals whose temporal message and reliability (SNR/qr) are determined by neuronal type. The final SNR of postsynaptic currents is set by the dendritic membrane area of a ganglion cell, which sets the numbers of bipolar cell synapses and thus the rate at which it receives quanta [SNR = qr × (SNR/qr)].