The performance of synapses that convey discrete graded potentials in an insect visual pathway

Synapses from nonspiking neurons transmit small graded changes in potential, but variability in their postsynaptic potential amplitudes has not been extensively studied. At synapses where the presynaptic signal is an all-or-none spike, the probabilistic manner of neurotransmitter release causes variation in the amplitudes of postsynaptic potentials. I have measured the reliability of the operation of synapses that convey small graded potentials between pairs of identified large, second-order neurons in the locust ocellar system. IPSPs are mediated by small rebound spikes, which are graded in amplitude, in the presynaptic neuron. A transfer curve plotting amplitudes of spikes against amplitudes of IPSPs has a characteristic S shape with a linear central portion where IPSP amplitude is between -0.2 and -0.6 as large as spike amplitude but shows appreciable scatter. Approximately half of the scatter is attributable to background noise, most of which originates in photoreceptors and persists in darkness. The remaining noise is intrinsic to the synapse itself and is usually 0.3-0.7 mV in amplitude. It limits the resolution with which two spike amplitudes can be distinguished from one another to approximately 2 mV and, because the linear part of the transfer curve occupies approximately 10 mV in spike amplitudes, limits the number of discrete signal levels that can be conveyed across the synapse to approximately five. The amplitude of the noise is constant throughout the synaptic operating range, which means it is unlikely that presynaptic membrane potential controls transmitter release by setting a single probability level for quantal release.