Reliability of Signal Transfer at a Tonically Transmitting, Graded Potential Synapse of the Locust Ocellar Pathway

Abstract

We assessed the performance of a synapse that transmits small, sustained, graded potentials between two classes of second-order ocellar "L-neurons" of the locust. We characterized the transmission of both fixed levels of membrane potential and fluctuating signals by recording postsynaptic responses to changes in presynaptic potential. To ensure repeatability between stimuli, we controlled presynaptic signals with a voltage clamp. We found that the synapse introduces noise above the level of background activity in the postsynaptic neuron. By driving the presynaptic neuron with slow-ramp changes in potential, we found that the number of discrete signal levels the synapse transmits is ϳ20. It can also transmit ϳ20 discrete levels when the presynaptic signal is a graded rebound spike. Synaptic noise level is constant over the operating range of the synapse, which would not be expected if presynaptic potential set the probability for the release of individual quanta of neurotransmitter according to Poisson statistics. Responses to individual quanta of neurotransmission could not be resolved, which is consistent with a synapse that operates with large numbers of vesicles evoking small responses. When challenged with white noise stimuli, the synapse can transmit information at rates up to 450 bits/s, a performance that is sufficient to transmit natural signals about changes in illumination.

Sparse but specific temporal coding by spikes in an insect sensory-motor ocellar pathway

“…The skew in voltage level distribution was too great in two out of every three experiments for us to make reasonable estimates of information rates. As in our previous experiments on graded potentials in L-neurons (Simmons and de Ruyter van Steveninck, 2005), we estimated information by dividing the power spectral density of the mean signal in DNI by the mean of the power spectral densities of noise (Shannon and Weaver, 1949;de Ruyter van Steveninck and Laughlin, 1996). From Fig.4B, we estimate that the graded potential in DNI carries 85bitss -1 in response to fluctuating light, and we made similar estimates in four different experiments (range 72-85bitss -1 ).…”

“…From Fig.4B, we estimate that the graded potential in DNI carries 85bitss -1 in response to fluctuating light, and we made similar estimates in four different experiments (range 72-85bitss -1 ). This indicates that the information rate carried by graded potentials recorded from the cell body of the DNI is considerably less than the capacity of excitatory synaptic output connections made by Lneurons (Simmons and de Ruyter van Steveninck, 2005).…”

“…The information in a single spike, I spike , is the difference between these entropies, calculated as: (Brenner et al, 2000), where r(t) is the time varying spike rate, and r is the time-averaged spike rate. To analyze the information rate transmitted by graded potentials, we used the same method we used previously (Simmons and de Ruyter van Steveninck, 2005), based…”

“…We have previously estimated that Lneurons and the excitatory output synapses they make carry information at several hundred bits per scond (Simmons and de Ruyter van Steveninck, 2005), or about four to five times greater than the information carrying capacity of trains of spikes in the DNI axon. To gain some further insight into information transmission within the ocellar pathway, we estimated the rate of information carried in underlying graded potential of the DNI, recorded from its cell body (individual postsynaptic processes are too small for stable recordings).…”

“…A presynaptic L-neuron can carry approximately 300bitss -1 (Simmons and de Ruyter van Steveninck, 2005), which indicates a loss of 60-80% in information between a graded potential in an L-neuron and spikes in a DN neuron axon. A large part of this loss is attributable to the way the synapse is used in transmitting information about fluctuations in light.…”