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The Journal of Neuroscience, August 17, 2005, 25(33):7529-7537; doi:10.1523/JNEUROSCI.1119-05.2005

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

Peter J. Simmons¹ and Rob de Ruyter van Steveninck²

¹School of Biology, Newcastle University, Newcastle upon Tyne NE1 7RU, United Kingdom, and ²Department of Physics, Indiana University Bloomington, Bloomington, Indiana 47405-7105

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 20. It can also transmit 20 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.

Key words: bit; visual; statistics; insect; information; voltage clamp

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Received March 22, 2005; revised June 30, 2005; accepted July 5, 2005.

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