Efficient Transmission in the Blowfly Early Visual Synapses Through the Regularization of Vesicle Release

Abstract

Early studies of synaptic transmission by Bernard Katz and colleagues suggested that neurotransmitter release at graded-potential synapses occurs through statistically independent (i.e. Poissonian) quanta [1, 2]. Subsequent experimental work supported this framework [3]. However, these measurements were performed in vitro on relatively simple synapses and under non-physiological conditions, often converting spiking neurons into graded-potential neurons through the use of channel blockers. Relying on the conventional assumption that vesicle exocytosis follows a Poisson process, measurements of the contrast power transfer spectrum and noise power spectral density of large monopolar cells (LMCs) in the blowfly C. vicina imply a sustained vesicle release rate exceeding 105 vesicles per second per LMC. Given the physical dimensions of photoreceptors and synaptic vesicles, such a release rate appears physiologically implausible. If vesicle release is more temporally structured, low-frequency noise could be suppressed, substantially reducing the vesicle release rate required to account for experimental observations. The reduction of noise at low frequencies is especially advantageous given inputs such as photoreceptor signals which are already low-pass filtered. Visual activity generates substantial extracellular potentials within the lamina cartridge [4]. We propose that these extracellular potentials regulate vesicle release by modulating the voltage sensors that trigger exocytosis. We provide experimental evidence for the connection between currents driving the LMC and the extracellular potentials during visual activity, and demonstrate, using simple models, how effective "Poisson" rates are maximized due to vesicle regularization.