The Impact of Multivesicular Release on the Transmission of Sensory Information by Ribbon Synapses

Abstract

The statistics of vesicle release determine how information is transferred at the synapse but the classical Poisson model of independent fusion does not hold at the first stages of vision and hearing. There, ribbon synapses encoding analogue signals can coordinate the release of two or more vesicles as a single event. The implications of such multivesicular release (MVR) for spike generation are not known. Here we investigate the hypothesis that MVR might provide advantages over Poisson synapses. We used leaky integrate-and-fire models incorporating the statistics of release measured experimentally from glutamatergic synapses of retinal bipolar cells and compared these with models assuming Poisson inputs constrained to operate at the same average rates. We find that MVR can increase the number of spikes generated per vesicle while reducing interspike intervals and latency to first spike. The combined effect was to increase the efficiency of information transfer (bits per spike) over a range of conditions mimicing retinal ganglion cells of different size. MVR was most advantageous in neurons with short time-constants and reliable synaptic inputs, when a lower degree of convergence was required to trigger spikes. In the special case of a single input driving a neuron with short time-constant, as occurs at the first synapse in hearing, MVR increased information transfer whenever spike generation required more than one vesicle. This study demonstrates how presynaptic integration of vesicles by MVR has the potential to compensate for less effective summation post-synaptically to increase the efficiency with which sensory information is transmitted.