The mammalian rod synaptic ribbon is essential for Ca_v channel facilitation and ultrafast fusion of the readily releasable pool of vesicles

Abstract

Rod photoreceptors (PRs) use ribbon synapses to transmit visual information. To signal ‘no light detected’ they release glutamate continually to activate post-synaptic receptors, and when light is detected glutamate release pauses. How a rod’s individual ribbon enables this process was studied here by recording evoked changes in whole-cell membrane capacitance from wild type and ribbonless (RIBEYE-ko) rods. Wild type rods created a readily releasable pool (RRP) of 92 synaptic vesicles (SVs) that emptied as a single kinetic phase with a τ < 0.4 msec. Lowering intracellular Ca²⁺-buffering accelerated Ca_v channel opening and facilitated release kinetics, but RRP size was unaltered. In contrast, ribbonless rods created an RRP of 24 SVs, and lacked Ca_v channel facilitation; however, Ca²⁺ channel-release coupling remained tight. The release deficits caused a sharp attenuation of rod-driven light responses measured from RIBEYE-ko mice. We conclude that the synaptic ribbon facilitates Ca²⁺-influx and establishes a large RRP of SVs.