Light regulation of Ca2+in the cone photoreceptor synaptic terminal

Abstract

AbstractRetinal cones are depolarized in darkness, keeping voltage-gated Ca2+channels open and sustaining exocytosis of synaptic vesicles. Light hyperpolarizes the membrane potential, closing Ca2+channels and suppressing exocytosis. Here, we quantify the Ca2+concentration in cone terminals, with Ca2+indicator dyes. Two-photon ratiometric imaging of fura-2 shows that global Ca2+averages ~360 nM in darkness and falls to ~190 nM in bright light. Depolarizing cones from their light to their dark membrane potential reveals hot spots of Ca2+that co-label with a fluorescent probe for the synaptic ribbon protein ribeye, consistent with tight localization of Ca2+channels near ribbons. Measurements with a low-affinity Ca2+indicator show that the local Ca2+concentration near the ribbon exceeds 4μM in darkness. The high level of Ca2+near the ribbon combined with previous estimates of the Ca2+sensitivity of release leads to a predicted dark release rate that is much faster than observed, suggesting that the cone synapse operates in a maintained state of synaptic depression in darkness.