Synaptic Ribbons Influence the Size and Frequency of Miniature-like Evoked Postsynaptic Currents

Nonspiking cells of several sensory systems respond to stimuli with graded changes in neurotransmitter release and possess specialized synaptic ribbons. Here, we show that manipulations to synaptic ribbons caused dramatic effects on mEPSC-like (mlEPSC) amplitude and frequency. Damage to rod-bipolar cell ribbons using fluorophore-assisted light inactivation resulted in the immediate reduction of mlEPSC amplitude and frequency, whereas the first evoked response after damage remained largely intact. The reduction in amplitude could not be recovered by increasing release frequency after ribbon damage. In parallel experiments, we looked at mlEPSCs from cones of hibernating ground squirrels, which exhibit dramatically smaller ribbons than awake animals. Fewer and smaller mlEPSCs were observed postsynaptic to cones from hibernating animals, although depolarized cones were able to generate larger mlEPSCs. Our results indicate that ribbon size may influence mlEPSC frequency and support a role for ribbons in coordinating multivesicular release. ► Acute ribbon damage reveals different vesicles for evoked release and tonic mlEPSCs ► Functional synaptic ribbons are necessary for multivesicular release ► Small ribbons in hibernating ground squirrels exhibit low tonic release rates ► Cones from hibernating animals retain capacity for multivesicular release Mehta et al. show that manipulations to synaptic ribbons, in ground squirrel cones and mouse rod-bipolar cells, influence the properties of miniature-like EPSCs. The results support a role for synaptic ribbons in setting release frequency and coordinating multivesicular release.