Ribbon synapses of tonically releasing sensory neurons must provide a large pool 
of releasable vesicles for sustained release, while minimizing spontaneous 
release in the absence of stimulation. Complexins are presynaptic proteins that 
may accomplish this dual task at conventional synapses by interacting with the 
molecular machinery of synaptic vesicle fusion at the active zone to retard 
spontaneous vesicle exocytosis yet facilitate release evoked by depolarization. 
However, ribbon synapses of photoreceptor cells and bipolar neurons in the 
retina express distinct complexin subtypes, perhaps reflecting the special 
requirements of these synapses for tonic release. To investigate the role of 
ribbon-specific complexins in transmitter release, we combined presynaptic 
voltage clamp, fluorescence imaging, electron microscopy, and behavioral assays 
of photoreceptive function in zebrafish. Acute interference with complexin 
function using a peptide derived from the SNARE-binding domain increased 
spontaneous synaptic vesicle fusion at ribbon synapses of retinal bipolar 
neurons without affecting release triggered by depolarization. Knockdown of 
complexin by injection of an antisense morpholino into zebrafish embryos 
prevented photoreceptor-driven migration of pigment in skin melanophores and 
caused the pigment distribution to remain in the dark-adapted state even when 
embryos were exposed to light. This suggests that loss of complexin function 
elevated spontaneous release in illuminated photoreceptors sufficiently to mimic 
the higher release rate normally associated with darkness, thus interfering with 
visual signaling. We conclude that visual system-specific complexins are 
required for proper illumination-dependent modulation of the rate of 
neurotransmitter release at visual system ribbon synapses.