Depolarization Redistributes Synaptic Membrane and Creates a Gradient of Vesicles on the Synaptic Body at a Ribbon Synapse

• Published in: Neuron (Cambridge, Mass.) Mass.), 2002-11, Vol.36 (4), p.649-659
• Main Authors: Lenzi, David, Crum, John, Ellisman, Mark H, Roberts, William M
• Format: Article
• Language: English
• Subjects: Animals; Cell Size - drug effects; Cell Size - physiology; Cytoplasm; Cytoskeleton - drug effects; Cytoskeleton - physiology; Cytoskeleton - ultrastructure; Electric Stimulation; Exocytosis - drug effects; Exocytosis - physiology; Freshwater; Frogs; Hair; Hair Cells, Vestibular - drug effects; Hair Cells, Vestibular - physiology; Hair Cells, Vestibular - ultrastructure; Intracellular Membranes - drug effects; Intracellular Membranes - physiology; Intracellular Membranes - ultrastructure; Membrane Potentials - drug effects; Membrane Potentials - physiology; Microscopy, Electron; Protein Transport - drug effects; Protein Transport - physiology; Rana; Rana pipiens; saccule; Saccule and Utricle - physiology; Saccule and Utricle - ultrastructure; Sensory Receptor Cells - drug effects; Sensory Receptor Cells - physiology; Sensory Receptor Cells - ultrastructure; Signal Transduction - drug effects; Signal Transduction - physiology; Synaptic Membranes - drug effects; Synaptic Membranes - physiology; Synaptic Membranes - ultrastructure; Synaptic Transmission - drug effects; Synaptic Transmission - physiology; Synaptic Vesicles - drug effects; Synaptic Vesicles - physiology
• ISSN: 0896-6273; 1097-4199
• DOI: 10.1016/S0896-6273(02)01025-5

We used electron tomography of frog saccular hair cells to reconstruct presynaptic ultrastructure at synapses specialized for sustained transmitter release. Synaptic vesicles at inhibited synapses were abundant in the cytoplasm and covered the synaptic body at high density. Continuous maximal stimulation depleted 73% of the vesicles within 800 nm of the synapse, with a concomitant increase in surface area of intracellular cisterns and plasmalemmal infoldings. Docked vesicles were depleted 60%–80% regardless of their distance from the active zone. Vesicles on the synaptic body were depleted primarily in the hemisphere facing the plasmalemma, creating a gradient of vesicles on its surface. We conclude that formation of new synaptic vesicles from cisterns is rate limiting in the vesicle cycle.