Activity-dependent development of synaptic varicosities at crayfish motor terminals

Tonically and phasically active crayfish motor terminals have well-characterized differences in synaptic physiology. During repetitive activation, the tonic terminals show facilitation and no depression, while the phasic terminals show dramatic synaptic fatigue. It has been proposed that this greater capacity for transmitter release from tonic terminals may be largely due to the presence of large synaptic varicosities along tonic terminals that contain large mitochondria, synapses, and numerous synaptic vesicles. In addition, a recent study indicates that in vivo tonic stimulation of a phasic terminal in young animals increases the fatigue resistance of the neuromuscular synapses and increases the number of synaptic varicosities, as well as the size of mitochondria and synapses. Because these previous morphological studies of crustacean motor terminals were performed using transmission electron microscopy, only short lengths of terminal were observed, and changes in synaptic varicosity frequency and size could not be thoroughly examined. In order to examine the synaptic varicosities along the terminal, motor terminals were injected with HRP, and the morphology of contrast-enhanced light microscopic images was examined. We report here that tonic terminals have much larger and more numerous synaptic varicosities than phasic terminals. In vivo stimulation of a phasic motoneuron results in an increase in the frequency of synaptic varicosities. This represents an increase in the total number of varicosities because terminal length appears to remain constant. These synaptic varicosities appear to form along preexisting terminals and persist for days after the final in vivo stimulation. The results indicate that the greater transmitter-releasing capabilities of tonic terminals compared to phasic terminals are due to their larger and more frequent synaptic varicosities. In addition, the development of these synaptic varicosities is activity dependent.