Fatigue and recovery of transmission at the Mauthner fiber-giant fiber synapse of the hatchetfish

When the Mauthner fiber-giant fiber synapse of the hatchetfish is activated at gradually increasing frequencies, postsynaptic potentials (PSPs) in the giant fiber become progressively smaller, but complete failures of transmission are not observed even when PSP size is as small or smaller than miniature PSPs (mPSPs) simultaneously recorded. On the assumption of a Poisson distribution of amplitudes, calculations from the absence of failures and from variance suggest that guantum number remains at least as high as 5--10 and that quantal size is greatly reduced. During tetanic stimulation the frequency of mPSPs first increases and then decreases again, sometimes to a very low frequency. However, mPSP amplitude is reduced by no more than about 50%, which indicates that quanta giving rise to mPSPs come from a different population of vesicles than those comprising evoked PSPs. During rest following a tetanus, calculated quantal size in evoked PSPs recovers within several hundred milliseconds to mPSP size simultaneouly recorded. Most of this recovery time represents time for filling, since vesicles can be supplied at much higher rates during tetanic stimulation. After one second rest PSP amplitude exceeds threshold but recovery for later PSPs in a short train requires many minutes. The slowness of this recovery is consistent with the morphological demonstration of slow recovery of the vesicle population after depletion. These data are interpreted in terms of vesicle release, depletion and membrane recycling. Following depletion new vesicles are released after only partial filling which accounts for small quanta. Very small mPSPs are not seen because filling time is short compared to time for release as mPSPs. Since quantal size can be gradually reduced, release can interrupt filling, and filling and release sites are likely to be the same. The data in combination with the morphological observations support the hypothesis of vesicular release of transmitter and provide new evidence as to rates and sites for filling of vesicles.