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The Journal of Neuroscience, November 5, 2003, 23(31):10164-10173
 Previous Article
Cellular/Molecular
Two Modes of Vesicle Recycling in the Rat Calyx of Held
R. P. J. de Lange,1
A. D. G. de Roos,2 and
J. G. G. Borst1
1Department of Neuroscience, Erasmus MC, University Medical Center, 3000 DR Rotterdam, The Netherlands, and 2Swammerdam Institute for Life Sciences, University of Amsterdam, 1098 SM Amsterdam, The Netherlands
Vesicle recycling was studied in the rat calyx of Held, a giant brainstem terminal involved in sound localization. Stimulation of brain slices containing the calyx-type synapse with a high extracellular potassium ion concentration in the presence of horseradish peroxidase resulted within several minutes in a reduction of the number of neurotransmitter vesicles and in the appearance of labeled endosome-like structures. After returning to normal solution, the endosome-like structures disappeared over a period of several minutes, whereas simultaneously the number of labeled vesicles increased. A comparison with afferent stimulation suggested that the endosome-like structures normally do not participate in the vesicle cycle. Afferent stimulation at 5 Hz resulted in sustained synaptic transmission, without vesicle depletion but with an estimated endocytotic activity of <0.2 synaptic vesicles per active zone per second. At 20 Hz, the presynaptic action potentials generally failed during prolonged stimulation. In identified synapses, the number of vesicles labeled by photoconversion after stimulation at 5 Hz in the presence of the styryl dye RH414 was much lower than the number of vesicles that were released, as determined by measuring EPSCs. No more than  5% of the vesicles were labeled after 20 min stimulation at 5 Hz, whereas this stimulation protocol was sufficient to largely destain a terminal after previous loading.
The results support a scheme for recycling in which two different modes coexist. At physiological demands, a pool of 5% of all vesicles provides sufficient vesicles for release. During intense stimulation, such as occurs in the presence of high extracellular K+, the synapse resorts to bulk endocytosis, a very slow mode of recycling.
Key words: presynaptic; vesicle cycle; readily releasable pool; photoconversion; ultrastructure; styryl dye; EPSC
Received July 17, 2003;
revised September 18, 2003;
accepted September 19, 2003.
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|
|
|
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|
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|
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|
|
|
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|
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|
|
|
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|
|
|
|
|
|
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[Full Text]
[PDF]
|
|
|
|
|
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|
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26(22):
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[Full Text]
[PDF]
|
|
|
|
|
|
|
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572(3):
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[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
V. C. Wimmer, H. Horstmann, A. Groh, and T. Kuner
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[Full Text]
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|
|
|
|
|
|
|
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[Full Text]
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|
|
|
|
|
|
|
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[Full Text]
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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|
|
|
|
|
|
|
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|
|
|
|
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