Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses

Yildirim Sara, Marina G. Mozhayeva, Xinran Liu, Ege T. Kavalali

Research output: Contribution to journalArticle

106 Citations (Scopus)

Abstract

High-frequency induced short-term synaptic depression is a common feature of central synapses in which synaptic responses rapidly decrease to a sustained level. A limitation in the availability of release-ready vesicles is thought to be a major factor underlying this phenomenon. Here, we studied the kinetics of vesicle reavailability and reuse during synaptic depression at hippocampal synapses. High-intensity stimulation of neurotransmitter release was induced by hyperosmolarity, high potassium, or action potential firing at 30 Hz to produce synaptic depression. Under these conditions, synaptic transmission rapidly depressed to a plateau level that was typically 10-40% of the initial response and persisted at this level for at least 5 min regardless of the developmental stage of synapses. This nondeclining phase of transmission was partly sustained by fast recycling and reuse of synaptic vesicles even after minutes of stimulation. Simultaneous electrical recording of postsynaptic responses and styryl dye destaining showed that after an initial round of exocytosis, vesicles were available for reuse with a delay between 1 and 3 sec during 30 Hz action potential or hypertonicity-induced stimulation. During these stimulation paradigms, there was a limited mobilization of vesicles from the reserve pool. During 10 Hz stimulation, however, the extent of vesicle reuse was minimal during the first 20 sec. These results suggest a role for fast vesicle recycling as a functional homeostatic mechanism that prevents vesicle depletion and maintains synaptic responses in the face of intense stimulation.

Original languageEnglish (US)
Pages (from-to)1608-1617
Number of pages10
JournalJournal of Neuroscience
Volume22
Issue number5
StatePublished - Mar 1 2002

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Recycling
Synaptic Transmission
Synapses
Action Potentials
Synaptic Vesicles
Exocytosis
Neurotransmitter Agents
Potassium
Coloring Agents

Keywords

  • Endocytosis
  • FM1-43
  • Hippocampal culture
  • Patch clamp
  • Synaptic depression
  • Synaptic vesicle recycling

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. / Sara, Yildirim; Mozhayeva, Marina G.; Liu, Xinran; Kavalali, Ege T.

In: Journal of Neuroscience, Vol. 22, No. 5, 01.03.2002, p. 1608-1617.

Research output: Contribution to journalArticle

Sara, Yildirim ; Mozhayeva, Marina G. ; Liu, Xinran ; Kavalali, Ege T. / Fast vesicle recycling supports neurotransmission during sustained stimulation at hippocampal synapses. In: Journal of Neuroscience. 2002 ; Vol. 22, No. 5. pp. 1608-1617.
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