Implications of all-or-none synaptic transmission and short-term depression beyond vesicle depletion: A computational study

Victor Matveev, Xiao-Jing Wang

Research output: Contribution to journalArticle

Abstract

The all-or-none character of transmission at central synapses is commonly viewed as evidence that only one vesicle can be released per action potential at a single release site. This interpretation is still a matter of debate; its resolution is important for our understanding of the nature of quantal response. In this work we explore observable consequences of the univesicular release hypothesis by studying a stochastic model of synaptic transmission. We investigated several alternative mechanisms for the all-or- none response: (1) the univesicular release constraint realized through lateral inhibition across presynaptic membrane, (2) the constraint of a single releasable vesicle per active zone, and (3) the postsynaptic receptor saturation. We show that both the univesicular release constraint and the postsynaptic receptor saturation lead to a limited amount of depression by vesicle depletion, so that depletion alone cannot account for the strong paired-pulse depression observed at some cortical synapses. Although depression can be rapid if there is only one releasable vesicle per active zone, this scenario leads to a limit on the transmission probability. We evaluate additional mechanisms beyond vesicle depletion, and our results suggest that the strong paired-pulse depression may be a result of activity- dependent inactivation of the exocytosis machinery. Furthermore, we found that the statistical analysis of release events, in response to a long stimulus train, might allow one to distinguish experimentally between univesicular and multivesicular release scenarios. We show that without the univesicular release constraint, the temporal correlation between release events is always negative, whereas it is typically positive with such a constraint if the vesicle fusion probability is sufficiently large.

Original languageEnglish (US)
Pages (from-to)1575-1588
Number of pages14
JournalJournal of Neuroscience
Volume20
Issue number4
StatePublished - Feb 15 2000

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Synaptic Transmission
Synapses
Exocytosis
Action Potentials
Membranes

Keywords

  • Central synapse
  • Exocytosis
  • Receptor saturation
  • Short-term depression
  • Stochastic model
  • Univesicular release

ASJC Scopus subject areas

  • Neuroscience(all)

Cite this

Implications of all-or-none synaptic transmission and short-term depression beyond vesicle depletion : A computational study. / Matveev, Victor; Wang, Xiao-Jing.

In: Journal of Neuroscience, Vol. 20, No. 4, 15.02.2000, p. 1575-1588.

Research output: Contribution to journalArticle

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