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The Journal of Neuroscience, October 13, 2004, 24(41):9076-9086; doi:10.1523/JNEUROSCI.2060-04.2004

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Cellular/Molecular
Optical Postsynaptic Measurement of Vesicle Release Rates for Hippocampal Synapses Undergoing Asynchronous Release during Train Stimulation

Yo Otsu^1,2 and Timothy H. Murphy^1,2,3

¹Kinsmen Laboratory and Brain Research Center, Departments of ²Psychiatry and ³Physiology, University of British Columbia, Vancouver, British Columbia, V6T 1Z3 Canada

Developing hippocampal neurons in microisland culture were found to undergo rapid depression of excitatory synaptic activity caused by consumption of their readily releasable pool (RRP) of vesicles in response to 20 Hz trains of stimulation. Associated with depression was a switch to an asynchronous release mode that maintained transmission at a high steady-state rate equivalent to 2.1 RRPs per second. We have applied postsynaptic Ca²⁺ imaging to directly monitor these asynchronous release events to estimate both the steady rate of transmitter release and the number of quanta within the RRP at individual hippocampal synapses. Based on the frequency of asynchronous release measured at individual synapses postsynaptically using Ca²⁺ imaging (5-17 sec after train stimulation) and with knowledge of the time course by which asynchronous release rates decay, we estimate that individual hippocampal synapses exhibit (in response to train stimulation) peak release rates of up to 21 quanta per second from an RRP that contains, on average, 10 quanta. Use-dependent block of evoked synaptic activity by MK-801 [(+)-5-methyl-10,11-dihydro-5H-dibenzo [a,d]cyclohepten-5,10-imine maleate] confirmed that synapses undergoing asynchronous release are not significantly different from the general population with regard to their composition of NMDA receptor and/or release probability. Given that high-frequency trains deplete the synapse of readily releasable quanta (and that these release rates can only be maintained for a few seconds), these high rates of asynchronous release likely reflect refilling of vesicles from a reserve pool and not necessarily the continuous action of a relatively slow clathrin- and endosome-dependent process.

Key words: calcium; dendrite; desynchronization; imaging; NMDA receptor; quantal

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Received May 27, 2004; revised August 31, 2004; accepted September 2, 2004.

This article has been cited by other articles:

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				M. R. Pagani, R. C. Reisin, and O. D. Uchitel Calcium signaling pathways mediating synaptic potentiation triggered by amyotrophic lateral sclerosis IgG in motor nerve terminals. J. Neurosci., March 8, 2006; 26(10): 2661 - 2672. [Abstract] [Full Text] [PDF]

				A. C. Ashton and Y. A. Ushkaryov Properties of Synaptic Vesicle Pools in Mature Central Nerve Terminals J. Biol. Chem., November 4, 2005; 280(44): 37278 - 37288. [Abstract] [Full Text] [PDF]

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