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The Journal of Neuroscience, December 26, 2007, 27(52):14286-14298; doi:10.1523/JNEUROSCI.4122-07.2007
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Cellular/Molecular
Quantitative Analysis of Calcium-Dependent Vesicle Recruitment and Its Functional Role at the Calyx of Held Synapse
Nobutake Hosoi,1 Takeshi Sakaba,2 andErwin Neher1 1Department of Membrane Biophysics and 2Research Group Biophysics of Synaptic Transmission, Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany
Correspondence should be addressed to Erwin Neher, Department of Membrane Biophysics, Max Planck Institute for Biophysical Chemistry, Am Fassberg, 37077 Göttingen, Germany. Email: eneher{at}gwdg.de
Recruitment of release-ready vesicles at synapses is one of the important factors, which determine dynamic properties of signaling between neurons in the brain. It has been shown that the rate of vesicle recruitment is accelerated by strong synaptic activity. An elevated concentration of calcium ions in the presynaptic terminal ([Ca2+]i) has been proposed to be responsible for this effect. However, the precise relationship between [Ca2+]i and recruitment has not been established yet, and the functional consequences of accelerated recruitment during synaptic activity have not been quantified experimentally. To probe the intracellular Ca2+ dependence of vesicle recruitment and to examine its functional role during trains of action potential (AP)-like stimuli, we monitored [Ca2+]i and synaptic responses simultaneously with paired recordings at the calyx of Held synapse. We found that a distinct, rapidly releasing vesicle pool is replenished with a rate that increases linearly with [Ca2+]i, without any apparent cooperativity. The slope factor for this increase is
1 pool/(µM·s). Blocking Ca2+-dependent recruitment specifically with a calmodulin binding peptide revealed that the steady-state EPSCs during 100 Hz AP-like trains were maintained through this Ca2+-dependent recruitment mechanism. Using a simple model of vesicle dynamics, we estimated that the recruitment rate accelerated 10-fold during the steady-state compared with the rate at resting [Ca2+]i. We could also demonstrate an approximate sixfold increase in release probability (facilitation) during the initial 5–15 AP-like stimuli of such trains in our experimental condition, regardless of EPSC depression.
Key words: vesicle recruitment; calcium; neurotransmitter release; vesicle pool; short-term plasticity; calyx of Held
Received Sept. 7, 2007; revised Oct. 29, 2007; accepted Oct. 29, 2007.
Correspondence should be addressed to Erwin Neher, Department of Membrane Biophysics, Max Planck Institute for Biophysical Chemistry, Am Fassberg, 37077 Göttingen, Germany. Email: eneher{at}gwdg.de
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