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The Journal of Neuroscience, December 31, 2008, 28(53):14450-14458; doi:10.1523/JNEUROSCI.4245-08.2008

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Cellular/Molecular
Synaptic Vesicles in Mature Calyx of Held Synapses Sense Higher Nanodomain Calcium Concentrations during Action Potential-Evoked Glutamate Release

Lu-Yang Wang,^1,2,3 Erwin Neher,⁴ and Holger Taschenberger⁴

¹The Program for Neurosciences and Mental Health and ²Division of Neurology, The Hospital for Sick Children, and ³Department of Physiology, University of Toronto, Toronto, Ontario, Canada M5G 1X8, and ⁴Max Planck Institute for Biophysical Chemistry, D-37077 Göttingen, Germany

Correspondence should be addressed to either of the following: Lu-Yang Wang, Division of Neurology, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8, Email: luyang.wang{at}utoronto.ca; or Holger Taschenberger, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany, Email: holger.taschenberger{at}mpi-bpc.mpg.de

During development of the calyx of Held synapse, presynaptic action potentials (APs) become substantially faster and briefer. Nevertheless, this synapse is able to upregulate quantal output triggered by arriving APs. Briefer APs lead to less effective gating of voltage-gated Ca²⁺ channels (VGCCs). Therefore, mechanisms downstream of Ca²⁺ entry must effectively compensate for the attenuated Ca²⁺ influx associated with shorter APs in more mature calyces. This compensation could be achieved by tighter spatial coupling between VGCCs and synaptic vesicles, so that the latter are exposed to higher intracellular Ca²⁺ concentration ([Ca²⁺]_i). Alternatively or additionally, the Ca²⁺ sensitivity of the release apparatus may increase during synapse development. To differentiate between these possibilities, we combined paired patch-clamp recordings with Ca²⁺ imaging and flash photolysis of caged Ca²⁺ and estimated the [Ca²⁺]_i requirements for vesicle release in the developing mouse calyx of Held synapse. Surprisingly, the dose–response relationship between [Ca²⁺]_i and release rate was shifted slightly to the right in more mature calyces, rendering their vesicles slightly less sensitive to incoming Ca²⁺. Taking into account the time course and peak rates of AP-evoked release transients for the corresponding developmental stages, we estimate the local [Ca²⁺]_i"seen" by the Ca²⁺ sensors on synaptic vesicles to increase from 35 to 56 µM [from postnatal day 9 (P9)–P11 to P16–P19]. Our results reinforce the idea that developmental tightening of the spatial coupling between VGCCs and synaptic vesicles plays a predominant role in enhancing quantal output at this synapse and possibly other central synapses.

Key words: development; EPSC; MNTB; calyx of Held; Ca²⁺ uncaging; transmitter release

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Received Sept. 5, 2008; revised Nov. 26, 2008; accepted Nov. 30, 2008.

Correspondence should be addressed to either of the following: Lu-Yang Wang, Division of Neurology, The Hospital for Sick Children, 555 University Avenue, Toronto, Ontario, Canada M5G 1X8, Email: luyang.wang{at}utoronto.ca; or Holger Taschenberger, Max Planck Institute for Biophysical Chemistry, Am Fassberg 11, D-37077 Göttingen, Germany, Email: holger.taschenberger{at}mpi-bpc.mpg.de

This article has been cited by other articles:

				J. A. M. Lorteije, S. I. Rusu, C. Kushmerick, and J. G. G. Borst Reliability and Precision of the Mouse Calyx of Held Synapse J. Neurosci., November 4, 2009; 29(44): 13770 - 13784. [Abstract] [Full Text] [PDF]

				O. Kochubey, Y. Han, and R. Schneggenburger Developmental regulation of the intracellular Ca2+ sensitivity of vesicle fusion and Ca2+\#8211;secretion coupling at the rat calyx of Held J. Physiol., June 15, 2009; 587(12): 3009 - 3023. [Abstract] [Full Text] [PDF]

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