Miniature IPSCs in hippocampal granule cells are triggered by voltage-gated Ca^(2+) channels via microdomain coupling

S. Goswami, I. Bucurenciu, P.M. Jonas, Journal of Neuroscience 32 (2012) 14294–14304.


Journal Article | Published | English
Department
Abstract
The coupling between presynaptic Ca^(2+) channels and Ca^(2+) sensors of exocytosis is a key determinant of synaptic transmission. Evoked release from parvalbumin (PV)-expressing interneurons is triggered by nanodomain coupling of P/Q-type Ca^(2+) channels, whereas release from cholecystokinin (CCK)-containing interneurons is generated by microdomain coupling of N-type channels. Nanodomain coupling has several functional advantages, including speed and efficacy of transmission. One potential disadvantage is that stochastic opening of presynaptic Ca^(2+) channels may trigger spontaneous transmitter release. We addressed this possibility in rat hippocampal granule cells, which receive converging inputs from different inhibitory sources. Both reduction of extracellular Ca^(2+) concentration and the unselective Ca^(2+) channel blocker Cd^(2+) reduced the frequency of miniature IPSCs (mIPSCs) in granule cells by ~50%, suggesting that the opening of presynaptic Ca^(2+) channels contributes to spontaneous release. Application of the selective P/Q-type Ca^(2+) channel blocker ω-agatoxin IVa had no detectable effects, whereas both the N-type blocker ω-conotoxin GVIa and the L-type blocker nimodipine reduced mIPSC frequency. Furthermore, both the fast Ca^(2+) chelator BAPTA-AM and the slow chelator EGTA-AM reduced the mIPSC frequency, suggesting that Ca^(2+)-dependent spontaneous release is triggered by microdomain rather than nanodomain coupling. The CB_(1) receptor agonist WIN 55212-2 also decreased spontaneous release; this effect was occluded by prior application of ω-conotoxin GVIa, suggesting that a major fraction of Ca^(2+)-dependent spontaneous release was generated at the terminals of CCK-expressing interneurons. Tonic inhibition generated by spontaneous opening of presynaptic N- and L-type Ca^(2+) channels may be important for hippocampal information processing.
Publishing Year
Date Published
2012-10-10
Journal Title
Journal of Neuroscience
Acknowledgement
This work was supported by grants from the Deutsche Forschungsgemeinschaft (TR 3/B10, Leibniz program, GSC-4 Spemann Graduate School) and the European Union (European Research Council Advanced Grant).
Volume
32
Issue
41
Page
14294 - 14304
IST-REx-ID

Cite this

Goswami S, Bucurenciu I, Jonas PM. Miniature IPSCs in hippocampal granule cells are triggered by voltage-gated Ca^(2+) channels via microdomain coupling. Journal of Neuroscience. 2012;32(41):14294-14304. doi:10.1523/JNEUROSCI.6104-11.2012
Goswami, S., Bucurenciu, I., & Jonas, P. M. (2012). Miniature IPSCs in hippocampal granule cells are triggered by voltage-gated Ca^(2+) channels via microdomain coupling. Journal of Neuroscience, 32(41), 14294–14304. https://doi.org/10.1523/JNEUROSCI.6104-11.2012
Goswami, Sarit, Iancu Bucurenciu, and Peter M Jonas. “Miniature IPSCs in Hippocampal Granule Cells Are Triggered by Voltage-Gated Ca^(2+) Channels via Microdomain Coupling.” Journal of Neuroscience 32, no. 41 (2012): 14294–304. https://doi.org/10.1523/JNEUROSCI.6104-11.2012.
S. Goswami, I. Bucurenciu, and P. M. Jonas, “Miniature IPSCs in hippocampal granule cells are triggered by voltage-gated Ca^(2+) channels via microdomain coupling,” Journal of Neuroscience, vol. 32, no. 41, pp. 14294–14304, 2012.
Goswami S, Bucurenciu I, Jonas PM. 2012. Miniature IPSCs in hippocampal granule cells are triggered by voltage-gated Ca^(2+) channels via microdomain coupling. Journal of Neuroscience. 32(41), 14294–14304.
Goswami, Sarit, et al. “Miniature IPSCs in Hippocampal Granule Cells Are Triggered by Voltage-Gated Ca^(2+) Channels via Microdomain Coupling.” Journal of Neuroscience, vol. 32, no. 41, Society for Neuroscience, 2012, pp. 14294–304, doi:10.1523/JNEUROSCI.6104-11.2012.

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