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J Neurosci. 2017 May 10;37(19):4913-4927. doi: 10.1523/JNEUROSCI.0159-17.2017. Epub 2017 Apr 14.

Short-Term Facilitation at a Detonator Synapse Requires the Distinct Contribution of Multiple Types of Voltage-Gated Calcium Channels.

Author information

1
Quebec Mental Health Institute, Department of Psychiatry and Neuroscience, Université Laval, Quebec City, Quebec, G1J 2G3 Canada.
2
Quebec Mental Health Institute, Department of Psychiatry and Neuroscience, Université Laval, Quebec City, Quebec, G1J 2G3 Canada toth.katalin@crulrg.ulaval.ca.

Abstract

Neuronal calcium elevations are shaped by several key parameters, including the properties, density, and the spatial location of voltage-gated calcium channels (VGCCs). These features allow presynaptic terminals to translate complex firing frequencies and tune the amount of neurotransmitter released. Although synchronous neurotransmitter release relies on both P/Q- and N-type VGCCs at hippocampal mossy fiber-CA3 synapses, the specific contribution of VGCCs to calcium dynamics, neurotransmitter release, and short-term facilitation remains unknown. Here, we used random-access two-photon calcium imaging together with electrophysiology in acute mouse hippocampal slices to dissect the roles of P/Q- and N-type VGCCs. Our results show that N-type VGCCs control glutamate release at a limited number of release sites through highly localized Ca2+ elevations and support short-term facilitation by enhancing multivesicular release. In contrast, Ca2+ entry via P/Q-type VGCCs promotes the recruitment of additional release sites through spatially homogeneous Ca2+ elevations. Altogether, our results highlight the specialized contribution of P/Q- and N-types VGCCs to neurotransmitter release.SIGNIFICANCE STATEMENT In presynaptic terminals, neurotransmitter release is dynamically regulated by the transient opening of different types of voltage-gated calcium channels. Hippocampal giant mossy fiber terminals display extensive short-term facilitation during repetitive activity, with a large several fold postsynaptic response increase. Though, how giant mossy fiber terminals leverage distinct types of voltage-gated calcium channels to mediate short-term facilitation remains unexplored. Here, we find that P/Q- and N-type VGCCs generate different spatial patterns of calcium elevations in giant mossy fiber terminals and support short-term facilitation through specific participation in two mechanisms. Whereas N-type VGCCs contribute only to the synchronization of multivesicular release, P/Q-type VGCCs act through microdomain signaling to recruit additional release sites.

KEYWORDS:

mossy fiber; short-term plasticity; voltage-gated calcium channels

PMID:
28411270
DOI:
10.1523/JNEUROSCI.0159-17.2017
[Indexed for MEDLINE]
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