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Functional coupling of diverse voltage‐gated Ca 2+ channels underlies high fidelity of fast dendritic Ca 2+ signals during burst firing
Author(s) -
Jaafari Nadia,
Canepari Marco
Publication year - 2016
Publication title -
the journal of physiology
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.802
H-Index - 240
eISSN - 1469-7793
pISSN - 0022-3751
DOI - 10.1113/jp271830
Subject(s) - dendritic spike , apical dendrite , dendrite (mathematics) , dendritic spine , hippocampal formation , chemistry , biophysics , neuroscience , bapta , patch clamp , voltage gated ion channel , ion channel , physics , electrophysiology , soma , excitatory postsynaptic potential , calcium , biology , receptor , biochemistry , geometry , mathematics , organic chemistry
Key points In neurons, the Ca 2+ signal associated with the dendritic back‐propagating action potential codes a chemical message to the different dendritic sites, playing a crucial role in electrical signalling, synaptic transmission and synaptic plasticity. The study of the underlying Ca 2+ current, mediated by different types of voltage‐gated Ca 2+ channels, cannot be achieved by using the patch clamp technique. In this article, we used a recently developed cutting‐edge optical technique to investigate the physiological behaviour of local Ca 2+ currents along the apical dendrite of CA1 hippocampal pyramidal neurons. We directly measure, for the first time, the synergistic activation and deactivation of the diverse dendritic voltage‐gated Ca 2+ channels operating during bursts of back‐propagating action potentials to precisely control the Ca 2+ signal. We demonstrate that the Ca 2+ loss via high‐voltage‐activated channels is compensated by the Ca 2+ entry via the other channels translating in high fidelity of Ca 2+ signalling.Abstract In CA1 hippocampal pyramidal neurons, the dendritic Ca 2+ signal associated with somatic firing represents a fundamental activation code for several proteins. This signal, mediated by voltage‐gated Ca 2+ channels (VGCCs), varies along the dendrites. In this study, using a recent optical technique based on the low‐affinity indicator Oregon Green 488 BAPTA‐5N, we analysed how activation and deactivation of VGCCs produced by back‐propagating action potentials (bAPs) along the apical dendrite shape the Ca 2+ signal at different locations in CA1 hippocampal pyramidal neurons of the mouse. We measured, at multiple dendritic sites, the Ca 2+ transients and the changes in membrane potential associated with bAPs at 50 μs temporal resolution and we estimated the kinetics of the Ca 2+ current. We found that during somatic bursts, the bAPs decrease in amplitude along the apical dendrite but the amplitude of the associated Ca 2+ signal in the initial 200 μm dendritic segment does not change. Using a detailed pharmacological analysis, we demonstrate that this effect is due to the perfect compensation of the loss of Ca 2+ via high‐voltage‐activated (HVA) VGCCs by a larger Ca 2+ component via low‐voltage‐activated (LVA) VGCCs, revealing a mechanism coupling the two VGCC families of K + channels. More distally, where the bAP does not activate HVA‐VGCCs, the Ca 2+ signal is variable during the burst. Thus, we demonstrate that HVA‐ and LVA‐VGCCs operate synergistically to stabilise Ca 2+ signals associated with bAPs in the most proximal 200 μm dendritic segment.