The global spike: conserved dendritic properties enable unique Ca2+ spike generation in low-threshold spiking neurons

Connelly, William M., Crunelli, Vincenzo ORCID: https://orcid.org/0000-0001-7154-9752 and Errington, Adam C. ORCID: https://orcid.org/0000-0002-2171-389X 2015. The global spike: conserved dendritic properties enable unique Ca2+ spike generation in low-threshold spiking neurons. Journal of Neuroscience 35 (47) , pp. 15505-15522. 10.1523/JNEUROSCI.2740-15.2015

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Abstract

Low-threshold Ca2+ spikes (LTS) are an indispensible signaling mechanism for neurons in areas including the cortex, cerebellum, basal ganglia, and thalamus. They have critical physiological roles and have been strongly associated with disorders including epilepsy, Parkinson's disease, and schizophrenia. However, although dendritic T-type Ca2+ channels have been implicated in LTS generation, because the properties of low-threshold spiking neuron dendrites are unknown, the precise mechanism has remained elusive. Here, combining data from fluorescence-targeted dendritic recordings and Ca2+ imaging from low-threshold spiking cells in rat brain slices with computational modeling, the cellular mechanism responsible for LTS generation is established. Our data demonstrate that key somatodendritic electrical conduction properties are highly conserved between glutamatergic thalamocortical neurons and GABAergic thalamic reticular nucleus neurons and that these properties are critical for LTS generation. In particular, the efficiency of soma to dendrite voltage transfer is highly asymmetric in low-threshold spiking cells, and in the somatofugal direction, these neurons are particularly electrotonically compact. Our data demonstrate that LTS have remarkably similar amplitudes and occur synchronously throughout the dendritic tree. In fact, these Ca2+ spikes cannot occur locally in any part of the cell, and hence we reveal that LTS are generated by a unique whole-cell mechanism that means they always occur as spatially global spikes. This all-or-none, global electrical and biochemical signaling mechanism clearly distinguishes LTS from other signals, including backpropagating action potentials and dendritic Ca2+/NMDA spikes, and has important consequences for dendritic function in low-threshold spiking neurons.

Item Type:	Article
Date Type:	Publication
Status:	Published
Schools:	Medicine Biosciences Neuroscience and Mental Health Research Institute (NMHRI)
Subjects:	R Medicine > RC Internal medicine > RC0321 Neuroscience. Biological psychiatry. Neuropsychiatry
Additional Information:	This is an Open Access article distributed under the terms of the Creative Commons Attribution License Creative Commons Attribution 4.0 International, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.
Publisher:	Society for Neuroscience
ISSN:	1529-2401
Funders:	Wellcome
Date of First Compliant Deposit:	30 March 2016
Date of Acceptance:	27 September 2015
Last Modified:	07 May 2023 19:16
URI:	https://orca.cardiff.ac.uk/id/eprint/83423

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