Variable action potential backpropagation during tonic firing and low-threshold spike bursts in thalamocortical but not thalamic reticular nucleus 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 2017. Variable action potential backpropagation during tonic firing and low-threshold spike bursts in thalamocortical but not thalamic reticular nucleus neurons. Journal of Neuroscience 37 (21) , pp. 5319-5333. 10.1523/JNEUROSCI.0015-17.2017

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Abstract

Backpropagating action potentials (bAPs) are indispensable in dendritic signaling. Conflicting Ca2-imaging data and an absence of dendritic recording data means that the extent of backpropagation in thalamocortical (TC) and thalamic reticular nucleus (TRN) neurons remains unknown. Because TRN neurons signal electrically through dendrodendritic gap junctions and possibly via chemical dendritic GABAergic synapses, as well as classical axonal GABA release, this lack of knowledge is problematic. To address this issue, we made two-photon targeted patch-clamp recordings from rat TC and TRN neuron dendrites to measure bAPs directly. These recordings reveal that “tonic”’ and low-threshold-spike (LTS) “burst” APs in both cell types are always recorded first at the soma before backpropagating into the dendrites while undergoing substantial distance-dependent dendritic amplitude attenuation. In TC neurons, bAP attenuation strength varies according to firing mode. During LTS bursts, somatic AP half-width increases progressively with increasing spike number, allowing late-burst spikes to propagate more efficiently into the dendritic tree compared with spikes occurring at burst onset. Tonic spikes have similar somatic half-widths to late burst spikes and undergo similar dendritic attenuation. In contrast, in TRN neurons, AP properties are unchanged between LTS bursts and tonic firing and, as a result, distance-dependent dendritic attenuation remains consistent across different firing modes. Therefore, unlike LTS-associated global electrical and calcium signals, the spatial influence of bAP signaling in TC and TRN neurons is more restricted, with potentially important behavioral-state-dependent consequences for synaptic integration and plasticity in thalamic neurons.

Item Type:	Article
Date Type:	Publication
Status:	Published
Schools:	Biosciences Medicine Neuroscience and Mental Health Research Institute (NMHRI)
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 Trust, Wellcome Trust
Date of First Compliant Deposit:	5 May 2017
Date of Acceptance:	27 March 2017
Last Modified:	06 May 2023 00:18
URI:	https://orca.cardiff.ac.uk/id/eprint/100329

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