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Variable action potential backpropagation during tonic firing and low-threshold spike bursts in thalamocortical but not thalamic reticular nucleus neurons

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Connelly, WM ORCID: 0000-0002-0986-6260, Crunelli, V and Errington, AC 2017 , 'Variable action potential backpropagation during tonic firing and low-threshold spike bursts in thalamocortical but not thalamic reticular nucleus neurons' , Journal of Neuroscience, vol. 37, no. 21 , pp. 5319-5333 , doi: 10.1523/JNEUROSCI.0015-17.2017.

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Abstract

Backpropagating action potentials (bAPs) are indispensable in dendritic signaling. Conflicting Ca 2-imaging data and an absence ofdendritic recording data meansthatthe extent of backpropagation inthalamocortical (TC) andthalamic reticular nucleus (TRN) neuronsremains unknown. Because TRN neurons signal electrically through dendrodendritic gap junctions and possibly via chemical dendriticGABAergic synapses, as well as classical axonal GABA release, this lack of knowledge is problematic. To address this issue, we madetwo-photon targeted patch-clamp recordings from rat TC and TRN neuron dendrites to measure bAPs directly. These recordings revealthat “tonic”’ and low-threshold-spike (LTS) “burst” APs in both cell types are always recorded first at the soma before backpropagatinginto the dendrites while undergoing substantial distance-dependent dendritic amplitude attenuation. In TC neurons, bAP attenuationstrength 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. Tonicspikes have similar somatic half-widths to late burst spikes and undergo similar dendritic attenuation. In contrast, in TRN neurons, APproperties are unchanged between LTS bursts and tonic firing and, as a result, distance-dependent dendritic attenuation remainsconsistent across different firing modes. Therefore, unlike LTS-associated global electrical and calcium signals, the spatial influence ofbAP signaling in TC and TRN neurons is more restricted, with potentially important behavioral-state-dependent consequences forsynaptic integration and plasticity in thalamic neurons.

Item Type: Article
Authors/Creators:Connelly, WM and Crunelli, V and Errington, AC
Keywords: Vision, thalamus, synaptic integration, non-linear systems
Journal or Publication Title: Journal of Neuroscience
Publisher: Soc Neuroscience
ISSN: 0270-6474
DOI / ID Number: 10.1523/JNEUROSCI.0015-17.2017
Copyright Information:

Copyright 2017 Connelly et al. Licensed under Creative Commons Attribution 4.0 International (CC BY 4.0) https://creativecommons.org/licenses/by/4.0/

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