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Featured ArticleArticles, Cellular/Molecular

The Global Spike: Conserved Dendritic Properties Enable Unique Ca2+ Spike Generation in Low-Threshold Spiking Neurons

William M. Connelly, Vincenzo Crunelli and Adam C. Errington
Journal of Neuroscience 25 November 2015, 35 (47) 15505-15522; DOI: https://doi.org/10.1523/JNEUROSCI.2740-15.2015
William M. Connelly
1Neuroscience Division, School of Biosciences, and
4Eccles Institute of Neuroscience, The John Curtin School of Medical Research, Australian National University, Canberra City, Australian Capital Territory 2600, Australia
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Vincenzo Crunelli
1Neuroscience Division, School of Biosciences, and
3Department of Physiology and Biochemistry, University of Malta, Msida MSD 2080, Malta, and
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Adam C. Errington
2Neuroscience and Mental Health Research Institute, School of Medicine, Cardiff University, Cardiff CF24 4HQ, United Kingdom,
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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.

SIGNIFICANCE STATEMENT Low-threshold Ca2+ spikes (LTS) are critical for important physiological processes, including generation of sleep-related oscillations, and are implicated in disorders including epilepsy, Parkinson's disease, and schizophrenia. However, the mechanism underlying LTS generation in neurons, which is thought to involve dendritic T-type Ca2+ channels, has remained elusive due to a lack of knowledge of the dendritic properties of low-threshold spiking cells. Combining dendritic recordings, two-photon Ca2+ imaging, and computational modeling, this study reveals that dendritic properties are highly conserved between two prominent low-threshold spiking neurons and that these properties underpin a whole-cell somatodendritic spike generation mechanism that makes the LTS a unique global electrical and biochemical signal in neurons.

  • dendrites
  • low-threshold spike
  • T-type Ca2+ channel
  • thalamic reticular nucleus
  • thalamocortical

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.

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The Journal of Neuroscience: 35 (47)
Journal of Neuroscience
Vol. 35, Issue 47
25 Nov 2015
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The Global Spike: Conserved Dendritic Properties Enable Unique Ca2+ Spike Generation in Low-Threshold Spiking Neurons
William M. Connelly, Vincenzo Crunelli, Adam C. Errington
Journal of Neuroscience 25 November 2015, 35 (47) 15505-15522; DOI: 10.1523/JNEUROSCI.2740-15.2015

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The Global Spike: Conserved Dendritic Properties Enable Unique Ca2+ Spike Generation in Low-Threshold Spiking Neurons
William M. Connelly, Vincenzo Crunelli, Adam C. Errington
Journal of Neuroscience 25 November 2015, 35 (47) 15505-15522; DOI: 10.1523/JNEUROSCI.2740-15.2015
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Keywords

  • dendrites
  • low-threshold spike
  • T-type Ca2+ channel
  • thalamic reticular nucleus
  • thalamocortical

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