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The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks

During non-rapid eye movement sleep and certain types of anaesthesia, neurons in the neocortex and thalamus exhibit a distinctive slow (<1 Hz) oscillation that consists of alternating UP and DOWN membrane potential states and which correlates with a pronounced slow (<1 Hz) rhythm in the electr...

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Autores principales: Crunelli, Vincenzo, Errington, Adam C., Hughes, Stuart W., Tóth, Tibor I.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society Publishing 2011
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3173871/
https://www.ncbi.nlm.nih.gov/pubmed/21893530
http://dx.doi.org/10.1098/rsta.2011.0126
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author Crunelli, Vincenzo
Errington, Adam C.
Hughes, Stuart W.
Tóth, Tibor I.
author_facet Crunelli, Vincenzo
Errington, Adam C.
Hughes, Stuart W.
Tóth, Tibor I.
author_sort Crunelli, Vincenzo
collection PubMed
description During non-rapid eye movement sleep and certain types of anaesthesia, neurons in the neocortex and thalamus exhibit a distinctive slow (<1 Hz) oscillation that consists of alternating UP and DOWN membrane potential states and which correlates with a pronounced slow (<1 Hz) rhythm in the electroencephalogram. While several studies have claimed that the slow oscillation is generated exclusively in neocortical networks and then transmitted to other brain areas, substantial evidence exists to suggest that the full expression of the slow oscillation in an intact thalamocortical (TC) network requires the balanced interaction of oscillator systems in both the neocortex and thalamus. Within such a scenario, we have previously argued that the powerful low-threshold Ca(2+) potential (LTCP)-mediated burst of action potentials that initiates the UP states in individual TC neurons may be a vital signal for instigating UP states in related cortical areas. To investigate these issues we constructed a computational model of the TC network which encompasses the important known aspects of the slow oscillation that have been garnered from earlier in vivo and in vitro experiments. Using this model we confirm that the overall expression of the slow oscillation is intricately reliant on intact connections between the thalamus and the cortex. In particular, we demonstrate that UP state-related LTCP-mediated bursts in TC neurons are proficient in triggering synchronous UP states in cortical networks, thereby bringing about a synchronous slow oscillation in the whole network. The importance of LTCP-mediated action potential bursts in the slow oscillation is also underlined by the observation that their associated dendritic Ca(2+) signals are the only ones that inform corticothalamic synapses of the TC neuron output, since they, but not those elicited by tonic action potential firing, reach the distal dendritic sites where these synapses are located.
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spelling pubmed-31738712011-10-13 The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks Crunelli, Vincenzo Errington, Adam C. Hughes, Stuart W. Tóth, Tibor I. Philos Trans A Math Phys Eng Sci Articles During non-rapid eye movement sleep and certain types of anaesthesia, neurons in the neocortex and thalamus exhibit a distinctive slow (<1 Hz) oscillation that consists of alternating UP and DOWN membrane potential states and which correlates with a pronounced slow (<1 Hz) rhythm in the electroencephalogram. While several studies have claimed that the slow oscillation is generated exclusively in neocortical networks and then transmitted to other brain areas, substantial evidence exists to suggest that the full expression of the slow oscillation in an intact thalamocortical (TC) network requires the balanced interaction of oscillator systems in both the neocortex and thalamus. Within such a scenario, we have previously argued that the powerful low-threshold Ca(2+) potential (LTCP)-mediated burst of action potentials that initiates the UP states in individual TC neurons may be a vital signal for instigating UP states in related cortical areas. To investigate these issues we constructed a computational model of the TC network which encompasses the important known aspects of the slow oscillation that have been garnered from earlier in vivo and in vitro experiments. Using this model we confirm that the overall expression of the slow oscillation is intricately reliant on intact connections between the thalamus and the cortex. In particular, we demonstrate that UP state-related LTCP-mediated bursts in TC neurons are proficient in triggering synchronous UP states in cortical networks, thereby bringing about a synchronous slow oscillation in the whole network. The importance of LTCP-mediated action potential bursts in the slow oscillation is also underlined by the observation that their associated dendritic Ca(2+) signals are the only ones that inform corticothalamic synapses of the TC neuron output, since they, but not those elicited by tonic action potential firing, reach the distal dendritic sites where these synapses are located. The Royal Society Publishing 2011-10-13 /pmc/articles/PMC3173871/ /pubmed/21893530 http://dx.doi.org/10.1098/rsta.2011.0126 Text en This journal is © 2011 The Royal Society http://creativecommons.org/licenses/by/3.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Crunelli, Vincenzo
Errington, Adam C.
Hughes, Stuart W.
Tóth, Tibor I.
The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks
title The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks
title_full The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks
title_fullStr The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks
title_full_unstemmed The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks
title_short The thalamic low-threshold Ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 Hz) sleep oscillation in thalamocortical networks
title_sort thalamic low-threshold ca(2+) potential: a key determinant of the local and global dynamics of the slow (<1 hz) sleep oscillation in thalamocortical networks
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3173871/
https://www.ncbi.nlm.nih.gov/pubmed/21893530
http://dx.doi.org/10.1098/rsta.2011.0126
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