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Electrotonic Coupling between Pyramidal Neurons in the Neocortex

Electrotonic couplings (i.e., electrical synapses or gap junctions) are fundamental to neuronal synchronization, and thus essential for many physiological functions and pathological disorders. Interneuron electrical synapses have been studied intensively. Although studies on electrotonic couplings b...

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Autores principales: Wang, Yun, Barakat, Amey, Zhou, Hongwei
Formato: Texto
Lenguaje:English
Publicado: Public Library of Science 2010
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2859939/
https://www.ncbi.nlm.nih.gov/pubmed/20436674
http://dx.doi.org/10.1371/journal.pone.0010253
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author Wang, Yun
Barakat, Amey
Zhou, Hongwei
author_facet Wang, Yun
Barakat, Amey
Zhou, Hongwei
author_sort Wang, Yun
collection PubMed
description Electrotonic couplings (i.e., electrical synapses or gap junctions) are fundamental to neuronal synchronization, and thus essential for many physiological functions and pathological disorders. Interneuron electrical synapses have been studied intensively. Although studies on electrotonic couplings between pyramidal cells (PCs) are emerging, particularly in the hippocampus, evidence is still rare in the neocortex. The electrotonic coupling of PCs in the neocortex is therefore largely unknown in terms of electrophysiological, anatomical and synaptological properties. Using multiple patch-clamp recording with differential interference contrast infrared videomicroscopy (IR-DIC) visualization, histochemical staining, and 3D-computer reconstruction, electrotonic coupling was recorded between close PCs, mainly in the medial prefrontal cortex as well as in the visual cortical regions of ferrets and rats. Compared with interneuron gap junctions, these electrotonic couplings were characterized by several special features. The recording probability of an electrotonic coupling between PCs is extremely low; but the junctional conductance is notably high, permitting the direct transmission of action potentials (APs) and even tonic firing between coupled neurons. AP firing is therefore perfectly synchronized between coupled PCs; Postjunctional APs and spikelets alternate following slight changes of membrane potentials; Postjunctional spikelets, especially at high frequencies, are summated and ultimately reach AP-threshold to fire. These properties of pyramidal electrotonic couplings largely fill the needs, as predicted by simulation studies, for the synchronization of a neuronal assembly. It is therefore suggested that the electrotonic coupling of PCs plays a unique role in the generation of neuronal synchronization in the neocortex.
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spelling pubmed-28599392010-04-30 Electrotonic Coupling between Pyramidal Neurons in the Neocortex Wang, Yun Barakat, Amey Zhou, Hongwei PLoS One Research Article Electrotonic couplings (i.e., electrical synapses or gap junctions) are fundamental to neuronal synchronization, and thus essential for many physiological functions and pathological disorders. Interneuron electrical synapses have been studied intensively. Although studies on electrotonic couplings between pyramidal cells (PCs) are emerging, particularly in the hippocampus, evidence is still rare in the neocortex. The electrotonic coupling of PCs in the neocortex is therefore largely unknown in terms of electrophysiological, anatomical and synaptological properties. Using multiple patch-clamp recording with differential interference contrast infrared videomicroscopy (IR-DIC) visualization, histochemical staining, and 3D-computer reconstruction, electrotonic coupling was recorded between close PCs, mainly in the medial prefrontal cortex as well as in the visual cortical regions of ferrets and rats. Compared with interneuron gap junctions, these electrotonic couplings were characterized by several special features. The recording probability of an electrotonic coupling between PCs is extremely low; but the junctional conductance is notably high, permitting the direct transmission of action potentials (APs) and even tonic firing between coupled neurons. AP firing is therefore perfectly synchronized between coupled PCs; Postjunctional APs and spikelets alternate following slight changes of membrane potentials; Postjunctional spikelets, especially at high frequencies, are summated and ultimately reach AP-threshold to fire. These properties of pyramidal electrotonic couplings largely fill the needs, as predicted by simulation studies, for the synchronization of a neuronal assembly. It is therefore suggested that the electrotonic coupling of PCs plays a unique role in the generation of neuronal synchronization in the neocortex. Public Library of Science 2010-04-26 /pmc/articles/PMC2859939/ /pubmed/20436674 http://dx.doi.org/10.1371/journal.pone.0010253 Text en Wang et al. http://creativecommons.org/licenses/by/4.0/ 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 author and source are properly credited.
spellingShingle Research Article
Wang, Yun
Barakat, Amey
Zhou, Hongwei
Electrotonic Coupling between Pyramidal Neurons in the Neocortex
title Electrotonic Coupling between Pyramidal Neurons in the Neocortex
title_full Electrotonic Coupling between Pyramidal Neurons in the Neocortex
title_fullStr Electrotonic Coupling between Pyramidal Neurons in the Neocortex
title_full_unstemmed Electrotonic Coupling between Pyramidal Neurons in the Neocortex
title_short Electrotonic Coupling between Pyramidal Neurons in the Neocortex
title_sort electrotonic coupling between pyramidal neurons in the neocortex
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2859939/
https://www.ncbi.nlm.nih.gov/pubmed/20436674
http://dx.doi.org/10.1371/journal.pone.0010253
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