The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina

Summary: The canonical cortical microcircuit has principally been defined by interlaminar excitatory connections among the six layers of the neocortex. However, excitatory neurons in layer 6 (L6), a layer whose functional organization is poorly understood, form relatively rare synaptic connections w...

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Main Authors:	Jaclyn Ellen Frandolig, Chanel Joylae Matney, Kihwan Lee, Juhyun Kim, Maxime Chevée, Su-Jeong Kim, Aaron Andrew Bickert, Solange Pezon Brown
Format:	Article
Language:	English
Published:	Elsevier 2019-09-01
Series:	Cell Reports
Online Access:	http://www.sciencedirect.com/science/article/pii/S2211124719310964

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spelling	doaj-6569539573ae4b1c9bc96c4d7067833d2020-11-25T01:29:11ZengElsevierCell Reports2211-12472019-09-01281231313143.e5The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical SublaminaJaclyn Ellen Frandolig0Chanel Joylae Matney1Kihwan Lee2Juhyun Kim3Maxime Chevée4Su-Jeong Kim5Aaron Andrew Bickert6Solange Pezon Brown7Solomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Biochemistry, Cellular, and Molecular Biology Graduate Program, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USASolomon H. Snyder Department of Neuroscience, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Kavli Neuroscience Discovery Institute, Johns Hopkins University School of Medicine, Baltimore, MD 21205, USA; Corresponding authorSummary: The canonical cortical microcircuit has principally been defined by interlaminar excitatory connections among the six layers of the neocortex. However, excitatory neurons in layer 6 (L6), a layer whose functional organization is poorly understood, form relatively rare synaptic connections with other cortical excitatory neurons. Here, we show that the vast majority of parvalbumin inhibitory neurons in a sublamina within L6 send axons through the cortical layers toward the pia. These interlaminar inhibitory neurons receive local synaptic inputs from both major types of L6 excitatory neurons and receive stronger input from thalamocortical afferents than do neighboring pyramidal neurons. The distribution of these interlaminar interneurons and their synaptic connectivity further support a functional subdivision within the standard six layers of the cortex. Positioned to integrate local and long-distance inputs in this sublayer, these interneurons generate an inhibitory interlaminar output. These findings call for a revision to the canonical cortical microcircuit. : Frandolig et al. show that the neuronal composition and circuit organization differs between two distinct sublayers in layer 6a. Interlaminar parvalbumin inhibitory interneurons represent the major inhibitory interneuron in upper layer 6a, integrate local and thalamocortical inputs, and contribute an interlaminar inhibitory projection to the canonical cortical microcircuit. Keywords: neocortex, parvalbumin interneurons, corticothalamic neurons, corticocortical neurons, layer 6, thalamus, fast-spiking interneuronshttp://www.sciencedirect.com/science/article/pii/S2211124719310964
collection	DOAJ
language	English
format	Article
sources	DOAJ
author	Jaclyn Ellen Frandolig Chanel Joylae Matney Kihwan Lee Juhyun Kim Maxime Chevée Su-Jeong Kim Aaron Andrew Bickert Solange Pezon Brown
spellingShingle	Jaclyn Ellen Frandolig Chanel Joylae Matney Kihwan Lee Juhyun Kim Maxime Chevée Su-Jeong Kim Aaron Andrew Bickert Solange Pezon Brown The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina Cell Reports
author_facet	Jaclyn Ellen Frandolig Chanel Joylae Matney Kihwan Lee Juhyun Kim Maxime Chevée Su-Jeong Kim Aaron Andrew Bickert Solange Pezon Brown
author_sort	Jaclyn Ellen Frandolig
title	The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina
title_short	The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina
title_full	The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina
title_fullStr	The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina
title_full_unstemmed	The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina
title_sort	synaptic organization of layer 6 circuits reveals inhibition as a major output of a neocortical sublamina
publisher	Elsevier
series	Cell Reports
issn	2211-1247
publishDate	2019-09-01
description	Summary: The canonical cortical microcircuit has principally been defined by interlaminar excitatory connections among the six layers of the neocortex. However, excitatory neurons in layer 6 (L6), a layer whose functional organization is poorly understood, form relatively rare synaptic connections with other cortical excitatory neurons. Here, we show that the vast majority of parvalbumin inhibitory neurons in a sublamina within L6 send axons through the cortical layers toward the pia. These interlaminar inhibitory neurons receive local synaptic inputs from both major types of L6 excitatory neurons and receive stronger input from thalamocortical afferents than do neighboring pyramidal neurons. The distribution of these interlaminar interneurons and their synaptic connectivity further support a functional subdivision within the standard six layers of the cortex. Positioned to integrate local and long-distance inputs in this sublayer, these interneurons generate an inhibitory interlaminar output. These findings call for a revision to the canonical cortical microcircuit. : Frandolig et al. show that the neuronal composition and circuit organization differs between two distinct sublayers in layer 6a. Interlaminar parvalbumin inhibitory interneurons represent the major inhibitory interneuron in upper layer 6a, integrate local and thalamocortical inputs, and contribute an interlaminar inhibitory projection to the canonical cortical microcircuit. Keywords: neocortex, parvalbumin interneurons, corticothalamic neurons, corticocortical neurons, layer 6, thalamus, fast-spiking interneurons
url	http://www.sciencedirect.com/science/article/pii/S2211124719310964
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The Synaptic Organization of Layer 6 Circuits Reveals Inhibition as a Major Output of a Neocortical Sublamina

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