title: Canonical Organization of Layer 1 Neuron-Led Cortical Inhibitory and Disinhibitory Interneuronal Circuits.
abstract: Interneurons play a key role in cortical function and dysfunction, yet organization of cortical interneuronal circuitry remains poorly understood. Cortical Layer 1 (L1) contains 2 general GABAergic interneuron groups, namely single bouquet cells (SBCs) and elongated neurogliaform cells (ENGCs). SBCs predominantly make unidirectional inhibitory connections (SBC→) with L2/3 interneurons, whereas ENGCs frequently form reciprocal inhibitory and electric connections (ENGC↔) with L2/3 interneurons. Here, we describe a systematic investigation of the pyramidal neuron targets of L1 neuron-led interneuronal circuits in the rat barrel cortex with simultaneous octuple whole-cell recordings and report a simple organizational scheme of the interneuronal circuits. Both SBCs→ and ENGC ↔ L2/3 interneuronal circuits connect to L2/3 and L5, but not L6, pyramidal neurons. SBC → L2/3 interneuronal circuits primarily inhibit the entire dendritic-somato-axonal axis of a few L2/3 and L5 pyramidal neurons located within the same column. In contrast, ENGC ↔ L2/3 interneuronal circuits generally inhibit the distal apical dendrite of many L2/3 and L5 pyramidal neurons across multiple columns. Finally, L1 interneuron-led circuits target distinct subcellular compartments of L2/3 and L5 pyramidal neurons in a L2/3 interneuron type-dependent manner. These results suggest that L1 neurons form canonical interneuronal circuits to control information processes in both supra- and infragranular cortical layers.
authors.affiliation: Department of Pharmacology Department of Biology.
authors.forename: Alice J
authors.initials: AJ
authors.lastname: Lee
authors.affiliation: Department of Pharmacology.
authors.forename: Guangfu
authors.initials: G
authors.lastname: Wang
authors.affiliation: Department of Pharmacology.
authors.forename: Xiaolong
authors.initials: X
authors.lastname: Jiang
authors.affiliation: Department of Pharmacology Department of Chemistry.
authors.forename: Seraphina M
authors.initials: SM
authors.lastname: Johnson
authors.affiliation: Department of Pharmacology Department of Psychology, School of Medicine and College of Arts and Sciences, University of Virginia, Charlottesville, VA 22908, USA.
authors.forename: Elizabeth T
authors.initials: ET
authors.lastname: Hoang
authors.affiliation: Department of Pharmacology.
authors.forename: Fabien
authors.initials: F
authors.lastname: Lanté
authors.affiliation: Department of Pharmacology.
authors.forename: Ruth L
authors.initials: RL
authors.lastname: Stornetta
authors.affiliation: Department of Pharmacology.
authors.forename: Mark P
authors.initials: MP
authors.lastname: Beenhakker
authors.affiliation: Department of Neurobiology and Key Laboratory of Medical Neurobiology of Chinese Ministry of Health, Zhejiang University School of Medicine, 388 Yu Hang Tang Road, Hangzhou 310058, PR China.
authors.forename: Ying
authors.initials: Y
authors.lastname: Shen
authors.affiliation: Department of Pharmacology Department of Neuroscience.
authors.forename: J
authors.initials: J
authors.lastname: Julius Zhu
mesh_terms: D000818:Animals; D005260:Female; D007395:Interneurons / Q000502:physiology* / Q000648:ultrastructure; D008297:Male; D008854:Microscopy, Electron; D009433:Neural Inhibition / Q000502:physiology*; D009434:Neural Pathways / Q000502:physiology / Q000648:ultrastructure; D018408:Patch-Clamp Techniques; D017966:Pyramidal Cells / Q000502:physiology / Q000648:ultrastructure; D017207:Rats, Sprague-Dawley; D013003:Somatosensory Cortex / Q000502:physiology* / Q000648:ultrastructure; D013569:Synapses / Q000502:physiology* / Q000648:ultrastructure; D046509:Tissue Culture Techniques; D014738:Vibrissae / Q000502:physiology
keywords: attention; circuits; cortex; disinhibition; inhibition; interneurons; salient selection