title: Behavior-dependent activity patterns of GABAergic long-range projecting neurons in the rat hippocampus.
abstract: Long-range glutamatergic and GABAergic projections participate in temporal coordination of neuronal activity in distributed cortical areas. In the hippocampus, GABAergic neurons project to the medial septum and retrohippocampal areas. Many GABAergic projection cells express somatostatin (SOM+) and, together with locally terminating SOM+ bistratified and O-LM cells, contribute to dendritic inhibition of pyramidal cells. We tested the hypothesis that diversity in SOM+ cells reflects temporal specialization during behavior using extracellular single cell recording and juxtacellular neurobiotin-labeling in freely moving rats. We have demonstrated that rare GABAergic projection neurons discharge rhythmically and are remarkably diverse. During sharp wave-ripples, most projection cells, including a novel SOM+ GABAergic back-projecting cell, increased their activity similar to bistratified cells, but unlike O-LM cells. During movement, most projection cells discharged along the descending slope of theta cycles, but some fired at the trough jointly with bistratified and O-LM cells. The specialization of hippocampal SOM+ projection neurons complements the action of local interneurons in differentially phasing inputs from the CA3 area to CA1 pyramidal cell dendrites during sleep and wakefulness. Our observations suggest that GABAergic projection cells mediate the behavior- and network state-dependent binding of neuronal assemblies amongst functionally-related brain regions by transmitting local rhythmic entrainment of neurons in CA1 to neuronal populations in other areas. © 2016 The Authors Hippocampus Published by Wiley Periodicals, Inc.
authors.affiliation: Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.|MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.|MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.
authors.forename: Linda
authors.identifier: 0000-0002-9942-4502
authors.initials: L
authors.lastname: Katona
authors.affiliation: MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.|MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.
authors.forename: Ben
authors.initials: B
authors.lastname: Micklem
authors.affiliation: Center for Brain Research, Medical University of Vienna, Vienna, A-1090, Austria.|Department of Biochemistry, Eötvös Loránd University, Budapest, 1117, Hungary.
authors.forename: Zsolt
authors.initials: Z
authors.lastname: Borhegyi
authors.affiliation: MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.
authors.forename: Daniel A
authors.initials: DA
authors.lastname: Swiejkowski
authors.affiliation: Center for Brain Research, Medical University of Vienna, Vienna, A-1090, Austria.|Department of Neurophysiology and Neuropharmacology, Center for Physiology and Pharmacology, Medical University of Vienna, Vienna, 1090, Austria.
authors.forename: Ornella
authors.initials: O
authors.lastname: Valenti
authors.affiliation: Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.|MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.|MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.
authors.forename: Tim J
authors.initials: TJ
authors.lastname: Viney
authors.affiliation: MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.
authors.forename: Dimitrios
authors.initials: D
authors.lastname: Kotzadimitriou
authors.affiliation: MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.|Center for Brain Research, Medical University of Vienna, Vienna, A-1090, Austria.
authors.forename: Thomas
authors.initials: T
authors.lastname: Klausberger
authors.affiliation: Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3QT, UK.|MRC Anatomical Neuropharmacology Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.|MRC Brain Network Dynamics Unit, Department of Pharmacology, University of Oxford, Mansfield Road, Oxford, OX1 3TH, UK.|Center for Brain Research, Medical University of Vienna, Vienna, A-1090, Austria.
authors.forename: Peter
authors.initials: P
authors.lastname: Somogyi
mesh_terms: D000200:Action Potentials / Q000502:physiology; D000818:Animals; D001710:Biotin / Q000031:analogs & derivatives; D004567:Electrodes, Implanted; D059330:GABAergic Neurons / Q000166:cytology* / Q000502:physiology*; D006624:Hippocampus / Q000166:cytology* / Q000502:physiology*; D008297:Male; D009043:Motor Activity / Q000502:physiology*; D017207:Rats, Sprague-Dawley; D012815:Signal Processing, Computer-Assisted; D012890:Sleep / Q000502:physiology*; D013826:Theta Rhythm / Q000502:physiology; D014851:Wakefulness / Q000502:physiology
chemical_list: C070614:neurobiotin; D001710:Biotin
keywords: CA1; dendritic inhibition; sharp wave-ripples; somatostatin; theta oscillations