title: Intraglomerular lateral inhibition promotes spike timing variability in principal neurons of the olfactory bulb.
abstract: The activity of mitral and tufted cells, the principal neurons of the olfactory bulb, is modulated by several classes of interneurons. Among them, diverse periglomerular (PG) cell types interact with the apical dendrites of mitral and tufted cells inside glomeruli at the first stage of olfactory processing. We used paired recording in olfactory bulb slices and two-photon targeted patch-clamp recording in vivo to characterize the properties and connections of a genetically identified population of PG cells expressing enhanced yellow fluorescent protein (EYFP) under the control of the Kv3.1 potassium channel promoter. Kv3.1-EYFP(+) PG cells are axonless and monoglomerular neurons that constitute ∼30% of all PG cells and include calbindin-expressing neurons. They respond to an olfactory nerve stimulation with a short barrage of excitatory inputs mediated by mitral, tufted, and external tufted cells, and, in turn, they indiscriminately release GABA onto principal neurons. They are activated by even the weakest olfactory nerve input or by the discharge of a single principal neuron in slices and at each respiration cycle in anesthetized mice. They participate in a fast-onset intraglomerular lateral inhibition between principal neurons from the same glomerulus, a circuit that reduces the firing rate and promotes spike timing variability in mitral cells. Recordings in other PG cell subtypes suggest that this pathway predominates in generating glomerular inhibition. Intraglomerular lateral inhibition may play a key role in olfactory processing by reducing the similarity of principal cells discharge in response to the same incoming input.
authors.affiliation: Institut National de la Santé et de la Recherche Médicale Unité 1128, and Université Paris Descartes, 75006 Paris, France.
authors.forename: Marion
authors.initials: M
authors.lastname: Najac
authors.affiliation: Institut des Neurosciences Cellulaires et Intégratives, Centre National de la Recherche Scientifique, Unité Propre de Recherche 3212, Université de Strasbourg, 67084 Strasbourg, France, and.
authors.forename: Alvaro
authors.initials: A
authors.lastname: Sanz Diez
authors.affiliation: Computational Biology, School of Computer Science and Communication, Royal Institute of Technology, Stockholm, SE-110 40, Sweden.
authors.forename: Arvind
authors.identifier: http://orcid.org/0000-0002-8044-9195
authors.initials: A
authors.lastname: Kumar
authors.affiliation: Institut des Neurosciences Cellulaires et Intégratives, Centre National de la Recherche Scientifique, Unité Propre de Recherche 3212, Université de Strasbourg, 67084 Strasbourg, France, and.
authors.forename: Nuria
authors.initials: N
authors.lastname: Benito
authors.affiliation: Institut National de la Santé et de la Recherche Médicale Unité 1128, and Université Paris Descartes, 75006 Paris, France, desaintjan@inci-cnrs.unistra.fr serge.charpak@parisdescartes.fr.
authors.forename: Serge
authors.initials: S
authors.lastname: Charpak
authors.affiliation: Institut National de la Santé et de la Recherche Médicale Unité 1128, and Université Paris Descartes, 75006 Paris, France, Institut des Neurosciences Cellulaires et Intégratives, Centre National de la Recherche Scientifique, Unité Propre de Recherche 3212, Université de Strasbourg, 67084 Strasbourg, France, and desaintjan@inci-cnrs.unistra.fr serge.charpak@parisdescartes.fr.
authors.forename: Didier
authors.identifier: http://orcid.org/0000-0002-2459-9703
authors.initials: D
authors.lastname: De Saint Jan
mesh_terms: D000200:Action Potentials / Q000502:physiology*; D000818:Animals; D064092:Calbindin 1 / Q000378:metabolism; D003401:Creatine / Q000378:metabolism; D018691:Excitatory Amino Acid Antagonists / Q000494:pharmacology; D019706:Excitatory Postsynaptic Potentials / Q000187:drug effects; D005260:Female; D049452:Green Fluorescent Proteins / Q000235:genetics / Q000378:metabolism; D066298:In Vitro Techniques; D053444:Inhibitory Postsynaptic Potentials / Q000187:drug effects; D008297:Male; D051379:Mice; D008822:Mice, Transgenic; D009415:Nerve Net / Q000502:physiology*; D009433:Neural Inhibition / Q000502:physiology*; D009474:Neurons / Q000502:physiology*; D009830:Olfactory Bulb / Q000166:cytology*; D018408:Patch-Clamp Techniques; D051670:Shaw Potassium Channels / Q000235:genetics / Q000378:metabolism; D013997:Time Factors; D014446:Tyrosine 3-Monooxygenase / Q000378:metabolism
chemical_list: D064092:Calbindin 1; D018691:Excitatory Amino Acid Antagonists; C490839:Kcnc1 protein, mouse; D051670:Shaw Potassium Channels; C485184:enhanced green fluorescent protein; D049452:Green Fluorescent Proteins; D014446:Tyrosine 3-Monooxygenase; D003401:Creatine
keywords: glomerulus; inhibition; olfactory bulb; periglomerular cell