PMID- 32312886 OWN - NLM STAT- MEDLINE DCOM- 20201007 LR - 20201007 IS - 1529-2401 (Electronic) IS - 0270-6474 (Print) IS - 0270-6474 (Linking) VI - 40 IP - 21 DP - 2020 May 20 TI - Synchronous Infra-Slow Oscillations Organize Ensembles of Accessory Olfactory Bulb Projection Neurons into Distinct Microcircuits. PG - 4203-4218 LID - 10.1523/JNEUROSCI.2925-19.2020 [doi] AB - The accessory olfactory system controls social and sexual behavior. In the mouse accessory olfactory bulb, the first central stage of information processing along the accessory olfactory pathway, projection neurons (mitral cells) display infra-slow oscillatory discharge with remarkable periodicity. The physiological mechanisms that underlie this default output state, however, remain controversial. Moreover, whether such rhythmic infra-slow activity patterns exist in awake behaving mice and whether such activity reflects the functional organization of the accessory olfactory bulb circuitry remain unclear. Here, we hypothesize that mitral cell ensembles form synchronized microcircuits that subdivide the accessory olfactory bulb into segregated functional clusters. We use a miniature microscope to image the Ca(2+) dynamics within the apical dendritic compartments of large mitral cell ensembles in vivo We show that infra-slow periodic patterns of concerted neural activity, indeed, reflect the idle state of accessory olfactory bulb output in awake male and female mice. Ca(2+) activity profiles are distinct and glomerulus-specific. Confocal time-lapse imaging in acute slices reveals that groups of mitral cells assemble into microcircuits that exhibit correlated Ca(2+) signals. Moreover, electrophysiological profiling of synaptic connectivity indicates functional coupling between mitral cells. Our results suggest that both intrinsically rhythmogenic neurons and neurons entrained by fast synaptic drive are key elements in organizing the accessory olfactory bulb into functional microcircuits, each characterized by a distinct default pattern of infra-slow rhythmicity.SIGNIFICANCE STATEMENT Information processing in the accessory olfactory bulb (AOB) plays a central role in conspecific chemosensory communication. Surprisingly, many basic physiological principles that underlie neuronal signaling in the AOB remain elusive. Here, we show that AOB projection neurons (mitral cells) form parallel synchronized ensembles both in vitro and in vivo Infra-slow synchronous oscillatory activity within AOB microcircuits thus adds a new dimension to chemosensory coding along the accessory olfactory pathway. CI - Copyright (c) 2020 Tsitoura et al. FAU - Tsitoura, Chryssanthi AU - Tsitoura C AUID- ORCID: 0000-0002-9856-0043 AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Malinowski, Sebastian T AU - Malinowski ST AUID- ORCID: 0000-0001-7877-5971 AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. AD - Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Mohrhardt, Julia AU - Mohrhardt J AUID- ORCID: 0000-0002-1939-7920 AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. AD - International Research Training Group 2150 The Neuroscience of Modulating Aggression and Impulsivity in Psychopathology, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Degen, Rudolf AU - Degen R AUID- ORCID: 0000-0002-8513-9030 AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. AD - Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, Aachen, D-52074, Germany. FAU - DiBenedictis, Brett T AU - DiBenedictis BT AD - Department of Biology, Boston University, Boston, Massachusetts 02115. FAU - Gao, Yuan AU - Gao Y AD - Department of Biology, Boston University, Boston, Massachusetts 02115. FAU - Watznauer, Katja AU - Watznauer K AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Gerhold, Kira AU - Gerhold K AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Nagel, Maximilian AU - Nagel M AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. AD - International Research Training Group 2150 The Neuroscience of Modulating Aggression and Impulsivity in Psychopathology, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Weber, Monika AU - Weber M AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Rothermel, Markus AU - Rothermel M AUID- ORCID: 0000-0002-0929-993X AD - Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, Aachen, D-52074, Germany. AD - Neuromodulation Group, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany. FAU - Hanganu-Opatz, Ileana L AU - Hanganu-Opatz IL AD - Developmental Neurophysiology, Center for Molecular Neurobiology, University Medical Center Hamburg-Eppendorf, Hamburg, D-20251, Germany. FAU - Ben-Shaul, Yoram AU - Ben-Shaul Y AUID- ORCID: 0000-0002-0407-4221 AD - Faculty of Medicine, Department of Medical Neurobiology, The Hebrew University of Jerusalem, Jerusalem 91120, Israel. FAU - Davison, Ian G AU - Davison IG AD - Department of Biology, Boston University, Boston, Massachusetts 02115. FAU - Spehr, Marc AU - Spehr M AUID- ORCID: 0000-0001-6616-4196 AD - Department of Chemosensation, Institute for Biology II, RWTH Aachen University, Aachen, D-52074, Germany m.spehr@sensorik.rwth-aachen.de. AD - Research Training Group 2416 MultiSenses-MultiScales, RWTH Aachen University, Aachen, D-52074, Germany. AD - International Research Training Group 2150 The Neuroscience of Modulating Aggression and Impulsivity in Psychopathology, RWTH Aachen University, Aachen, D-52074, Germany. LA - eng GR - R01 DC017234/DC/NIDCD NIH HHS/United States PT - Journal Article PT - Research Support, N.I.H., Extramural PT - Research Support, Non-U.S. Gov't PT - Research Support, U.S. Gov't, Non-P.H.S. DEP - 20200420 PL - United States TA - J Neurosci JT - The Journal of neuroscience : the official journal of the Society for Neuroscience JID - 8102140 SB - IM MH - Action Potentials/physiology MH - Animals MH - Mice MH - Nerve Net/*physiology MH - Neurons/*physiology MH - Olfactory Bulb/*physiology MH - Olfactory Pathways/*physiology PMC - PMC7244196 OTO - NOTNLM OT - accessory olfactory bulb OT - chemosensory coding OT - ensemble formation OT - mitral cells OT - neural oscillations OT - vomeronasal system EDAT- 2020/04/22 06:00 MHDA- 2020/10/08 06:00 PMCR- 2020/05/20 CRDT- 2020/04/22 06:00 PHST- 2019/12/09 00:00 [received] PHST- 2020/02/28 00:00 [revised] PHST- 2020/03/23 00:00 [accepted] PHST- 2020/04/22 06:00 [pubmed] PHST- 2020/10/08 06:00 [medline] PHST- 2020/04/22 06:00 [entrez] PHST- 2020/05/20 00:00 [pmc-release] AID - JNEUROSCI.2925-19.2020 [pii] AID - JN-RM-2925-19 [pii] AID - 10.1523/JNEUROSCI.2925-19.2020 [doi] PST - ppublish SO - J Neurosci. 2020 May 20;40(21):4203-4218. doi: 10.1523/JNEUROSCI.2925-19.2020. Epub 2020 Apr 20.