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Comprehensive Connectivity of the Mouse Main Olfactory Bulb: Analysis and Online Digital Atlas

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Comprehensive Connectivity of the Mouse Main Olfactory Bulb: Analysis and Online Digital Atlas ORIGINAL RESEARCH ARTICLE published: 07 August 2012 NEUROANATOMY doi: 10.3389/fnana.2012.00030 Comprehensive connectivity of the mouse main olfactory bulb: analysis and online digital atlas Houri Hintiryan , Lin Gou , Brian Zingg , Seita Yamashita , Hannah M. Lyden , Monica Y. Song , Arleen K. Grewal , Xinhai Zhang , Arthur W. Toga and Hong-Wei Dong* Laboratory of Neuro Imaging, Department of Neurology, David Geffen School of Medicine, University of California, Los Angeles, Los Angeles, CA, USA Edited by: We introduce the first open resource for mouse olfactory connectivity data produced as Jorge A. Larriva-Sahd, Universidad part of the Mouse Connectome Project (MCP) at UCLA. The MCP aims to assemble a Nacional Autónoma de México, whole-brain connectivity atlas for the C57Bl/6J mouse using a double coinjection tracing Mexico method. Each coinjection consists of one anterograde and one retrograde tracer, which Reviewed by: Marco Aurelio M. Freire, Edmond affords the advantage of simultaneously identifying efferent and afferent pathways and and Lily Safra International Institute directly identifying reciprocal connectivity of injection sites. The systematic application for Neurosciences of Natal, Brazil of double coinjections potentially reveals interaction stations between injections and Juan Andrés De Carlos, Instituto allows for the study of connectivity at the network level. To facilitate use of the data, Cajal (Consejo Superior de Investigaciones Científicas), Spain raw images are made publicly accessible through our online interactive visualization *Correspondence: tool, the iConnectome, where users can view and annotate the high-resolution, Hong-Wei Dong, Laboratory of multi-fluorescent connectivity data (www.MouseConnectome.org). Systematic double Neuro Imaging, Department of coinjections were made into different regions of the main olfactory bulb (MOB) and data Neurology, David Geffen School of from 18 MOB cases (∼72 pathways; 36 efferent/36 afferent) currently are available to Medicine, University of California, Los Angeles, 635 Charles E. Young view in iConnectome within their corresponding atlas level and their own bright-field Drive South, Suite 225, Los cytoarchitectural background. Additional MOB injections and injections of the accessory Angeles, CA 90095-7334, USA. olfactory bulb (AOB), anterior olfactory nucleus (AON), and other olfactory cortical areas e-mail: [email protected] gradually will be made available. Analysis of connections from different regions of the MOB revealed a novel, topographically arranged MOB projection roadmap, demonstrated disparate MOB connectivity with anterior versus posterior piriform cortical area (PIR), and exposed some novel aspects of well-established cortical olfactory projections. Keywords: main olfactory bulb, piriform cortical area, lateral olfactory tract, online digital atlas, connectome, neural tract tracing Abbreviations: AAA, anterior amygdalar area; ACAd, anterior cingulate area, INTRODUCTION dorsal part; aco, anterior commissure, olfactory limb; AMd, anteromedial thala- mic nucleus, dorsal part; AOB, accessory olfactory bulb; AON, anterior olfactory In his pioneering work, Ramon y Cajal (1904) elegantly illus- nucleus; AONd, anterior olfactory nucleus, dorsal part; AONe, anterior olfac- trated the cytoarchitecture of the main olfactory bulb (MOB) tory nucleus, external part; AONm, anterior olfactory nucleus, medial part; and its general pathways to cortical destinations using the Golgi AONpv, anterior olfactory nucleus, posteroventral part; ARA, allen reference stain. Since then, olfactory pathways have been thoroughly exam- atlas; BA, bed nucleus of accessory olfactory tract; BDA, biotinylated dextran amine; BST, bed nuclei of stria terminalis; COAa, cortical amygdalar area, ante- ined using more advanced techniques, ranging from circuit rior part; COApl, cortical amygdalar area, posterior part, lateral zone; COApm, tracers to cell-type specific viral tracers (Cragg, 1961; Powell cortical amygdalar area, posterior part, medial zone; CTb, cholera toxin subunit et al., 1965; Price, 1973; Scalia and Winans, 1975; Shipley b; DP, dorsal peduncular area; ENT, entorhinal area; ENTl, entorhinal area, lat- and Adamek, 1984; Pro-Sistiaga et al., 2007; Yan et al., 2008; eral part; ENTm, entorhinal area, medial part; FG, Fluorogold; gr, granule cell; int, internal capsule; lot, lateral olfactory tract; lotd, lateral olfactory tract, dor- Nagayama et al., 2010; Miyamichi et al., 2011; Sosulski et al., 2011; sal part; MA, magnocellular nucleus; MCP, mouse connectome project; MEAav, for reviews see Haberly, 2001; Friedrich, 2011). Technological medial amygdalar area, anteroventral part; mi, mitral cell; MOB, main olfac- advancements also have improved presentation of neurocon- tory bulb; MOBgl, main olfactory bulb, glomerular layer; MOBgr, main olfactory bulb, granule layer; MOBipl, main olfactory bulb, inner plexiform layer; MOBmi, nectivity data. High cost and space limitations typically allow main olfactory bulb, mitral layer; MOBopl, main olfactory bulb, outer plexi- publication of figures depicting connectivity that is of most form layer; MOp, primary motor area; NLOT, nucleus of the lateral olfactory interest, precluding presentation of the majority of the data. tract; NT, NeuroTrace®; OSN, olfactory sensory neuron; OT, olfactory tubercle; Unfortunately, this provides only a partial view of the whole OTl, olfactory tubercle, lateral part; OTm, olfactory tubercle, medial part; PAA, piriform-amygdalar area; PHAL, Phaseolus vulgaris-leucoagglutinin; PIR, piriform picture. Presently, advanced imaging equipment and computer area; PIRa, piriform area, anterior part; PIR-OT, piriform-olfactory tubercle junc- technology have revolutionized neuroanatomy such that whole- tion; PIRp, piriform area, posterior part; py, pyramidal cell; RT, reticular nucleus of brain high-resolution images can be acquired and made publicly the thalamus; SSp, primary somatosensory area; SSs, supplemental somatosensory area; tf, tufted cell; TR, postpiriform transition area; TTd, taenia tecta, dor- accessible for world-wide use (Dong, 2007; Jones et al., 2011). sal part; TTv, taenia tecta, ventral part; VISC, visceral area; VNO, vomeronasal At the forefront of this new neuroanatomy era is the iCon- organ. necome, where systematically accumulated multi-fluorescent Frontiers in Neuroanatomy www.frontiersin.org August 2012 | Volume 6 | Article 30 | 1 Hintiryan et al. MOB connectivity analysis and atlas connectivity data can be accessed (www.MouseConnectome. CIRCUIT TRACING APPROACH org). Whole-brain coronal sections starting from rostral regions The Mouse Connectome Project (MCP) at UCLA aims to gen- of the olfactory bulb and extending to the caudal regions erate a connectivity map of the mouse brain using a dou- of the hindbrain are available for each case. For example, ble coinjection tracing strategy, which was first reported for olfactory cortical projections from the MOB and accessory olfac- studying neuronal connectivity in the rat (Thompson and tory bulbs (AOBs) extend long distances reaching the cau- Swanson, 2010). Each of the two non-overlapping coinjec- dal ends of the entorhinal cortical area (ENT) (Figures 1A–E). tions consists of one anterograde and one retrograde tracer. Coronal sections with all of the labeling from each injection Phaseolus vulgaris-leucoagglutinin (PHAL: anterograde: green) site are available in iConnectome and provide a comprehen- is coinjected with cholera toxin subunit b (CTb: retrograde: sive view of connections associated with each injected structure magenta) while biotinylated dextran amine (BDA: antero- (Figure 1E). grade: red) is coinjected with Fluorogold (FG: retrograde: gold) FIGURE 1 | Sagittal images of anterograde tracers Phaseolus to caudal regions of the brain (E; −0.955 to −3.88 mm from bregma). vulgaris-leucoagglutinin (PHAL; green) and biotinylated dextran Case numbers SW101215-02A (A); SW101213-01A (E). Scale bar, 1 mm amine (BDA; red) injections in MOB (A, magnified in B). Fibers originating (A,C);200µm (B,D). Abbreviations: MOB, main olfactory bulb; MOBgr, from MOB injections travel long distances across cortical olfactory areas (C). MOB granule layer; AOB, accessory olfactory bulb; PIR, piriform cortical Magnified image of fibers in (D) shows BDA fibers in AON, PIR, and lot. area; OT, olfactory tubercle; AON, anterior olfactory nucleus; PHAL, Note the decrease in BDA axons across the PIR-OT junction (C,D). Phaseolus vulgaris-leucoagglutinin; BDA, biotinylated dextran amine; NT, Whole-brain coronal sections of PHAL fibers from MOB traveling from rostral neurotrace blue. Frontiers in Neuroanatomy www.frontiersin.org August 2012 | Volume 6 | Article 30 | 2 Hintiryan et al. MOB connectivity analysis and atlas (Figure 2A). These double coinjections allow concurrent exam- The purpose of this publicly accessible connectivity data is to ination of input and output pathways from each injection help neuroscientists generate testable hypotheses regarding finer and yield four times the amount of data collected from clas- scale brain circuitry, brain function, behavior, and disease. Two sic single tracer injections, reducing cost, processing time, features that ease the analysis of the connectivity data are available and number of animals used. Coinjections also expose topo- in iConnectome. The first is a channel that allows each section to graphically distinct connectional patterns associated with the be viewed within its own bright-field Nissl cytoarchitectural back-
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