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The Topological Distribution of Olfactory Receptor Neuron Axons in The Yale University EliScholar – A Digital Platform for Scholarly Publishing at Yale Yale Medicine Thesis Digital Library School of Medicine 1996 The opt ological distribution of olfactory receptor neuron axons in the olfactory bulb glomeruli of the rat : a confocal microscopic study with DiI staining Jeffrey Marc Dembner Yale University Follow this and additional works at: http://elischolar.library.yale.edu/ymtdl Recommended Citation Dembner, Jeffrey Marc, "The opot logical distribution of olfactory receptor neuron axons in the olfactory bulb glomeruli of the rat : a confocal microscopic study with DiI staining" (1996). Yale Medicine Thesis Digital Library. 2518. http://elischolar.library.yale.edu/ymtdl/2518 This Open Access Thesis is brought to you for free and open access by the School of Medicine at EliScholar – A Digital Platform for Scholarly Publishing at Yale. It has been accepted for inclusion in Yale Medicine Thesis Digital Library by an authorized administrator of EliScholar – A Digital Platform for Scholarly Publishing at Yale. For more information, please contact [email protected]. YALE MEDICAL LIBRARY 3 9002 08676 1005 The Topological Distribution of Olfactory Receptor Neuron ;■ SIomeru'Hr of; ihe fiat;'JjS YALE UNIVERSITY CUSHING/WHITNEY MEDICAL LIBRARY Permission to photocopy or microfilm processing of this thesis for the purpose of individual scholarly consultation or reference is hereby granted by the author. This permission is not to be interpreted as affecting publication of this work or otherwise placing it in the public domain, and the author reserves all rights of ownership guaranteed under common law protection of unpublished manuscripts. Signature of Author Date Digitized by the Internet Archive in 2017 with funding from The National Endowment for the Humanities and the Arcadia Fund https://archive.org/details/topologicaldistrOOdemb The Topological Distribution of Olfactory Receptor Neuron Axons in the Olfactory Bulb Glomeruli of the Rat: A Confocal Microscopic Study with Dil Staining A Thesis Submitted to the Yale University School of Medicine in Partial Fulfillment of the Requirements for the Degree of Doctor of Medicine Jeffrey Marc Dembner YALE MfWr.M LIBRARY AUG 1 3 1996 \A£V TU3 4-YlZ y\ 1 ACKNOWLEDGMENTS Although the authorship of this thesis lists only one name, it would not have been produced without the support, advice, and guidance of a host of individuals, to whom I owe my thanks. I would especially like to thank Dr. Charles A. Greer who, with a zest for learning and discovery, conceived of the project outlined in this volume. I am grateful for the many hours of personal instruction he has provided me, for the countless times he was willing to review my results, and for offering his keen insight when the significance seemed obscure. Most importantly, I must acknowledge his willingness to act as a personal academic advisor during my four years at Yale, and especially when I was completing applications for a residency in neurosurgery. As I have told many others: I did not choose to study olfaction, I chose to work with Charlie. I have enjoyed my tenure in his lab, appreciated the opportunity to learn from him, and hope that the completion of this thesis compensates for my long and frequent periods of absence. I would also like to thank Chris Kaliszewski for the seemingly inexhaustible patience she has displayed in response to my endless questions about the location of materials. Similarly, my thanks go out to Dr. Bill Stewart who often found himself faced with my queries when Charlie could not be found. I am truly indebted to those individuals who guided me through Adobe Photoshop, Canvas, and the use of Photo-Mount, and without whom the figures contained in this document would never have come to fruition: Karl Kofitz, Artis Montague, and Kara Salvagno. In addition, Paul Kingston 11 must be credited for instructing me in the art of perspective, as depicted in Figure 8. Of course, I cannot forget the extreme patience shown by Jill Obata. Although I am sure it became exasperating, she only rarely protested when I would request that we go to the library to find just one more reference: "It will only take ten minutes. Just give me ten minutes." In addition, the trips to Staples and Tycos did not go without notice. Finally to Delores Montoya, your big smile and warm greeting were just what I needed when everything around me seemed to be going poorly. This study was supported in part by NIH NS10174 and DC00210 to Charles Greer. Ill ABSTRACT THE TOPOLOGICAL DISTRIBUTION OF OLFACTORY RECEPTOR NEURON AXONS IN THE OLFACTORY BULB GLOMERULI OF THE RAT: A CONFOCAL MICROSCOPIC STUDY WITH DII STAINING. Jeffrey M. Dembner and Charles A. Greer. Section of Neurosurgery, Department of Surgery, Yale University School of Medicine, New Haven, CT The olfactory system encompasses three anatomical sites. Initial detection begins in the posterior aspect of the nasal cavity where specialized olfactory receptor neurons transduce odorants into neural signals. These signals are then transmitted to the central nervous system where they undergo elaborate processing within spherical shaped regions of neuropil in the first relay station of the olfactory pathway, the olfactory bulb glomeruli. The resulting bulbar signal is then propagated to numerous cortical structures. Although the precise code employed by the olfactory system to discriminate between individual odorants remains to be elucidated, the existence of an odortopic map is supported by converging lines of evidence. The singularly unique pattern of activity across the glomerular layer of the olfactory bulb produced by a particular odorant appears to encode its identity. The activity of any single glomerulus thus represents the fundamental unit of this code. Furthering an understanding of olfactory processing, therefore, requires a detailed analysis of the anatomy of those processes contributing to the complex neuropil of the olfactory bulb glomerulus, especially that of the primary afferent projections from the neuroepithelium. It has been previously demonstrated in Golgi-impregnated specimen that single olfactory IV receptor neuron axons occupy only a limited region of the glomerular neuropil (Halasz and Greer, 1993). In the present study, we extend these findings by performing a confocal examination of the distribution of Dil stained axons and fascicles as they approach, penetrate, and arborize within glomeruli. Olfactory bulbs from two week old Sprague-Dawley rats were immersion fixed in 4% paraformaldehyde, implanted with 2-3 Dil crystals in the olfactory nerve layer, incubated at room temperature and in the dark for an average of 3.5 weeks, and cut transversely at 100pm with a vibratome. Thin optical images, 0.5-lgm, were then captured in series with a BioRad 600 confocal laser and reconstructed in two and three dimensions for analysis. Single axons were easily resolved and exhibited both en passant varicosities and terminal boutons among intraglomerular axonal collaterals, which ranged from 2-6. Consistent with Golgi-impregnated samples, individual axons appeared to arborize within only a small proportion of the glomerulus. Most significantly, fascicles of primary afferent axons were demonstrated to distribute within spatially restricted domains, rather than ramifying homogeneously throughout the glomerulus. The terminal arbors of olfactory receptor neuron axons from the same fascicle appear to colocalize within a limited region of the glomerular neuropil, mostly segregated from the terminal arbors of those axons from a different fascicle. In addition, the terminal arbors of primary afferent fibers appear to be concentrated in the peripheral shell of the glomerulus with few penetrating into the glomerular core. These data thus support a sub-compartmental organization of the olfactory bulb glomerulus. Glomerular sub-compartments may represent the segregation of parallel afferent pathways from the neuroepithelium to the olfactory bulb, or alternatively, could be involved in the individualized processing of differential odorant information within a single glomerulus. TABLE OF CONTENTS Introduction.1 Olfactory System I: General Overview and Anatomy.2 Olfactory Neuroepithelium: Histology, Cytology, and Odorant Transduction..2 Olfactory Bulb: Histology and Cytology.12 Cortical Substrates of Olfaction: Targets of the Lateral Olfactory Tract.23 Olfactory System II: Odorant Processing and Discrimination.23 Synaptic Architecture of the Olfactory Bulb: An Input-Output Processor.24 Discriminatory Code of the Olfactory System.29 Statement of Purpose.36 Materials and Methods.37 Results...45 General Anatomy of the Olfactory Bulb.45 Architecture and Topological Distribution of Single Primary Afferent Fibers.48 Fascicles of Olfactory Receptor Neuron Axons Target Specific Glomeruli.53 Topological Distribution of Fascicles of Olfactory Receptor Neuron Axons.56 Targeting by Olfactory Receptor Neuron Axons.63 Principal and Periglomerular Elements. ,68 VI Discussion......73 Dil Labeling with Confocal Analysis Offers Advantages Over Previous Studies....73 Confocal Analysis of Dil Staining.74 Corroborating Evidence for Sub-compartmentalization from Invertebrates.82 Parallel Pathways of Primary Afferent Projections to the Olfactory Bulb.86 Multiple Odorant Specificity within Individual Glomeruli.88 Conclusions. 93 References.94 Vll FIGURE INDEX Introduction Olfactory Neuroepithelium.4 Odorant Transduction Pathway.9 Olfactory Bulb: Cresyl-Violet Stain.14 Cyto-architecture of Sub-populations
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