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Structure and Emergence of Specific Olfactory Glomeruli in the Mouse

Potter, Steve M. and Zheng, Chen and Koos, David S. and Feinstein, Paul and Fraser, Scott E. and Mombaerts, Peter (2001) Structure and Emergence of Specific Olfactory Glomeruli in the Mouse. Journal of Neuroscience, 21 (24). pp. 9713-9723. ISSN 0270-6474. PMCID PMC2570017. https://resolver.caltech.edu/CaltechAUTHORS:20160212-073756013

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Abstract

Olfactory sensory neurons (OSNs) expressing a given odorant receptor (OR) gene project their axons to a few specific glomeruli that reside at recognizable locations in the olfactory bulb. Connecting ∼1000 populations of OSNs to the ∼1800 glomeruli of the mouse bulb poses a formidable wiring problem. Additional progress in understanding the mechanisms of neuronal connectivity is dependent on knowing how these axonal pathways are organized and how they form during development. Here we have applied a genetic approach to this problem. We have constructed by gene targeting novel strains of mice in which either all OSNs or those that express a specific OR gene, M72 or M71, also produce green fluorescent protein (GFP) or a fusion of tau with GFP. We visualized OSNs and their axons in whole mounts with two-photon laser scanning microscopy. The main conclusion we draw from the three-dimensional reconstructions is the high degree of morphological variability of mature glomeruli receiving axonal input from OR-expressing OSNs and of the pathways taken by the axons to those glomeruli. We also observe that axons of OR-expressing OSNs do not innervate nearby glomeruli in mature mice. Postnatally, a tangle of axons from M72-expressing OSNs occupies a large surface area of the bulb and coalesces abruptly into a protoglomerulus at a reproducible stage of development. These results differ in several aspects from those reported for the development of glomeruli receiving input from OSNs expressing the P2 OR, suggesting the need for a more systematic examination of OR-specific glomeruli.


Item Type:Article
Related URLs:
URLURL TypeDescription
http://www.jneurosci.org/content/21/24/9713.shortPublisherArticle
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC2570017/PubMed CentralArticle
ORCID:
AuthorORCID
Fraser, Scott E.0000-0002-5377-0223
Additional Information:© 2001 Society for Neuroscience. For the first six months after publication SfN’s license will be exclusive. Beginning six months after publication the Work will be made freely available to the public on SfN’s website to copy, distribute, or display under a Creative Commons Attribution 4.0 International (CC BY 4.0) license (https://creativecommons.org/licenses/by/4.0/). Received July 2, 2001; revised Sept. 17, 2001; accepted Sept. 20, 2001. This work was supported by the Beckman Institute (S.M.P., D.S.K., S.E.F.), the National Institutes of Health (NIH) (S.M.P., S.E.F., P.M.), and the Human Frontier Science Program (P.M.). Postdoctoral fellowship support was provided by The Norman and Rosita Winston Foundation (C.Z.), Bristol-Myers Squibb, the Kirby Center for Sensory Neuroscience at The Rockefeller University (P.F.), and NIH (C.Z., P.F.). P.M. was an Alfred P. Sloan, Basil O’Connor, Guggenheim, Irma T. Hirschl, Klingenstein, McKnight, Rita Allen, and Searle scholar or fellow. We thank Karel Svoboda, Rafa Yuste, Kai Zinn, and in particular Charles Greer for discussions and thoughtful comments on this manuscript. We thank Janet Baer, David Crotty, and Mary Flowers (Caltech) for logistical help in mouse shipments. We acknowledge Clontech for providing enhanced GFP-1 before commercial release. All authors contributed equally to this work.
Funders:
Funding AgencyGrant Number
Caltech Beckman InstituteUNSPECIFIED
NIHUNSPECIFIED
Human Frontier Science ProgramUNSPECIFIED
Norman and Rosita Winston FoundationUNSPECIFIED
Bristol-Myers SquibbUNSPECIFIED
Rockefeller UniversityUNSPECIFIED
Alfred P. Sloan FoundationUNSPECIFIED
March of Dimes FoundationUNSPECIFIED
John Simon Guggenheim FoundationUNSPECIFIED
Irma T. Hirschl/Monique Weill-Caulier TrustUNSPECIFIED
Klingenstein FoundationUNSPECIFIED
McKnight FoundationUNSPECIFIED
Rita Allen FoundationUNSPECIFIED
Searle Scholars ProgramUNSPECIFIED
Subject Keywords:olfaction; olfactory system; olfactory bulb; glomerulus; sensory neuron; olfactory receptor; odorant receptor; tau; green fluorescent protein; two-photon microscopy; axon guidance
Issue or Number:24
PubMed Central ID:PMC2570017
Record Number:CaltechAUTHORS:20160212-073756013
Persistent URL:https://resolver.caltech.edu/CaltechAUTHORS:20160212-073756013
Official Citation:Structure and Emergence of Specific Olfactory Glomeruli in the Mouse Steve M. Potter, Chen Zheng, David S. Koos, Paul Feinstein, Scott E. Fraser, and Peter Mombaerts The Journal of Neuroscience, 15 December 2001, 21(24):9713-9723
Usage Policy:No commercial reproduction, distribution, display or performance rights in this work are provided.
ID Code:64447
Collection:CaltechAUTHORS
Deposited By: Ruth Sustaita
Deposited On:19 Feb 2016 19:28
Last Modified:03 Oct 2019 09:38

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