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How the Olfactory Bulb Got Its Glomeruli’ May Be More Complex, and Rough Organization Is Specified Genetically More Revealing, Than Has Been Supposed

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How the Olfactory Bulb Got Its Glomeruli’ May Be More Complex, and Rough Organization Is Specified Genetically More Revealing, Than Has Been Supposed PERSPECTIVES cess) effectively determines the identity of the OPINION sensory neuron, dictating what odours will activate it and where its axons will project. How the olfactory bulb got its These data gave rise to an ancillary prin- ciple of olfactory wiring for which there is glomeruli: a just so story? less direct support, but which has none- theless become generally accepted. This principle states that there is a stereotypical, Dong-Jing Zou, Alexander Chesler and Stuart Firestein animal-invariant, topographical map of the Abstract | The nearly 2,000 glomeruli that cover the surface of the olfactory bulb glomeruli. Each glomerulus has a position and identity that is endowed by the odor- are so distinctive that they were noted specifically in the earliest of Cajal’s ant receptor expressed by the innervating catalogues. They have variously been considered a functional unit, an organizational neurons. A corollary of this principle is unit and a crucial component of the olfactory coding circuit. Despite their central that the cues for determining the location position in olfactory processing, the development of the glomeruli has only recently of a glomerulus and signals that enable the begun to be investigated with new and powerful genetic tools. Some unexpected axon to locate a specific glomerulus are almost entirely genetically determined — findings have been made that may lead to a new understanding of the processes largely by the choice of receptor gene. This involved in wiring sensory regions of the brain. It may no longer be sufficient to is a significant departure from the strategy simply invoke genes, spikes and their interplay in the construction of brain circuits. used by other sensory systems, in which a The story of ‘how the olfactory bulb got its glomeruli’ may be more complex, and rough organization is specified genetically more revealing, than has been supposed. during early development and then refined postnatally by experience16–18. Although the organization of the glomer- The mammalian olfactory nerve is composed The axons of cells expressing one of the more uli suggests that they have a crucial early of the axons of the primary olfactory sensory than 1,000 odorant receptor genes were seen functional role in the transformation of a neurons (OSNs), the cell bodies of which to travel from distant portions of the olfactory chemical stimulus into an olfactory percept, are located in the olfactory epithelium. The epithelium and converge with astonishing new findings from several laboratories have first synapse made by these axons occurs in precision in one or two of the 1,800 olfactory cast some doubt on this tidy scheme and a glomerulus, a specialized structure in the glomeruli (FIG. 1). In adult mice, the axons alternative views are emerging. These new olfactory bulb. Each glomerulus is devoid of all cells expressing the same receptor, data require us to reconsider our ideas about of cell somas and consists of incoming OSN and only those axons, converge into a single both olfactory bulb development and the axons, the dendrites of both second-order glomerulus7. Furthermore, when the entire ways in which information is passed from the projection neurons and local interneurons, receptor was replaced or parts of its sequence periphery to the first central synapse. It now and the processes of astrocytes. The glomer- were changed, the axons were redirected to seems that the glomerular layout can vary, uli are among the structures of the nervous other glomeruli6,8–11. Thus, the receptor itself even between genetically identical individu- system containing the highest density of syn- was identified as a crucial component of the als, and that neural activity may have a sig- apses. For many years glomeruli have been axon-guidance process. The importance of nificant role in determining the position and referred to and characterized as functional this finding has yet to be fully appreciated — composition of a glomerulus. Perhaps more units of olfactory processing1–3. it is one of the first instances in which G pro- importantly, this activity is not necessarily The olfactory system was the first neural tein-coupled receptors (GPCRs) have been electrical, differing from the classical view system in which the wiring diagram was implicated in the process of axon guidance. that axons ‘fire together and wire together’. In determined by molecular, rather than physi- One attribute of this relationship between this Perspective article, we outline the recent ological, techniques. These studies revealed receptor expression and axon target is espe- progress in understanding the development the remarkable organization of the glomeru- cially important. There are over 1,000 odor- of the mammalian glomeruli, with a particu- lar layer of the mouse olfactory bulb. Early ant receptor genes in the mouse genome; lar focus on the roles of signalling. We pro- in situ hybridization studies indicated that however, it seems that an individual sensory pose that glomeruli provide a developmental each glomerulus contained a population of neuron chooses only one of these genes solution to the problem of organizing 1,000 axons from OSNs expressing the same odor- (indeed only one allele of one gene) for trans- populations of axons, rather than acting ant receptor4,5, and later pioneering gene lation into protein12,13 (however, this conclu- mainly as functional units. Furthermore, we targeting studies visualized the glomeruli sion has been questioned by some; see REFS suggest that activity of the odorant receptor- with unprecedented resolution and further 14,15). It has been proposed that the choice mediated signalling cascade has a crucial role substantiated this cardinal wiring principle6. of odorant receptor (a still mysterious pro- in this organizational process. NATURE REVIEWS | NEUROSCIENCE VOLUME 10 | AUGUST 2009 | 611 © 2009 Macmillan Publishers Limited. All rights reserved PERSPECTIVES Background Cl– channels. Unlike many neurons, OSNs single glomerulus. Mitral and tufted cells also The molecular era in research of the olfac- maintain a high intracellular Cl– concentra- have lateral dendrites that extend great dis- tory system began with the publication in tion, and opening these channels produces tances around the olfactory bulb and synapse 1991 of the landmark discovery by Buck and a Cl– efflux, further depolarizing the cell extensively with a population of interneurons Axel of a large family of GPCRs expressed membrane and generating action potentials known as granule cells (FIG. 3). The axons of by mammalian OSNs19. This finding allowed that are propagated down the axon to the mitral cells, fasciculating as the lateral olfac- the use of molecular and genetic tools to synapses in the glomerulus20 (FIG. 2). tory tract, project to the piriform cortex, the decipher how we detect and discriminate presumed site of higher olfactory processing. between an enormous number and variety Glomerular circuitry. The glomeruli, Tufted cells seem to project both within the of chemical compounds. After more than a located on the surface of the olfactory bulb olfactory bulb and to the anterior olfactory decade of intense investigation the periph- just under the layer of incoming axons, are nucleus. Their axons have been shown to eral mechanisms used by OSNs to generate bounded by glial cells and by periglomerular connect the glomeruli that are innervated by odour-dependent signals are now generally cells, a diverse population of mostly inhibi- an identical population of sensory cell axons, well understood20. tory interneurons that extend neurites (that either within the same bulb or between the is, both dendrites and axons) into multiple bulbs on each side of a mouse21–23. A common second messenger transduction glomeruli in a local neighbourhood. The In the glomerular neuropil there are cascade. Binding of odorant compounds to glomerulus is also innervated by the apical three basic synaptic circuits. Axodendritic odorant receptors initiates a transduction dendrites of mitral and tufted cells. Mitral synapses connect the axons of OSNs with cascade involving a G protein and activa- cells lie mainly in a thin layer ~400–500 the dendrites of mitral or tufted cells and tion of adenylyl cyclase 3 (AC3), a potent μm deep in the olfactory bulb, whereas periglomerular cells. This is a site of tremen- catalyst that produces the second messen- tufted cells lie in the external plexiform dous convergence: up to 25,000 OSN axons ger cyclic AMP (cAMP). cAMP binds to a layer between the mitral cell layer and the form synapses on the apical dendrites of up cyclic nucleotide-gated (CNG) ion chan- glomeruli. These two populations of cells are to 100 mitral and tufted cells (in rabbits24). nel, increasing its open time and allowing both pyramidal-like excitatory projection These OSNs are the sole source of primary the influx of cations, which depolarize the neurons. The apical dendrite of a mitral or sensory information to the glomerulus cell membrane. Ca2+ entering through this tufted cell branches extensively once it enters and, effectively, to the brain. Reciprocal channel can also activate Ca2+-dependent the glomerulus, but it innervates only a dendrodentritic synapses between mitral or tufted cell dendrites and periglomerular cell abdendrites provide a second source of input to periglomerular cells. Finally, inhibitory A synapses between the axons of periglomeru- LL lar cells and mitral or tufted cell dendrites mediate feedback or feedforward inhibition (FIG. 3). Recently, an excitatory synapse from OE OB a periglomerular cell to a mitral cell has been identified25, although its role in processing is as yet unclear. M71L What do the glomeruli do? The glomerulus seems properly positioned cdAmyl acetate Peanut butter to act as a functional unit in which sensory input signals converge and activate circuitry that shapes the signal before transmitting it to higher centres. One might expect the output from the glomerulus to cortical areas to be information rich, given that there is only one more synapse in the cortex at which to transform this message into at least an elementary percept.
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