Elsevier

Neuroscience Research

Volume 30, Issue 2, February 1998, Pages 101-110
Neuroscience Research

How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells

https://doi.org/10.1016/S0168-0102(98)00002-9Get rights and content

Abstract

Recent progress in the studies of the olfactory system, especially in the molecular biological studies, makes it one of the useful sensory model systems for understanding neural mechanisms for the information processing. In the olfactory bulb, the primary center of the olfactory system, glomeruli are regarded as important functional units in the transmission of odorant signals and in processing the olfactory information, but have been believed to be composed by only a small number of neuronal types and thus to be simple in their neuronal and synaptic organization. However, accumulating morphological data reveal that each type of neurons might further consist of several different subpopulations, indicating that the organization of glomeruli might not be so simple as it was believed. Here we describe an aspect of the structural organization of glomeruli, focusing on the heterogeneities of periglomerular neurons in mammalian main olfactory bulb.

Introduction

The olfactory system might be an underdeveloped field in neuroscience, presumably because olfaction is considered less important in the human race than other senses such as vision. However, recent progress in the studies of olfactory systems of vertebrate (the most comprehensive review of the vertebrate olfactory systems is presented by Halász, 1990) as well as of the invertebrate, revealed that they can be one of useful sensory model systems for understanding neural mechanisms for the information processing and the memory, from the molecular to the behavioral levels. Recent findings suggest that olfactory transduction and neural processing involve a common set of neural mechanisms across phyla, as represented by the main olfactory bulb (MOB) and accessory olfactory bulb (AOB) in mammals, olfactory bulb of teleosts and antennae in insects (Dulac, 1997, Hildebrans and Shepherd, 1997).

The molecular biological studies (Buck and Axel, 1991) made it clear that odor receptor proteins are one of a multigene family within the seven-transmembrane-domain G-protein-coupled receptors, which activate the cyclic AMP second messenger pathway. These analyses have further revealed that each olfactory receptor neuron expresses only a single receptor type and that axons from olfactory receptor neurons expressing a given receptor converge on only two glomeruli per bulb (Reesler et al., 1994, Vassar et al., 1994, Mombaerts et al., 1996). These observations are in accord with physiological experiments demonstrating that different odorants elicit spatially defined patterns of glomerular activity in the OB (Shepherd, 1994, Mori and Yoshihara, 1995, Friedrich and Korsching, 1997). Glomeruli (or glomerular modules in teleosts) of the OB are now considered to serve as functional units in processing the olfactory information. In this article we describe the organization of glomeruli in the rat MOB, especially focusing on the chemical and structural heterogeneities of so-called periglomerular cells.

Section snippets

Anatomical organization of glomeruli

Glomeruli are one of the most distinctive structures in the brain, analogous to barrels or columns in the cerebral cortex (Shepherd, 1994). In mammalian OB, they are compactly packed almost two-dimensionally near the OB surface. Each glomerulus is composed of neuropil rich spheroidal structures surrounded by a distinctive shell of small to medium-sized neurons (periglomerular neurons) and glial cells (astrocytes). Classical Golgi studies (Ramón y Cajal, 1911, Pinching and Powell, 1971a,

Chemical organization of glomeruli

In spite of classical structural analyses proposing a rather simple organization of glomeruli, immunocytochemical and neurochemical analyses have revealed that glomeruli consist of a wide variety of neuronal elements different in their chemical properties (Halász, 1990). Table 1 summarizes chemical markers in the glomerular layer, which is modified from tables shown in Halász (1990) and Shipley et al. (1995). Although mitral/tufted cells are also characterized by several chemical substances as

Conclusion

The olfactory bulb is occasionally compared with the retina; both consists of only several types of neurons. However, as it is well known, each type of retinal neuron groups consists of a variety of subtypes different from one another functionally, chemically and morphologically. Similarly, recent analyses on the olfactory bulb are revealing that each type of olfactory bulb neuron groups also consists of a variety of subtypes different from one another chemically, morphologically and probably

Acknowledgements

The authors would like to thank Ms A. Oda for her secretarial assistance. This work was supported by Grants-in-aid for General Scientific Research (09480213 to T. Kosaka and 09680746 to K. Kosaka) from the Japanese Ministry of Education, Science and Culture, and grant from the Ichiro Kanehara Foundation to K.K.

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