How simple is the organization of the olfactory glomerulus?: the heterogeneity of so-called periglomerular cells
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.
References (61)
- et al.
Immunohistochemical localization of calcium-binding protein in the cerebellum, hippocampal formation and olfactory bulb of the rat
Brain Res.
(1982) - et al.
Differential afferent regulation of dopaminergic and GABAergic neurons in the mouse main olfactory bulb
Brain Res.
(1988) - et al.
Olfactory afferent regulation of the dopamine phenotype in the fetal rat olfactory system
Neuroscience
(1993) - et al.
Distribution of enkephalin-like immunoreactivity in the rat main olfactory bulb
Neuroscience
(1982) - et al.
A novel multigene family may encode odorant receptors: a molecular basis for odor recognition
Cell
(1991) Calbindin D-28k and parvalbumin in the rat nervous system
Neuroscience
(1990)How does the brain smell?
Neuron
(1997)- et al.
Transneuronal regulation of neuronal specific gene expression in the mouse olfactory bulb
Mol. Brain Res.
(1990) - et al.
Combinatorial and chemotopic odorant coding in the zebrafish olfactory bulb visualized by optical imaging
Neuron
(1997) - et al.
Principles of organization of the vertebrate olfactory glomerulus: an hypothesis
Neuroscience
(1986)
Transmitter histochemistry of the rat olfactory bulb. I. Immunohistochemical localization of monoamine synthesizing enzymes. Support for intrabulbar, periglomerular dopamine neurons
Brain Res.
Tyrosine hydroxylase and 28K-Vitamin D-dependent calcium binding protein are localized in different subpopulations of periglomerular cells of the rat olfactory bulb
Neurosci. Lett.
Fast spiking cells in rat hippocampus (CA1 region) contain the calcium-binding protein parvalbumin
Brain Res.
Postnatal development of neurons containing both catecholaminergic and GABAergic traits in the rat main olfactory bulb
Brain Res.
Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb
Neurosci. Res.
Differentiation of chemically defined neuronal populations in the transplanted olfactory bulb without olfactory receptor innervation
Neurosci. Res.
Coexistence of immunoreactivities for glutamate decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb: possible coexistence of gamma-aminobutyric acid (GABA) and dopamine
Brain Res.
An aspect of the organization of the GABAergic system in the rat main olfactory bulb: laminar distribution of immunohistochemically defined subpopulations of GABAergic neurons
Brain Res.
Differential effect of functional olfactory deprivation on the GABAergic and catecholaminergic traits in the rat main olfactory bulb
Brain Res.
Development of olfactory marker protein and tyrosine hydroxylase immunoreactivity in the transplanted rat olfactory bulb
Exp. Neurol.
Morphometry of rat olfactory bulbs stained for cytochrome oxidase reveals that the entire population of glomeruli forms early in the neonatal period
Dev. Brain Res.
Visualizing an olfactory sensory map
Cell
Immunocytochemical localization of GABAergic neurons and dopaminergic neurons in the rat main and accessory olfactory bulbs
Neurosci. Lett.
Glutamate decarboxylase localization in neurons of the olfactory bulb
Brain Res.
Immunohistochemical markers in rat brain: colocalization of calretinin and calbindin-D28k with tyrosine hydroxylase
Brain Res.
Discrimination of the molecular signals by the olfactory receptor neuron
Neuron
Thyrotropin-releasing hormone (TRH)-immunoreactive neuron populations in the rat olfactory bulb
Brain Res.
Formation of an olfactory glomerulus: morphological aspects of development and organization
Neuroscience
Topographic organization of sensory projections to the olfactory bulb
Cell
Synaptic organization of the mammalian olfactory glomerulus: new findings including an intraspecific variation
Brain Res.
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