The sense of smell, its signalling pathways, and the dichotomy of cilia and microvilli in olfactory sensory cells

Abstract

Smell is often regarded as an ancillary perception in primates, who seem so dominated by their sense of vision. In this paper, we will portray some aspects of the significance of olfaction to human life and speculate on what evolutionary factors contribute to keeping it alive. We then outline the functional architecture of olfactory sensory neurons and their signal transduction pathways, which are the primary detectors that render olfactory perception possible. Throughout the phylogenetic tree, olfactory neurons, at their apical tip, are either decorated with cilia or with microvilli. The significance of this dichotomy is unknown. It is generally assumed that mammalian olfactory neurons are of the ciliary type only. The existence of so-called olfactory microvillar cells in mammals, however, is well documented, but their nature remains unclear and their function orphaned. This paper discusses the possibility, that in the main olfactory epithelium of mammals ciliated and microvillar sensory cells exist concurrently. We review evidence related to this hypothesis and ask, what function olfactory microvillar cells might have and what signalling mechanisms they use.

Figure 1

Olfactory bulb. Section through the olfactory bulb of a 16 days old rat brain. The tissue has been fixed and immunoperoxidase-stained with antibodies against GABAA-receptor_1-subunit (brown) as described elsewhere [157]. Nissl staining was performed to counter stain (blue). Clearly visible are the accessory olfactory bulb (AOB), to which chemosensory neurons from the vomeronasal organ project, the intensely labelled layer of mitral cells (MC), and the glomeruli (G), which represent the first relay station for sensory information transmitted from the nose to the brain (Jacques Paysan, unpublished).

Figure 2

Olfactory epithelium. This image shows a vertical projection of a stack of confocal images taken from a transgenic mouse, in which green fluorescent protein (GFP) is expressed in all ciliated olfactory sensory neurons. GFP brightly labels the olfactory neuronal cell bodies (OCB), their apical dendrites (AD), and terminal knobs (TK). Staining does not extend into the sensory cilia, which remain invisible in this preparation. Basally to the olfactory neuronal cell bodies is the unstained layer of basal stem cells (LBC), from which degenerating neurons are constantly regenerated. The olfactory axons grow in bundles (AB) through the basal lamina (BL), and then fasciculate to form the tracts of the olfactory nerve, which projects into the brain. (Rebecca Elsaesser and Jacques Paysan, unpublished).

Figure 3

Microvillar and ciliated olfactory sensory cells. Electron micrograph showing the apical poles of an olfactory microvillar cell (MVC) and a typical olfactory sensory neuron (OSN). This image was generated in 1975 at the Centre de microscopie électronique (Claude Bernard University, Lyon 1, France) and kindly provided by François Jourdan. See [130] for details.