Mechanisms of stimulation of olfactory neurons: an essay

It is widely believed that the mechanism by which olfactory neurons are stimulated by odorants is via specific receptor proteins located on or in the apical cell membranes of the neurons. In this review alternative mechanisms are explored and a model is presented in which sensitivity and specificity can be accounted for by the general irritability of cells to chemicals. The premises on which the model is based are: (i) Groups of olfactory nerves fire action potentials which are summated at the first synapse, in the olfactory bulb. These neurons fire spontaneously because their resting potentials are unstable. (ii) What we call olfactory quality is encoded in patterns of firing of different olfactory neurons. (iii) Olfactory neurons are not identical. The sources of their individuality include differences in their age, spatial location in the plane of the tissue, depth within the tissue and distance from the nearest capillary. The heterogeneity will be reflected as differences in their metabolism and chemical composition. (iv) Most of the surface area of olfactory neurons is bathed in mucus that is secreted by Bowman's glands and sustentacular cells. Therefore, the resting potential and firing frequency of each will depend upon the composition of the mucus. It follows from these premises that alterations in the mucus composition, extracellular fluid composition, metabolic state or properties of neuronal membranes will alter the resting potential and, therefore, the firing frequency of each neuron. The effects will vary among neurons because of their individuality even if the stimulus is distributed uniformly across the olfactory mucosa, different regions will be exposed to different patterns of stimulus concentration because odorants are differentially adsorbed and metabolized. According to this scheme qualitatively different patterns of neural activity will result from different odorants, the firing of some neurons being inhibited and that of others being stimulated in each case. This will be true independently of the existence of specific receptor proteins, the effects of which must be superimposed upon the general effects of nonspecific irritability.