The electrostatic basis of insect olfaction

The sense of olfaction relies on the capture and detection of volatile molecules. Organisms like insects have the particularity of possessing externally facing olfactory systems, an arrangement substantially different from the internalised olfactory epithelia of most vertebrates. In insects, olfactory sensory structures take the form of thousands of small porous hairs often located on the antennae. Inside these hairs reside specialised sensory neurones with terminal dendrites rich in membrane-borne receptor molecules. These receptors confer sensitivity and specificity to odour reception. Whilst the olfactory process is remarkably well-understood in its molecular and neural details, large questions remain as to how air-borne odorant molecules reach dendritic terminals, where actual detection takes place. How and how fast do volatiles from the air medium move across the cushion of air, the boundary layer, surrounding cuticular olfactory sensors? Current evidence and theories accommodate transport through passive diffusion and/or invoke active antennal motion. The latter is deemed to break the boundary layer, enabling a greater and faster availability of odorants at the receptor level inside the olfactory hairs. Albeit empirically supported, this process may not act alone and does not entirely explain the notable efficiency and rapid sampling rate observed in many insect species. We have identified a potentially additional mechanism.

We have developed a novel theory of olfaction that involves the relative electrostatic charging of receptor structures, whereby cuticular arthropod hairs interact with odorant molecules endowed with charge or a dipole moment. Notably, this interaction is predicted to occur outside the receptor and distinct from known nanoscale electrostatic attachment of odorant to membrane-borne receptor in the liquid phase.