Honeybees (Apis mellifera) learn to discriminate the smell of organic compounds from their respective deuterated isotopomers

Abstract

The understanding of physiological and molecular processes underlying the sense of smell has made considerable progress during the past three decades, revealing the cascade of molecular steps that lead to the activation of olfactory receptor (OR) neurons. However, the mode of primary interaction of odorant molecules with the OR proteins within the sensory cells is still enigmatic. Two different concepts try to explain these interactions: the 'odotope hypothesis' suggests that OR proteins recognize structural aspects of the odorant molecule, whereas the 'vibration hypothesis' proposes that intra-molecular vibrations are the basis for the recognition of the odorant by the receptor protein. The vibration hypothesis predicts that OR proteins should be able to discriminate compounds containing deuterium from their common counterparts which contain hydrogen instead of deuterium. This study tests this prediction in honeybees (Apis mellifera) using the proboscis extension reflex learning in a differential conditioning paradigm. Rewarding one odour (e.g. a deuterated compound) with sucrose and not rewarding the respective analogue (e.g. hydrogen-based odorant) shows that honeybees readily learn to discriminate hydrogen-based odorants from their deuterated counterparts and supports the idea that intra-molecular vibrations may contribute to odour discrimination.

Implausibility of the vibrational theory of olfaction

“…The principal experimental evidence supporting the vibrational theory has been the deuterium isotope effect at the perceptual (behavioral) level (14,36,38). However, we find no experimental evidence supporting the theory at the molecular level.…”

“…Earlier claims that human subjects can distinguish odors of acetophenone isotopomers (9,35) have been shown to be untrue (14,31). Recent studies indicate that Drosophila melanogaster can distinguish acetophenone isotopomers (36,37) and that Apis mellifera L., the honey bee, can be trained to discriminate pairs of isotopomers (38). These studies differ from earlier insect studies in which isotopomer discrimination was not found.…”

Experimental evaluation of the generalized vibrational theory of G protein-coupled receptor activation

“…has arisen and has gained both supporters (13)(14)(15)(16) and detractors (17,18); the novelty of this incarnation of the VTO is ascribable to its nonthermal-and nonphoton-based mechanism. Turin's theory is a contemporary reincarnation of the more classical theory proposed by Dyson (19), Wright (20), and Wright and Serenius (21), where the activation of the olfactory receptor is performed-or sensitive to-the molecular vibrations of the olfactant.…”

“…Additionally, more modern examinations of this theory with both humans and insect subjects have provided mixed and controversial results. (14,(16)(17)(18)(22)(23)(24).…”

“…Additionally, more modern examinations of this theory with both humans and insect subjects have provided mixed and controversial results. (14,(16)(17)(18)(22)(23)(24).There have been several tests of the previous iterations of the VTO, including odor blending (25,26) and isotope exchange (20,(27)(28)(29)(30); each of these methods-odor blending (11, 18) and isotope exchange (11, 31)-has been used to evaluate the modern VTO. Initial justifications of the VTO correlated characteristics of the vibrational spectra with olfactory perception (12), continued within ORs (32), and expanded into non-OR GPCRs (33-36).…”