A Variant Mode of Mammalian Olfaction

Abstract

Olfaction – the sense of smell – informs animals about food, mates, threats, and other chemical signals. The odors most relevant to survival and reproduction vary across species and ecology; for this reason, olfactory nervous systems have evolved to perceive select stimuli and to elicit adaptive responses. The mammalian olfactory system accomplishes this with families of olfactory receptors – proteins that bind characteristic odor molecules and signal through parallel neural pathways. Each animal expresses a diverse repertoire of receptors, geared to its chemical environment, in a canonical mode of one receptor gene per olfactory sensory neuron. This arrangement produces precise neural representations for individual odors, which are capable of driving a range of behaviors. However, it is not known whether this conserved architecture is suited for all aspects of odor sensation. Here I report that part of the olfactory system breaks from this predominant organization. An atypical sensory subsystem, the so-called olfactory “necklace,” does not express traditional olfactory receptors, but instead detects several classes of chemical stimuli with the previously unknown Ms4a receptor family. Ms4a proteins are unrelated to other olfactory receptors, suggesting that they have evolved to detect distinct odors and to transduce signals by a different mechanism. Moreover, multiple members of the Ms4a family are expressed in each necklace neuron. The violation of the “one receptor per neuron” rule endows this subsystem with broader sensory responses than granted by a single receptor. By way of this variant organization, the necklace may play a unique role in shaping odor perception.