Animals are constantly bombarded by a wide-range of environmental stimuli that they must rapidly and accurately process in their central nervous systems. Regardless of a stimulus' modality, be it light, sound, chemical or mechanical, sensory processing in the mammalian brain begins with signal transduction in the periphery of the nervous system. Primary sensory neurons, such as photoreceptors in the eye, express specialized receptor proteins that undergo conformational changes in the presence of an appropriate stimulus, generating electrical signals that propagate into the brain. The receptor's mechanism of signal transduction in primary sensory neurons helps determine the organization and functional logic of sensory processing.
Mammalian olfaction provides a great system for neuroscientists seeking to understand peripheral transduction and sensory processing in the brain. Despite the large array of unique chemical receptors involved in the olfactory system (approximately 1,400 in mice and 1,000 in humans), individual olfactory receptor neurons (OSNs) express only a single type of chemical receptor. Additionally, OSNs that express the same receptor type extend and gather their axons into distinct and separated zones (glomeruli) in the first olfactory relay station in the brain. This 'one neuron–one receptor' expression pattern, combined with the anatomical segregation of axons that transfer sensory signals, has defined the functional logic of olfactory processing for over two decades.
In a recent study by a group at Harvard, a new twist on this logic has been discovered in certain primary olfactory sensory neurons (Cell doi: 10.1016/j.cell.2016.05.001; published online 26 May 2016). Using a combination of genetics and functional imaging in mice, Greer et al. identified that a specific set of OSNs transduce olfactory signals using various receptor proteins in the MS4A protein family. These OSNs make up the 'necklace' subsystem, which is named for the necklace-like shape that these neurons form in the deep recesses of the olfactory nasal epithelium. MS4A receptors are structurally different from the typical G-protein-coupled receptors that are present in most OSNs, and various types of MS4A receptors are expressed promiscuously across necklace OSNs, violating the 'one neuron–one receptor' rule. Each OSN in the necklace subsystem therefore responds to signals transduced by multiple types of MS4A receptors, pooling odor information together rather than segregating it into unique channels. This discovery uncovers a novel logical operating principle for the olfactory system and suggests that multiple unique streams of information are processed in parallel, potentially allowing for enhanced odor perception and behavioral decision-making.
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Graham, D. Reexamining the logic of olfactory transduction. Lab Anim 45, 243 (2016). https://doi.org/10.1038/laban.1054
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DOI: https://doi.org/10.1038/laban.1054