Tuning to Odor Solubility and Sorption Pattern in Olfactory Epithelial Responses

Abstract

Odor information is first represented as a spatial activation pattern across the olfactory epithelium, when odor is drawn into the nose through breathing. This epithelial pattern likely results from both the intrinsic olfactory sensory neuron (OSN) sensitivity and the sorptive patterns imposed by the interaction of nasal aerodynamics with physiochemical properties of odorants, although the precise contributions of each are ill defined. Here, we used a computational fluid dynamics (CFD) model of rat nasal cavity to simulate the nasal aerodynamics and sorption patterns for a large number of odorants, and compared the results with the spatial neural activities measured by electro-olfactogram (EOG) under same flow conditions. The computational and experimental results both indicate greater sorption and response to a narrow range odorants as a function of their mucosal solubility, and this range can be further modulated by changes of intranasal flow rates and direction (orthonasal vs retronasal flow). A striking finding is that the profile of intrinsic EOG response measured in surgically opened nose without airflow constraints is similar to the shape of the sorption profile imposed by nasal airflow, strongly indicating a tuning process. As validation, combining the intrinsic response with the mucosal concentration estimated by CFD in nonlinear regression successfully accounts for the measured retronasal and orthonasal EOG response at all flow rates and positions. These observations redefine the role of sorption properties in olfaction and suggest that the peripheral olfactory system, especially the central zone, may be strategically arranged spatially to optimize its functionality, depending on the incoming stimuli.