Abstract

BackgroundOdorant stimuli can access the olfactory epithelium either orthonasally, by inhalation through the external nares, or retronasally by reverse airflow from the oral cavity. There is evidence that odors perceived through these two routes can differ in quality and intensity. We were curious whether such differences might potentially have a neural basis in the peripheral mechanisms of odor coding. To explore this possibility, we compared olfactory receptor input to glomeruli in the dorsal olfactory bulb evoked by orthonasal and retronasal stimulation. Maps of glomerular response were acquired by optical imaging of transgenic mice expressing synaptopHluorin (spH), a fluorescent reporter of presynaptic activity, in olfactory nerve terminals.ResultsWe found that retronasally delivered odorants were able to activate inputs to multiple glomeruli in the dorsal olfactory bulb. The retronasal responses were smaller than orthonasal responses to odorants delivered at comparable concentrations and flow rates, and they displayed higher thresholds and right-shifted dose–response curves. Glomerular maps of orthonasal and retronasal responses were usually well overlapped, with fewer total numbers of glomeruli in retronasal maps. However, maps at threshold could be quite distinct with little overlap. Retronasal responses were also more narrowly tuned to homologous series of aliphatic odorants of varying carbon chain length, with longer chain, more hydrophobic compounds evoking little or no response at comparable vapor levels.ConclusionsSeveral features of retronasal olfaction are possibly referable to the observed properties of glomerular odorant responses. The finding that retronasal responses are weaker and sparser than orthonasal responses is consistent with psychophysical studies showing lower sensitivity for retronasal olfaction in threshold and suprathreshold tests. The similarity and overlap of orthonasal and retronasal odor maps at suprathreshold concentrations agrees with generally similar perceived qualities for the same odorant stimuli administered by the two routes. However, divergence of maps near threshold is a potential factor in perceptual differences between orthonasal and retronasal olfaction. Narrower tuning of retronasal responses suggests that they may be less influenced by chromatographic adsorption effects.

Highlights

  • Odorant stimuli can access the olfactory epithelium either orthonasally, by inhalation through the external nares, or retronasally by reverse airflow from the oral cavity

  • Olfaction begins with the delivery of volatile organic compounds to the olfactory epithelium where airborne molecules partition into the olfactory mucosa and are detected by olfactory receptors (ORs) expressed in olfactory sensory neurons (OSNs)

  • Orthonasal odorants are conveyed to the olfactory epithelium by varied sampling behaviors that can range from passive, low frequency (~ 1 – 3 Hz) inhalation locked to the respiratory cycle, to active high frequency (~ 3 – 12 Hz) bouts of investigative sniffing [46,47]

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Summary

Introduction

Odorant stimuli can access the olfactory epithelium either orthonasally, by inhalation through the external nares, or retronasally by reverse airflow from the oral cavity. We were curious whether such differences might potentially have a neural basis in the peripheral mechanisms of odor coding To explore this possibility, we compared olfactory receptor input to glomeruli in the dorsal olfactory bulb evoked by orthonasal and retronasal stimulation. In 1982, Rozin [1] first argued that olfaction is a dual sense, in which odor stimuli delivered via orthonasal and retronasal routes are processed and perceived differently. This idea has been investigated by several studies comparing orthonasal and retronasal olfaction in humans. Orthonasal and retronasal presentations of the same odorants evoked cortical event-related potentials with different amplitudes and latencies [2,9,10], and activated different brain areas visualized by functional magnetic resonance imaging [2,11,12]

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