Glomerular input patterns in the mouse olfactory bulb evoked by retronasal odor stimuli

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.

Retronasal odor concentration coding in glomeruli of the rat olfactory bulb

“…These two modes of olfaction are associated with two overlapping but separate neural networks ( Small et al, 2005 ). Studies further indicate that retronasal smell, at both threshold and suprathreshold odor concentrations, is less sensitive than orthonasal smell in humans ( Heilmann and Hummel, 2004 ; Hummel et al, 2006 ; Furudono et al, 2013 ). These sensitivity differences may in part be explained by difference in direction-dependent flow patterns across the olfactory epithelium ( Zhao et al, 2006 ) in interaction with flow rate and non-uniform receptor distributions ( Schoenfeld and Cleland, 2006 ), in addition to differences in higher level mechanisms as learning ( Bender et al, 2009 ).…”

“…In humans, odor concentration has been shown to be directly proportional to perceived odor intensity, as well as olfactory receptor neuron population responses ( Lapid et al, 2009 ). While odor identity coding during orthonasal smell has been fairly well studied ( Stewart et al, 1979 ; Rubin and Katz, 1999 ; Meister and Bonhoeffer, 2001 ; Spors et al, 2006 ; Verhagen et al, 2007 ), and ignored odor direction, studies on the retronasal odor identity coding have only recently begun ( Scott et al, 2007 ; Gautam and Verhagen, 2012b ; Furudono et al, 2013 ). Furthermore, a systematic study of the coding of retronasal odor intensities in the olfactory bulb (OB) of any species is yet to be reported.…”

Multivariate statistical analysis of a large odorants database aimed at revealing similarities and links between odorants and odors

“…We focused as much as possible on orthonasal perception of odors and did not account for the description of flavors. The retronasal perception of numerous odorants differs from their orthonasal perception, and some hypotheses have been proposed to explain this difference, which remains unclear …”

Experience-dependent c-Fos expression in the primary chemosensory cortices of the rat

“…Previous work has shown that smelling novel odors increased c-Fos expression in piriform cortex (Illig and Haberly, 2003) and odor-evoked responses habituate with experience (Wilson, 1998); however, odors were only presented orthonasally (detection of odors via inhalation). Retronasal olfaction is necessary for odor-taste associations and differs from orthonasal olfaction both perceptually (Heilmann and Hummel, 2004; Hummel et al, 2006) and physiologically (Furudono et al, 2013; Gautam and Verhagen, 2012b). For example, food odors given retronasally, even in the absence of liquid, are localized to the mouth (Lim and Johnson, 2012) and the controlled delivery of odors orthonasally or retronasally evoked different patterns of activity in the olfactory bulb (Gautam et al, 2014).…”