Photoactivation of olfactory sensory neurons does not affect action potential conduction in individual trigeminal sensory axons innervating the rodent nasal cavity.

Margot Maurer,Richard W Carr,Julika Sertel-Nakajima,Karl Messlinger,Stephan Frings,Markus Schueler,Roberto De Col,Frank Möhrlen,Nunzia Papotto,Hiroaki Matsunami

doi:10.1371/journal.pone.0211175

Margot Maurer, Richard W Carr + Show 8 more

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https://doi.org/10.1371/journal.pone.0211175

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Abstract

Olfactory and trigeminal chemosensory systems reside in parallel within the mammalian nose. Psychophysical studies in people indicate that these two systems interact at a perceptual level. Trigeminal sensations of pungency mask odour perception, while olfactory stimuli can influence trigeminal signal processing tasks such as odour localization. While imaging studies indicate overlap in limbic and cortical somatosensory areas activated by nasal trigeminal and olfactory stimuli, there is also potential cross-talk at the level of the olfactory epithelium, the olfactory bulb and trigeminal brainstem. Here we explored the influence of olfactory and trigeminal signaling in the nasal cavity. A forced choice water consumption paradigm was used to ascertain whether trigeminal and olfactory stimuli could influence behaviour in mice. Mice avoided water sources surrounded by both volatile TRPV1 (cyclohexanone) and TRPA1 (allyl isothiocyanate) irritants and the aversion to cyclohexanone was mitigated when combined with a pure odorant (rose fragrance, phenylethyl alcohol, PEA). To determine whether olfactory-trigeminal interactions within the nose could potentially account for this behavioural effect we recorded from single trigeminal sensory axons innervating the nasal respiratory and olfactory epithelium using an isolated in vitro preparation. To circumvent non-specific effects of chemical stimuli, optical stimulation was used to excite olfactory sensory neurons in mice expressing channel-rhodopsin (ChR2) under the olfactory marker protein (OMP) promoter. Photoactivation of olfactory sensory neurons produced no modulation of axonal action potential conduction in individual trigeminal axons. Similarly, no evidence was found for collateral branching of trigeminal axon that might serve as a conduit for cross-talk between the olfactory and respiratory epithelium and olfactory dura mater. Using direct assessment of action potential activity in trigeminal axons we observed neither paracrine nor axon reflex mediated cross-talk between olfactory and trigeminal sensory systems in the rodent nasal cavity. Our current results suggest that olfactory sensory neurons exert minimal influence on trigeminal signals within the nasal cavity.

Highlights

The sensory innervation of the mammalian nasal cavity by the trigeminal and the olfactory systems endows the nasal epithelium with a broad spectrum of sensory modalities
In co-ordination with the olfactory system, trigeminal chemesthesis contributes to a continual analysis of the composition of the inhaled air for harmful and useful compounds with the trigeminal signaling being implicated in the induction of protective reflexes, pain perception [10] and subsequent behavioural responses
Previous reports suggest that cross-talk between olfactory and trigeminal chemosensory signals might take place within the nose, either through paracrine effects mediated by local release of neurotransmitters [23] or through axon reflex signaling in branched trigeminal afferents [42]

Summary

Introduction

The sensory innervation of the mammalian nasal cavity by the trigeminal and the olfactory systems endows the nasal epithelium with a broad spectrum of sensory modalities. It is well established that nasal olfactory and trigeminal sensory systems interact with one another on multiple levels, beginning with the fact that most odorants can stimulate trigeminal fibres and that most irritants have an odour [11]. Work on human nasal sensation has led to the concept that chemical stimulation of the nose triggers a multimodal response, which is often described as an integrated afferent signal rather than as two separate streams of trigeminal and olfactory information [11,12,13,14,15,16,17,18,19,20,21]. There is no clear understanding of the molecular pathways nor the anatomical sites at which olfactory signaling might affect trigeminal activity. Clinical evidence indicates that olfactory stimuli can affect the course of primary headache disorders, in particular in migraine [27,28,29,30,31,32] for which modulation within the trigeminal brainstem nuclei is implicated [32,33]

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