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

Date Published: August 14, 2019

Publisher: Public Library of Science

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

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

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.

Partial Text

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. Trigeminal fibres originating from the ethmoid and nasopalatine nerves [1] detect irritants, temperature changes and mechanical stimuli [2,3], while olfactory receptor neurons respond specifically to odorants and non-specifically to mechanical stimuli [4]. In addition to the extended trigeminal network innervating the nasal respiratory epithelium, the olfactory sensory epithelium also contains trigeminal fibres [5–8] [9]. 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.

Animal housing and all experimental procedures were carried out in compliance with the guidelines for the welfare of experimental animals as stipulated by the Federal Republic of Germany. Animal experiments were approved by the Regierungspraesidium Karlsruhe, Germany (approval number 35–9185.81/G-104/16).

This study set out to examine interactions between the dual olfactory and trigeminal chemosensory systems in the nose. Using a forced choice behavioural assay in wild type mice, a combination of odorant and irritant stimuli mitigated the otherwise prominent aversion to irritant stimuli alone. 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]. We tested each of these proposals by recording directly from trigeminal axons innervating the nasal cavity. Using optogenetic techniques to activate olfactory sensory neurons exclusively we were unable to discern any modulation of axonal conduction in individual trigeminal afferent axons. We also found no evidence for axon reflex signaling within individual trigeminal axons in the ethmoid nerve that might otherwise form a nexus between the olfactory epithelium and the olfactory bulb. An inability to verify cross-modal interactions between olfactory and trigeminal structures within the nasal cavity suggests that behavioural manifestations of olfactory-trigeminal cross-talk are most likely to occur at more central sites such as trigeminal brainstem nuclei.

 

Source:

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

 

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