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

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 focused on potential interactions between olfactory and trigeminal signaling in the nasal cavity. We first used a forced choice paradigm to ascertain whether trigeminal and olfactory stimuli could influence behavior in mice. Mice avoided water sources associated with volatile TRPV1 and TRPA1 irritants, however, this aversion 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 behavioral effect we recorded from single trigeminal sensory axons innervating the nasal 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 a mouse line expressing channel-rhodopsin under the olfactory marker protein. During photoactivation of olfactory sensory neurons there was no modulation of action potential conduction in individual trigeminal axons. Similarly, no evidence was found for trigeminal axon collateral branching that might serve as a conduit for cross-talk between the olfactory epithelium and olfactory dura mater. Using direct assessment of trigeminal signals emanating from the mouse nasal cavity we see no evidence for paracrine nor axon reflex mediated cross-talk between olfactory and trigeminal sensory systems in the nasal cavity.