Trigeminal innervation and tactile responses in mouse tongue

• Published in: Cell reports (Cambridge) Vol. 43; no. 9; p. 114665
• Main Authors: Zhang, Linghua, Nagel, Maximilian, Olson, William P., Chesler, Alexander T., O’Connor, Daniel H.
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 24.09.2024
• Subjects: Animals; LTMR; Male; mechanoreceptor; Mechanoreceptors - metabolism; Mechanoreceptors - physiology; Mice; Mice, Inbred C57BL; somatosensation; taste bud; Taste Buds - physiology; tongue; Tongue - innervation; Tongue - physiology; touch; Touch - physiology; trigeminal; trigeminal ganglion; Trigeminal Ganglion - physiology; mechanoreceptor; tongue; CP: Neuroscience; trigeminal ganglion; somatosensation; touch; taste bud; trigeminal; LTMR
• ISSN: 2211-1247; 2211-1247
• DOI: 10.1016/j.celrep.2024.114665

The neural basis of tongue mechanosensation remains largely mysterious despite the tongue’s high tactile acuity, sensitivity, and relevance to ethologically important functions. We studied terminal morphologies and tactile responses of lingual afferents from the trigeminal ganglion. Fungiform papillae, the taste-bud-holding structures in the tongue, were convergently innervated by multiple Piezo2+ trigeminal afferents, whereas single trigeminal afferents branched into multiple adjacent filiform papillae. In vivo single-unit recordings from the trigeminal ganglion revealed lingual low-threshold mechanoreceptors (LTMRs) with distinct tactile properties ranging from intermediately adapting (IA) to rapidly adapting (RA). The receptive fields of these LTMRs were mostly less than 0.1 mm2 and concentrated at the tip of the tongue, resembling the distribution of fungiform papillae. Our results indicate that fungiform papillae are mechanosensory structures and suggest a simple model that links functional and anatomical properties of tactile sensory neurons in the tongue. [Display omitted] •The tip of the tongue is heavily innervated by lingual mechanoreceptors•Lingual LTMRs have small receptive fields and high sensitivity and adapt rapidly•Lingual afferents exhibit distinct innervation patterns in different papilla types•Fungiform papillae, the lingual papillae containing taste buds, are touch sensors The tip of the tongue, one of the most tactile-sensitive areas in the body, is enriched with taste-bud-containing fungiform papillae. Zhang et al. reveal that fungiform papillae are touch sensors and suggest a model linking functional and anatomical properties of tactile sensory neurons in the tongue.