Anatomical Characteristics of Tongue-Innervating Mechanoreceptors

Abstract

Mechanosensory innervation of the oral cavity enables us to detect the texture and location of the foods we consume. Our goal was to find a genetic identifier for a mechanoreceptive subtype. Toward this goal, we examined neurons expressing the neurotrophin receptor TrkC (TrkC-tdTomato), parvalbumin (Pvalb), or glutamate transporter, Vglut3. We found that the majority of Pvalb-lineage, Vglut3-lineage, and TrkC-tdTomato neurons innervating the tongue are separate trigeminal neuron populations. Because different papilla types contribute to food detection in different ways, we examined the innervation patterns of these neuron subtypes. We found that Pvalb-lineage and Vglut3-lineage neurons were fungiform papilla-specific, whereas TrkC+ fibers innervated both papilla types. We found that all Pvalb-lineage nerve fibers are labeled with neurofilament heavy chain (NFH), have axons that are surrounded by myelin basic protein, and lack calcitonin gene-related peptide. This indicates that these are all myelinated neurons. In contrast, Vglut3-lineage and TrkC-tdTomato nerve fibers were a mixed population of NFH+ nerve fibers and NFH− nerve fibers, as well as myelinated and unmyelinated nerve fibers. When we examined the axonal ending morphologies of the three genetic populations, we found that the Pvalb-lineage neurons consistently displayed a “basket-like” axonal ending that surrounded the taste bud. While TrkC+ and Vglut3-lineage neurons sometimes displayed this “basket-like” axonal ending, other axonal endings lacked this structure. When compared across groups, the Vglut3-lineage axonal endings displayed the greatest degree of morphological variability. Collectively, these data show that Pvalb-lineage may be a genetic identifier for a single myelinated mechanoreceptor innervating fungiform papillae.