Molecularly Distinct, Meissner-Corpuscle-Associated Mechanoreceptors: A Potential Strategy for Efficient Enhancement of Spatial Acuity

Abstract

Tactile perception involves a diverse cadre of receptor types that extract distinct but often overlapping features of mechanical forces impinging on the skin. The stimulus features that a receptor responds to can reveal a receptor’s explicit function; however, when receptors overlap in their feature selectivity, the purpose of such apparent redundancy is more enigmatic. We have found that the Meissner corpuscle, a sensory structure in mammalian glabrous skin, contains two molecularly distinct afferent types. Since its first anatomical characterization in the 1850s, the Meissner corpuscle has often been described as a multi-afferented receptor. Electrophysiological studies have nonetheless identified only one neuron type attributed to the Meissner corpuscle: a fast-conducting, rapidly adapting detector of dynamic skin deformations and low-frequency vibrations known as the Aβ RAI-LTMR. We discovered that each Meissner corpuscle receives two myelinated afferent types, one that expresses Ret prior to embryonic day 11.5 and another that expresses TrkB prior to postnatal day 5. In vivo dorsal root ganglion (DRG) loose-patch recordings revealed that these neurons are both fast-conducting, rapidly adapting, and sensitive to innocuous touch. Furthermore, both neuronal types form terminals in the dorsal column nuclei, suggesting that both participate in the direct dorsal column pathway and may contribute to conscious tactile perception. In the skin, the peripheral receptive fields of both populations are homotypically tiled, and the majority of Meissner corpuscles receive both subtypes. This suggests an overlapping arrangement of developmentally orthogonal sensory neuron mosaics. We propose that such an architecture is optimal for ensuring complete coverage of the skin surface while encoding spatial detail in RAI population responses using the minimizing the number of neurons. Our findings support a new model in which the Meissner corpuscle contains two overlapping, parallel pathways that together provide a distributed representation of mechanical deformation of the skin.