Architecture and function of lamellar cells in Meissner corpuscle

Meissner corpuscles detect transient touch and vibration in glabrous skin, but their ultrastructure and mechanism of function are poorly understood. The Meissner corpuscle sensory core contains the terminal neurite(s) of the mechanoreceptor afferent surrounded by Schwann cell-derived lamellar cells. The afferent is thought to be the sole touch-sensing element within the corpuscle, whereas the role of lamellar cells is unclear. Here, we present a high-resolution three-dimensional ultrastructure of an avian Meissner (Grandry) corpuscle in intact skin acquired using the enhanced focused ion beam scanning electron microscopy (FIB-SEM), followed by machine learning based segmentation and reconstruction. We show that the afferent splits within the corpuscle into several disk-shaped endings layered between flattened lamellar cells. Each lamellar cell contains numerous exocytotic dense core vesicles and forms large-area contacts with adjacent afferent disks. Together with single-corpuscle RNA sequencing and electrophysiology, our FIB-SEM data reveal lamellar cells as secretory sensors of touch. We developed a method for direct electrophysiological recordings of afferent activity from an individual corpuscle in the skin and show that activation of a single mechanosensitive lamellar cell is sufficient to trigger action potentials in the afferent. These results reveal comprehensive Meissner (Grandry) corpuscle architecture and demonstrate a dual sensory mechanism comprised of a mechanoreceptor afferent and lamellar cells. Overall design: Gene expression analysis and differential transcriptomics of single Meissner corpuscles (n = 5 biological replicates) compared to bill skin (n=6 biological replicates) in duck.