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Tiling and somatotopic alignment of mammalian low-threshold mechanoreceptors

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  • Tiling and somatotopic alignment of mammalian low-threshold mechanoreceptors
    Search 10.1073/pnas.1901378116. at Scihub for full text.
    The sense of touch is essential for perceiving the physical world, sensory-motor control, and social exchange. The first step of touch perception is activation of low-threshold mechanoreceptor (LTMR) neurons that innervate the skin. LTMRs extend one axonal branch to the skin and another to the spinal cord dorsal horn. There exist at least five LTMR subtypes that innervate mouse hairy skin, each with distinct morphologies, response properties, and presumably functions. We used genetic labeling and whole-mount visualization strategies to reveal spatial relationships between axons of individual LTMRs across 2D areas of skin and the extent to which these relationships are topographically arranged within the 3D space of the spinal cord, uncovering organizational principles of the mammalian tactile sensory system.
    Innocuous mechanical stimuli acting on the skin are detected by sensory neurons, known as low-threshold mechanoreceptors (LTMRs). LTMRs are classified based on their response properties, action potential conduction velocity, rate of adaptation to static indentation of the skin, and terminal anatomy. Here, we report organizational properties of the cutaneous and central axonal projections of the five principal hairy skin LTMR subtypes. We find that axons of neurons within a particular LTMR class are largely nonoverlapping with respect to their cutaneous end organs (e.g., hair follicles), with Aβ rapidly adapting-LTMRs being the sole exception. Individual neurons of each LTMR class are mostly nonoverlapping with respect to their associated hair follicles, with the notable exception of C-LTMRs, which exhibit multiple branches that redundantly innervate individual hair follicles. In the spinal cord, LTMR central projections exhibit rostrocaudal elongation and mediolateral compression, compared with their cutaneous innervation patterns, and these central projections also exhibit a fine degree of homotypic topographic adjacency. These findings thus reveal homotypic tiling of LTMR subtype axonal projections in hairy skin and a remarkable degree of spatial precision of spinal cord axonal termination patterns, suggesting a somatotopically precise tactile encoding capability of the mechanosensory dorsal horn.