The early ontogeny of the afferent nerves and papillary ridges in human digital glabrous skin

Abstract

The present study examines the early ontogeny of afferent nerves in human embryonic glabrous digital skin and documents the onset of cutaneous innervation and papillary (sweat duct) ridge formation by light and electron microscopy. The skin examined in this study was taken from 3 developmental stages of decreasing embryonic age: embryos older than 10 weeks estimated gestational age (EGA) representing the period of primary ridge formation, embryos of 8–9 weeks EGA representing the period immediately prior to ridge formation; and embryos 6–8 weeks EGA representing the period weeks before the onset of ridge formation. The earliest papillary ridges are present in 10 week EGA embryos, with small ridges present in two sites: the center of the proximal third and also at the tip of the distal phalangeal or apical pad. These papillary ridges typically contained Merkel cells. Papillary ridges formed progressively in a radial manner from these central foci. The proximal focus corresponds to the geometric center of the mature dermatoglyphic pattern of loops, arches, or whorls. This radial wave of ridge differentiation is discontinuous with the abrupt cessation of ridge formation responsible for the discontinuities in the mature papillary ridges and the corresponding dermatoglyphic print. Skin over the proximal and middle phalanges developed papillary ridges beginning in the 12th week. No papillary ridges could be identified in embryos of 8–9 weeks EGA, but a large number of growth cones are present in the superficial dermis subjacent to differentiating Merkel cells. The basal lamina of the epidermis was discontinuous wherever growth cones abutted Merkel cells. Merkel cells not directly associated with axons were also present in the epidermis of embryos of 8–9 weeks EGA. The embryos of 6–8 weeks EGA lack any sign of Merkel cells and/or melanocytes, but developing neurovascular bundles with axonal growth cones near the epidermis could be identified by light and electron microscopy. Presumptive Schwann and perineural cells are also seen in the dermis. We conclude that the developing afferent nerve fibers provide a grid which influences the temporal and/or spatial factors involved in the sequential onset and cessation of formation of papillary ridges. Thus the dermatoglyph can reflect the ontogeny of the afferent nervous system that occurred prior to papillary ridge development. These observations lend support to the concept that successive waves of afferent neural development have an important role in the spatial and temporal sequence of papillary ridge formation and thus the formation of both the dermatotopic map of the digits and the dermatoglyph.