Central anatomy of individual rapidly adapting low-threshold mechanoreceptors innervating the "hairy" skin of newborn mice: Early maturation of hair follicle afferents

Adult skin sensory neurons exhibit characteristic projection patterns in th e dorsal horn of the spinal gray matter that are tightly correlated with mo dality. However, little is known about how these patterns come about during the ontogeny of the distinct subclasses of skin sensory neurons. To this e nd, we have developed an intact ex vivo somatosensory system preparation in neonatal mice, allowing single, physiologically identified cutaneous affer ents to be iontophoretically injected with Neurobiotin for subsequent histo logical analyses. The present report, centered on rapidly adapting mechanor eceptors, represents the first study of the central projections of identifi ed skin sensory neurons in neonatal animals. Cutaneous afferents exhibiting rapidly adapting responses to sustained natural stimuli were encountered a s early as recordings were made. Well-stained representatives of coarse (ty lotrich and guard) and fine-diameter (down) hair follicle afferents, along with a putative Pacinian corpuscle afferent, were recovered from 2-7-day-ol d neonates. All were characterized by narrow, uninflected somal action pote ntials and generally low mechanical thresholds, and many could be activated via deflection of recently erupted hairs. The central collaterals of hair follicle afferents formed recurrent, flame-shaped arbors that were essentia lly miniaturized replicas of their adult counterparts, with identical lamin ar terminations. The terminal arbors of down hair afferents, previously und escribed in rodents, were distinct and consistently occupied a more superfi cial position than tylotrich and guard hair afferents. Nevertheless, the fo rmer extended no higher than the middle of the incipient substantia gelatin osa, leaving a clear gap more dorsally. In all major respects, therefore, h air follicle afferents display the same laminar specificity in neonates as they do in adults. The widely held misperception that their collaterals ext end exuberant projections into pain-specific regions of the dorsal horn dur ing early postnatal life is shown to have multiple, deep-rooted underpinnin gs. (C) 2001 Wiley-Liss, Inc.