Payne, Jonathan Henry; (1993) The development of cutaneous sensory innervation in the rat. Doctoral thesis (Ph.D), UCL (University College London).

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Abstract

An electrophysiological and morphological study has been made of the postnatal development of innervation in the skin of the rat hindpaw. Extracellular recording from a total of 213 units at P(postnatal day)3, P10 and P20 revealed that receptive field properties are mature shortly after birth, and undergo only slight maturation thereafter. The mean receptive field size of units and their von Frey threshold to low-intensity cutaneous stimuli are similar at each age studied. It was found that from P10 to P20 rapidly adapting units in hairy skin fire more action potentials (response amplitude) to a fixed stimulus. There was a general increase in peak frequency of firing and conduction velocity. An attempt was made to alter these receptive field properties by extirpating a single dorsal root ganglion at PO. This presents neurons in adjacent ganglia with a greater amount of target tissue. The manipulation was found to produce an increase in receptive size and peak frequency of firing, restricted to units innervating hairy skin. The results from the developmental survey suggest that receptive field properties such as receptive field size and von Frey threshold are intrinsic to neurons. However, when the number of axons innervating an area of hairy skin is reduced by ganglionectomy, these properties exhibit a greater degree of plasticity. A variety of staining methods were used to investigate the anatomical development of sensory endings over this period. Winkelmann silver stain was used describe the development of endings on hair follicles and parvalbumen to describe that of Merkel cell-neurite complexes in glabrous skin. Maturation of these receptor-neurite complexes is not complete at P3 at which time receptive field properties are similar to those found at later ages. Calbinden D-28k and PGP (protein gene-product 9.5) are less specific neuronal markers and gave more generalized descriptions of the development of cutaneous innervation. The effect of the ganglionectomy described above on the morphology of endings was investigated, using PGP immunostaining. The results obtained suggest that endings of peripheral fibres maintain their original density of innervation when presented with an increased amount of target tissue, presumably as a result of local sprouting of endings. The overall conclusion from the project is that responses to skin stimlation are mature shortly after birth and probably before that (Fitzgerald, 1987). The later anatomical maturation of endings may produce discrete changes to the functional properties of neurons. Some functional plasticity of their receptive field properties is possible and this appears to be most marked for units in hairy skin. The early development of responses to skin stimulation may have considerable importance for the development of higher levels of the somatosensory system.

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