Domains and mechanosensory nerve fields in salamander skin

Abstract

We have studied, in the salamander (Ambystoma tigrinum), an apparent hindrance to the sprouting of certain segmental nerves into adjacent skin supplied by neighbouring segmental nerves. The mechanosensory fields of the dorsal skin of the hindlimb were examined by recording the afferent impulses evoked by a fine bristle applied to the skin. Three segmental nerves normally supply the hindlimb, and together divide the dorsal skin into two major mechanosensory fields, an anterior one innervated by both the 15th spinal nerve (N15) and the anterior division of N16 (N16A), and a posterior one innervated by N17 and N16P. Denervations were done so as to leave only one of the two major fields intact, that of N15 (with or without an intact N16A) or of N17 (with or without N16P). The results were surprising: after a small (but significant) expansion of the remaining N15 or N17 field the sprouting of either of these nerves into the adjacent denervated skin ceased for a total post-operative period of at least two months; however, when N16A or N16P was present the N16 axons sprouted apparently without hindrance into the adjacent skin (showing that there was nomechanicalbarrier to sprouting at the frontier zone). The failure of N15 or N17 to invade the adjacent territory was not be­cause their axons had reached an upper limit in their capacity to enlarge the size of their terminal fields: when a proportion of the axons of a remaining N17 was eliminated, the remainder sprouted progressively over the following weeks. Significantly they invaded denervated skin that was almost entirely confined to the territory of the ‘parent’ N17; the immedi­ately adjacent skin formerly supplied by N15 was largely ignored. These results, and similar ones for N14, N16 and N18, suggest that the seg­mental cutaneous axons are hindered from sprouting to any great extent into skin normally occupied by a neighbouring segmental nerve, even when that nerve is removed. The axons will sprout readily within the territory of the parent nerve, and we call these territories ‘domains’; their borders usually correspond fairly closely to those of the segmental dermatomesRegeneratingnerves freely invaded ‘foreign’ skin, and thus were not susceptible to these spatial constraints. After a two month period the intact axons of a remaining N17 began freely to invade the adjacent domain, as though the constraint had suddenly disappeared. To test for skin ‘specificity’, skin flaps were excised, and reimplanted after rotation by 0-180°, in limbs that were either fully innervated or partially dener­vated. In about half of the instances the segmental nerves sprouted to re-establish their former spatial territories in the flapswith respect to the coordinates of the limb, without regard for the type of skin that they inner­vated (i.e. their former skin or ‘foreign’ skin). In the remaining cases the invasion of the flaps was often indiscriminate, as though byregeneratingnerves. The spatial constraint thus seemed to operate at thebordersof domains, and to relate to the limb as a whole, rather than to skin itself. The possible genesis of domains, and their significance, are discussed.