In this paper the pattern of innervation of one of the simplest forms of skin, the integument of amphioxus (covering the dorsal fin in the middle third of the animal) is compared and contrasted with that of the cornea and of the skin in man. An account is given of the results of stimulation experiments in which the integument in this region was irradiated with infra-red rays. The observations which have been made can be summarized briefly as follows: 1. No neuro-epithelial cells were encountered in the epidermis in the region chosen for study. 2. Evidence is given which suggests that the nuclei along the course of the nerve-trunks which combine to form the ‘dorsal roots’ of the nerve-cord are not those of the first sensory neurone. They appear to be analogous to the Schwann-cell nuclei of vertebrates. 3. The ratio of epidermal cells to parent sensory axons in randomly selected metameres of integument in the selected region is as low as 7:1. From this it has been calculated that the density of innervation is comparable with that in the cornea and in the skin of vertebrates. 4. Every epidermal cell has two or more terminal filaments ending in relationship to it. 5. Pre-terminal axons from parent axons of different diameters are widely and apparently randomly scattered beneath the epidermis. 6. Each and every epidermal cell is related to terminals which approach from different directions and serve more than one parent axon. 7. The patterned arrangement of the nerves serving the integument of amphioxus is comparable with that observed in the skin of teleost fish, in the cornea of a number of vertebrate species, and in the skin of man. 8. The nerves in the integument in the selected region can transduce non-injurious infra-red stimuli, although the stimuli were of a kind not normally encountered by the animal in its natural habitat. 9. In the light of these observations and of experimental observations in man (Weddell, 1955; Lele and Weddell, 1956; Weddell, 1957), it is difficult to subscribe to the notion that information concerning the environment is transmitted to the central nervous system from the skin by a restricted series of nerves having terminals which only transduce stimuli having quite specific physical attributes. Rather, it seems likely that information reaches the central nervous system in the form of a space-time pattern of action potentials from endings which are either more or less available to a range of stimuli having different physical characteristics. In other words, different stimuli must evoke different patterns of activity, which are analysed by the central nervous system acting in a role of an analogue as opposed to a digital computer.
1. An account is given of the innervation of the skin from selected regions of the body in man, the rhesus monkey, and the rabbit. It is based on a critical evaluation of methylene blue and silver preparations in skin which had been treated with the enzyme hyaluronidase before removal from the body and in skin which had not thus been treated. 2. The nerve fibres and terminals in preparations treated with hyaluronidase resemble those seen in fresh specimens of cornea under phase contrast conditions. 3. The numerous artifacts seen in the cornea following methylene blue staining or silver impregnation, the origin of which is known, resemble those seen in specimens of skin not treated with hyaluronidase. 4. It is shown that cutaneous nerves ultimately terminate in an arborization of fine naked axoplasmic filaments. The naked filaments always arise from ensheathed stem fibres of varying diameters and they all end freely and extracellularly in relation to a variety of tissue elements in the skin. 5. The actual terminal filaments wherever they end in relation to the epidermis, dermal connective tissue, blood-vessels, sweat glands, hair follicles, or within capsules of epithelial cells, cannot be distinguished from one another on the basis of inherent morphological differences. 6. Terminal filaments from neighbouring stem fibres are always intimately related to one another and to the tissues in which they lie. 7. The stem fibres and axoplasmic filaments to which they give rise in encapsulated endings and hair follicles are so arranged that the slightest deformation of capsule or of follicle will alter the relationship of the terminal filaments to their stem fibres. 8. Encapsulated nerve-endings may be served by more than one stem fibre but none of the terminals of these fuse with one another. Likewise, the terminals derived from individual stem fibres ending in relation to hair follicles do not enter into protoplasmic continuity with one another. 9. The number and length of the axoplasmic filaments varies greatly from stem fibre to stem fibre. 10. Our observations on the behaviour of the cutaneous nerve fibres and their terminals under different histological conditions provides us with a standard by which we can distinguish artifacts and thus re-evaluate the observations on cutaneous innervation which have been reported in the literature. 11. Evidence is brought forward which suggests that the naked axoplasmic filaments derived from sensory stem fibres may be responsible for ‘flare’ and other ‘nocifensor reactions’ (Lewis), in addition to and apart from their sensory functions. 12. The relationship of these observations to the mechanism of cutaneous sensibility is discussed.