Physiological properties of primary sensory neurons appropriately and inappropriately innervating skin in the adult rat.
1. We have studied the physiology of sensory neurons innervating skin of the rat hindlimb, in three groups of animals: 1) normal animals; 2) animals in which the sural nerve (Sn) had regenerated to its original cutaneous target; and 3) animals in which the gastrocnemius muscle nerve (Gn) had previously been cut and cross anastomosed with the distal stump of the cut Sn so that its axons regenerated to a foreign target, skin. 2. Single-unit recordings were made from 222 afferents in normal, intact animals. They had conduction velocities of 0.5-53.1 m/s. The conduction velocity distribution had distinct peaks at approximately 37.5, 2.5, and 1.25 m/s, presumably corresponding to A alpha beta-, A delta-, and C-fiber populations. Eighty-two percent of the characterized myelinated fibers had low-threshold mechanosensitive receptive fields, whereas 16% were high threshold, and only 2% appeared to have no receptive field. The very large majority of low-threshold mechanosensitive receptive fields (87%) were rapidly adapting hair follicle afferents. 3. In animals with regenerated Sn, 308 afferents were recorded with conduction velocities of 0.4-58.8 m/s. However, the mean conduction velocity was lower than in control animals (P less than 0.05), and only one peak, at 27.5 m/s, was apparent for myelinated fibers. Eighty-six percent of myelinated fibers were low-threshold mechanosensitive afferents, 8.5% were high-threshold mechanoreceptors (HTMRs), and 5.5% appeared to have no receptive fields. Fewer low-threshold mechanoreceptors (LTMRs; compared with controls) were activated by hair movement (63 vs. 87%). Most of the remainder appeared to be field receptors (which were therefore more commonly observed here than in normal animals). 4. In animals in which the Gn had regenerated to skin, 430 afferents were recorded. These had conduction velocities ranging from 0.6 to 71.4 m/s, and again only one peak was apparent in the myelinated conduction velocity histogram, at approximately 17.5 m/s. Of the myelinated fibers, 79% had low-threshold mechanosensitive receptive fields in skin and 10% high-threshold mechanosensitive receptive fields. The remaining 11% apparently had no receptive field (cf. 5.5% in regenerated Sn). In contrast to normal or regrown sural afferents, only 58% of low-threshold gastrocnemius afferents in skin were rapidly adapting. Of the 42% slowly adapting afferents, many surprisingly responded to hair movement. Thus some gastrocnemius afferents seemed to have retained the adaptation properties characteristic of muscle afferents. Also surprisingly, given that the Gn contains fewer fibers than the Sn, receptive-field areas were not significantly different from regrown or normal sural fibers.(ABSTRACT TRUNCATED AT 400 WORDS)
Lewin
G R
GR
United Medical School, London, United Kingdom.
McMahon
S B
SB
D000818:Animals; D001369:Axons / Q000502:physiology; D004594:Electrophysiology; D005528:Foot / Q000294:innervation; D006614:Hindlimb / Q000294:innervation / Q000502:physiology; D008297:Male; D008465:Mechanoreceptors / Q000502:physiology; D009132:Muscles / Q000294:innervation; D009186:Myelin Sheath / Q000502:physiology; D009411:Nerve Endings / Q000187:drug effects; D009412:Nerve Fibers / Q000502:physiology; D009416:Nerve Regeneration / Q000502:physiology; D009431:Neural Conduction / Q000502:physiology; D009475:Neurons, Afferent / Q000502:physiology*; D051381:Rats; D011919:Rats, Inbred Strains; D012684:Sensory Thresholds / Q000502:physiology; D012867:Skin / Q000294:innervation*; D013116:Spinal Cord / Q000166:cytology / Q000502:physiology; D013497:Sural Nerve / Q000502:physiology