Skip to main content
NCBI home page
The Journal of Physiology logoLink to The Journal of Physiology
. 1997 Nov 15;505(Pt 1):177–191. doi: 10.1111/j.1469-7793.1997.00177.x

Relationship of substance P to afferent characteristics of dorsal root ganglion neurones in guinea-pig.

S N Lawson 1, B A Crepps 1, E R Perl 1
PMCID: PMC1160103  PMID: 9409481

Abstract

1. The relationship between the afferent properties and substance P-like immunoreactivity (SP-LI) of L6 and S1 dorsal root ganglion (DRG) neuronal somata was examined in anaesthetized guinea-pigs. Glass pipette microelectrodes filled with fluorescent dyes were used to make intracellular recordings and to label DRG somata. The dorsal root conduction velocity (CV) and the afferent receptive properties of each unit were categorized according to criteria established in other species. Categories included a variety of low threshold mechanoreceptive classes, innocuous thermoreceptive and several nociceptive classes. Nociceptive units were further subdivided on the basis of CV and the locus of the receptive field (superficial cutaneous, deep cutaneous or subcutaneous). 2. SP-LI was determined using the avidin-biotin complex method and the relative staining intensity determined by image analysis. The possible significance of labelling intensity is discussed. Clear SP-LI appeared in twenty-nine of 117 dye-labelled neurones. All SP-LI positive units with identified receptive properties were nociceptive but not all categories of nociceptors were positive. The intensity of SP-LI labelling varied, often systematically, in relation to afferent properties. There was a tendency for nociceptive neurones with slower CVs and/or smaller cell bodies to show SP-LI. 3. Nineteen of fifty-one C fibre neurones showed SP-LI. Fewer than half the C polymodal nociceptors (CPMs) were positive. The most intensely labelled units were the deep cutaneous nociceptors and some of the CPMs in glabrous skin. C low threshold mechanoreceptors and cooling-sensitive units did not show SP-LI. 4. Ten of sixty-six A fibre neurones exhibited SP-LI, including eight of sixteen A delta nociceptors and two of fifteen A alpha/beta nociceptors. A fibre neurones exhibiting SP-LI included seven of eight deep cutaneous mechanical nociceptors and some superficial cutaneous mechano-heat nociceptors of hairy skin. In contrast, none of twenty superficial cutaneous A high threshold mechanoreceptor units or the thirty-five A fibre low threshold units (D-hair and other units) showed detectable SP-LI. 5. We conclude that SP-LI labelling in guinea-pig DRG neurones is related to (a) afferent receptive properties, (b) the tissue in which the peripheral receptive terminals are located, (c) the CV and (d) the soma size.

Full text

PDF
177

Images in this article

180Figure 2
on p.180
182Figure 3
on p.182

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Bessou P., Burgess P. R., Perl E. R., Taylor C. B. Dynamic properties of mechanoreceptors with unmyelinated (C) fibers. J Neurophysiol. 1971 Jan;34(1):116–131. doi: 10.1152/jn.1971.34.1.116. [DOI] [PubMed] [Google Scholar]
  2. Bessou P., Perl E. R. Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J Neurophysiol. 1969 Nov;32(6):1025–1043. doi: 10.1152/jn.1969.32.6.1025. [DOI] [PubMed] [Google Scholar]
  3. Bharali L. A., Lisney S. J. The relationship between unmyelinated afferent type and neurogenic plasma extravasation in normal and reinnervated rat skin. Neuroscience. 1992;47(3):703–712. doi: 10.1016/0306-4522(92)90178-5. [DOI] [PubMed] [Google Scholar]
  4. Burgess P. R., Perl E. R. Myelinated afferent fibres responding specifically to noxious stimulation of the skin. J Physiol. 1967 Jun;190(3):541–562. doi: 10.1113/jphysiol.1967.sp008227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Duggan A. W., Hendry I. A., Morton C. R., Hutchison W. D., Zhao Z. Q. Cutaneous stimuli releasing immunoreactive substance P in the dorsal horn of the cat. Brain Res. 1988 Jun 7;451(1-2):261–273. doi: 10.1016/0006-8993(88)90771-8. [DOI] [PubMed] [Google Scholar]
  6. Harper A. A., Lawson S. N. Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol. 1985 Feb;359:31–46. doi: 10.1113/jphysiol.1985.sp015573. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hensel H., Iggo A. Analysis of cutaneous warm and cold fibres in primates. Pflugers Arch. 1971;329(1):1–8. doi: 10.1007/BF00586896. [DOI] [PubMed] [Google Scholar]
  8. Horch K. W., Tuckett R. P., Burgess P. R. A key to the classification of cutaneous mechanoreceptors. J Invest Dermatol. 1977 Jul;69(1):75–82. doi: 10.1111/1523-1747.ep12497887. [DOI] [PubMed] [Google Scholar]
  9. Hökfelt T., Kellerth J. O., Nilsson G., Pernow B. Substance p: localization in the central nervous system and in some primary sensory neurons. Science. 1975 Nov 28;190(4217):889–890. doi: 10.1126/science.242075. [DOI] [PubMed] [Google Scholar]
  10. Kuraishi Y., Hirota N., Sato Y., Hanashima N., Takagi H., Satoh M. Stimulus specificity of peripherally evoked substance P release from the rabbit dorsal horn in situ. Neuroscience. 1989;30(1):241–250. doi: 10.1016/0306-4522(89)90369-2. [DOI] [PubMed] [Google Scholar]
  11. Leah J. D., Cameron A. A., Snow P. J. Neuropeptides in physiologically identified mammalian sensory neurones. Neurosci Lett. 1985 May 23;56(3):257–263. doi: 10.1016/0304-3940(85)90252-6. [DOI] [PubMed] [Google Scholar]
  12. Lembeck F., Donnerer J., Tsuchiya M., Nagahisa A. The non-peptide tachykinin antagonist, CP-96,345, is a potent inhibitor of neurogenic inflammation. Br J Pharmacol. 1992 Mar;105(3):527–530. doi: 10.1111/j.1476-5381.1992.tb09013.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. McCarthy P. W., Lawson S. N. Cell type and conduction velocity of rat primary sensory neurons with substance P-like immunoreactivity. Neuroscience. 1989;28(3):745–753. doi: 10.1016/0306-4522(89)90019-5. [DOI] [PubMed] [Google Scholar]
  14. O'Brien C., Woolf C. J., Fitzgerald M., Lindsay R. M., Molander C. Differences in the chemical expression of rat primary afferent neurons which innervate skin, muscle or joint. Neuroscience. 1989;32(2):493–502. doi: 10.1016/0306-4522(89)90096-1. [DOI] [PubMed] [Google Scholar]
  15. Otsuka M., Yoshioka K. Neurotransmitter functions of mammalian tachykinins. Physiol Rev. 1993 Apr;73(2):229–308. doi: 10.1152/physrev.1993.73.2.229. [DOI] [PubMed] [Google Scholar]
  16. Réthelyi M., Mohapatra N. K., Metz C. B., Petrusz P., Lund P. K. Colchicine enhances mRNAs encoding the precursor of calcitonin gene-related peptide in brainstem motoneurons. Neuroscience. 1991;42(2):531–539. doi: 10.1016/0306-4522(91)90395-5. [DOI] [PubMed] [Google Scholar]
  17. Shea V. K., Perl E. R. Sensory receptors with unmyelinated (C) fibers innervating the skin of the rabbit's ear. J Neurophysiol. 1985 Sep;54(3):491–501. doi: 10.1152/jn.1985.54.3.491. [DOI] [PubMed] [Google Scholar]
  18. Stefanini M., De Martino C., Zamboni L. Fixation of ejaculated spermatozoa for electron microscopy. Nature. 1967 Oct 14;216(5111):173–174. doi: 10.1038/216173a0. [DOI] [PubMed] [Google Scholar]
  19. Tiseo P. J., Adler M. W., Liu-Chen L. Y. Differential release of substance P and somatostatin in the rat spinal cord in response to noxious cold and heat; effect of dynorphin A(1-17). J Pharmacol Exp Ther. 1990 Feb;252(2):539–545. [PubMed] [Google Scholar]
  20. Waddell P. J., Lawson S. N., McCarthy P. W. Conduction velocity changes along the processes of rat primary sensory neurons. Neuroscience. 1989;30(3):577–584. doi: 10.1016/0306-4522(89)90152-8. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES