Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Article
  • Published:

Are there separate central nervous system pathways for touch and pain?

Abstract

Information about bodily events is conveyed by primary sensory fibres to higher brain centres through neurons in the dorsal column nuclei (DCN) and spinal dorsal horn. The DCN route is commonly considered a ‘touch pathway’, separate from the spinal ‘pain pathway’, in part because DCN neurons respond to gentle tactile stimulation of small skin areas. Here we report that DCN neurons can additionally respond to gentle and noxious stimulation of viscera and widespread skin regions. These and other experimental and clinical data suggest that the DCN and spinal routes cooperate, rather than operate separately, to produce the many perceptions of touch and pain, an ensemble view that encourages novel approaches to health care and research.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Spiller, W.G. & Martin, E. The treatment of persistent pain of organic origin in the lower part of the body by division of the flnterolateral column of the spinal cord. JAMA 58, 1489–1490 (1912).

    Google Scholar 

  2. Willis, W.D. Jr & Coggeshall, R.E. Sensory Mechanisms of the Spinal Cord, 2nd edn (Plenum, New York, 1991).

    Google Scholar 

  3. McMahon, S.B., Lewin, G.R. & Wall, P.D. Central hyperexcitability triggered by noxious inputs. Curr. Opin. Neurobiol. 3, 602–610. 1993.

    CAS  PubMed  Google Scholar 

  4. Fields, H.L. & Liebskind, J.C. (eds) Pharmacological Approaches to the Treatment of Chronic Pain: New Concepts and Critical Issues (IASP Press, Seattle, 1994).

    Google Scholar 

  5. Gybels, J.M. & Sweet, W.H. Neurosurgical treatment of peristent pain. in Pain and Headache, vol 11 (ed. Gildenberg, P.L.) 1–442 (Karger, Basel, 1989).

    Google Scholar 

  6. Maslany, S., Crockett, D.P. & Egger, M.D. Soniatotopic organization of the dorsal column nuclei in the rat: Transganglionic labelling with B-HRP and WGA-HRP. Brain Res. 564, 56–65. 1991.

    CAS  PubMed  Google Scholar 

  7. Berkley, K.J., Budell, R.J., Blomqvist, A. & Bull, M.S. Output systems of the dorsal column nuclei in the cat. Brain Res. Rev. 11, 199–225. 1986.

    Google Scholar 

  8. McMahon, S.B. & Wall, P.D. Plasticity in the nucleus gracilis of the rat. Exp. Neurol. 80, 195–207. 1983.

    CAS  PubMed  Google Scholar 

  9. Nathan, P.W., Smith, M.C. & Cook, A.W. Sehsory effects in man of lesions of the posterior columns and of some other afferent pathways. Brain 109, 1003–1041. 1986.

    PubMed  Google Scholar 

  10. Berkley, K.J., Robbins, A. & Sato, Y. Functional differences between afferent fibers in the hypogastric and pelvic nerves innervating female reproductive organs in the rat. J. Neurophysiol. 69, 533–544. 1993.

    CAS  PubMed  Google Scholar 

  11. Berkley, K.J., Wood, E., Scofield, S.L. & Little, I.M. Behavioral responses to uterine or vaginal distension in the rat. Pain 61, 121–131. 1995.

    CAS  PubMed  Google Scholar 

  12. Berkley, K.J., Hubscher, C.H. & Wall, P.D. Neiironal responses to stimulation of the cervix, uterus, colon and skin in the rat spinal cord. J. Neurophysiol. 69, 545–556. 1993.

    CAS  PubMed  Google Scholar 

  13. Berkley, K.J., Guilbaud, G., Benoist, J.M. & Gautron, M. Responses of neurons in and near the thalamic ventrobasal complex of the rat to stimulation of uterus, cervix, vagina, colon and skin. J. Neurophysiol. 69, 557–568. 1993.

    CAS  PubMed  Google Scholar 

  14. Apkarian, A.V., Bruggemann, J., Shi, T. & Airapftian, L.R. A thalamic model for referred pain. in Visceral Pain (ed.Gebhart, G.F.) 217–259 (IASP Press, Seattle, 1995).

    Google Scholar 

  15. Cliffer, K.D. & Giesler, G.J. Jr Postsynaptic d0rsal column pathway of the rat III. Distribution of ascending afferent fibers. J. Neurosci. 9, 3146–3168. 1989.

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Cechetto, D.F. Central representation of visceral function. Fed. Proc. 46, 17–23. 1987.

    CAS  PubMed  Google Scholar 

  17. Hubscher, C.H. & Berkley, K.J. Responses of neurons in caudal solitary nucleus of female rats to stimulation of vagina, cervix, uterine horn and colon. Brain Res. 664, 1–8. 1994.

    CAS  PubMed  Google Scholar 

  18. DeLorey, T.M. & Olsen, R.W. GABA and glycine.in Basic Neurochemistry: Molecular, Cellular, and Medical Aspects5th edn (eds Siegel, G.J., Agranoff, B.W., Albers, R.W. & Molinoff, P.B.) 389–399 (Raven, New York, 1994).

    Google Scholar 

  19. Gahery, Y. & Vigier, D. Inhibitory effects in the cuneate nucleus produced by vago-aortic afferent fibers. Brain Res. 75, 241–246. 1974.

    CAS  PubMed  Google Scholar 

  20. Rigamonti, D.D. & Hancock, M.B. Viscerosomatic convergence in the dorsal column nuclei of the cat. Exp. Neurol. 61, 337–348. 1978.

    CAS  PubMed  Google Scholar 

  21. Feldman, S.G. & Kruger, L. An axonal transport study of the ascending projection of medial lemniscal neurons in the rat. J. comp. Neurol. 192, 427–454. 1980.

    CAS  PubMed  Google Scholar 

  22. Pfaff, D.W., Schwartz-Giblin, S., McCarthy, M.M. & Kow, L.M. Cellular and molecular mechanisms of female reproductive behaviors. in The Physiology of Reproduction, 2nd edn, vol 2 (eds Knobil, E. et al) 107–220 (Raven, New York, 1994).

    Google Scholar 

  23. Neuhuber, W. The central projections of visceral primary afferent neurons of the inferior mesenteric plexus and hypogastric nerve and the location of the related sensory and preganglionic sympathetic cell bodies in the rat. Anat. Embryol. 164, 413–425. 1982.

    CAS  PubMed  Google Scholar 

  24. Coggeshall, R.E. Unmyelinated primary afferent fibers in the dorsal column, a possible alternate ascending pathway for noxious information. in Recent Achievements in Restorative Neurology, vol 3, Altered Sensation and Pain (eds Dimitrijevic, M.R., Wall, P.D. & Lindblom, U.) 128–131 (Karger, Basel, 1990).

    Google Scholar 

  25. Giuffrida, R. & Rustioni, A. Dorsal root ganglion neurons projecting to the dorsal column nuclei of rats. J. comp. Neurol. 316, 206–220. 1992.

    CAS  PubMed  Google Scholar 

  26. De Pommery, J., Roudier, F. & Menetrey, D. Postsynaptic fibers reaching the dorsal column nuclei in the rat. Neurosci. Lett. 50, 319–323. 1984.

    CAS  PubMed  Google Scholar 

  27. Weinberg, R.J. & Rustioni, A. Brainstem projections to the rat cuneate nucleus. J. comp. Neurol. 282, 142–156. 1989.

    CAS  PubMed  Google Scholar 

  28. Cliffer, K.D., Hasegawa, T. & Willis, E.D. Responses of neurons in the gracile nucleus of cats to innocuous and noxious stimuli: Basic characterization and antidromic activation from the thalamus. J. Neurophysiol. 68, 818–832. 1992.

    CAS  PubMed  Google Scholar 

  29. Dostrovsky, J.O. & Millar, J. Receptive fields of gracile neurons after transection of the dorsal columns. Exp. Neurol. 56, 610–621. 1977.

    CAS  PubMed  Google Scholar 

  30. Davidson, N. & Southwick, C.A.P. Amino acids and presynaptic inhibition in the rat cuneate nucleus. J. Physiol. (Lond.) 219, 689–708. 1971.

    CAS  Google Scholar 

  31. Weinberg, R.J., Pierce, J.P. & Rustioni, A. Single fiber studies of ascending input to the cuneate nucleus of cats I. Morphometry of primary afferent fibers. J. comp. Neurol. 300, 113–133. 1990.

    CAS  PubMed  Google Scholar 

  32. Wall, P.D. Do nerve impulses penetrate terminal arborizations? A pre-presynap-tic control mechanism. Trends Neurosci. 18, 99–103. 1995.

    CAS  PubMed  Google Scholar 

  33. Barbaresi, P., Spreafico, R., Frassoni, C. & Rustioni, A. GABAergic neurons are present in the dorsal column nuclei but not in the ventroposterior complex of rats. Brain Res. 382, 305–326. 1986.

    CAS  PubMed  Google Scholar 

  34. Banna, N.R. & Jabbur, S.J. Neurochemical transmission in the dorsal column nuclei. Somatosens. Motor Res. 6, 237–251. 1989.

    CAS  Google Scholar 

  35. Pettit, M.J. & Schwark, H.D. Receptive field reorganization in dorsal column nuclei during temporary denervation. Science 262, 2054–2056. 1993.

    CAS  PubMed  Google Scholar 

  36. Dostrovsky, J.O., Millar, J. & Wall, P.D. The immediate shift of afferent drive of dorsal column nucleus cells following deafferentation: A comparison of acute and chronic deafferentation in gracile nucleus and spinal cord. Exp. Neurol. 52, 480–495. 1976.

    CAS  PubMed  Google Scholar 

  37. Frye, C.A., Cuevas, C.A. & Kanarek, R.B. Diet and estrous cycle influence pain sensitivity in rats. Biochem. Behav. 45, 255–260. 1993.

    CAS  Google Scholar 

  38. Lahuerta, J., Bowsher, D., Lipton, S. & Buxton, P.H. Percutaneous cervical cor-dotomy: A review of 181 operations on 146 patients with a study on the location of ‘pain fibers’ in the C-2 spinal cord segment of 29 cases. J. Neurosurg. 80, 975–985. 1994.

    CAS  PubMed  Google Scholar 

  39. White, J.C. & Sweet, W.H. Pain and the Neurosurgeon (Charles C Thomas, Springfield, Illinois, 1969).

    Google Scholar 

  40. Gildenberg, P.L. & Hirshberg, R.M. Limited myelotomy for the treatment of intractable cancer pain. J. Neurol. Neurosurg. Psychiat. 47, 94–96. 1984.

    CAS  PubMed  Google Scholar 

  41. Saadé, N.E. et al. Supraspinal modulation of nociception in awake rats by stimulation of the dorsal column nuclei. Brain Res. 369, 307–310. 1986.

    PubMed  Google Scholar 

  42. Saadé, N.E., Atweh, S.F., Jabbur, S.J. & Wall, P.D. Effects of lesions in the an-terolateral columns and dorsolateral funiculi on self-mutilation behavior in rats. Pain 42, 313–321. 1990.

    PubMed  Google Scholar 

  43. Berkley, K.J. Suspension of neural pathways for pain and nociception. J. Cardiovasc. Electrophysiol. 2, S13S17 1991.

    Google Scholar 

  44. Krainick, J.U. & Thoden, U. Spinal cord stimulation. in Textbook of Pain, 3rd edn (eds Wall, P. D. & Melzack, R.) 1219–1223 (Churchill Livingstone, Edinburgh, 1994.).

    Google Scholar 

  45. Triggs, W.J. & Beric, A. Dysaesthesiae induced by physiological and electrical activation of posterior column afferents after stroke. J. Neurol. Neurosurg. Psychiat. 57, 1077–1081. 1994.

    CAS  PubMed  Google Scholar 

  46. Ranee, N.E., McArthur, J.C., Cornblath, D.R., Landstrom, D.L., Griffin, J.W. & Price, D.L. Gracile tract degeneration in patients with sensory neuropathy and AIDS. Neurology 38, 265–271. 1988.

    Google Scholar 

  47. Wall, P.D. & Noordenbos, W. Sensory functions which remain in man after complete transections of dorsal columns. Brain 100, 641–653. 1977.

    CAS  PubMed  Google Scholar 

  48. Melzack, R. Phantom limbs, the self and the brain (the D.O. Hebb memorial lecture). Can. Psychol. 30, 1–16. 1989.

    Google Scholar 

  49. Wall, P.D. Introduction to the edition after this one. in Textbook of Pain, 3rd edn (eds Wall, P.D. & Melzack, R.) 1–7 (Churchill Livingstone, Edinburgh, 1994).

    Google Scholar 

  50. Damassio, A.R. Descartes Error (Putnam's Sons, New York, 1994).

    Google Scholar 

  51. Beric, A., Dimitrijevic, M.R. & Lindblom, U. Central dysesthesia syndrome in spinal cord injury patients. Pain 34, 109–116. 1988.

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berkley, K., Hubscher, C. Are there separate central nervous system pathways for touch and pain?. Nat Med 1, 766–773 (1995). https://doi.org/10.1038/nm0895-766

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nm0895-766

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing