Skip to main content
SpringerLink
Log in

Modern concepts on the mechanisms of encoding visceral nociceptive stimuli

  • Published:
Human Physiology Aims and scope Submit manuscript

Abstract

This paper reviews the existing concepts on the physiology of visceral pain and mechanisms of processing nociceptive stimuli at the level of sensor neurons of surface segments of the spinal dorsal horns. Data on the ion channels and receptors involved in the transduction of the pain signals are discussed.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Sherrington, Ch., Integrativnaya deyatel’nost’ nervnoi sistemy (The Integrative Action of the Nervous System), Leningrad, 1969.

  2. Almeida, T.F., Roizenblatt, S., and Tufik, S., Afferent Pain Pathways: A Neuroanatomical Review, Brain Res., 2004, vol. 1000, nos. 1–2, p. 40.

    Article  CAS  PubMed  Google Scholar 

  3. Chernigovskii, V.N., Interotseptory (Interoceptors), Moscow: Medgiz, 1960.

    Google Scholar 

  4. Nozdrachev, A.D., Kortikosteroidy i simpaticheskaya nervnaya sistema (Corticosteroids and the Sympathetic Nervous System), Leningrad: Nauka, 1969.

    Google Scholar 

  5. Nozdrachev, A.D., Vegetativnaya reflektornaya duga (Autonomic Reflex Arc), Leningrad: Nauka, 1978.

    Google Scholar 

  6. Nozdrachev, A.D., Fiziologiya vegetativnoi nervnoi sistemy (Physiology of the Autonomic Nervous System), Leningrad: Meditsina, 1983.

    Google Scholar 

  7. Jänig, W. and Koltzenburg, M., On the Function of Spinal Primary Afferent Fibres Supplying Colon and Urinary Bladder, J. Autonom. Nerv. Syst., 1990, vol. 30.

  8. Nozdrachev, A.D., Two Views on the Metasympathetic Nervous System, Ros. Fiziol. Zh. im. I.M. Sechenova, 1991, vol. 77, issue 9, p. 21.

    Google Scholar 

  9. Jänig, W., Neurobiology of Visceral Afferent Neurons: Neuroanatomy, Functions, Organ Regulations and Sensation, Biol. Physiol., 1996, vol. 42, p. 29.

    Google Scholar 

  10. Bagaev, V.A., Nozdrachev, A.D., and Panteleev, S.S., Vagovagal’naya reflektornaya duga. Elementy strukturno-funktsional’noi organizatsii (The Vagovagal Reflex Arc: Structural-Functional Organization Elements), St. Petersburg: St. Peterb. Gos. Univ., 1997.

    Google Scholar 

  11. Mileikovskii, B.Yu. and Nozdrachev, A.D., Tormozhenie dvigatel’noi aktivnosti. Stvolovye mekhanizmy (Inhibition of Locomotor Activity: Stem Mechanisms), St. Petersburg: St. Peterb. Gos. Univ., 1998.

    Google Scholar 

  12. Nozdrachev, A.D. and Chumasov, E.I., Perifericheskaya nervnaya sistema: struktura, razvitie, transplantatsiya i regeneratsiya (Peripheral Nervous System: Structure, Development, Transplantation, and Regeneration), St. Petersburg: Nauka, 1999.

    Google Scholar 

  13. Jänig, W., Khasar, S.G., Levine, J.D., and Miao, F.J.-P. The Role of Vagal Visceral Afferents in the Control of Nociception, Prog. Brain Res., 2000, vol. 22, p. 273.

    Google Scholar 

  14. Jänig, W. and Habler, H.J., Physiology and Pathophysiology of Visceral Pain, Schmerz, 2002, vol. 16, no. 6, p. 429.

    Article  PubMed  Google Scholar 

  15. Nozdrachev, A.D., Bazhenov, Yu.I., Barannikova, I.A., et al., Nachala fiziologii (Principles of Physiology), St. Petersburg: Lan’, 1988.

    Google Scholar 

  16. Nozdrachev, A.D. and Fateev, M.M., Zvezdchatyi ganglii. Struktura i funktsii (Stellate Ganglion: Structure and Functions), St. Petersburg: Nauka, 2002.

    Google Scholar 

  17. Breslav, I.S. and Nozdrachev, A.D., Dykhanie. Vistseral’nyi i povedencheskii aspekty (Respiration: Visceral and Behavioral Aspects), St. Petersburg: Nauka, 2005.

    Google Scholar 

  18. Jänig, W., The Integrative Action of the Autonomic Nervous System. Neurobiology of Homeostasis, Cambridge: University Press, 2006.

    Google Scholar 

  19. Filippova, L.V. and Nozdrachev, A.D., Interotseptsiya i neiroimmunnye vzaimodeistviya (Interoception and Neuroimmune Interactions), St. Petersburg: Nauka, 2007.

    Google Scholar 

  20. Melzack, R. and Wall, P.D., Pain Mechanisms: A New Theory, Science, 1965, vol. 150, no. 3699, p. 971.

    Article  CAS  PubMed  Google Scholar 

  21. Gebhart, G.F., Pathobiology of Visceral Pain: Molecular Mechanisms and Therapeutic Implications. IV. Visceral Afferent Contributions to the Pathobiology of Visceral Pain, Amer. J. Physiol. Gastrointest. Liver Physiol., 2000, vol. 278, p. G834.

    CAS  Google Scholar 

  22. Kirkup, A.J., Brunsden, A.M., and Grundy, D., Receptors and Transmission in the Brain-Gut Axis: Potential for Novel Therapies. 1. Receptors on Visceral Afferents, Am. J. Physiol. Gastrointest. Liver Physiol., 2001, vol. 280, p. G787.

    CAS  PubMed  Google Scholar 

  23. Grundy, D., What Activates Visceral Afferents?, Gut, 2004, vol. 53, no. Suppl. 2, p. 15.

    Google Scholar 

  24. McMahon, S.B., Sensitisation of Gastrointestinal Tract Afferents, Gut, 2004, vol. 53, p. 13.

    Article  Google Scholar 

  25. Coderre, T.J., Katz, J., Vaccarino, A.L., and Melzack, R., Contribution of Central Neuroplasticity to Pathological Pain: Review of Clinical and Experimental Evidence, Pain, 1993, vol. 52, p. 259.

    Article  CAS  PubMed  Google Scholar 

  26. Kukushkin, M.L. and Khitrov, N.K., Obshchaya patologiya boli: rukovodstvo dlya vrachei (General Pain Pathology: A Physician’s Guide), Moscow, 2004.

  27. Ren, K. and Dubner, R., Enhanced Descending Modulation of Nociception in Rats with Persistent Hindpaw Inflammation, J. Neurophysiol., 1996, vol. 76, p. 3025.

    CAS  PubMed  Google Scholar 

  28. McNally, G.P., Pain Facilitatory Circuits in the Mammalian Central Nervous System: Their Behavioral Significance and Role in Morphine Analgesic Tolerance, Neurosci. Biobehav. Rev., 1999, vol. 23, p. 1059.

    Article  CAS  PubMed  Google Scholar 

  29. Urban, M.O. and Gebhart, G.F., Supraspinal Contributions to Hyperalgesia, Proc. Natl. Acad. Sci. USA, 1999, vol. 96, no. 14, p. 7687.

    Article  CAS  PubMed  Google Scholar 

  30. Kiss, J.P. and Vizi, S., Nitric Oxide: A Novel Link between Synaptic and Nonsynaptic Transmission, Trends Neurosci., 2001, vol. 4, p. 211.

    Article  Google Scholar 

  31. Millan, M.J., Descending Control of Pain, Prog. Neurobiol., 2002, vol. 66, p. 355.

    Article  CAS  PubMed  Google Scholar 

  32. Graham, B.A., Brichta, A.M., and Callister, R.J., Moving from an Averaged to Specific View of Spinal Cord Pain Processing Circuits, J. Neurophysiol., 2007, vol. 98, p. 1057.

    Article  CAS  PubMed  Google Scholar 

  33. Mason, P., Deconstructing Endogenous Pain Modulations, J. Neurophysiol., 2005, vol. 94, p. 1659.

    Article  CAS  PubMed  Google Scholar 

  34. Patapoutian, A., Peier, A.M., Story, G.M., and Viswanath, V., ThermoTRP Channels and Beyond: Mechanisms of Temperature Sensation, Nat. Rev. Neurosci., 2003, vol. 4, p. 529.

    Article  CAS  PubMed  Google Scholar 

  35. Ikoma, A., Steinhoff, M., Stander, S., et al., The Neurobiology of Itch, Nat. Rev. Neurosci., 2006, vol. 7, p. 535.

    Article  CAS  PubMed  Google Scholar 

  36. Light, A.R. and Perl, E.R., Re-Examination of the Dorsal Root Projection to the Spinal Dorsal Horn Including Observations on the Differential Termination of Coarse and Fine Fibers, J. Comp. Neurol., 1979, vol. 186, p. 117.

    Article  CAS  PubMed  Google Scholar 

  37. Ohara, P.T., Vit, J.P., and Jasmin, L., Cortical Modulation of Pain, Cell. Mol. Life Sci., 2005, vol. 62, p. 44.

    Article  CAS  PubMed  Google Scholar 

  38. Spike, R.C., Puskar, Z., Andrew, D., and Todd, A.J., A Quantitative and Morphological Study of Projection Neurons in Lamina I of the Rat Lumbar Spinal Cord, Eur. J. Neurosci., 2003, vol. 18, p. 2433.

    Article  CAS  PubMed  Google Scholar 

  39. Polgar, E., Gray, S., Riddell, J.S., and Todd, A.J., Lack of Evidence for Significant Neuronal Loss in Laminae I–III of the Spinal Dorsal Horn of the Rat in the Chronic Constriction Injury Model, Pain, 2004, vol. 111, p. 144.

    Article  CAS  PubMed  Google Scholar 

  40. Galhardo, V. and Lima, D., Structural Characterization of Marginal (Lamina I) Spinal Cord Neurons in the Cat: a Golgi Study, J. Comp. Neurol., 1999, vol. 414, p. 315.

    Article  CAS  PubMed  Google Scholar 

  41. Grudt, T.J. and Perl, E.R., Correlations between Neuronal Morphology and Electrophysiological Features in the Rodent Superficial Dorsal Horn, J. Physiol., 2002, vol. 540, p. 189.

    Article  CAS  PubMed  Google Scholar 

  42. Ruscheweyh, R. and Sandkuhler, J., Lamina-Specific Membrane and Discharge Properties of Rat Spinal Dorsal Horn Neurones in Vitro, J. Physiol., 2002, vol. 541, p. 231.

    Article  CAS  PubMed  Google Scholar 

  43. Prescott, S.A. and De Koninck, Y., Four Cell Types with Distinctive Membrane Properties and Morphologies in Lamina I of the Spinal Dorsal Horn of the Adult Rat, J. Physiol., 2002, vol. 539, p. 817.

    Article  CAS  PubMed  Google Scholar 

  44. Han, Z.S., Zhang, E.T., and Craig, A.D., Nociceptive and Thermoreceptive Lamina I Neurons Are Anatomically Distinct, Nat. Neurosci., 1998, vol. 1, p. 218.

    Article  CAS  PubMed  Google Scholar 

  45. Melnick, I.V., Santos, S.F.A., and Safronov, B.V., Mechanism of Spike Frequency Adaptation in Substantia Gelatinosa Neurones of Rat, J. Physiol., 2004, vol. 559, p. 383.

    Article  CAS  PubMed  Google Scholar 

  46. Pol, A.N., Ghosh, P.K., Liu R.-J., et al., Hypocretin (Orexin) Enhances Neuron Activity and Cell Synchrony in Developing Mouse GFP-Expressing Locus Coeruleus, J. Physiol., 2002, vol. 541, p. 169.

    Article  PubMed  Google Scholar 

  47. Hantman, A.W., Pol, A.N., and Perl, E.R., Morphological and Physiological Features of a Set of Spinal Substantia Gelatinosa Neurons Defined by Green Fluorescent Protein Expression, J. Neurosci., 2004, vol. 24, p. 836.

    Article  CAS  PubMed  Google Scholar 

  48. Heinke, B., Ruscheweyh, R., Forsthuber, L., et al., Physiological, Neurochemical and Morphological Properties of a Subgroup of GABAergic Spinal Lamina II Neurones Identified by Expression of Green Fluorescent Protein in Mice, J. Physiol., 2004, vol. 560, p. 249.

    Article  CAS  PubMed  Google Scholar 

  49. Todd, A.J., Hughes, D.I., Polgar, E., et al., The Expression of Vesicular Glutamate Transporters VGLUT1 and VGLUT2 in Neurochemically Defined Axonal Populations in the Rat Spinal Cord with Emphasis on the Dorsal Horn, Eur. J. Neurosci., 2003, vol. 17, p. 13.

    Article  CAS  PubMed  Google Scholar 

  50. Lu, Y. and Perl, E.R., Modular Organization of Excitatory Circuits between Neurons of the Spinal Superficial Dorsal Horn (Laminae I and II), J. Neurosci., 2005, vol. 25, p. 3900.

    Article  CAS  PubMed  Google Scholar 

  51. Santos, S.F.A., Rebelo, S., Derkach, V.A., and Safronov, B.V., Excitatory Interneurons Dominate Sensory Processing in the Spinal Substantia Gelatinosa of Rat, J. Physiol., 2007, vol. 581, p. 241.

    Article  CAS  PubMed  Google Scholar 

  52. Graham, B.A., Brichta, A.M., and Callister, R.J., An in vivo Mouse Spinal Cord Preparation for Patch-Clamp Analysis of Nociceptive Processing, J. Neurosci. Methods, 2004, vol. 136, p. 221.

    Article  CAS  PubMed  Google Scholar 

  53. Furue, H., Narikawa, K., Kumamoto, E., and Yoshimura, M., Responsiveness of Rat Substantia Gelatinosa Neurones to Mechanical but Not Thermal Stimuli Revealed by in Vivo Patch-Clamp Recording, J. Physiol., 1999, vol. 521, p. 529.

    Article  CAS  PubMed  Google Scholar 

  54. Gao, K., Kim, Y.H., and Mason, P., Serotonergic Pontomedullary Neurons Are not Activated by Antinociceptive Stimulation in the Periaqueductal Gray, J. Neurosci., 1997, vol. 17, p. 3285.

    CAS  PubMed  Google Scholar 

  55. Gao, K. and Mason, P., Serotonergic Raphe Magnus Cells That Respond to Noxious Tail Heat are not ON or OFF Cells, J. Neurophysiol., 2000, vol. 84, p. 1719.

    CAS  PubMed  Google Scholar 

  56. Kalyuzhny, A.E. and Wessendorf, M.W., Relationship of Muand Delta-Opioid Receptors to GABAergic Neurons in the Central Nervous System, Including Antinociceptive Brainstem Circuits, J. Comp. Neurol., 1998, vol. 392, p. 528.

    Article  CAS  PubMed  Google Scholar 

  57. Kato, G., Yasaka, T., Katafuchi, T., et al., Direct GABAergic and Glycinergic Inhibition of the Substantia Gelatinosa from the Rostral Ventromedial Medulla Revealed by in Vivo Patch-Clamp Analysis in Rats, J. Neurosci., 2006, vol. 26, p. 1787.

    Article  CAS  PubMed  Google Scholar 

  58. Mody, I. and Pearce, R.A., Diversity of Inhibitory Neurotransmission through GABAA Receptors, Trends Neurosci., 2004, vol. 27, p. 569.

    Article  CAS  PubMed  Google Scholar 

  59. Johnston, G.A., GABAA Receptor Channel Pharmacology, Curr. Pharm. Des., 2005, vol. 11, p. 1867.

    Article  CAS  PubMed  Google Scholar 

  60. Rudolph, U. and Mohler, H., GABA-Based Therapeutic Approaches: GABAA Receptor Subtype Functions, Curr. Opin. Pharmacol., 2006, vol. 6, p. 18.

    Article  CAS  PubMed  Google Scholar 

  61. Hartmann, B., Ahmadi, S., Heppenstall, P.A., et al., The AMPA Receptor Subunits GluR-A and GluR-B Reciprocally Modulate Spinal Synaptic Plasticity and Inflammatory Pain, Neuron, 2004, vol. 44, p. 637.

    Article  CAS  PubMed  Google Scholar 

  62. Harvey, R.J., Depner, U.B., Wassle, H., et al., GlyR Alpha3: An Essential Target for Spinal PGE2-Mediated Inflammatory Pain Sensitization, Science, 2004, vol. 304, p. 884.

    Article  CAS  PubMed  Google Scholar 

  63. Zeilhofer, H.U., Synaptic Modulation in Pain Pathways, Rev. Physiol. Biochem. Pharmacol., 2005, vol. 154, p. 73.

    Article  CAS  PubMed  Google Scholar 

  64. Lynch, J.W. and Callister, R.J., Glycine Receptors: A New Therapeutic Target in Pain Pathways, Curr. Opin. Investig. Drugs, 2006, vol. 7, p. 48.

    CAS  PubMed  Google Scholar 

  65. Hu, H.-J., Carrasquillo, Y., Karim, F., et al., The Kv4.2 Potassium Channel Subunit Is Required for Pain Plasticity, Neuron, 2006, vol. 50, p. 89.

    Article  CAS  PubMed  Google Scholar 

  66. Lee, Y., Lee, C.H., and Oh, U., Painful Channels in Sensory Neurons, Mol. Cells, 2005, vol. 20, no. 3, p. 315.

    CAS  PubMed  Google Scholar 

  67. Foulkes, T. and Wood, J.N., Pain Genes, PLoS Genet., 2008, vol. 4, no. 7, p. 1.

    Article  Google Scholar 

  68. Kissin, I., Vanilloid-Induced Conduction Analgesia: Selective, Dose-Dependent, Long-Lasting, with a Low Level of Potential Neurotoxicity, Anesth. Analg., 2008, vol. 107, p. 271.

    Article  CAS  PubMed  Google Scholar 

  69. Rosenbaum, T.., Gordon-Shaag, A., Munari, M., Gordon, S.E., et al., Ca2+/Calmodulin Modulates TRPV1 Activation by Capsaicin, J. Gen. Physiol., 2004, vol. 123, p. 53.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Pavlov Institute of Physiology, Russian Academy of Sciences, Makarova nab. 6, St. Petersburg, 199034, Russia

    L. V. Filippova & A. D. Nozdrachev

  2. St. Petersburg State University, Universitetskaya nab. 7/9, St. Petersburg, 199164, Russia

    A. D. Nozdrachev

Authors
  1. L. V. Filippova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. A. D. Nozdrachev
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Original Russian Text © L.V. Filippova, A.D. Nozdrachev, 2010, published in Fiziologiya Cheloveka, 2010, Vol. 36, No. 1, pp. 125–137.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Filippova, L.V., Nozdrachev, A.D. Modern concepts on the mechanisms of encoding visceral nociceptive stimuli. Hum Physiol 36, 107–117 (2010). https://doi.org/10.1134/S0362119710010159

Download citation

  • Received:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S0362119710010159

Keywords

Search

Navigation