Advertisement

Springer Nature is making SARS-CoV-2 and COVID-19 research free. View research | View latest news | Sign up for updates

Thresholds and encoding of neuronal responses to mechanical stimuli in the ventro-basal thalamus during carrageenin-induced hyperalgesic inflammation in the rat

Summary

Neuronal response thresholds and the encoding of mechanical stimulus intensity in the ventro-basal (VB) thalamus was analyzed in anaesthetized rats before and during the first two hours following induction of hyperalgesic inflammation. This inflammation was induced by the intra-plantar injection of carrageenin in the hindpaw contralateral to the recorded neurones. Only neurones exclusively driven by noxious stimuli and with a receptiv field on or including the injected paw were considered. In this early phase of the inflammatory process, there was no significant modification of the response threshold to the mechanical stimulus (indentation of about 300μm). This suggests the involvement of additional neuronal population(s) to account for the decrease in the vocalisation threshold to pressure observed in the freely moving animal at this time of the inflammation, A liner encoding of the indentation depth was observed before and after the carrageenin injection although the slope of the stimulus response-curve was steeper after the injection. The data emphasize that the carrageenin-sensitization acts differentially on the liminal and supra-liminal responses of the same neurone to a skin indentation, since in the first hour following the initiation of the inflammation the sensitization is essentially observed for responses obtained with stimulus intensity largely above the threshold value. With regard to previous observations using thermal stimulation, the results also illustrate that the carrageenin induced sensitization of responses differs depending on the stimulus intensity and modality used.

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

References

  1. Adriaensen H, Gybels J, Handwerker HO, Van Hees J (1984) Suppression of C-fibre discharges upon repeated heat stimulation may explain characteristics of concomitant pain sensations. Brain Res 302: 203–211

  2. Anton F, Kocher L, Reeh PW, Handwerker HO (1985) The effect of carrageenin induced inflammation on the excitability of unmyelinated skin nociceptors in the rat. Neurosci Lett Suppl 22: S31

  3. Benoist JM, Kayser V, Gautron M, Guilbaud G (1984) Letter to editor. Pain 18: 410–411

  4. Benoist JM, Kayser V, Gautron M, Guilbaud G (1985) Changes in responses of ventro-basal thalamic neurons during carrageenin-induced inflammation in the rat. In: Fields HL et al. (eds) Advances in pain research and therapy, Vol 9. Raven Press, New York, pp 295–303

  5. Benoist JM, Kayser V, Gautron M, Neil A, Guilbaud G (1985) Threshold responses and encoding properties of noxious ventro-basal neurones before and after carrageenin evoked inflammation in rat. Neurosci Lett Suppl 22: S474

  6. Bessou P, Perl ER (1969) Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J Neurophysiol 32: 1025–1043

  7. Campbell JN, Meyer RA (1983) Sensitization of unmyelinated nociceptive afferents in monkey varies with skin type. J Neurophysiol 49: 98–110

  8. Campbell JN, Meyer RA, La Motte RH (1979) Sensitization of myelinated nociceptive afferents that innervate monkey hand. J Neurophysiol 42: 1669–1679

  9. Di Rosa M, Giroud JP, Willoughby DA (1971) Studies of the mediators of the acute inflammation response induced in rats in different sites by carrageenin and turpentine. J Pathol 104: 15–29

  10. Finney DJ (1976) Statistical method in biological assay. Griffin C et Co Ltd, London, Chap IV

  11. Fitzgerald M, Lynn B (1977) The Sensitization of high threshold mechanoreceptors with myelinated axons by repeated heating. J Physiol 365: 549–563

  12. Fleischer E, Handwerker HO, Joukahadar S (1983) Unmyelinated nociceptive units in two skin areas of the rat. Brain Res 267: 81–92

  13. Garattini S, Jori A, Bernardi D, Carrara C, Paglialunga S, Segre D (1965) Sensitivity of local oedemas to systemic pharmacological effects. In: Garratini S, Dukes MNG (eds) Nonsteroidal anti-inflammatory drugs. Excerpta Medica Foundation, Amsterdam, pp 151–161

  14. Guilbaud G, Benoist JM, Kayser V, Neil A (1987) Responses of ventrobasal thalamic neurones to carrageenin-produced inflammation in the rat. In: Schmidt RF et al. (eds) Fine afferent nerve fibers and pain. VCH Verlagsgesellschaft mbH, Weinheim, pp 412–425

  15. Guilbaud G, Benoist JM, Neil A, Kayser V, Gautron M (1987) Neuronal response thresholds to and encoding of thermal stimuli during carrageenin-hyperalgesic-inflammation in the ventro-basal thalamus of rat. Exp Brain Res 66: 412–431

  16. Guilbaud G, Iggo A, Tegner R (1985) Sensory receptors in ankle joint capsules of normal and arthritic rats. Exp Brain Res 58: 29–40

  17. Guilbaud G, Kayser V, Benoist JM, Gautron M (1986) Modifications in the responsiveness of rat ventro-basal thalamic neurons at different stages of carrageenin-produced inflammation. Brain Res 385: 86–98

  18. Guilbaud G, Peschanski M, Gautron M, Binder D (1980) Neurones responding to noxious stimulations in V.B. complex and caudal adjacent regions in the thalamus of the rat. Pain 8: 303–318

  19. Hardy JD, Wolff HG, Goodell H (1967) Pain sensations and reactions. Hafner Publishing Company, New York

  20. Kayser V, Guilbaud G (1987) Local and remote modifications of the nociceptive sensitivity during carrageenin-induced inflammation. Pain 8: 99–108

  21. Kenshalo DR Jr, Giesler GJ Jr, Leonard RB, Willis WD (1980) Responses of neurons in primate ventral posterior lateral nucleus to noxious stimuli. J Neurophysiol 43: 1594–1614

  22. La Motte RH, Thalhammer JG, Robinson CJ (1983) Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: a comparison of neural events in monkey with sensory judgments in human. J Neurophysiol 50: 1–26

  23. Lewis T (1935–36) Experiments relating to cutaneous hyperalgesia and its spread through somatic nerves. Clin Sci 373–423

  24. Lindblom U (1979) Sensory abnormalities in neuralgia. In: Bonica JJ et al. (eds) Advances in pain research and therapy, Vol 3. Raven Press, New York, pp 111–120

  25. Lindblom U (1985) Assessment of abnormal evoked pain in neurological pain patients and its relation to spontaneous pain: a descriptive and conceptual model with some analytical results. In: Fields HL et al. (eds) Advances in pain research and therapy, Vol 9. Raven Press, New York, pp 409–423

  26. Lynn B (1979) The heat sensitization of polymodal nociceptors in the rabbit and its independance of the local blood flow. J Physiol 287: 493–507

  27. Lynn B, Carpenter SE (1982) Primary afferent units from the hairy skin of the rat hind limb. Brain Res 238: 29–43

  28. Meyer RA, Campbell JN, Raja SN (1985) Peripheral neural mechanisms of cutaneous hyperalgesia. In: Fields HL et al. (eds) Advances in pain research and therapy, Vol 9. Raven Press, New York, pp 53–71

  29. Mountcastle VB (1967) The problem of sensing and the neural coding of sensory events. Rockefeller University Press, New York

  30. Neil A, Benoist JM, Kayser V, Guilbaud G (1987) Initial nociceptive sensitization in carrageenin-induced rat paw inflammation is dependent on amine autacoid mechanisms: electrophysiologcal and behavioural evidence obtained with a quaternary anti-histamine, thiazinamium. Exp Brain Res 65: 343–351

  31. Peschanski M, Guilbaud G, Gautron M, Besson JM (1980) Encoding property of noxious heat messages in neurons of the ventrobasal thalamic complex of the rat. Brain Res 197: 401–413

  32. Pubols BJ Jr (1982) Factors affecting cutaneous mechanoreceptor response. II. Changes in mechanical properties of skin with repeated stimulation. J Neurophysiol 47: 530–542

  33. Raja SN, Campbell JN, Meyer RA (1984) Evidence for different mechanisms of primary and secondary hyperalgesia following heat injury to the glabrous skin. Brain 107: 1179–1188

  34. Thalhammer JG, La Motte RH (1982) Spatial properties of nociceptor sensitization following heat injury of the skin. Brain Res 231: 257–265

  35. Torebjörk HE, La Motte RH, Robinson CJ (1984) Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: simultaneous recordings in humans of sensory judgments of pain and evoked responses in nociceptors with C-fibers. J Neurophysiol 51: 325–339

  36. Van Arman CG, Begany AJ, Miller LM, Pless HH (1965) Some details of the inflammations caused by yeast and carrageenin. J Pharmacol 150: 328–334

  37. Vinegar R, Schreiber W, Hugo R (1969) Biphasic development of carrageenin edema in rats. J Pharmacol Exp Ther 166: 6–103

  38. Winter CA, Flataker L (1965) Reaction thresholds to pressure in oedematous hindpaws of rats: responses to analgesic drugs. J Pharmacol Exp Ther 150: 165–171

Download references

Author information

Correspondence to G. Guilbaud.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Guilbaud, G., Neil, A., Benoist, J.M. et al. Thresholds and encoding of neuronal responses to mechanical stimuli in the ventro-basal thalamus during carrageenin-induced hyperalgesic inflammation in the rat. Exp Brain Res 68, 311–318 (1987). https://doi.org/10.1007/BF00248797

Download citation

Key words

  • Carrageenin hyperalgesia
  • Rat
  • Ventro-basal thalamic neurones
  • Responses to mechanical stimuli