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. 1997 Dec 15;505(Pt 3):769–783. doi: 10.1111/j.1469-7793.1997.769ba.x

Quantitative analysis of cuneate neurone responsiveness in the cat in association with reversible, partial deafferentation.

S P Zhang 1, M J Rowe 1
PMCID: PMC1160051  PMID: 9457651

Abstract

1. Partial deafferentation, based on peripheral nerve section or local anaesthetic blockade, has been reported to induce both immediate loss of responsiveness and/or immediate reorganization in receptive fields of neurones in the somatosensory system. In the present study, in anaesthetized cats, we have used a rapid, reversible deafferentation procedure based on cold block of the median nerve in order to evaluate quantitatively the response characteristics of cuneate neurones (n = 39) before, during and after partial deafferentation. 2. The first hypothesis tested was that cuneate neurones with input from ulnar or superficial radial nerve fields in the vicinity of the median nerve field should undergo, in association with median nerve blockade, an increased level of responsiveness to tactile stimuli within the ulnar or radial nerve zone, and an expansion of their cutaneous receptive fields. However, among eighteen cuneate neurones of this type, there was no evidence for any systematic enhancement of responsiveness nor, in at least sixteen of the eighteen neurones, any evidence for receptive field expansion. 3. The second hypothesis tested was that cuneate neurones whose input came from both the median nerve and another peripheral nerve source should undergo, in association with median nerve blockade, an increase in responsiveness to the remaining input and an expansion of the receptive field into the field of that remaining nerve source. However, in none of thirteen neurones of this type tested was there evidence of such a change. 4. The third hypothesis was that cuneate neurones whose control' receptive fields were within the median nerve zone of deafferentation should show an emergence of novel receptive fields and responsiveness from areas around the field of innervation of the median nerve. However, in none of eight neurones of this type was there evidence for such changes in adjacent skin areas. 5. In conclusion, with the use of cold block of the median nerve for partial deafferentation, the present study has confirmed previous findings of denervation-related loss of responsiveness in dorsal column nuclei neurones. The conflicting findings in studies of central nervous system plasticity indicate the need to understand better factors that do and do not lead to acute central changes.

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Selected References

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  1. Baumann T. K., Simone D. A., Shain C. N., LaMotte R. H. Neurogenic hyperalgesia: the search for the primary cutaneous afferent fibers that contribute to capsaicin-induced pain and hyperalgesia. J Neurophysiol. 1991 Jul;66(1):212–227. doi: 10.1152/jn.1991.66.1.212. [DOI] [PubMed] [Google Scholar]
  2. Brown A. G., Brown P. B., Fyffe R. E., Pubols L. M. Effects of dorsal root section on spinocervical tract neurones in the cat. J Physiol. 1983 Apr;337:589–608. doi: 10.1113/jphysiol.1983.sp014644. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Brown A. G., Fyffe R. E., Noble R., Rowe M. J. Effects of hind limb nerve section on lumbosacral dorsal horn neurones in the cat. J Physiol. 1984 Sep;354:375–394. doi: 10.1113/jphysiol.1984.sp015382. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Calford M. B., Tweedale R. Acute changes in cutaneous receptive fields in primary somatosensory cortex after digit denervation in adult flying fox. J Neurophysiol. 1991 Feb;65(2):178–187. doi: 10.1152/jn.1991.65.2.178. [DOI] [PubMed] [Google Scholar]
  5. Calford M. B., Tweedale R. Immediate expansion of receptive fields of neurons in area 3b of macaque monkeys after digit denervation. Somatosens Mot Res. 1991;8(3):249–260. doi: 10.3109/08990229109144748. [DOI] [PubMed] [Google Scholar]
  6. DOUGLAS W. W., MALCOLM J. L. The effect of localized cooling on conduction in cat nerves. J Physiol. 1955 Oct 28;130(1):53–71. doi: 10.1113/jphysiol.1955.sp005392. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Darian-Smith C., Gilbert C. D. Topographic reorganization in the striate cortex of the adult cat and monkey is cortically mediated. J Neurosci. 1995 Mar;15(3 Pt 1):1631–1647. doi: 10.1523/JNEUROSCI.15-03-01631.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Devor M., Wall P. D. Effect of peripheral nerve injury on receptive fields of cells in the cat spinal cord. J Comp Neurol. 1981 Jun 20;199(2):277–291. doi: 10.1002/cne.901990209. [DOI] [PubMed] [Google Scholar]
  9. Dostrovsky J. O., Millar J., Wall P. D. The immediate shift of afferent drive to dorsal column nucleus cells following deafferentation: a comparison of acute and chronic deafferentation in gracile nucleus and spinal cord. Exp Neurol. 1976 Sep;52(3):480–495. doi: 10.1016/0014-4886(76)90219-3. [DOI] [PubMed] [Google Scholar]
  10. Ferrington D. G., Rowe M. J. Functional capacities of tactile afferent fibres in neonatal kittens. J Physiol. 1980 Oct;307:335–353. doi: 10.1113/jphysiol.1980.sp013438. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Ferrington D. G., Rowe M. J., Tarvin R. P. Actions of single sensory fibres on cat dorsal column nuclei neurones: vibratory signalling in a one-to-one linkage. J Physiol. 1987 May;386:293–309. doi: 10.1113/jphysiol.1987.sp016535. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Franz D. N., Iggo A. Conduction failure in myelinated and non-myelinated axons at low temperatures. J Physiol. 1968 Dec;199(2):319–345. doi: 10.1113/jphysiol.1968.sp008656. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Gilbert C. D., Wiesel T. N. Receptive field dynamics in adult primary visual cortex. Nature. 1992 Mar 12;356(6365):150–152. doi: 10.1038/356150a0. [DOI] [PubMed] [Google Scholar]
  14. Kelahan A. M., Doetsch G. S. Time-dependent changes in the functional organization of somatosensory cerebral cortex following digit amputation in adult raccoons. Somatosens Res. 1984;2(1):49–81. [PubMed] [Google Scholar]
  15. Kennett R. P., Gilliatt R. W. Nerve conduction studies in experimental non-freezing cold injury: I. Local nerve cooling. Muscle Nerve. 1991 Jun;14(6):553–562. doi: 10.1002/mus.880140610. [DOI] [PubMed] [Google Scholar]
  16. Kitchell R. L., Canton D. D., Johnson R. D., Maxwell S. A. Electrophysiologic studies of cutaneous nerves of the forelimb of the cat. J Comp Neurol. 1982 Oct 1;210(4):400–410. doi: 10.1002/cne.902100406. [DOI] [PubMed] [Google Scholar]
  17. Koerber H. R., Brown P. B. Quantitative analysis of dorsal horn cell receptive fields following limited deafferentation. J Neurophysiol. 1995 Nov;74(5):2065–2076. doi: 10.1152/jn.1995.74.5.2065. [DOI] [PubMed] [Google Scholar]
  18. Li C. X., Waters R. S., Oladehin A., Johnson E. F., McCandlish C. A., Dykes R. W. Large unresponsive zones appear in cat somatosensory cortex immediately after ulnar nerve cut. Can J Neurol Sci. 1994 Aug;21(3):233–247. doi: 10.1017/s0317167100041214. [DOI] [PubMed] [Google Scholar]
  19. Lisney S. J. Changes in the somatotopic organization of the cat lumbar spinal cord following peripheral nerve transection and regeneration. Brain Res. 1983 Jan 17;259(1):31–39. doi: 10.1016/0006-8993(83)91064-8. [DOI] [PubMed] [Google Scholar]
  20. McMahon S. B., Wall P. D. Plasticity in the nucleus gracilis of the rat. Exp Neurol. 1983 Apr;80(1):195–207. doi: 10.1016/0014-4886(83)90016-x. [DOI] [PubMed] [Google Scholar]
  21. Merzenich M. M., Kaas J. H., Wall J. T., Sur M., Nelson R. J., Felleman D. J. Progression of change following median nerve section in the cortical representation of the hand in areas 3b and 1 in adult owl and squirrel monkeys. Neuroscience. 1983 Nov;10(3):639–665. doi: 10.1016/0306-4522(83)90208-7. [DOI] [PubMed] [Google Scholar]
  22. Metzler J., Marks P. S. Functional changes in cat somatic sensory-motor cortex during short-term reversible epidural blocks. Brain Res. 1979 Nov 16;177(2):379–383. doi: 10.1016/0006-8993(79)90790-x. [DOI] [PubMed] [Google Scholar]
  23. Millar J., Basbaum A. I., Wall P. D. Restructuring of the somatotopic map and appearance of abnormal neuronal activity in the gracile nucleus after partial deafferentation. Exp Neurol. 1976 Mar;50(3):658–672. doi: 10.1016/0014-4886(76)90035-2. [DOI] [PubMed] [Google Scholar]
  24. Nicolelis M. A., Lin R. C., Woodward D. J., Chapin J. K. Induction of immediate spatiotemporal changes in thalamic networks by peripheral block of ascending cutaneous information. Nature. 1993 Feb 11;361(6412):533–536. doi: 10.1038/361533a0. [DOI] [PubMed] [Google Scholar]
  25. Northgrave S. A., Rasmusson D. D. The immediate effects of peripheral deafferentation on neurons of the cuneate nucleus in raccoons. Somatosens Mot Res. 1996;13(2):103–113. doi: 10.3109/08990229609051398. [DOI] [PubMed] [Google Scholar]
  26. Paintal A. S. Block of conduction in mammalian myelinated nerve fibres by low temperatures. J Physiol. 1965 Sep;180(1):1–19. [PMC free article] [PubMed] [Google Scholar]
  27. Panetsos F., Nuñez A., Avendaño C. Local anaesthesia induces immediate receptive field changes in nucleus gracilis and cortex. Neuroreport. 1995 Dec 29;7(1):150–152. [PubMed] [Google Scholar]
  28. Pettit M. J., Schwark H. D. Capsaicin-induced rapid receptive field reorganization in cuneate neurons. J Neurophysiol. 1996 Mar;75(3):1117–1125. doi: 10.1152/jn.1996.75.3.1117. [DOI] [PubMed] [Google Scholar]
  29. Pettit M. J., Schwark H. D. Receptive field reorganization in dorsal column nuclei during temporary denervation. Science. 1993 Dec 24;262(5142):2054–2056. doi: 10.1126/science.8266104. [DOI] [PubMed] [Google Scholar]
  30. Rasmusson D. D., Louw D. F., Northgrave S. A. The immediate effects of peripheral denervation on inhibitory mechanisms in the somatosensory thalamus. Somatosens Mot Res. 1993;10(1):69–80. doi: 10.3109/08990229309028825. [DOI] [PubMed] [Google Scholar]
  31. Rasmusson D. D., Turnbull B. G. Immediate effects of digit amputation on SI cortex in the raccoon: unmasking of inhibitory fields. Brain Res. 1983 Dec 12;288(1-2):368–370. doi: 10.1016/0006-8993(83)90120-8. [DOI] [PubMed] [Google Scholar]
  32. Turman A. B., Ferrington D. G., Ghosh S., Morley J. W., Rowe M. J. Parallel processing of tactile information in the cerebral cortex of the cat: effect of reversible inactivation of SI on responsiveness of SII neurons. J Neurophysiol. 1992 Feb;67(2):411–429. doi: 10.1152/jn.1992.67.2.411. [DOI] [PubMed] [Google Scholar]
  33. Turnbull B. G., Rasmusson D. D. Acute effects of total or partial digit denervation on raccoon somatosensory cortex. Somatosens Mot Res. 1990;7(4):365–389. doi: 10.3109/08990229009144714. [DOI] [PubMed] [Google Scholar]
  34. Vickery R. M., Gynther B. D., Rowe M. J. Synaptic transmission between single slowly adapting type I fibres and their cuneate target neurones in cat. J Physiol. 1994 Feb 1;474(3):379–392. doi: 10.1113/jphysiol.1994.sp020030. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Waite P. M. Rearrangement of neuronal responses in the trigeminal system of the rat following peripheral nerve section. J Physiol. 1984 Jul;352:425–445. doi: 10.1113/jphysiol.1984.sp015301. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Wilson P. Absence of mediolateral reorganization of dorsal horn somatotopy after peripheral deafferentation in the cat. Exp Neurol. 1987 Feb;95(2):432–447. doi: 10.1016/0014-4886(87)90150-6. [DOI] [PubMed] [Google Scholar]

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