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Expansion of innervation territory by afferents involved in plasma extravasation after nerve regeneration in adult and neonatal rats

Summary

The capacity of the saphenous nerve for collateral sprouting was examined by electrophysiological recordings of the activity of low threshold mechanoreceptors and plasma extravasation after C-fiber stimulation in rats. When the sciatic nerve was sectioned neonatally or in adults little evidence was obtained for collateral sprouting of either mechanoreceptors or fibers involved in plasma extravasation in the intact saphenous nerve0 In rats where the sciatic nerve was sectioned and the saphenous nerve was crushed either neonatally or in adults, expansive regenerative reinnervation by thin fibers, but not mechanoreceptors, was observed particularly in glabrous skin. Saphenous crush alone did not cause expansive regenerative reinnervation. The results indicate that much of the collateral sprouting or regenerative reinnervation of the skin observed in morphological studies may represent the presence of fibers not responding to the stimuli used in the present study. It is also suggested that some observations of collateral sprouting may represent changes in responsiveness to stimulation of skin areas with overlapping innervation territories.

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References

  1. Aldskogius H, Risling M (1981) Effect of sciatic neurectomy on neuronal number and size distribution in the L7 ganglion of kittens. Exp Neurol 74: 597–604

  2. Beuerman RW, Rózsa AJ (1984) Collateral sprouts are replaced by regenerating neurites in the wounded corneal epithelium. Neurosci Lett 44: 99–104

  3. Bisby MA, Keen P (1986) Regeneration of primary afferent neurons containing substance P-like immunoreactivity. Brain Res 365: 85–95

  4. Bondok AA, Sansone FM (1984) Retrograde and transganglionic degeneration of sensory neurons after a peripheral nerve lesion at birth. Exp Neurol 86: 322–330

  5. Brenan A (1986) Collateral reinnervation of skin by C-fibres following nerve injury in the rat. Brain Res 385: 152–155

  6. Devor M, Schonfield D, Seltzer Z, Wall PD (1979) Two modes of cutaneous reinnervation following peripheral nerve injury. J Comp Neurol 185: 211–220

  7. Diamond J (1982) Modeling and competition in the nervous system: clues from the sensory innervation of skin. Current Topics Dev Biol 17: 147–205

  8. Doucette R, Theriault E, Diamond J (1987) Regionally selective elimination of cutaneous thermal nociception in rats by neonatal capsaicin. J Comp Neurol 261: 583–591

  9. Hoffert MJ, Greenberg RP, Wolskee PJ, Gracely RH, Wirdzek PR, Vinayakom K, Dubner R (1984) Abnormal and collateral innervations of sympathetic and peripheral sensory fields associated with a case of causalgia. Pain 20: 1–12

  10. Horch K (1981) Absence of functional collateral sprouting of mechanoreceptor axons into denervated areas of mammalian skin. Exp Neurol 74: 313–318

  11. Inbal R, Rousso M, Ashur H, Wall PD, Devor M (1987) Collateral sprouting in skin and sensory recovery after nerve injury in man. Pain 28: 141–154

  12. Jackson PC, Diamond J (1981) Regenerating axons reclaim sensory targets from collateral nerve sprouts. Science 214: 926–928

  13. Jackson PC, Diamond J (1983) Failure of intact cutaneous mechanosensory axons to sprout functional collaterals in skin of adult rabbits. Brain Res 273: 277–283

  14. Jackson PC, Diamond J (1984) Temporal and spatial constraints on the collateral sprouting of low-threshold mechanosensory nerves in the skin of rats. J Comp Neurol 226: 336–345

  15. Jancsó G, Király E (1983) Cutaneous nerve regeneration in the rat: reinnervation of the denervated skin by regenerative but not by collateral sprouting. Neurosci Lett 36: 133–137

  16. Kenins P (1981) Identification of the unmyelinated sensory nerves which evoke plasma extravasation in response to antidromic stimulation. Neurosci Lett 25: 137–141

  17. Kinnman E, Aldskogius H (1986) Collateral sprouting of sensory axons in the glabrous skin of the hindpaw after chronic sciatic nerve lesion in adult and neonatal rats: a morphological study. Brain Res 377: 73–82

  18. Kruger L, Sampogna SL, Rodin BE, Clague J, Brecha N, Yeh Y (1985) Thin-fiber cutaneous innervation and its intraepidermal contribution studied by labeling methods and neurotoxin treatment in rats. Somatosens Res 4: 335–356

  19. Lembeck F, Holzer P (1979) Substance P as neurogenic mediator of antidromic vasodilation and neurogenic plasma extravasation. Naunyn-Schmiedeberg's Arch Pharmacol 310: 175–183

  20. Leonard MH (1973) Return of skin sensation in children without repair of nerves. Clin Ortop Rel Res 95: 273–277

  21. Livingston WK (1947) Evidence of active invasion of denervated areas by sensory fibers from neighbouring nerves in man. J Neurosurg 4: 140–145

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

  23. Markus H, Pomeranz B, Krushelnycky D (1984) Spread of saphenous somatotopic projection map in spinal cord and hypersensitivity of the foot after chronic sciatic denervation in adult rats. Brain Res 296: 27–39

  24. Nixon BJ, Doucette R, Jackson PC, Diamond J (1984) Impulse activity evokes precocious sprouting of nociceptive nerves into denervated skin. Somatosens Res 2: 97–126

  25. Pomeranz B, Mullen M, Markus H (1984) Effect of applied electrical fields on sprouting of intact saphenous nerve in adult rat. Brain Res 303: 331–336

  26. Rich KM, Yip HK, Osborne A, Schmidt RE, Johnson EM Jr (1984) Role of nerve growth factor in the adult dorsal root ganglia neuron and its response to injury. J Comp Neurol 230: 110–118

  27. Risling M, Aldskogius H, Hildebrand C (1983) Effect of sciatic nerve crush on the L7 spinal roots and dorsal root ganglia in kittens. Exp Neurol 79: 176–187

  28. Risling M, Aldskogius H, Hildebrand C, Remahl S (1983) Effects of sciatic nerve resection on L7 spinal roots and dorsal root ganglia in adult cats. Exp Neurol 82: 568–580

  29. Robinson PP (1981) Reinnervation of teeth, mucous membrane and skin following section of the inferior alveolar nerve in the cat. Brain Res 220: 241–253

  30. Robinson PP (1983) Recession of sensory loss from the midline following trigeminal sensory root section: collateral sprouting from the normal side? Brain Res 259: 177–180

  31. Robinson PP (1984) Regenerating nerve fibers do not displace the collateral reinnervation of cat teeth. Brain Res 310: 303–310

  32. Wall JT, Cusick CG (1984) Cutaneous responsiveness in primary somatosensory (S-I) hindpaw cortex before and after partial hindpaw deafferentation in adult rats. J Neurosci 4: 1499–1515

  33. Wall JT, Cusick CG (1986) The representation of peripheral nerve inputs in the S-I hindpaw cortex of rats raised with incompletely innervated hindpaws. J Neurosci 6: 1129–1147

  34. Weddell G, Guttmann L, Guttmann E (1941) The local extension of nerve fibers into denervated areas of skin. J Neurol Psychiat 4: 206–225

  35. Wiesenfeld-Hallin Z (1988) Partially overlapping territories of nerves to hindlimb foot skin demonstrated by plasma extravasation to antidromic C-fiber stimulation in the rat. Neurosci Lett 84: 261–265

  36. Wiesenfeld-Hallin Z, Kinnman E, Aldskogius H (1988) Studies of normal and expansive cutaneous innervation territories of intact and regenerating C-fibres in the hindlimb of the rat. Agents Actions 25: 260–262

  37. Yip HK, Rich KM, Lampe PA, Johnson EM Jr (1984) The effects of nerve growth factor and its antiserum on the postnatal development and survival after injury of sensory neurons in rat dorsal root ganglia. J Neurosci 4: 2986–2992

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Correspondence to Z. Wiesenfeld-Hallin.

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Wiesenfeld-Hallin, Z., Kinnman, E. & Aldskogius, H. Expansion of innervation territory by afferents involved in plasma extravasation after nerve regeneration in adult and neonatal rats. Exp Brain Res 76, 88–96 (1989). https://doi.org/10.1007/BF00253626

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Key words

  • Collateral sprouting
  • Nerve regeneration
  • Mechanoreceptors
  • C-fibers
  • Plasma extravasation
  • Evans blue
  • Skin
  • Rat