Misdirection of regenerating motor axons after nerve injury and repair in the rat sciatic nerve model

Experimental Neurology

Volumn 211, Issue 2, 2008, Pages 339-350

  de Ruiter, Godard C W ^a   Malessy, Martijn J A ^b   Alaid, Awad O ^a   Spinner, Robert J ^a   Engelstad, JaNean K ^a   Sorenson, E J ^a   Kaufman, K R ^a   Dyck, Peter J ^a   Windebank, Anthony J ^a  

^a MAYO CLINIC   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Aberrant reinnervation; Accuracy of regeneration; Ankle motion analysis; Double labeling; Sequential retrograde tracing

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANKLE; ARTICLE; CONTROLLED STUDY; MORPHOMETRICS; MOTONEURON; MOTOR NERVE; MYELINATED NERVE; NERVE FIBER REGENERATION; NERVE INJURY; NEUROTROPISM; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ACTION POTENTIALS; ANIMALS; AXONS; DISEASE MODELS, ANIMAL; MOTOR NEURONS; NERVE REGENERATION; RATS; RATS, SPRAGUE-DAWLEY; RECOVERY OF FUNCTION; SCIATIC NEUROPATHY;

EID: 43449120386     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2007.12.023     Document Type: Article

References (52)

1. Abernethy D.A., Rud A., and Thomas P.K. Neurotropic influence of the distal stump of transected peripheral nerve on axonal regeneration: absence of topographic specificity in adult nerve. J. Anat. 180 (1992) 395-400
2. Aldskogius H., and Thomander L. Selective reinnervation of somatotopically appropriate muscles after facial nerve transection and regeneration in the neonatal rat. Brain Res. 375 (1986) 126-134
3. Aldskogius H., Molander C., Persson J., and Thomander L. Specific and nonspecific regeneration of motor axons after sciatic nerve injury and repair in the rat. J. Neurol. Sci. 80 (1987) 249-257
4. Beer G.M., Steurer J., and Meyer V.E. Standardizing nerve crushes with a non-serrated clamp. J. Reconstr. Microsurg. 17 (2001) 531-534
5. Bernstein J.J., and Guth L. Nonselectivity in establishment of neuromuscular connections following nerve regeneration in the rat. Exp. Neurol. 4 (1961) 262-275
6. Birch R., Bonney G., and Wynn Parry C.B. Surgical Disorders of the Peripheral Nerves (1998), Churchill Livingstone, Edinburgh
7. Bodine-Fowler S.C., Meyer R.S., Moskovitz A., Abrams R., and Botte M.J. Inaccurate projection of rat soleus motoneurons: a comparison of nerve repair techniques. Muscle Nerve 20 (1997) 29-37
8. Brooke M.H., and Kaiser K.K. Some comments on the histochemical characterization of muscle adenosine triphosphatase. J. Histochem. Cytochem. 17 (1969) 431-432
9. Brushart T.M. Preferential reinnervation of motor nerves by regenerating motor axons. J. Neurosci. 8 (1988) 1026-1031
10. Brushart T.M.E. The mechanical and humoral control of specificity in nerve repair. In: Gelberman R.H. (Ed). Operative Nerve Repair and Reconstruction vol. 1 (1991), J. B. Lippincott Company, Philadelphia 215-230
11. Brushart T.M. Motor axons preferentially reinnervate motor pathways. J. Neurosci. 13 (1993) 2730-2738
12. Brushart T.M., and Mesulam M.M. Alteration in connections between muscle and anterior horn motoneurons after peripheral nerve repair. Science 208 (1980) 603-605
13. Brushart T.M., Jari R., Verge V., Rohde C., and Gordon T. Electrical stimulation restores the specificity of sensory axon regeneration. Exp. Neurol. 194 (2005) 221-229
14. de Medinaceli L. Functional consequences of experimental nerve lesions: effects of reinnervation blend. Exp. Neurol. 100 (1988) 166-178
15. de Ruiter G.C., Spinner R.J., Alaid A.O., Koch A.J., Wang H., Malessy M.J., Currier B.L., Yaszemski M.J., Kaufman K.R., and Windebank A.J. Two-dimensional digital video ankle motion analysis for assessment of function in the rat sciatic nerve model. J. Peripher. Nerv. Syst. 12 (2007) 216-222
16. Dyck P.J., Lambert E.H., Wood M.B., and Linscheid R.L. Assessment of nerve regeneration and adaptation after median nerve reconnection and digital neurovascular flap transfer. Neurology 38 (1988) 1586-1591
17. Dyck P.J., Dyck P.J.B., and Engelstad J. Pathologic alterations of nerves. In: Dyck P.J., and Thomas P.K. (Eds). Peripheral Neuropathy. 4th ed. vol. 1 (2005), Elsevier Saunders, Philadelphia 733-829
18. Evans P.J., Bain J.R., Mackinnon S.E., Makino A.P., and Hunter D.A. Selective reinnervation: a comparison of recovery following microsuture and conduit nerve repair. Brain Res. 559 (1991) 315-321
19. Fu S.Y., and Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J. Neurosci. 15 (1995) 3876-3885
20. Fu S.Y., and Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged denervation. J. Neurosci. 15 (1995) 3886-3895
21. Giannini C., Lais A.C., and Dyck P.J. Number, size, and class of peripheral nerve fibers regenerating after crush, multiple crush, and graft. Brain Res. 500 (1989) 131-138
22. Gillespie M.J., Gordon T., and Murphy P.R. Reinnervation of the lateral gastrocnemius and soleus muscles in the rat by their common nerve. J. Physiol. 372 (1986) 485-500
23. Gorio A., Carmignoto G., Finesso M., Polato P., and Nunzi M.G. Muscle reinnervation. II. Sprouting, synapse formation and repression. Neuroscience 8 (1983) 403-416
24. Hare G.M., Evans P.J., Mackinnon S.E., Best T.J., Bain J.R., Szalai J.P., and Hunter D.A. Walking track analysis: a long-term assessment of peripheral nerve recovery. Plast. Reconstr. Surg. 89 (1992) 251-258
25. Hennig R., and Dietrichs E. Transient reinnervation of antagonistic muscles by the same motoneuron. Exp. Neurol. 130 (1994) 331-336
26. Lutz B.S. The role of a barrier between two nerve fascicles in adjacency after transection and repair of a peripheral nerve trunk. Neurol. Res. 26 (2004) 363-370
27. Mackinnon S.E., Dellon A.L., and O'Brien J.P. Changes in nerve fiber numbers distal to a nerve repair in the rat sciatic nerve model. Muscle Nerve 14 (1991) 1116-1122
28. Madison R.D., Archibald S.J., and Brushart T.M. Reinnervation accuracy of the rat femoral nerve by motor and sensory neurons. J. Neurosci. 16 (1996) 5698-5703
29. Miledi R., and Stefani E. Non-selective re-innervation of slow and fast muscle fibres in the rat. Nature 222 (1969) 569-571
30. Molander C., and Aldskogius H. Directional specificity of regenerating primary sensory neurons after peripheral crush or transection and epineural suture: a sequential double labeling study in the rat. Restor. Neurol. Neurosci. 4 (1992) 339-344
31. Nguyen Q.T., Sanes J.R., and Lichtman J.W. Pre-existing pathways promote precise projection patterns. Nat. Neurosci. 5 (2002) 861-867
32. Politis M.J. Specificity in mammalian peripheral nerve regeneration at the level of the nerve trunk. Brain Res. 328 (1985) 271-276
33. Puigdellivol-Sanchez A., Prats-Galino A., Ruano-Gil D., and Molander C. Fast blue and diamidino yellow as retrograde tracers in peripheral nerves: efficacy of combined nerve injection and capsule application to transected nerves in the adult rat. J. Neurosci. Methods 95 (2000) 103-110
34. Puigdellivol-Sanchez A., Valero-Cabré A., Prats-Galino A., Navarro X., and Molander C. On the use of fast blue, fluoro-gold and diamidino yellow for retrograde tracing after peripheral nerve injury: uptake, fading, dye interactions, and toxicity. J. Neurosci. Methods 115 (2002) 115-127
35. Puigdellivol-Sanchez A., Prats-Galino A., Ruano-Gil D., and Molander C. Persistence of tracer in the application site: a potential confounding factor in nerve regeneration studies. J Neurosci. Methods 127 (2003) 105-110
36. Jul. 7. Puigdellivol-Sanchez A., Prats-Galino A., and Molander C. Jul 7. Estimations of topographically correct regeneration to nerve branches and skin after peripheral nerve injury and repair. Brain Res. 1098 (2006) 49-60 Electronic publication ahead of print 2006 Jun 14
37. Ramón y Cajal S. Degeneration & Regeneration of the Nervous System (Translated and edited by RM May) (1928), Oxford, London, University Press
38. Rende M., Granato A., Lo Monaco M., Zelano G., and Toesca A. Accuracy of reinnervation by peripheral nerve axons regenerating across a 10-mm gap within an impermeable chamber. Exp. Neurol. 111 (1991) 332-339
39. Robinson G.A., and Madison R.D. Developmentally regulated changes in femoral nerve regeneration in the mouse and rat. Exp. Neurol. 197 (2006) 341-346
40. Strasberg S.R., Watanabe O., Mackinnon S.E., Tarasidis G., Hertl M.C., and Wells M.R. Wire mesh as a post-operative physiotherapy assistive device following peripheral nerve graft repair in the rat. J. Peripher. Nerv. Syst. 1 (1996) 73-76
41. Sulaiman O.A.R., Midah R., Munro C.A., Matsuyama T., Al-Majed A., and Gordon T. Chronic Schwann cell denervation and the presence of a sensory nerve reduce motor axonal regeneration. Exp. Neurol. 176 (2002) 342-354
42. Sunderland S. Nerve Injuries and Their Repair: A Critical Appraisal (1991), Churchill Livingstone, Edinburgh
43. Swett J.E., Wikholm R.P., Blanks R.H., Swett A.L., and Conley L.C. Motoneurons of the rat sciatic nerve. Exp. Neurol. 93 (1986) 227-252
44. Swett J.E., Hong C.Z., and Miller P.G. All peroneal motoneurons of the rat survive crush injury but some fail to reinnervate their original targets. J. Comp. Neurol. 304 (1991) 234-252
45. Valero-Cabre A., Tsironis K., Skouras E., Perego G., Navarro X., and Neiss W.F. Superior muscle reinnervation after autologous nerve graft or poly-l-lactide-epsilon-caprolactone (PLC) tube implantation in comparison to silicone tube repair. J. Neurosci. Res. 63 (2001) 214-223
46. Varejao A.S., Cabrita A.M., Meek M.F., Bulas-Cruz J., Gabriel R.C., Filipe V.M., Melo-Pinto P., and Winter D.A. Motion of the foot and ankle during the stance phase in rats. Muscle Nerve 26 (2002) 630-635
47. Varejao A.S., Cabrita A.M., Meek M.F., Bulas-Cruz J., Filipe V.M., Gabriel R.C., Ferreira A.J., Geuna S., and Winter D.A. Ankle kinematics to evaluate functional recovery in crushed rat sciatic nerve. Muscle Nerve 27 (2003) 706-714
48. Varejao A.S., Cabrita A.M., Meek M.F., Bulas-Cruz J., Melo-Pinto P., Raimondo S., Geuna S., and Giacobini-Robecchi M.G. Functional and morphological assessment of a standardized rat sciatic nerve crush injury with a non-serrated clamp. J. Neurotrauma 21 (2004) 1652-1670
49. Vleggeert-Lankamp C.L., de Ruiter G.C., Wolfs J.F., Pego A.P., Feirabend H.K., Lakke E.A., and Malessy M.J. Type grouping in skeletal muscles after experimental reinnervation: another explanation. Eur. J. Neurosci. 21 (2005) 1249-1256
50. Weiss P., and Taylor A.C. Further experimental evidence against "neurotropism" in nerve regeneration. J. Exp. Zool. 95 (1944) 233-257
51. Witzel C., Rohde C., and Brushart T.M. Pathway sampling by regenerating peripheral axons. J. Comp. Neurol. 485 (2005) 183-190
52. Zhao Q., Dahlin L.B., Kanje M., and Lundborg G. Specificity of muscle reinnervation following repair of the transected sciatic nerve: a comparative study of different repair techniques in the rat. J. Hand Surg. [Br]. 17 (1992) 257-261