Selective plasticity of primary afferent innervation to the dorsal horn and autonomic nuclei following lumbosacral ventral root avulsion and reimplantation in long term studies

Experimental Neurology

Volumn 233, Issue 2, 2012, Pages 758-766

  Wu, Lisa ^a   Wu, Jun ^a   Chang, Huiyi H ^a,b,c   Havton, Leif A ^a,b,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Cauda equina; CGRP; Major pelvic ganglion; Parasympathetic preganglionic neurons; Root avulsion; Root reimplantation; Sensory plasticity; Spinal cord injury; Sympathetic preganglionic neurons; VGLUT1

Indexed keywords

BIOLOGICAL MARKER; CALCITONIN GENE RELATED PEPTIDE; VESICULAR GLUTAMATE TRANSPORTER 1;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVE; AVULSION INJURY; CELL LABELING; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EFFERENT NERVE; FEMALE; IMMUNOHISTOCHEMISTRY; LUMBOSACRAL SPINE; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NONHUMAN; PARASYMPATHETIC INNERVATION; PREGANGLIONIC NERVE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; REIMPLANTATION; SENSORY GANGLION; SENSORY NERVE; SPINAL CORD DORSAL HORN; SPINAL CORD INJURY; SPINAL ROOT; SYMPATHETIC INNERVATION; TARGET CELL;

ANIMALS; AUTONOMIC NERVOUS SYSTEM; FEMALE; LUMBAR VERTEBRAE; NEURONAL PLASTICITY; NEURONS, AFFERENT; POSTERIOR HORN CELLS; RADICULOPATHY; RATS; RATS, SPRAGUE-DAWLEY; SACRUM; SPINAL NERVE ROOTS; TIME FACTORS; TISSUE TRANSPLANTATION;

EID: 84856546683     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.11.034     Document Type: Article

References (44)

1. Akhavan M., Hoang T.X., Havton L.A. Improved detection of fluorogold-labeled neurons in long-term studies. J. Neurosci. Methods 2006, 152:156-162.
2. Alvarez F.J., Villalba R.M., Zerda R., Schneider S.P. Vesicular glutamate transporters in the spinal cord, with special reference to sensory primary afferent synapses. J. Comp. Neurol. 2004, 472:257-280.
3. Baron R., Jänig W. Afferent and sympathetic neurons projecting into lumbar visceral nerves of the male rat. J. Comp. Neurol. 1991, 314:429-436.
4. Bigbee A.J., Hoang T.X., Havton L.A. At-level neuropathic pain is induced by lumbosacral ventral root avulsion injury and ameliorated by root reimplantation into the spinal cord. Exp. Neurol. 2007, 204:273-282.
5. Bigbee A.J., Hoang T.X., Havton L.A. Reimplantation of avulsed lumbosacral ventral roots in the rat ameliorates injury-induced degeneration of primary afferent axon collaterals in the spinal dorsal columns. Neuroscience 2008, 152:338-345.
6. Chang H.Y., Havton L.A. Re-established micturition reflexes show differential activation patterns after lumbosacral ventral root avulsion injury and repair in rats. Exp. Neurol. 2008, 212:291-297.
7. Chang H.Y., Havton L.A. Surgical implantation of avulsed lumbosacral ventral roots promotes restoration of bladder morphology in rats. Exp. Neurol. 2008, 214:117-124.
8. Chang H.Y., Havton L.A. Anatomical tracer injections into the lower urinary tract may compromise cystometry and external urethral sphincter electromyography in female rats. Neuroscience 2010, 166:212-219.
9. Chang, H.H., Havton, L.A., in press. Systemic administration for Fluorogold for anatomical pre-labeling of autonomic and motor neurons in the rat spinal cord compromise urodynamic recordings in acute but not long-term studies. Neurourol. Urodyn. doi:. doi:10.1002/nau.21184.
10. Christianson J.A., Traub R.J., Davis B.M. Differences in spinal distribution and neurochemical phenotype of colonic afferents in mouse and rat. J. Comp. Neurol. 2006, 494:246-259.
11. Chung K., Won T.L., Park M.J. Spinal projections of pelvic visceral afferents of the rat: a calcitonin gene-related peptide (CGRP) immunohistochemical study. J. Comp. Neurol. 1993, 337:63-69.
12. de Groat W.C. Neuropeptides in pelvic afferent pathways. Experientia 1987, 43:801-813.
13. de Groat W.C. Anatomy and physiology of the lower urinary tract. Urol. Clin. North Am. 1993, 20:383-401.
14. Fowler C.J., Griffiths D., de Groat W.C. The neural control of micturition. Nat. Rev. Neurosci. 2008, 9:453-466.
15. Harji F., Gonzales J., Galindo R., Dail W.G. Preganglionic fibers in the rat hypogastric nerve project bilaterally to pelvic ganglia. Anat. Rec. 1998, 252:229-234.
16. Havton L.A., Carlstedt T. Repair and rehabilitation of plexus and root avulsions in animal models and patients. Curr. Opin. Neurol. 2009, 22:570-574.
17. Hoang T.X., Havton L.A. Novel repair strategies to restore bladder function following cauda equina/conus medullaris injuries. Prog. Brain Res. 2006, 152:195-204.
18. Hoang T.X., Havton L.A. A single re-implanted ventral root exerts neurotropic effects over multiple spinal cord segments in the adult rat. Exp. Brain Res. 2006, 169:208-217.
19. Hoang T.X., Nieto J.H., Tillakaratne N.J., Havton L.A. Autonomic and motor neuron death is progressive and parallel in a lumbosacral ventral root avulsion model of cauda equina injury. J. Comp. Neurol. 2003, 467:477-486.
20. Hoang T.X., Nieto J.H., Dobkin B.H., Tillakaratne N.J., Havton L.A. Acute implantation of an avulsed lumbosacral ventral root into the rat conus medullaris promotes neuroprotection and graft reinnervation by autonomic and motor neurons. Neuroscience 2006, 138:1149-1160.
21. Hoang T.X., Pikov V., Havton L.A. Functional reinnervation of the rat lower urinary tract after cauda equina injury and repair. J. Neurosci. 2006, 26:8672-8679.
22. Hosoya Y., Nadelhaft I., Wang D., Kohno K. Thoracolumbar sympathetic preganglionic neurons in the dorsal commissural nucleus of the male rat: an immunohistochemical study using retrograde labeling of cholera toxin subunit B. Exp. Brain Res. 1994, 98:21-30.
23. Hou S., Duale H., Rabchevsky A.G. Intraspinal sprouting of unmyelinated pelvic afferents after complete spinal cord injury is correlated with autonomic dysreflexia induced by visceral pain. Neuroscience 2009, 159:369-379.
24. Hwang S.J., Oh J.M., Valtschanoff J.G. The majority of bladder sensory afferents to the rat lumbosacral spinal cord are both IB4- and CGRP-positive. Brain Res. 2005, 1062:86-91.
25. Keast J.R., de Groat W.C. Segmental distribution and peptide content of primary afferent neurons innervating the urogenital organs and colon of male rats. J. Comp. Neurol. 1992, 319:615-623.
26. Kihara K., de Groat W.C. Sympathetic efferent pathways projecting to the bladder neck and proximal urethra in the rat. J. Auton. Nerv. Syst. 1997, 62:134-142.
27. Llewellyn-Smith I.J. Anatomy of synaptic circuits controlling the activity of sympathetic preganglionic neurons. J. Chem. Anat. 2009, 38:231-239.
28. Llewellyn-Smith I.J., Martin C.L., Fenwick N.M., DiCarlo S.E., Lujan H.L., Schreihofer A.N. VGLUT1 and VGLUT2 innervation in autonomic regions of intact and transected rat spinal cord. J. Comp. Neurol. 2007, 503:741-767.
29. Maynard F.M., Bracken M.B., Creasey G., Ditunno J.F., Donovan W.H., Ducker T.B., Garber S.L., Marino R.J., Stover S.L., Tator C.H., Waters R.L., Wilberger J.E., Young W. International standards for neurological and functional classification of spinal cord injury. American Spinal Injury Association. Spinal Cord 1997, 35:266-274.
30. Molander C., Xu Q., Grant G. The cytoarchitectonic organization of the spinal cord in the rat. I. The lower thoracic and lumbosacral cord. J. Comp. Neurol. 1984, 230:133-141.
31. Moossy J.J., Nashold B.S., Osborne D., Friedman A.H. Conus medullaris nerve root avulsions. J. Neurosurg. 1987, 66:835-841.
32. Nadelhaft I., Booth A.M. The location and morphology of preganglionic neurons and the distribution of visceral afferents from the rat pelvic nerve: a horseradish peroxidase study. J. Comp. Neurol. 1984, 226:238-245.
33. Nadelhaft I., McKenna K.E. Sexual dimorphism in sympathetic preganglionic neurons of the rat hypogastric nerve. J. Comp. Neurol. 1987, 256:308-315.
34. Nadelhaft I., Vera P.L. Central nervous system neurons infected by pseudorabies virus injected into the rat urinary bladder following unilateral transection of the pelvic nerve. J. Comp. Neurol. 1995, 359:443-456.
35. Neuhuber W. The central projections of visceral primary afferent neurons of the inferior mesenteric plexus and hypogastric nerve and the location of the related sensory and preganglionic sympathetic cell bodies in the rat. Anat. Embryol. 1982, 164:413-425.
36. Nieto J.H., Hoang T.X., Warner E.A., Franchini B.T., Westerlund U., Havton L.A. Titanium mesh implantation-a method to stabilize the spine and protect the spinal cord following a multilevel laminectomy in the adult rat. J. Neurosci. Methods 2005, 147:1-7.
37. Ohlsson M., Hoang T.X., Wu J., Havton L.A. Glial reactions in a rodent cauda equina injury and repair model. Exp. Brain Res. 2006, 170:52-60.
38. Oliveira A.L., Hydling F., Olsson E., Shi T., Edwards R.H., Fujiyama F., Kaneko T., Hökfelt T., Cullheim S., Meister B. Cellular localization of three vesicular glutamate transporter mRNAs and proteins in rat spinal cord and dorsal root ganglia. Synapse 2003, 50:117-129.
39. Pavlakis A.J., Siroky M.B., Goldstein I., Krane R.J. Neurourologic findings in conus medullaris and cauda equina injury. Arch. Neurol. 1983, 40:570-573.
40. Rouzade-Dominguez M.L., Miselis R., Valentino R.J. Central representation of bladder and colon revealed by dual transsynaptic tracing in the rat: substrates for pelvic visceral coordination. Eur. J. Neurosci. 2003, 18:3311-3324.
41. Sampson J.H., Cashman R.E., Nashold B.S., Friedman A.H. Dorsal root entry zone lesions for intractable pain after trauma to the conus medullaris and cauda equina. J. Neurosurg. 1995, 82:28-34.
42. Taylor T.K., Coolican M.J. Injuries of the conus medullaris. Paraplegia 1988, 26:393-400.
43. Vizzard M.A., Erdman S.L., de Groat W.C. Increased expression of neuronal nitric oxide synthase (NOS) in visceral neurons after nerve injury. J. Neurosci. 1995, 15:4033-4045.
44. Wang H.F., Shortland P., Park M.J., Grant G. Retrograde and transganglionic transport of horseradish peroxidase-conjugated cholera toxin B subunit, wheatgerm agglutinin and isolectin B4 from griffonia simplicifolia I in primary afferent neurons innervating the rat urinary bladder. Neuroscience 1998, 87:275-288.