Bilateral bulbospinal projections to pudendal motoneuron circuitry after chronic spinal cord hemisection injury as revealed by transsynaptic tracing with pseudorabies virus

Journal of Neurotrauma

Volumn 28, Issue 4, 2011, Pages 595-605

  Johnson, Richard D ^a   Chadha, Harpreet K ^b   Dugan, Victoria P ^a   Gupta, Daya S ^b   Ferrero, Sunny L ^a   Hubscher, Charles H ^b  

^a University of Florida   (United States)

^b University of Louisville School of Medicine   (United States)

Author keywords

animal studies; electrophysiology; immunohistochemistry; in vivo studies; spinal cord injury

Indexed keywords

TRACER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; LABELING INDEX; MALE; MOTONEURON; NONHUMAN; PSEUDORABIES HERPETOVIRUS; PUDENDAL NERVE; RAT; RETICULOSPINAL TRACT; SPINAL CORD HEMISECTION; SPINAL CORD INJURY;

ANIMALS; ELECTROPHYSIOLOGY; HERPESVIRUS 1, SUID; IMMUNOHISTOCHEMISTRY; MALE; MEDULLA OBLONGATA; MOTOR NEURONS; NEURAL PATHWAYS; NEURONAL TRACT-TRACERS; RATS; RATS, WISTAR; RECOVERY OF FUNCTION; SPINAL CORD; SPINAL CORD INJURIES; STATISTICS, NONPARAMETRIC; SYNAPSES;

EID: 79953827534     PISSN: 08977151     EISSN: None     Source Type: Journal    
DOI: 10.1089/neu.2009.1180     Document Type: Article

References (52)

1. Anderson, K.D. (2004). Targeting recovery: priorities of the spinal cord-injured population. J. Neurotrauma 21, 1371-1383. (Pubitemid 39435314)
2. Anderson, K.D., Borisoff, J.F., Johnson, R.D., Stiens, S.A., and Elliot, S.L. (2006). Long-term effects of spinal cord injury on sexual function in men: Implications for neuroplasticity. Spinal Cord 45, 338-348.
3. Aston-Jones, G., and Card, J.P. (2000). Use of pseudorabies virus to delineate multisynaptic circuits in brain: opportunities and limitations. J. Neurosci. Methods 103, 51-61.
4. Babu, R.S., and Namasivayam, A. (2008). Recovery of bipedal locomotion in bonnet macaques after spinal cord injury: footprint analysis. Synapse 62, 432-447. (Pubitemid 351614768)
5. Card, J.P., Rinamen, L., Lynn, R.B., Lee, B.H., Meade, R.P., Miselis, RR., and Enquist, L.W. (1993). Pseudorabies virus infection of the rat central nervous system: ultrastructural characterization of viral replication, transport, and pathogen-esis. J. Neurosci. 13, 2515-2539. (Pubitemid 23151767)
6. Card, J.P., Rinamen, L., Schwaber, J.S., Miselis, RR., Whealy, M.E., Robbins, A.K., and Enquist, L.W. (1990). Neurotropic properties of pseudorabies virus: uptake and transneuronal passage in the rat central nervous system. J. Neurosci. 10, 1974-1994.
7. Collins, W.F., III, Erichsen, J.T., and Rose, R.D. (1991). Pudendal motor and premotor neurons in the male rat: A WGA trans-neuronal study. J. Comp. Neurol. 308, 28-41.
8. Daniels, D., Miselis, RR., and Flanagan-Cato, L.M. (2001). Transneuronal tracing from sympathectomized lumbar epax-ial muscle in female rats. J. Neurobiol. 15, 278-290. (Pubitemid 32751481)
9. Duale, H., Hou, S., Derbenev, A.V., Smith, B.N., and Rab-chevsky, A.G (2009). Spinal cord injury reduces the efficacy of pseudorabies virus labeling of sympathetic preganglionic neurons. J. Neuropathol. Exp. Neurol. 68, 168-178.
10. Elliott, S.L. (2003). Sexual dysfunction and infertility in men with spinal cord disorders, in: Spinal Cord Medicine: Principles and Practice. V. Lin (ed). Demos Medical Publishing: New York, pps. 350-365.
11. Enquist, L.W. (2002). Exploiting circuit-specific spread of pseu-dorabies virus in the central nervous system: insights to pathogenesis and circuit tracers. J. Infect. Dis. 186, Suppl. 2, S209-S214. (Pubitemid 35370483)
12. Ferrero, S.L., Dugan, V.P., Hubscher, C.H., and Johnson, R.D. (2007). Depression of pudendal motoneuron segmental re-flexes from microstimulation of the lateral paragigantocellularis nucleus involves presynaptic inhibition of pudendal but not pelvic nerve afferent inputs, Soc Neurosci. Abst., 521.13.
13. Giuliano, F., Bernabé, J., Gengo, P., Alexandre, L., and Clément, P. (2007). Effect of acute dapoxetine administration on the pudendal motoneuron reflex in anesthetized rats: comparison with paroxetine. J. Urol. 177, 386-389. (Pubitemid 44879485)
14. Goshgarian, H.G. (2003). The crossed phrenic phenomenon: a model for plasticity in the respiratory pathways following spinal cord injury. J. Appl. Physiol. 94, 795-810. (Pubitemid 36158259)
15. Hermann, G.E., Holmes, G.M., Rogers, R.C., Beattie, M.S., and Bresnahan, J.C. (2003). Descending spinal projections from the rostral gigantocellular reticular nuclei complex. J. Comp. Neurol. 455, 210-221. (Pubitemid 35424258)
16. Holmes, G.M., Hermann, G.E., Rogers, R.C., Bresnahan, J.C., and Beattie, M.S. (2002). Dissociation of the effects of nu-cleus raphe obscurus or rostral ventrolateral medulla lesions on eliminatory and sexual reflexes. Physiol. Behav.75, 49-55. (Pubitemid 34226894)
17. Holmes, G.M., Rogers, RC., Bresnahan, J.C., and Beattie, M.S. (1998). External anal sphincter hyperreflexia following spinal transection in the rat. J. Neurotrauma 15, 451-457. (Pubitemid 28262279)
18. Holmes, G.M., Van Meter, M.J., Beattie, M.S., and Bresnahan, J.C. (2005). Serotonergic fiber sprouting to external anal sphincter motoneurons after spinal cord contusion. Exp. Neurol. 193, 29-42. (Pubitemid 40463265)
19. Hubscher, C.H., and Johnson, RD. (1999). Effects of acute and chronic midthoracic spinal cord injury on neural circuits for male sexual function. I. Ascending pathways. J. Neurophysiol. 82, 1381-1389.
20. Hubscher, C.H., and Johnson, RD. (2000). Effects of acute and chronic midthoracic spinal cord injury on neural circuits for male sexual function. II. Descending pathways. J. Neurophy-siol., 83, 2508-2518. (Pubitemid 30321445)
21. Hubscher, C.H., Reed, W.R., Kaddumi, E.G., Armstrong, J.E., and Johnson, R.D. (2010). Select spinal lesions reveal multiple ascending pathways in the rat conveying input from the male genitalia. J. Physiol. 588, 1073-1083.
22. Johnson, RD., and Hubscher, C.H. (2000). Brainstem micro-stimulation activates sympathetic fibers in pudendal nerve motor branch. Neuroreport 11, 1-4.
23. Johnson, RD., and Hubscher, C.H. (1998). Brainstem micro-stimulation differentially inhibits pudendal motoneuron reflex inputs. Neuroreport 9, 341-345. (Pubitemid 28081413)
24. Johnson, RD. (2006). Descending pathways modulating the spinal circuitry for ejaculation: effects of chronic spinal cord injury, in: Autonomic Dysfunction after Spinal Cord Injury. L.C. Weaver and C. Polosa (eds). Elsevier: Amsterdam, pps. 401-414.
25. Kerman, I.A., Enquist, L.W., Watson, S.J., and Yates, B.J. (2003). Brainstem substrates of sympatho-motor circuitry identified using trans-synaptic tracing with pseudorabies virus recom-binants. J. Neurosci. 23, 4657-4666. (Pubitemid 36706194)
26. Kim, E.S., Kim, G.M., Lu, X., Hsu, C.Y., and Xu, X.M. (2002). Neural circuitry of the adult rat central nervous system after spinal cord injury: a study using fast blue and the Bartha strain of pseudorabies virus. J. Neurotrauma 19, 787-800. (Pubitemid 34761340)
27. Lee, J.W., and Erskine, M.S. (2000). Pseudorabies virus tracing of neural pathways between the uterine cervix and CNS: effects of survival time, estrogen treatment, rhizotomy, and pelvic nerve transection. J. Comp. Neurol. 20, 484-503. (Pubitemid 30127690)
28. Little, J.W., Harris, RM., and Lerner, S.J. (1991). Immobilization impairs recovery after spinal cord injury. Arch. Phys. Med. Rehabil. 72, 408-412.
29. Loewy, A.D. (1998). Viruses as transneuronal tracers for defining neural circuits. Neurosci. Biobehav. Rev. 22, 679-684. (Pubitemid 28493440)
30. Marson, L., and Carson, C.C. (1999). Central nervous system innervation of the penis, prostate, and perineal muscles: A transneuronal tracing study. Mol. Urol. 3, 43-50. (Pubitemid 29367883)
31. Marson, L., and McKenna, K.E. (1996). CNS cell groups involved in the control of ischiocavernosus and bulbospongiosus mus-cles: a transneuronal tracing study using pseudorabies virus. J. Comp. Neurol. 374, 161-179. (Pubitemid 26357183)
32. Marson, L., and McKenna, K.E. (1990). The identification of a brainstem site controlling spinal sexual reflexes in male rats. Brain Res. 515, 303-308. (Pubitemid 20176130)
33. Marson, L., and Murphy, A.Z. (2006). Identification of neural circuits involved in female genital responses in the rat: a dual virus and anterograde tracing study. Am. J. Physiol. 291, R419-R428. (Pubitemid 44035650)
34. Marson, L., Platt, K.B., and McKenna, K.E. (1993). Central ner-vous system innervation of the penis as revealed by the transneuronal transport of pseudorabies virus. Neuroscience 55, 263-280. (Pubitemid 23195002)
35. McKenna, K.E., and Nadelhaft, I. (1989). The pudendo-pudendal reflex in male and female rats. J. Autonom. Nerv. Syst. 27, 67-77. (Pubitemid 19180535)
36. Meisel, RL., and Sachs, B.D. (1994). The physiology of male sexual behavior, in: The Physiology of Reproduction, Vol. 2. E. Knobil, and J.D.D. Neill (eds). Raven Press: New York, pps. 3-105.
37. Monaghan, E.P., and Breedlove, S.M. (1991). Brain sites pro-jecting to the spinal nucleus of the bulbocavernosus. J. Comp. Neurol. 307, 370-374.
38. Nadelhaft, I., and Vera, P.L. (1996). Neurons in the rat brain and spinal cord labeled after pseudorabies virus injected into the external urethral sphincter. J. Comp. Neurol. 375, 502-517. (Pubitemid 26374787)
39. Paxinos, G., and Watson, C. (1998). The Rat Brain in Stereotaxic Coordinates, 4th ed. Academic Press: San Diego.
40. Petruska, J.C., Cooper, BY., Gu, J.G., Rau, K.K., and Johnson, RD. (2000). Distribution of P2x1, P2x2, and P2x3 receptor subunits in rat DRG: Relation to population markers and specific cell types. J. Chem. Neuroanat. 20, 141-162.
41. Pritchard, C.D., Slotkin, J.R., Yu, D., Dai, H., Lawrence, M.S., Bronson, R.T., Reynolds, F.M., Teng, Y.D., Woodard, E.J., and Langer, RS. (2010). Establishing a model spinal cord injury in the African green monkey for the preclinical evaluation of biodegradable polymer scaffolds seeded with human neural stem cells. J. Neurosci. Methods 188, 258-269.
42. Rau, K.K., Cooper, BY., and Johnson, R.D. (2006). Expression of TWIK-related acid sensitive K+ channels in capsaicin sensi-tive and insensitive cells of rat dorsal root ganglia. Neu-roscience 141, 955-963. (Pubitemid 44066666)
43. Rinaman, L., Card, J.P., and Enquist, L.W. (1993). Spatio-temporal responses of astrocytes, ramified microglia, and brain macrophages to central nervous system infection with pseudorabies virus. J. Neurosci. 13, 685-702. (Pubitemid 23045151)
44. Schucht, P., Raineteau, O., Schwab, M.E., and Fouad, K. (2002). Anatomical correlates of locomotor recovery following dorsal and ventral lesions of the rat spinal cord. Exp. Neurol. 176, 143-153. (Pubitemid 34762114)
45. Scivoletto, G., Cosentino, E., Morganti, B., Farchi, S., and Moli-nari, M. (2008). Clinical prognostic factors for bladder function recovery of patients with spinal cord and cauda equina le-sions. Disabil. Rehabil. 30, 330-337. (Pubitemid 351260448)
46. Shen, P., Arnold, A.P., and Micevych, P.E. (1990). Supraspinal projections to the ventromedial lumbar spinal cord in adult male rats. J. Comp. Neurol. 300, 263-272. (Pubitemid 20361333)
47. Thor, K.B., Katofiasc, M.A., Danuser, H., Springer, J., and Schaus, J.M. (2002). The role of 5-HT(1A) receptors in control of lower urinary tract function in cats. Brain Res. 946, 290-297. (Pubitemid 34876342)
48. Vizzard, M.A., Erickson, V.L., Card, J.P., Roppolo, J.R., and de Groat, W.C. (1995). Transneuronal labeling of neurons in the adult rat brainstem and spinal cord after injection of pseudorabies virus into the urethra. J. Comp. Neurol. 355, 629-640.
49. Wieder, JA., Brackett, N.L., Lynne, C.M., Green, J.T., and Aballa, T.C. (2000). Anesthetic block of the dorsal penile nerve inhibits vibratory-induced ejaculation in men with spinal cord injuries. Urology 55, 915-917. (Pubitemid 30330799)
50. Yang, C.C., and Bradley, W.E. (1999). Somatic innervation of the human bulbocavernosus muscle. Clin. Neurophysiol. 110, 412-418. (Pubitemid 29207490)
51. Yells, D.P., Hendricks, S.E., and Prendergast, M.A. (1992). Le-sions of the nucleus paragigantocellularis: effects on mating behavior in male rats. Brain Res. 596,73-79.
52. Yu, X., Xu, L., Zhang, X.D., and Cui, F.Z. (2003). Effect of spinal cord injury on urinary bladder spinal neural pathway: a ret-rograde transneuronal tracing study with pseudorabies virus. Urology 62, 755-759. (Pubitemid 37205028)