Skip to main content

Advertisement

SpringerLink
Log in

Sexual Function after Spinal Cord Injury: Innervation, Assessment, and Treatment

  • Preclinical and Psychophysiology (J Pfaus and L Marson, Section Editors)
  • Published:
Current Sexual Health Reports Aims and scope Submit manuscript

Abstract

Sexual function is a high priority quality of life issue among the spinal cord injury (SCI) population. Over 12,000 new cases are reported in the USA annually, with males being twice as likely to incur a SCI compared to females. SCI males may suffer from erectile and ejaculatory dysfunction and infertility, while SCI females may suffer from dysfunctions of sexual arousal and orgasm. Assessment of sexual dysfunction in SCI individuals relies on questionnaires and reflex circuitries, highlighting the need for better quantitative assessment and outcome measures. Treatments for SCI males include pharmacotherapy, physical aids, and surgical interventions; however, treatments for SCI females is severely lacking. Advancements in assessments and treatments in both animal models and humans will pave the way for greater sexual dysfunction intervention in SCI individuals.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

Papers of particular interest, published recently, have been highlighted as: • Of importance •• Of major importance

  1. Center NSCIS. Complete public version of the 2014 annual statistical report for the spinal cord injury model systems. Birmingham, Alabama: University of Alabama at Birmingham; 2014.

    Google Scholar 

  2. Anderson KD. Targeting recovery: priorities of the spinal cord-injured population. J Neurotrauma. 2004;21(10):1371–83.

    Article  PubMed  Google Scholar 

  3. Anderson KD, Borisoff JF, Johnson RD, Stiens SA, Elliott SL. The impact of spinal cord injury on sexual function: concerns of the general population. Spinal Cord. 2007;45(5):328–37. doi:10.1038/sj.sc.3101977.

    CAS  PubMed  Google Scholar 

  4. Albright TH, Grabel Z, DePasse JM, Palumbo MA, Daniels AH. Sexual and reproductive function in spinal cord injury and spinal surgery patients. Orthop Rev. 2015;7(3):5842. doi:10.4081/or.2015.5842.

    Article  Google Scholar 

  5. Siosteen A, Lundqvist C, Blomstrand C, Sullivan L, Sullivan M. Sexual ability, activity, attitudes and satisfaction as part of adjustment in spinal cord-injured subjects. Paraplegia. 1990;28(5):285–95. doi:10.1038/sc.1990.38.

    Article  CAS  PubMed  Google Scholar 

  6. Kreuter M, Sullivan M, Siosteen A. Sexual adjustment and quality of relationship in spinal paraplegia: a controlled study. Arch Phys Med Rehabil. 1996;77(6):541–8.

    Article  CAS  PubMed  Google Scholar 

  7. Biering-Sorensen I, Hansen RB, Biering-Sorensen F. Sexual function in a traumatic spinal cord injured population 10–45 years after injury. J Rehabil Med. 2012;44(11):926–31. doi:10.2340/16501977-1057.

    Article  PubMed  Google Scholar 

  8. Anderson KD, Borisoff JF, Johnson RD, Stiens SA, Elliott SL. Long-term effects of spinal cord injury on sexual function in men: implications for neuroplasticity. Spinal Cord. 2007;45(5):338–48. doi:10.1038/sj.sc.3101978.

    CAS  PubMed  Google Scholar 

  9. Guttmann L. The sexual problem (chapter 29). In: Guttmann L, editor. Spinal cord injuries. Comprehensive management and research. 2nd ed. Oxford, London, Edinburgh, Melbourne: Blackwell Scientific Publications; 1976. p. 474–505.

    Google Scholar 

  10. Biering-Sorensen F, Sonksen J. Sexual function in spinal cord lesioned men. Spinal Cord. 2001;39(9):455–70. doi:10.1038/sj.sc.3101198.

    Article  CAS  PubMed  Google Scholar 

  11. Courtois FJ, Charvier KF, Leriche A, Raymond DP. Sexual function in spinal cord injury men. I. Assessing sexual capability. Paraplegia. 1993;31(12):771–84. doi:10.1038/sc.1993.120.

    Article  CAS  PubMed  Google Scholar 

  12. Giuliano F, Rampin O. Central neural regulation of penile erection. Neurosci Biobehav Rev. 2000;24(5):517–33.

    Article  CAS  PubMed  Google Scholar 

  13. Hancock MB, Peveto CA. Preganglionic neurons in the sacral spinal cord of the rat: an HRP study. Neurosci Lett. 1979;11(1):1–5.

    Article  CAS  PubMed  Google Scholar 

  14. Nadelhaft I, Booth AM. 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(2):238–45. doi:10.1002/cne.902260207.

    Article  CAS  PubMed  Google Scholar 

  15. Steers WD. Neural pathways and central sites involved in penile erection: neuroanatomy and clinical implications. Neurosci Biobehav Rev. 2000;24(5):507–16.

    Article  CAS  PubMed  Google Scholar 

  16. Lue TF, Takamura T, Schmidt RA, Palubinskas AJ, Tanagho EA. Hemodynamics of erection in the monkey. J Urol. 1983;130(6):1237–41.

    CAS  PubMed  Google Scholar 

  17. Andersson PO, Bloom SR, Mellander S. Haemodynamics of pelvic nerve induced penile erection in the dog: possible mediation by vasoactive intestinal polypeptide. J Physiol. 1984;350:209–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sjostrand NO, Klinge E. Principal mechanisms controlling penile retraction and protrusion in rabbits. Acta Physiol Scand. 1979;106(2):199–214. doi:10.1111/j.1748-1716.1979.tb06390.x.

    Article  CAS  PubMed  Google Scholar 

  19. Quinlan DM, Nelson RJ, Partin AW, Mostwin JL, Walsh PC. The rat as a model for the study of penile erection. J Urol. 1989;141(3):656–61.

    CAS  PubMed  Google Scholar 

  20. Giuliano F, Rampin O, Bernabe J, Rousseau JP. Neural control of penile erection in the rat. J Auton Nerv Syst. 1995;55(1–2):36–44.

    Article  CAS  PubMed  Google Scholar 

  21. Alexander MS, Biering-Sorensen F, Bodner D, Brackett NL, Cardenas D, Charlifue S, et al. International standards to document remaining autonomic function after spinal cord injury. Spinal Cord. 2009;47(1):36–43. doi:10.1038/sc.2008.121.

    Article  CAS  PubMed  Google Scholar 

  22. Tajkarimi K, Burnett AL. The role of genital nerve afferents in the physiology of the sexual response and pelvic floor function. J Sex Med. 2011;8(5):1299–312. doi:10.1111/j.1743-6109.2011.02211.x.

    Article  PubMed  Google Scholar 

  23. McKenna KE, Nadelhaft I. The pudendo-pudendal reflex in male and female rats. J Auton Nerv Syst. 1989;27(1):67–77.

    Article  CAS  PubMed  Google Scholar 

  24. Bodner DR, Lindan R, Leffler E, Kursh ED, Resnick MI. The application of intracavernous injection of vasoactive medications for erection in men with spinal cord injury. J Urol. 1987;138(2):310–1.

    CAS  PubMed  Google Scholar 

  25. Monaghan EP, Arjomand J, Breedlove SM. Brain lesions affect penile reflexes. Horm Behav. 1993;27(1):122–31. doi:10.1006/hbeh.1993.1009.

    Article  CAS  PubMed  Google Scholar 

  26. Marson L, List MS, McKenna KE. Lesions of the nucleus paragigantocellularis alter ex copula penile reflexes. Brain Res. 1992;592(1–2):187–92.

    Article  CAS  PubMed  Google Scholar 

  27. Kondo Y, Sachs BD, Sakuma Y. Importance of the medial amygdala in rat penile erection evoked by remote stimuli from estrous females. Behav Brain Res. 1998;91(1–2):215–22.

    CAS  PubMed  Google Scholar 

  28. Georgiadis JR, Holstege G. Human brain activation during sexual stimulation of the penis. J Comp Neurol. 2005;493(1):33–8. doi:10.1002/cne.20735.

    Article  PubMed  Google Scholar 

  29. Janig W, McLachlan EM. Organization of lumbar spinal outflow to distal colon and pelvic organs. Physiol Rev. 1987;67(4):1332–404.

    CAS  PubMed  Google Scholar 

  30. Diederichs W, Stief CG, Benard F, Bosch R, Lue TF, Tanagho EA. The sympathetic role as an antagonist of erection. Urol Res. 1991;19(2):123–6.

    Article  CAS  PubMed  Google Scholar 

  31. Lorenz TA, Harte CB, Hamilton LD, Meston CM. Evidence for a curvilinear relationship between sympathetic nervous system activation and women’s physiological sexual arousal. Psychophysiology. 2012;49(1):111–7. doi:10.1111/j.1469-8986.2011.01285.x.

    Article  PubMed  PubMed Central  Google Scholar 

  32. Liu YC, Salamone JD, Sachs BD. Impaired sexual response after lesions of the paraventricular nucleus of the hypothalamus in male rats. Behav Neurosci. 1997;111(6):1361–7.

    Article  CAS  PubMed  Google Scholar 

  33. Liu YC, Salamone JD, Sachs BD. Lesions in medial preoptic area and bed nucleus of stria terminalis: differential effects on copulatory behavior and noncontact erection in male rats. J Neurosci. 1997;17(13):5245–53.

    CAS  PubMed  Google Scholar 

  34. Miyagawa Y, Tsujimura A, Fujita K, Matsuoka Y, Takahashi T, Takao T, et al. Differential brain processing of audiovisual sexual stimuli in men: comparative positron emission tomography study of the initiation and maintenance of penile erection during sexual arousal. NeuroImage. 2007;36(3):830–42. doi:10.1016/j.neuroimage.2007.03.055.

    Article  PubMed  Google Scholar 

  35. Chehensse C, Bahrami S, Denys P, Clement P, Bernabe J, Giuliano F. The spinal control of ejaculation revisited: a systematic review and meta-analysis of an ejaculation in spinal cord injured patients. Hum Reprod Update. 2013;19(5):507–26. doi:10.1093/humupd/dmt029.

    Article  CAS  PubMed  Google Scholar 

  36. Seftel AD, Oates RD, Krane RJ. Disturbed sexual function in patients with spinal cord disease. Neurol Clin. 1991;9(3):757–78.

    CAS  PubMed  Google Scholar 

  37. Ver Voort SM. Infertility in spinal-cord injured male. Urology. 1987;29(2):157–65.

    Article  CAS  PubMed  Google Scholar 

  38. Mallidis C, Lim TC, Hill ST, Skinner DJ, Brown DJ, Johnston WI, et al. Collection of semen from men in acute phase of spinal cord injury. Lancet. 1994;343(8905):1072–3.

    Article  CAS  PubMed  Google Scholar 

  39. Naderi AR, Safarinejad MR. Endocrine profiles and semen quality in spinal cord injured men. Clin Endocrinol. 2003;58(2):177–84.

    Article  CAS  Google Scholar 

  40. Elliott SP, Orejuela F, Hirsch IH, Lipshultz LI, Lamb DJ, Kim ED. Testis biopsy findings in the spinal cord injured patient. J Urol. 2000;163(3):792–5.

    Article  CAS  PubMed  Google Scholar 

  41. Brown DJ, Hill ST, Baker HW. Male fertility and sexual function after spinal cord injury. Prog Brain Res. 2006;152:427–39. doi:10.1016/S0079-6123(05)52029-6.

    Article  CAS  PubMed  Google Scholar 

  42. McKenna KE. Ejaculation. In: Knobil EN J, editor. Encycolopedia of reproduction. New York: Academic Press; 1999. p. 1002–8.

    Google Scholar 

  43. Newman HF, Reiss H, Northup JD. Physical basis of emission, ejaculation, and orgasm in the male. Urology. 1982;19(4):341–50.

    Article  CAS  PubMed  Google Scholar 

  44. Colpi G, Weidner W, Jungwirth A, Pomerol J, Papp G, Hargreave T, et al. EAU guidelines on ejaculatory dysfunction. Eur Urol. 2004;46(5):555–8. doi:10.1016/j.eururo.2004.07.020.

    Article  CAS  PubMed  Google Scholar 

  45. Giuliano F, Clement P. Neuroanatomy and physiology of ejaculation. Annu Rev Sex Res. 2005;16:190–216.

    PubMed  Google Scholar 

  46. Shafik A, El-Sibai O. Mechanism of ejection during ejaculation: identification of a urethrocavernosus reflex. Arch Androl. 2000;44(1):77–83.

    Article  CAS  PubMed  Google Scholar 

  47. Motofei IG, Rowland DL. Neurophysiology of the ejaculatory process: developing perspectives. BJU Int. 2005;96(9):1333–8. doi:10.1111/j.1464-410X.2005.05850.x.

    Article  CAS  PubMed  Google Scholar 

  48. Yavetz H, Yogev L, Hauser R, Lessing JB, Paz G, Homonnai ZT. Retrograde ejaculation. Hum Reprod. 1994;9(3):381–6.

    CAS  PubMed  Google Scholar 

  49. Fode M, Krogh-Jespersen S, Brackett NL, Ohl DA, Lynne CM, Sonksen J. Male sexual dysfunction and infertility associated with neurological disorders. Asian J Androl. 2012;14(1):61–8. doi:10.1038/aja.2011.70.

    Article  PubMed  PubMed Central  Google Scholar 

  50. Giuliano F, Clement P. Physiology of ejaculation: emphasis on serotonergic control. Eur Urol. 2005;48(3):408–17. doi:10.1016/j.eururo.2005.05.017.

    Article  PubMed  Google Scholar 

  51. Carro-Juarez M, Rodriguez-Manzo G. The spinal pattern generator for ejaculation. Brain Res Rev. 2008;58(1):106–20. doi:10.1016/j.brainresrev.2007.12.002.

    Article  PubMed  Google Scholar 

  52. Carro-Juarez M, Cruz SL, Rodriguez-Manzo G. Evidence for the involvement of a spinal pattern generator in the control of the genital motor pattern of ejaculation. Brain Res. 2003;975(1–2):222–8.

    Article  CAS  PubMed  Google Scholar 

  53. Chapelle PA, Roby-Brami A, Yakovleff A, Bussel B. Neurological correlations of ejaculation and testicular size in men with a complete spinal cord section. J Neurol Neurosurg Psychiatry. 1988;51(2):197–202.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Markowski VP, Eaton RC, Lumley LA, Moses J, Hull EM. A D1 agonist in the MPOA facilitates copulation in male rats. Pharmacol Biochem Behav. 1994;47(3):483–6.

    Article  CAS  PubMed  Google Scholar 

  55. Marson L, McKenna KE. Stimulation of the hypothalamus initiates the urethrogenital reflex in male rats. Brain Res. 1994;638(1–2):103–8.

    Article  CAS  PubMed  Google Scholar 

  56. Kippin TE, Sotiropoulos V, Badih J, Pfaus JG. Opposing roles of the nucleus accumbens and anterior lateral hypothalamic area in the control of sexual behaviour in the male rat. Eur J Neurosci. 2004;19(3):698–704.

    Article  PubMed  Google Scholar 

  57. Marson L, McKenna KE. A role for 5-hydroxytryptamine in descending inhibition of spinal sexual reflexes. Exp Brain Res. 1992;88(2):313–20.

    Article  CAS  PubMed  Google Scholar 

  58. Marson L, McKenna KE. The identification of a brainstem site controlling spinal sexual reflexes in male rats. Brain Res. 1990;515(1–2):303–8.

    Article  CAS  PubMed  Google Scholar 

  59. Antal M, Petko M, Polgar E, Heizmann CW, Storm-Mathisen J. Direct evidence of an extensive GABAergic innervation of the spinal dorsal horn by fibres descending from the rostral ventromedial medulla. Neuroscience. 1996;73(2):509–18.

    Article  CAS  PubMed  Google Scholar 

  60. Basbaum AI, Fields HL. The origin of descending pathways in the dorsolateral funiculus of the spinal cord of the cat and rat: further studies on the anatomy of pain modulation. J Comp Neurol. 1979;187(3):513–31. doi:10.1002/cne.901870304.

    Article  CAS  PubMed  Google Scholar 

  61. Casey KL. Somatic stimuli, spinal pathways, and size of cutaneous fibers influencing unit activity in the medial medulary reticular formation. Exp Neurol. 1969;25(1):35–56.

    Article  CAS  PubMed  Google Scholar 

  62. Chaouch A, Menetrey D, Binder D, Besson JM. Neurons at the origin of the medial component of the bulbopontine spinoreticular tract in the rat: an anatomical study using horseradish peroxidase retrograde transport. J Comp Neurol. 1983;214(3):309–20. doi:10.1002/cne.902140308.

    Article  CAS  PubMed  Google Scholar 

  63. Gallager DW, Pert A. Afferents to brain stem nuclei (brain stem raphe, nucleus reticularis pontis caudalis and nucleus gigantocellularis) in the rat as demonstrated by microiontophoretically applied horseradish peroxidase. Brain Res. 1978;144(2):257–75.

    Article  CAS  PubMed  Google Scholar 

  64. Hermann GE, Holmes GM, Rogers RC, Beattie MS, Bresnahan JC. Descending spinal projections from the rostral gigantocellular reticular nuclei complex. J Comp Neurol. 2003;455(2):210–21. doi:10.1002/cne.10455.

    Article  PubMed  Google Scholar 

  65. Odutola AB. On the location of reticular neurons projecting to the cuneo-gracile nuclei in the rat. Exp Neurol. 1977;54(1):54–9.

    Article  CAS  PubMed  Google Scholar 

  66. Mtui EP, Anwar M, Reis DJ, Ruggiero DA. Medullary visceral reflex circuits: local afferents to nucleus tractus solitarii synthesize catecholamines and project to thoracic spinal cord. J Comp Neurol. 1995;351(1):5–26. doi:10.1002/cne.903510103.

    Article  CAS  PubMed  Google Scholar 

  67. Tomasulo KC, Emmers R. Activation of neurons in the gracile nucleus by two afferent pathways in the rat. Exp Neurol. 1972;36(1):197–206.

    Article  CAS  PubMed  Google Scholar 

  68. Holstege G, Georgiadis JR, Paans AM, Meiners LC, van der Graaf FH, Reinders AA. Brain activation during human male ejaculation. J Neurosci. 2003;23(27):9185–93.

    CAS  PubMed  Google Scholar 

  69. Sonksen J, Ohl DA. Penile vibratory stimulation and electro ejaculation in the treatment of ejaculatory dysfunction. Int J Androl. 2002;25(6):324–32.

    Article  PubMed  Google Scholar 

  70. Ibrahim E, Lynne CM, Brackett NL. Male fertility following spinal cord injury: an update. Andrology. 2016;4(1):13–26. doi:10.1111/andr.12119.

    Article  CAS  PubMed  Google Scholar 

  71. Truitt WA, Coolen LM. Identification of a potential ejaculation generator in the spinal cord. Science. 2002;297(5586):1566–9. doi:10.1126/science.1073885.

    Article  CAS  PubMed  Google Scholar 

  72. Linsenmeyer TA. Sexual function and infertility following spinal cord injury. Phys Med Rehabil Clin N Am. 2000;11(1):141–56. ix.

    CAS  PubMed  Google Scholar 

  73. Sipski ML, Alexander CJ, Rosen RC. Physiological parameters associated with psychogenic sexual arousal in women with complete spinal cord injuries. Arch Phys Med Rehabil. 1995;76(9):811–8.

    Article  CAS  PubMed  Google Scholar 

  74. Berard EJ. The sexuality of spinal cord injured women: physiology and pathophysiology. A review. Paraplegia. 1989;27(2):99–112. doi:10.1038/sc.1989.16.

    Article  CAS  PubMed  Google Scholar 

  75. Sipski ML, Alexander CJ, Rosen RC. Physiologic parameters associated with sexual arousal in women with incomplete spinal cord injuries. Arch Phys Med Rehabil. 1997;78(3):305–13.

    Article  CAS  PubMed  Google Scholar 

  76. Salonia A, Giraldi A, Chivers ML, Georgiadis JR, Levin R, Maravilla KR, et al. Physiology of women’s sexual function: basic knowledge and new findings. J Sex Med. 2010;7(8):2637–60. doi:10.1111/j.1743-6109.2010.01810.x.

    Article  PubMed  Google Scholar 

  77. McKenna KE. The neurophysiology of female sexual function. World J Urol. 2002;20(2):93–100. doi:10.1007/s00345-002-0270-7.

    Article  PubMed  Google Scholar 

  78. Park K, Goldstein I, Andry C, Siroky MB, Krane RJ, Azadzoi KM. Vasculogenic female sexual dysfunction: the hemodynamic basis for vaginal engorgement insufficiency and clitoral erectile insufficiency. Int J Impot Res. 1997;9(1):27–37.

    Article  CAS  PubMed  Google Scholar 

  79. Berkley KJ, Hubscher CH, Wall PD. Neuronal responses to stimulation of the cervix, uterus, colon, and skin in the rat spinal cord. J Neurophysiol. 1993;69(2):545–56.

    CAS  PubMed  Google Scholar 

  80. Hubscher CH. Central convergence of viscerosomatic inputs from spinal and vagal sources. In: King HH, Jӓnig W, Patterson MM, editors. The science and clinical application of manual therapy. Edinburg, London, New York, Oxford, Philadelphia, St. Louis, Sydney, Toronto: Churchill Livingstone Elsevier; 2011.

    Google Scholar 

  81. Levin RJ. Can the controversy about the putative role of the human female orgasm in sperm transport be settled with our current physiological knowledge of coitus? J Sex Med. 2011;8(6):1566–78. doi:10.1111/j.1743-6109.2010.02162.x.

    Article  PubMed  Google Scholar 

  82. Sato S, Hayashi RH, Garfield RE. Mechanical responses of the rat uterus, cervix, and bladder to stimulation of hypogastric and pelvic nerves in vivo. Biol Reprod. 1989;40(2):209–19.

    Article  CAS  PubMed  Google Scholar 

  83. Levin RJ. Do women gain anything from coitus apart from pregnancy? Changes in the human female genital tract activated by coitus. J Sex Marital Ther. 2003;29 Suppl 1:59–69. doi:10.1080/713847134.

    Article  PubMed  Google Scholar 

  84. De Blok S. The connective tissue of the adult female pelvic region. A musculo-fibrous apparatus. Acta Morphol Neerl Scand. 1982;20(4):347–62.

    PubMed  Google Scholar 

  85. Sipski ML, Rosen RC, Alexander CJ, Gomez-Marin O. Sexual responsiveness in women with spinal cord injuries: differential effects of anxiety-eliciting stimulation. Arch Sex Behav. 2004;33(3):295–302. doi:10.1023/B:ASEB.0000026629.33441.cf.

    Article  PubMed  Google Scholar 

  86. Sipski ML, Alexander CJ, Rosen R. Sexual arousal and orgasm in women: effects of spinal cord injury. Ann Neurol. 2001;49(1):35–44.

    Article  CAS  PubMed  Google Scholar 

  87. Sipski ML, Arenas A. Female sexual function after spinal cord injury. Prog Brain Res. 2006;152:441–7. doi:10.1016/S0079-6123(05)52030-2.

    Article  PubMed  Google Scholar 

  88. Atterbury JL, Groome LJ. Pregnancy in women with spinal cord injuries. Nurs Clin N Am. 1998;33(4):603–13.

    CAS  Google Scholar 

  89. Reame NE. A prospective study of the menstrual cycle and spinal cord injury. Am J Phys Med Rehabil. 1992;71(1):15–21.

    Article  CAS  PubMed  Google Scholar 

  90. Cross LL, Meythaler JM, Tuel SM, Cross AL. Pregnancy, labor and delivery post spinal cord injury. Paraplegia. 1992;30(12):890–902. doi:10.1038/sc.1992.166.

    Article  CAS  PubMed  Google Scholar 

  91. Komisaruk BR, Gerdes CA, Whipple B. ‘Complete’ spinal cord injury does not block perceptual responses to genital self-stimulation in women. Arch Neurol. 1997;54(12):1513–20.

    Article  CAS  PubMed  Google Scholar 

  92. Ortega-Villalobos M, Garcia-Bazan M, Solano-Flores LP, Ninomiya-Alarcon JG, Guevara-Guzman R, Wayner MJ. Vagus nerve afferent and efferent innervation of the rat uterus: an electrophysiological and HRP study. Brain Res Bull. 1990;25(3):365–71.

    Article  CAS  PubMed  Google Scholar 

  93. Papka RE, Williams S, Miller KE, Copelin T, Puri P. CNS location of uterine-related neurons revealed by trans-synaptic tracing with pseudorabies virus and their relation to estrogen receptor-immunoreactive neurons. Neuroscience. 1998;84(3):935–52.

    Article  CAS  PubMed  Google Scholar 

  94. Komisaruk BR, Bianca R, Sansone G, Gomez LE, Cueva-Rolon R, Beyer C, et al. Brain-mediated responses to vaginocervical stimulation in spinal cord-transected rats: role of the vagus nerves. Brain Res. 1996;708(1–2):128–34.

    Article  CAS  PubMed  Google Scholar 

  95. Hubscher CH, Berkley KJ. Responses of neurons in caudal solitary nucleus of female rats to stimulation of vagina, cervix, uterine horn and colon. Brain Res. 1994;664(1–2):1–8.

    Article  CAS  PubMed  Google Scholar 

  96. Menetrey D, De Pommery J. Origins of spinal ascending pathways that reach central areas involved in visceroception and visceronociception in the rat. Eur J Neurosci. 1991;3(3):249–59.

    Article  PubMed  Google Scholar 

  97. Kawatani M, Tanowitz M, de Groat WC. Morphological and electrophysiological analysis of the peripheral and central afferent pathways from the clitoris of the cat. Brain Res. 1994;646(1):26–36.

    Article  CAS  PubMed  Google Scholar 

  98. Bradshaw HB, Berkley KJ. Estrous changes in responses of rat gracile nucleus neurons to stimulation of skin and pelvic viscera. J Neurosci. 2000;20(20):7722–7.

    CAS  PubMed  Google Scholar 

  99. Berkley KJ, Hubscher CH. Are there separate central nervous system pathways for touch and pain? Nat Med. 1995;1(8):766–73.

    Article  CAS  PubMed  Google Scholar 

  100. Berkley KJ, Guilbaud G, Benoist JM, Gautron M. Responses of neurons in and near the thalamic ventrobasal complex of the rat to stimulation of uterus, cervix, vagina, colon, and skin. J Neurophysiol. 1993;69(2):557–68.

    CAS  PubMed  Google Scholar 

  101. Reed WR, Chadha HK, Hubscher CH. Effects of 17beta-estradiol on responses of viscerosomatic convergent thalamic neurons in the ovariectomized female rat. J Neurophysiol. 2009;102(2):1062–74. doi:10.1152/jn.00165.2009.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Rosen RC, Riley A, Wagner G, Osterloh IH, Kirkpatrick J, Mishra A. The international index of erectile function (IIEF): a multidimensional scale for assessment of erectile dysfunction. Urology. 1997;49(6):822–30.

    Article  CAS  PubMed  Google Scholar 

  103. Lombardi G, Musco S, Kessler TM, Li Marzi V, Lanciotti M, Del Popolo G. Management of sexual dysfunction due to central nervous system disorders: a systematic review. BJU Int. 2015;115 Suppl 6:47–56. doi:10.1111/bju.13055.

    Article  PubMed  Google Scholar 

  104. Rosen RC, Althof SE, Giuliano F. Research instruments for the diagnosis and treatment of patients with erectile dysfunction. Urology. 2006;68(3 Suppl):6–16. doi:10.1016/j.urology.2006.05.046.

    Article  PubMed  Google Scholar 

  105. Alexander MS, Brackett NL, Bodner D, Elliott S, Jackson A, Sonksen J, et al. Measurement of sexual functioning after spinal cord injury: preferred instruments. J Spinal Cord Med. 2009;32(3):226–36.

    PubMed  PubMed Central  Google Scholar 

  106. Rushworth G. Diagnostic value of the electromyographic study of reflex activity in man. Electroencephalogr Clin Neurophysiol. 1967;1967 Suppl 25:65–73.

    Google Scholar 

  107. Granata G, Padua L, Rossi F, De Franco P, Coraci D, Rossi V. Electrophysiological study of the bulbocavernosus reflex: normative data. Funct Neurol. 2013;28(4):293–5. doi:10.11138/FNeur/2013.28.4.293. Normative bulbocavernosus reflex data on a large sample size.

    PubMed  PubMed Central  Google Scholar 

  108. Bird VG, Brackett NL, Lynne CM, Aballa TC, Ferrell SM. Reflexes and somatic responses as predictors of ejaculation by penile vibratory stimulation in men with spinal cord injury. Spinal Cord. 2001;39(10):514–9. doi:10.1038/sj.sc.3101200.

    Article  CAS  PubMed  Google Scholar 

  109. Alexander MS, Biering-Sorensen F, Elliott S, Kreuter M, Sonksen J. International spinal cord injury male sexual function basic data set. Spinal Cord. 2011;49(7):795–8. doi:10.1038/sc.2010.192.

    Article  CAS  PubMed  Google Scholar 

  110. Rosen R, Brown C, Heiman J, Leiblum S, Meston C, Shabsigh R, et al. The female sexual function index (FSFI): a multidimensional self-report instrument for the assessment of female sexual function. J Sex Marital Ther. 2000;26(2):191–208. doi:10.1080/009262300278597.

    Article  CAS  PubMed  Google Scholar 

  111. Lombardi G, Mondaini N, Macchiarella A, Cilotti A, Del Popolo G. Clinical female sexual outcome after sacral neuromodulation implant for lower urinary tract symptom (LUTS). J Sex Med. 2008;5(6):1411–7. doi:10.1111/j.1743-6109.2008.00812.x.

    Article  PubMed  Google Scholar 

  112. Cardenas DD, Ditunno JF, Graziani V, McLain AB, Lammertse DP, Potter PJ, et al. Two phase 3, multicenter, randomized, placebo-controlled clinical trials of fampridine-SR for treatment of spasticity in chronic spinal cord injury. Spinal Cord. 2014;52(1):70–6. doi:10.1038/sc.2013.137.

    Article  CAS  PubMed  Google Scholar 

  113. Lombardi G, Mondaini N, Macchiarella A, Del Popolo G. Female sexual dysfunction and hormonal status in spinal cord injured (SCI) patients. J Androl. 2007;28(5):722–6. doi:10.2164/jandrol.106.002113.

    Article  CAS  PubMed  Google Scholar 

  114. Celik EC, Akman Y, Kose P, Arioglu P, Karatas M, Erhan B. Sexual problems of women with spinal cord injury in Turkey. Spinal Cord. 2014;52(4):313–5. doi:10.1038/sc.2013.161.

    Article  CAS  PubMed  Google Scholar 

  115. Hajiaghababaei M, Javidan AN, Saberi H, Khoei EM, Khalifa DA, Koenig HG, et al. Female sexual dysfunction in patients with spinal cord injury: a study from Iran. Spinal Cord. 2014;52(8):646–9. doi:10.1038/sc.2014.99. Prevalence and risk factors associated with sexual function amongst females with spinal cord injury.

    Article  CAS  PubMed  Google Scholar 

  116. Symonds T, Abraham L, Bushmakin AG, Williams K, Martin M, Cappelleri JC. Sexual function questionnaire: further refinement and validation. J Sex Med. 2012;9(10):2609–16. doi:10.1111/j.1743-6109.2011.02627.x.

    Article  PubMed  Google Scholar 

  117. Alexander MS, Rosen RC, Steinberg S, Symonds T, Haughie S, Hultling C. Sildenafil in women with sexual arousal disorder following spinal cord injury. Spinal Cord. 2011;49(2):273–9. doi:10.1038/sc.2010.107.

    Article  CAS  PubMed  Google Scholar 

  118. Laan E, Everaerd W. Physiological measures of vaginal vasocongestion. Int J Impot Res. 1998;10 Suppl 2:S107–10. discussion S24-5.

    PubMed  Google Scholar 

  119. Sipski ML, Rosen RC, Alexander CJ, Hamer RM. Sildenafil effects on sexual and cardiovascular responses in women with spinal cord injury. Urology. 2000;55(6):812–5.

    Article  CAS  PubMed  Google Scholar 

  120. Sipski ML, Rosen RC, Alexander CJ. Physiological parameters associated with the performance of a distracting task and genital self-stimulation in women with complete spinal cord injuries. Arch Phys Med Rehabil. 1996;77(5):419–24.

    Article  CAS  PubMed  Google Scholar 

  121. Sipski ML, Alexander CJ, Gomez-Marin O, Grossbard M, Rosen R. Effects of vibratory stimulation on sexual response in women with spinal cord injury. J Rehabil Res Dev. 2005;42(5):609–16.

    Article  PubMed  Google Scholar 

  122. Alexander MS, Biering-Sorensen F, Elliott S, Kreuter M, Sonksen J. International spinal cord injury female sexual and reproductive function basic data set. Spinal Cord. 2011;49(7):787–90. doi:10.1038/sc.2011.7.

    Article  CAS  PubMed  Google Scholar 

  123. Chung SK, McVary KT, McKenna KE. Sexual reflexes in male and female rats. Neurosci Lett. 1988;94(3):343–8.

    Article  CAS  PubMed  Google Scholar 

  124. Hubscher CH, Johnson RD. Effects of acute and chronic midthoracic spinal cord injury on neural circuits for male sexual function. II. Descending pathways. J Neurophysiol. 2000;83(5):2508–18.

    CAS  PubMed  Google Scholar 

  125. Nout YS, Bresnahan JC, Culp E, Tovar CA, Beattie MS, Schmidt MH. Novel technique for monitoring micturition and sexual function in male rats using telemetry. Am J Physiol Regul Integr Comp Physiol. 2007;292(3):R1359–67. doi:10.1152/ajpregu.00532.2006.

    Article  CAS  PubMed  Google Scholar 

  126. Kozyrev N, Staudt MD, Brown A, Coolen LM. Chronic contusion spinal cord injury impairs ejaculatory reflexes in male rats: partial recovery by systemic infusions of dopamine D3 receptor agonist 7OHDPAT. J Neurotrauma. 2016. doi:10.1089/neu.2015.4232. D3 receptor agonist improves ejaculatory reflexes in male rats with a chronic contusion spinal cord injury.

    PubMed  Google Scholar 

  127. Chao R, Clowers DE. Experience with intracavernosal tri-mixture for the management of neurogenic erectile dysfunction. Arch Phys Med Rehabil. 1994;75(3):276–8.

    Article  CAS  PubMed  Google Scholar 

  128. Soler JM, Previnaire JG, Denys P, Chartier-Kastler E. Phosphodiesterase inhibitors in the treatment of erectile dysfunction in spinal cord-injured men. Spinal Cord. 2007;45(2):169–73. doi:10.1038/sj.sc.3101950.

    Article  CAS  PubMed  Google Scholar 

  129. Giuliano F, Sanchez-Ramos A, Lochner-Ernst D, Del Popolo G, Cruz N, Leriche A, et al. Efficacy and safety of tadalafil in men with erectile dysfunction following spinal cord injury. Arch Neurol. 2007;64(11):1584–92. doi:10.1001/archneur.64.11.nct70001.

    Article  PubMed  Google Scholar 

  130. Giuliano F, Rubio-Aurioles E, Kennelly M, Montorsi F, Kim ED, Finkbeiner AE, et al. Vardenafil improves ejaculation success rates and self-confidence in men with erectile dysfunction due to spinal cord injury. Spine. 2008;33(7):709–15. doi:10.1097/BRS.0b013e3181695040.

    Article  PubMed  Google Scholar 

  131. Lombardi G, Macchiarella A, Cecconi F, Del Popolo G. Efficacy and safety of medium and long-term tadalafil use in spinal cord patients with erectile dysfunction. J Sex Med. 2009;6(2):535–43. doi:10.1111/j.1743-6109.2008.01106.x.

    Article  CAS  PubMed  Google Scholar 

  132. Lombardi G, Macchiarella A, Cecconi F, Del Popolo G. Ten-year follow-up of sildenafil use in spinal cord-injured patients with erectile dysfunction. J Sex Med. 2009;6(12):3449–57. doi:10.1111/j.1743-6109.2009.01426.x.

    Article  PubMed  Google Scholar 

  133. Del Popolo G, Li Marzi V, Mondaini N, Lombardi G. Time/duration effectiveness of sildenafil versus tadalafil in the treatment of erectile dysfunction in male spinal cord-injured patients. Spinal Cord. 2004;42(11):643–8. doi:10.1038/sj.sc.3101617.

    Article  PubMed  Google Scholar 

  134. Zasler ND, Katz PG. Synergist erection system in the management of impotence secondary to spinal cord injury. Arch Phys Med Rehabil. 1989;70(9):712–6.

    CAS  PubMed  Google Scholar 

  135. Denil J, Ohl DA, Smythe C. Vacuum erection device in spinal cord injured men: patient and partner satisfaction. Arch Phys Med Rehabil. 1996;77(8):750–3.

    Article  CAS  PubMed  Google Scholar 

  136. Moemen MN, Fahmy I, AbdelAal M, Kamel I, Mansour M, Arafa MM. Erectile dysfunction in spinal cord-injured men: different treatment options. Int J Impot Res. 2008;20(2):181–7. doi:10.1038/sj.ijir.3901600.

    Article  CAS  PubMed  Google Scholar 

  137. Sonksen J, Biering-Sorensen F, Kristensen JK. Ejaculation induced by penile vibratory stimulation in men with spinal cord injuries. The importance of the vibratory amplitude. Paraplegia. 1994;32(10):651–60. doi:10.1038/sc.1994.105.

    Article  CAS  PubMed  Google Scholar 

  138. Brackett NL, Ibrahim E, Iremashvili V, Aballa TC, Lynne CM. Treatment for ejaculatory dysfunction in men with spinal cord injury: an 18-year single center experience. J Urol. 2010;183(6):2304–8. doi:10.1016/j.juro.2010.02.018.

    Article  PubMed  Google Scholar 

  139. Brackett NL, Kafetsoulis A, Ibrahim E, Aballa TC, Lynne CM. Application of 2 vibrators salvages ejaculatory failures to 1 vibrator during penile vibratory stimulation in men with spinal cord injuries. J Urol. 2007;177(2):660–3. doi:10.1016/j.juro.2006.09.044.

    Article  PubMed  Google Scholar 

  140. Castle SM, Jenkins LC, Ibrahim E, Aballa TC, Lynne CM, Brackett NL. Safety and efficacy of a new device for inducing ejaculation in men with spinal cord injuries. Spinal Cord. 2014;52 Suppl 2:S27–9. doi:10.1038/sc.2014.110. Safety and efficacy of the new Viberect-X3 device for ejaculation in spinal cord injured men.

    Article  PubMed  Google Scholar 

  141. Iwatsubo E, Tanaka M, Takahashi K, Akatsu T. Non-inflatable penile prosthesis for the management of urinary incontinence and sexual disability of patients with spinal cord injury. Paraplegia. 1986;24(5):307–10. doi:10.1038/sc.1986.43.

    Article  CAS  PubMed  Google Scholar 

  142. Zermann DH, Kutzenberger J, Sauerwein D, Schubert J, Loeffler U. Penile prosthetic surgery in neurologically impaired patients: long-term followup. J Urol. 2006;175(3 Pt 1):1041–4. doi:10.1016/S0022-5347(05)00344-7. discussion 4.

    Article  PubMed  Google Scholar 

  143. Deforge D, Blackmer J, Garritty C, Yazdi F, Cronin V, Barrowman N, et al. Male erectile dysfunction following spinal cord injury: a systematic review. Spinal Cord. 2006;44(8):465–73. doi:10.1038/sj.sc.3101880.

    Article  CAS  PubMed  Google Scholar 

  144. Raviv G, Madgar I, Elizur S, Zeilig G, Levron J. Testicular sperm retrieval and intra cytoplasmic sperm injection provide favorable outcome in spinal cord injury patients, failing conservative reproductive treatment. Spinal Cord. 2013;51(8):642–4. doi:10.1038/sc.2013.44. Testicular sperm extraction prognosis for spinal cord injured patients failing electro ejaculation or penile vibratory stimulation.

    Article  CAS  PubMed  Google Scholar 

  145. Overgoor ML, de Jong TP, Cohen-Kettenis PT, Edens MA, Kon M. Increased sexual health after restored genital sensation in male patients with spina bifida or a spinal cord injury: the TOMAX procedure. J Urol. 2013;189(2):626–32. doi:10.1016/j.juro.2012.10.020. Restoration of genital sensation in men with a low spinal lesion.

    Article  CAS  PubMed  Google Scholar 

  146. Leroi AM, Michot F, Grise P, Denis P. Effect of sacral nerve stimulation in patients with fecal and urinary incontinence. Dis Colon Rectum. 2001;44(6):779–89.

    Article  CAS  PubMed  Google Scholar 

  147. Lombardi G, Mondaini N, Giubilei G, Macchiarella A, Lecconi F, Del Popolo G. Sacral neuromodulation for lower urinary tract dysfunction and impact on erectile function. J Sex Med. 2008;5(9):2135–40. doi:10.1111/j.1743-6109.2008.00948.x.

    Article  PubMed  Google Scholar 

  148. van der Aa HE, Alleman E, Nene A, Snoek G. Sacral anterior root stimulation for bladder control: clinical results. Arch Physiol Biochem. 1999;107(3):248–56. doi:10.1076/apab.107.3.248.4330.

    Article  PubMed  Google Scholar 

  149. Lombardi G, Nelli F, Mencarini M, Del Popolo G. Clinical concomitant benefits on pelvic floor dysfunctions after sacral neuromodulation in patients with incomplete spinal cord injury. Spinal Cord. 2011;49(5):629–36. doi:10.1038/sc.2010.176.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomical Sciences and Neurobiology, University of Louisville, 511 S. Floyd Street, Louisville, KY, 40202, USA

    Casey J. Steadman & Charles H. Hubscher

Authors
  1. Casey J. Steadman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Charles H. Hubscher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Charles H. Hubscher.

Ethics declarations

Conflicts of Interest

CJS and CHH declare that they have no conflicts of interest.

Human and Animal Rights and Informed Consent

All reported studies/experiments with human or animal subjects performed by the authors have been previously published and complied with all applicable ethical standards (including the Helsinki Declaration and its amendments, institutional/national research committee standards, and international/national/institutional guidelines).

Additional information

This article is part of the Topical Collection on Preclinical and Psychophysiology

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Steadman, C.J., Hubscher, C.H. Sexual Function after Spinal Cord Injury: Innervation, Assessment, and Treatment. Curr Sex Health Rep 8, 106–115 (2016). https://doi.org/10.1007/s11930-016-0067-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11930-016-0067-0

Keywords

Search

Navigation