Penile erection and micturition events triggered by electrical stimulation of the mesopontine tegmental area

American Journal of Physiology - Regulatory Integrative and Comparative Physiology

Volumn 294, Issue 1, 2008, Pages

  Toledo Salas, Juan Carlos ^a   Iwasaki, Hiroshi ^b   Jodo, Eiichi ^a   Schmidt, Markus H ^c   Kawauchi, Akihiro ^d   Miki, Tsuneharu ^d   Kayama, Yukihiko ^a   Otsuki, Manabu ^e   Koyama, Yoshimasa ^f  

^a FUKUSHIMA MEDICAL UNIVERSITY   (Japan)

^b MINAMI OSAKA GENERAL HOSPITAL   (Japan)

^c Ohio Sleep Medicine and Neuroscience Institute   (United States)

^d KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

^e Otsuki Sleep Clinic   (Japan)

^f FUKUSHIMA UNIVERSITY   (Japan)

Author keywords

Electrical stimulation; Laterodorsal tegmental nucleus; Penile erection

Indexed keywords

ANIMAL EXPERIMENT; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN STEM; CHOLINERGIC ACTIVITY; CONTROLLED STUDY; CORPUS CAVERNOSUM; ELECTROMYOGRAPHY; ELECTROSTIMULATION; MALE; MICTURITION; NONHUMAN; PENILE BLOOD FLOW; PENIS ERECTION; PRIORITY JOURNAL; RAT; REM SLEEP; TEGMENTUM;

ANIMALS; BRAIN STEM; ELECTRIC STIMULATION; ELECTROMYOGRAPHY; HYPOTHALAMUS; MALE; PENILE ERECTION; PONS; PREOPTIC AREA; RATS; RATS, SPRAGUE-DAWLEY; URINATION; VENTRAL TEGMENTAL AREA;

EID: 38149132248     PISSN: 03636119     EISSN: 15221490     Source Type: Journal    
DOI: 10.1152/ajpregu.00226.2007     Document Type: Article

References (65)

1. Adachi H, Sato Y, Kato R, Hisasue S, Suzuki K, Masumori N, Itoh N, Tsukamoto T. Direct evidence of facilitative actions of dopamine in the medial preoptic area on reflexive and noncontact erections in male rats. J Urol 169: 386-389, 2003.
2. Berk ML, Finkelstein JA. Afferent projections to the preoptic area and hypothalamic regions in the rat brain. Neuroscience 6: 1601-1624, 1981.
3. Bernabe J, Rampin O, Sachs BD, Giuliano F. Intracavernous pressure during erection in rats: an integrative approach based on telemetric recording. Am J Physiol Regul Integr Comp Physiol 276: R441-R449, 1999.
4. Bondy CA, Russell JT. Dendrotoxin and 4-aminopyridine potentiate neurohypophysial hormone secretion during low frequency electrical stimulation. Brain Res 453: 397-400, 1988.
5. Burnett AL, Lowenstein CJ, Bredt DS, Chang TS, Snyder SH. Nitric oxide: a physiologic mediator of penile erection. Science 257: 401-403, 1992.
6. Chen KK, Chang LS. Effect of excitatory amino acid receptor agonists on penile erection after administration into paraventricular nucleus of hypothalamus in the rat. Urology 62: 575-580, 2003.
7. Coolen LM. Neural control of ejaculation. J Comp Neurol 493: 39-45, 2005.
8. Demotes-Mainard J, Chauveau J, Rodriguez F, Vincent JD, Poulain DA. Septal release of vasopressin in response to osmotic, hypovolemic and electrical stimulation in rats. Brain Res 381: 314-321, 1986.
9. Dominguez JM, Hull EM. Dopamine, the medial preoptic area, and male sexual behavior. Physiol Behav 86: 356-368, 2005.
10. El Mansari M, Sakai K, Jouvet M. Unitary characteristics of presumptive cholinergic tegmental neurons during the sleep-waking cycle in freely moving cats. Exp Brain Res 76: 519-529, 1989.
11. Giordano M, Guemes M, Lopez-Arias V, Paredes RG. Socio-sexual behavior in male rats after lesions of the dorsolateral tegmentum. Physiol Behav 65: 89-94, 1998.
12. Giuliano F, Bernabe J, Brown K, Droupy S, Benoit G, Rampin O. Erectile response to hypothalamic stimulation in rats: role of peripheral nerves. Am J Physiol Regul Integr Comp Physiol 273: R1990-R1997, 1997.
13. Giuliano F, Rampin O, Brown K, Courtois F, Benoit G, Jardin A. Stimulation of the medial preoptic area of the hypothalamus in the rat elicits increases in intracavernous pressure. Neurosci Lett 209: 1-4, 1996.
14. Gulia KK, Mallick HN, Kumar VM. Sleep-related penile erections do not occur in rats during carbachol-induced rapid eye movement sleep. Behav Brain Res 154: 585-587, 2004.
15. Hansen S, Kohler C, Ross SB. On the role of the dorsal mesencephalic tegmentum in the control of masculine sexual behavior in the rat: effects of electrolytic lesions, ibotenic acid and DSP 4. Brain Res 240: 311-320, 1982.
16. Hart BL, Melese-D'Hospital PY. Penile mechanisms and the role of the striated penile muscles in penile reflexes. Physiol Behav 31: 807-813, 1983.
17. Hawthorn J, Andrews PL, Ang VT, Jenkins JS. Differential release of vasopressin and oxytocin in response to abdominal vagal afferent stimulation or apomorphine in the ferret. Brain Res 438: 193-198, 1988.
18. Hermann DM, Luppi PH, Peyron C, Hinckel P, Jouvet M. Afferent projections to the rat nuclei raphe magnus, raphe pallidus and reticularis gigantocellularis pars alpha demonstrated by iontophoretic application of choleratoxin (subunit b). J Chem Neuroanat 13: 1-21, 1997.
19. Hobson JA. Evolving concepts of sleep cycle regulation: from brain centers to neural populations. Behav Brain Sci 9: 371-448, 1986.
20. Holmes GM, Hermann GE, Rogers RC, Bresnahan JC, Beattie MS. Dissociation of the effects of nucleus raphe obscurus or rostral ventrolateral medulla lesions on eliminatory and sexual reflexes. Physiol Behav 75: 49-55, 2002.
21. Kayama Y, Ohta M, Jodo E. Firing of "possibly" cholinergic neurons in the rat laterodorsal tegmental nucleus during sleep and wakefulness. Brain Res 569: 210-220, 1992.
22. Kita I, Yoshida Y, Nishino S. An activation of parvocellular oxytocinergic neurons in the paraventricular nucleus in oxytocin-induced yawning and penile erection. Neurosci Res 54: 269-275, 2006.
23. Koyama Y, Schmidt M, Iwasaki H, Takahashi K, Kodama T, Kayama Y. Role of the mesopontine tegmental cholinergic neurons on the regulation of penile erection during paradoxical sleep. In: The Paradox of Sleep: an Unfinished Story. An International Meeting in the Honor of Michel Jouvet. Lyon, France: Cephalon, 2003.
24. Kruse MN, Mallory BS, Noto H, Roppolo JR, de Groat WC. Modulation of the spinobulbospinal micturition reflex pathway in cats. Am J Physiol Regul Integr Comp Physiol 262: R478-R484, 1992.
25. 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 17: 5245-5253, 1997.
26. MacLean PD, Denniston RH, Dua S. Further studies on cerebral representation of penile erection: caudal thalamus, midbrain and pons. J Neurophysiol 26: 273-293, 1963.
27. Marson L. Lesions of the periaqueductal gray block the medial preoptic area-induced activation of the urethrogenital reflex in male rats. Neurosci Lett 367: 278-282, 2004.
28. Marson L, Foley KA. Identification of neural pathways involved in genital reflexes in the female: a combined anterograde and retrograde tracing study. Neuroscience 127: 723-736, 2004.
29. Marson L, List MS, McKenna KE. Lesions of the nucleus paragigantocellularis alter ex copula penile reflexes. Brain Res 592: 187-192, 1992.
30. McCarley RW, Greene RW, Rainnie D, Portas CM. Brainstem neuromodulation and REM sleep. Semin Neurosci 7: 341-354, 1995.
31. Melis MR, Argiolas A. Nitric oxide donors induce penile erection and yawning when injected in the central nervous system of male rats. Eur J Pharmacol 294: 1-9, 1995.
32. Melis MR, Argiolas A, Gessa GL. Oxytocin-induced penile erection and yawning: site of action in the brain. Brain Res 398: 259-265, 1986.
33. Melis MR, Argiolas A, Gessa GL. Apomorphine-induced penile erection and yawning: site of action in brain. Brain Res 415: 98-104, 1987.
34. Melis MR, Succu S, Iannucci U, Argiolas A. N-methyl-D-aspartic acid-induced penile erection and yawning: role of hypothalamic paraventricular nitric oxide. Eur J Pharmacol 328: 115-123, 1997.
35. Miyazaki M, Kayama Y, Kihara T, Kawasaki K, Yamaguchi E, Wada Y, Ikeda M. Possible release of nitric oxide from cholinergic axons in the thalamus by stimulation of the rat laterodorsal tegmental nucleus as measured with voltammetry. J Chem Neuroanat 10: 203-207, 1996.
36. Noto H, Roppolo JR, Steers WD, de Groat WC. Excitatory and inhibitory influences on bladder activity elicited by electrical stimulation in the pontine micturition center in the rat. Brain Res 492: 99-115, 1989.
37. 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 292: R1359-R1367, 2007.
38. Nout YS, Schmidt MH, Tovar CA, Culp E, Beattie MS, Bresnahan JC. Telemetric monitoring of corpus spongiosum penis pressure in conscious rats for assessment of micturition and sexual function following spinal cord contusion injury. J Neurotrauma 22: 429-441, 2005.
39. Ohlmeyer P, Brilmayer H, Hullstrung H. Periodische vorgange in schlaf. Pflugers Arch 248: 559-560, 1944.
40. Perachio AA, Marr LD, Alexander M. Sexual behavior in male rhesus monkeys elicited by electrical stimulation of preoptic and hypothalamic areas. Brain Res 177: 127-144, 1979.
41. Rampin O, Monnerie R, Jerome N, McKenna K, Maurin Y. Spinal control of erection by glutamate in rats. Am J Physiol Regul Integr Comp Physiol 286: R710-R718, 2004.
42. Ranson RN, Motawei K, Pyner S, Coote JH. The paraventricular nucleus of the hypothalamus sends efferents to the spinal cord of the rat that closely appose sympathetic preganglionic neurones projecting to the stellate ganglion. Exp Brain Res 120: 164-172, 1998.
43. Rizvi TA, Ennis M, Aston-Jones G, Jiang M, Liu WL, Behbehani MM, Shipley MT. Preoptic projections to Barrington's nucleus and the pericoerulear region: architecture and terminal organization. J Comp Neurol 347: 1-24, 1994.
44. Romero-Carbente JC, Camacho FJ, Paredes RG. The role of the dorsolateral tegmentum in the control of male sexual behavior: a reevaluation. Behav Brain Res 170: 262-270, 2006.
45. Sakai K. Central mechanisms of paradoxical sleep. Exp Brain Res Suppl 8: 3-18, 1984.
46. Sato Y, Christ GJ. Differential ICP responses elicited by electrical stimulation of medial preoptic area. Am J Physiol Heart Circ Physiol 278: H964-H970, 2000.
47. Sato Y, Tsukamoto T. Effects of nitric oxide stimulation on the brain. Drugs Today 36: 83-92, 2000.
48. Schmidt M, Gervasoni D, Luppi P, Fort P. Carbachol administration into the lateral preoptic area induces erections and wakefulness. In: Abstract Volume of the Society for Neuroscience 31st Annual Meeting. Washington, DC: Society for Neuroscience, 2001.
49. Schmidt MH, Valatx JL, Sakai K, Debilly G, Jouvet M. Corpus spongiosum penis pressure and perineal muscle activity during reflexive erections in the rat. Am J Physiol Regul Integr Comp Physiol 269: R904-R913, 1995.
50. Schmidt MH, Valatx JL, Sakai K, Fort P, Jouvet M. Role of the lateral preoptic area in sleep-related erectile mechanisms and sleep generation in the rat. J Neurosci 20: 6640-6647, 2000.
51. Schmidt MH, Valatx JL, Schmidt HS, Wauquier A, Jouvet M. Experimental evidence of penile erections during paradoxical sleep in the rat. Neuroreport 5: 561-564, 1994.
52. Semba K, Reiner PB, Fibiger HC. Single cholinergic mesopontine tegmental neurons project to both the pontine reticular formation and the thalamus in the rat. Neuroscience 38: 643-654, 1990.
53. Shibata H. Ascending projections to the mammillary nuclei in the rat: a study using retrograde and anterograde transport of wheat germ agglutinin conjugated to horseradish peroxidase. J Comp Neurol 264: 205-215, 1987.
54. Simerly RB, Swanson LW. Projections of the medial preoptic nucleus: a Phaseolus vulgaris leucoagglutinin anterograde tract-tracing study in the rat. J Comp Neurol 270: 209-242, 1988.
55. Steriade M, Datta S, Pare D, Oakson G, Curro Dossi RC. Neuronal activities in brain-stem cholinergic nuclei related to tonic activation processes in thalamocortical systems. J Neurosci 10: 2541-2559, 1990.
56. Sugaya K, Ogawa Y, Hatano T, Koyama Y, Miyazato T, Oda M. Evidence for involvement of the subcoeruleus nucleus and nucleus raphe magnus in urine storage and penile erection in decerebrate rats. J Urol 159: 2172-2176, 1998.
57. Takakusaki K, Ohta Y, Mori S. Single medullary reticulospinal neurons exert postsynaptic inhibitory effects via inhibitory interneurons upon alpha-motoneurons innervating cat hindlimb muscles. Exp Brain Res 74: 11-23, 1989.
58. Valentino RJ, Page ME, Luppi PH, Zhu Y, Van Bockstaele E, Aston-Jones G. Evidence for widespread afferents to Barrington's nucleus, a brainstem region rich in corticotropin-releasing hormone neurons. Neuroscience 62: 125-143, 1994.
59. Vignozzi L, Filippi S, Luconi M, Morelli A, Mancina R, Marini M, Vannelli GB, Granchi S, Orlando C, Gelmini S, Ledda F, Forti G, Maggi M. Oxytocin receptor is expressed in the penis and mediates an estrogen-dependent smooth muscle contractility. Endocrinology 145: 1823-1834, 2004.
60. Vincent SR, Satoh K, Armstrong DM, Fibiger HC. NADPH-diaphorase: a selective histochemical marker for the cholinergic neurons of the pontine reticular formation. Neurosci Lett 43: 31-36, 1983.
61. Woolf NJ, Butcher LL. Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16: 603-637, 1986.
62. Yamao Y, Koyama Y, Akihiro K, Yukihiko K, Tsuneharu M. Discrete regions in the laterodorsal tegmental area of the rat regulating the urinary bladder and external urethral sphincter. Brain Res 912: 162-170, 2001.
63. Yoshiyama M, Roppolo JR, De Groat WC. Alteration by urethane of glutamatergic control of micturition. Eur J Pharmacol 264: 417-425, 1994.
64. Yoshiyama M, Roppolo JR, De Groat WC. Interactions between NMDA and AMPA/kainate receptors in the control of micturition in the rat. Eur J Pharmacol 287: 73-78, 1995.
65. Zahran AR, Vachon P, Courtois F, Carrier S. Increases in intracavernous penile pressure following injections of excitatory amino acid receptor agonists in the hypothalamic paraventricular nucleus of anesthetized rats. J Urol 164: 1793-1797, 2000.