Striated perineal muscles: Location of autonomic, sensory, and somatic neurons projecting to the male pig bulbospongiosus muscle

Anatomical Record

Volumn 292, Issue 11, 2009, Pages 1756-1763

  Botti, Maddalena ^a   Ragionieri, Luisa ^a   Gazza, Ferdinando ^a   Acone, Franca ^b   Minelli, Luisa Bo ^a   Panu, Rino ^a  

^a Department of Animal Health   (Italy)

^b UNIVERSITY OF SASSARI   (Italy)

Author keywords

Bulbospongiosus muscle; Fast blue; Male pig; Retrograde neuronal tracer; Striated perineal muscle

Indexed keywords

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTONOMIC NERVOUS SYSTEM; BULBOSPONGIOSUS MUSCLE; CELLULAR DISTRIBUTION; MALE; MORPHOMETRICS; MUSCLE FUNCTION; NERVE PROJECTION; NONHUMAN; PERINEUM; PREFRONTAL CORTEX; PRIORITY JOURNAL; REFLEX ARC; SENSORY NERVE CELL; SENSORY SYSTEM; SOMATIC CELL; SWINE; SYMPATHETIC TRUNK;

AMIDINES; ANIMALS; AUTONOMIC NERVOUS SYSTEM; EJACULATION; FLUORESCENT DYES; FUNCTIONAL LATERALITY; HYPOGASTRIC PLEXUS; LUMBOSACRAL PLEXUS; MALE; MOTOR NEURONS; MUSCLE, SKELETAL; NEUROANATOMICAL TRACT-TRACING TECHNIQUES; NEURONAL TRACT-TRACERS; PENIS; PERINEUM; SENSORY RECEPTOR CELLS; SUS SCROFA;

SUIDAE;

EID: 70449657812     PISSN: 19328486     EISSN: 19328494     Source Type: Journal    
DOI: 10.1002/ar.20962     Document Type: Article

References (95)

1. Baez S. 1973. An open cremaster muscle preparation for the study of blood vessels by in vivo microscopy. Microvasc Res 5:384-394.
2. 2c receptors on spinal neurons controlling penile erection in the rat. Neuroscience 92:1523-1537.
3. Barker D, Saito M. 1981. Autonomic innervation of receptors and muscle fibres in cat skeletal muscle. Proc R Soc Lond B 212:317-332.
4. Berg BR, Cohen KD, Sarelius IH. 1997. Direct coupling between blood flow and metabolism at the capillary level in striated muscle. Am J Physiol 272 (6 Part 2):H2693-H2700. (Pubitemid 127751093)
5. Blok BFM, Roukema G, Geerdes B, Holstege G. 1996. Location of external anal sphincter motoneurons in the sacral cord of the female domestic pig. Neurosci Lett 216:203-206. (Pubitemid 26336569)
6. Bossowska A. 2002. Distribution of primary afferent neurons associated with the porcine inferior mesenteric ganglion (IMG). Folia Histochem Cytobiol 40:367-372. (Pubitemid 35230053)
7. Botti M, Bo Minelli L, Gazza F, Ragionieri L, Acone F, Panu R, Palmieri G. 2006. Sensory, motor somatic, and autonomic neurons projecting to the porcine cremaster muscle. Anat Rec A Discov Mol Cell Evol Biol 288:1050-1058. (Pubitemid 44521959)
8. Bowen JM, Hughes BJ, Bradley WE. 1984. Anatomic, physiologic and pharmacologic properties of the feline bulbospongiosus muscle. Am J Vet Res 45:308-313.
9. Breedlove SM, Arnold AP. 1980. Hormone accumulation in a sexually dimorphic motor nucleus of the rat spinal cord. Science 210:564-566.
10. Breedlove SM, Jordan CL, Arnold AP. 1983. Neurogenesis of motoneurons in the sexually dimorphic spinal nucleus of the bulbocavernosus in rats. Brain Res 9:39-43.
11. Crissinger KD, Burney DL, Velasquez OR, Gonzalez E. 1994. An animal model of necrotizing enterocolitis induced by infant formula and ischemia in developing piglets. Gastroenterology 106:1215-1222. (Pubitemid 24129237)
12. Crowe R, Burnstock G, Light JK. 1989. Adrenergic innervation of the striated muscle of the intrinsic external urethral sphincter from patients with lower motor spinal cord lesion. J Urol 141:47-49. (Pubitemid 19028821)
13. Dail WG. 1996. The pelvic plexus: innervation of pelvic and extrapelvic tissues. Microsc Res Tech 35:95-106.
14. Dekker JJ, Lawrence DG, Kuypers HGJM. 1973. The location of longitudinally running dendrites in the ventral horn of cat spinal cord. Brain Res 51:319-325.
15. Dhami D, Mitchell BS. 1991. Specific patterns of immunoreactivity in neuronal elements of the anterior major pelvic ganglion of the male guinea-pig. J Anat 176:197-210.
16. Dodds WJ. 1982. The pig model for biomedical research. Fed Proc 41:247-256.
17. El-Badawi A, Shenk EA. 1974. A new theory of the innervation of bladder musculature. Part 4: Innervation of the vesicourethral junction and external urethral sphincter. J Urol 111:613-615.
18. Fleming BP, Barron KW, Howes TW, Smith JK. 1987. Response of the microcirculation in rat cremaster muscle to peripheral and central sympathetic stimulation. Circ Res 61 (Suppl II):II26-II31.
19. Fleming BP, Gibbins IL, Morris JL, Gannon BJ. 1989. Noradrenergic and peptidergic innervation of the extrinsic vessels and microcirculation of the rat cremaster muscle. Microvasc Res 38:255-268.
20. Franken RJPM, Peter F-W, Anderson GL, Wang WZ, Werker PMN, Schuschke DA, Kon M, Barker JH. 1996. Anatomy of the feeding blood vessels of the cremaster muscle in the rat. Microsurgery 17:402-408. (Pubitemid 28006294)
21. Gazza F, Botti M, Ragionieri L, Bo Minelli L, Acone F, Panu R. 2005. Peripheral sympathetic and sensory neurons projecting to a skeletal muscle of the pig hindlimb. Ital J Anat Embryol 110:138.
22. Getty R. 1982. Anatomia degli Animali Domestici di Sisson e Grossman, Vol.2. Padova: Piccin Ed.
23. Gorczynski RJ, Klitzman B, Duling BR. 1978 Interrelations between contracting striated muscle and precapillary microvessels. Am J Physiol Heart Circ Physiol 235:H494-H504. (Pubitemid 9256831)
24. Grant RT. 1966. The effects of denervation on skeletal muscle blood vessels (rat cremaster). J Anat 100:305-316.
25. Grasby DJ, Gibbins IL, Morris JL. 1997. Projections of sympathetic non-noradrenergic neurons to skeletal muscle arteries in guinea-pig limbs vary with the metabolic character of muscles. J Vasc Res 34:351-364.
26. Heym C, Lang R. 1986. Transmitters in sympathetic postganglionic neurons. In: Panula P, Paivarinta H, Soinila S, editors. Neurochemistry: modern methods and applications. New York: Alan Liss. p 493-525.
27. Holstege G. 2005. Central nervous system control of ejaculation. World J Urol 23:109-114. (Pubitemid 41051500)
28. Holstege G, Tan J. 1987. Supraspinal control of motoneurons innervating the striated muscles of the pelvic floor including urethral and anal sphincters in the cat. Brain 110:1323-1344. (Pubitemid 17168006)
29. Hsu G-L, Hsieh C-H, Wen H-S, Hsu W-L, Wu C-H, Fong T-H, Chen S-C, Tseng G-F. 2004. Anatomy of the human penis: the relationship of the architecture between skeletal and smooth muscles. J Androl 3:426-431.
30. Jen PYP, Dixon JS, Gosling JA. 1997. Co-localization of nitric oxide synthase, neuropeptides and tyrosine hydrosylase in nerves supplying the human post-natal vas deferens and seminal vesicle. Br J Urol 80:291-299. (Pubitemid 28318899)
31. Kaleczyc J. 1997. Neurons of the pelvic plexus of the male pig: distribution and immunohistochemical characterisation with special emphasis on neurons supplying the vas deferens. Acta Acad Agric Tech Olst Vet 24 (A):1-70.
32. Kaleczyc J. 1998. Origin and neurochemical characteristics of nerve fibres supplying the mammalian vas deferens. Microsc Res Tech 42:409-422. (Pubitemid 28476226)
33. Kaleczyc J, Scheuermann DW, Pidsudko Z, Majewski M, Lakomy M, Timmermans J-P. 2002. Distribution, immunohistochemical characteristics and nerve pathways of primary sensory neurons supplying the porcine vas deferens. Cell Tissue Res 310:9-17.
34. Kaleczyc J, Timmermans J-P, Majewski M, Lakomy M, Scheuermann DW. 1995. Distribution and immunohistochemical characteristics of neurons in the porcine caudal mesenteric ganglion projecting to the vas deferens and seminal vesicle. Cell Tissue Res 282:59-68.
35. Kaleczyc J, Timmermans J-P, Majewski M, Lakomy M, Scheuermann W. 1999. Immunohistochemical properties of nerve fibres supplying the accessory male genital glands in the pig. A colocalisation study. Histochem Cell Biol 111:217-228. (Pubitemid 29148245)
36. Katagiri T, Gibson SJ, Su HC, Polak JM. 1986. Composition and central projections of the pudendal nerve in the rat investigated by combined peptide immunocytochemistry and retrograde fluorescent labelling. Brain Res 372:313-322. (Pubitemid 16023392)
37. Keast JR. 1991. Patterns of co-existence of peptides and differences of nerve fibre types associated with noradrenergic and non-noradrenergic (putative cholinergic) neurons in the major pelvic ganglion of the male rat. Cell Tissue Res 266:405-415.
38. Keast JR. 1995. Visualization and immunohistochemical characterization of sympathetic and parasympathetic neurons in the male rat major pelvic ganglion. Neuroscience 66:655-662.
39. Keast JR. 1999. Unusual autonomic ganglia: connections, chemistry, and plasticity of pelvic ganglia. Int Rev Cytol 193:1-69. Review.
40. Kepper M, Keast J. 1995. Immunohistochemical properties and spinal connections of pelvic autonomic neurons that innervate the rat prostate gland. Cell Tissue Res 281:533-542.
41. Kiernan JA, Hudson AJ. 1993. Changes in shape of surviving motor neurons in amyotrophic lateral sclerosis. Brain 116:203-215. (Pubitemid 23087043)
42. Kolbeck SC, Steers WD. 1993. Origin of neurons supplying the vas deferens of the rat. J Urol 149:918-921. (Pubitemid 23111112)
43. Konishi A, Sato M, Mizuno N, Itoh K, Nomura S, Sugimoto T. 1978. An electron microscope study of the area of the Onuf's nucleus in the cat. Brain Res 156:333-338. (Pubitemid 9134492)
44. Kuba K, Tomita T. 1971. Noradrenaline action on nerve terminal in the rat diaphragm. J Physiol (Lond) 217:19-31.
45. Kurjiaka DT. 2004. The conduction of dilation along an arteriole is diminished in the cremaster muscle of hypertensive hamsters. J Vasc Res 41:517-524.
46. Kurz EM, Bowers CA, Sengelaub DR. 1990. Morphology of rat spinal motoneurons with normal and hormonally altered specificity. J Comp Neurol 292:638-650. (Pubitemid 20076643)
47. Kuzuhara S, Kanazawa I, Nakanishi T. 1980. Topographical localization of the Onuf's nucleus neurons innervating the rectal and vesical striated sphincter muscles: a retrograde fluorescent double labelling in cat and dog. Neurosci Lett 16:125-130. (Pubitemid 10097432)
48. Majewski M. 1999. Synaptogenesis and structure of the autonomic ganglia. Folia Morphol (Warsz) 58 (3 Suppl 2):65-99. Review.
49. Majewski M, Heym C. 1991. The origin of ovarian neuropeptide Y (NPY)-immunoreactive nerve fibres from the inferior mesenteric ganglion in the pig. Cell Tissue Res 266:591-596.
50. Majewski M, Heym C. 1992. Immunohistochemical localization of calcitonine gene-related peptide and cotransmitters in a subpopulation of postganglionic neurons in the porcine inferior mesenteric ganglion. Acta Histochem 92:138-146.
51. Majewski M, Kaleczyc J, Mayer B, Schemann M, Weihe E, Lakomy M. 1999. Innervation of the fibro-elastic type of the penis: an immunohistochemical study in the male pig. Acta Histochem 101:71-101. (Pubitemid 29119932)
52. Mannen T, Iwata M, Toyokura Y, Nagashima K. 1978. Notes on a certain motoneuron group of the sacral cord in ALS and the Shy-Drager syndrome. In: Tsubaki T, Toyokura Y, editors. Proceeding of the International Symposium on ALS. Tokyo. pp 201-207.
53. Mannen T, Iwata M, Toyokura Y, Nagashima K. 1982. The Onuf 's nucleus and the external anal sphincter in amyotrophic lateral sclerosis and Shy-Drager syndrome. Acta Neuropathol 58:255-260. (Pubitemid 13217378)
54. Marshall JM, Tandon HC. 1984. Direct observations of muscle arterioles and venules following contraction of skeletal muscle fibres in the rat. J Physiol 350:447-459.
55. Marson L, Carson CC, III. 1999. Central nervous system innervation of the penis, prostate, and perineal muscles: a transneuronal tracing study. Mol Urol 3:43-50.
56. Marson L, McKenna KE. 1996. CNS cell groups involved in the control of the ischiocavernosus and bulbospongiosus muscles: a transneuronal tracing study using psudorabies virus. J Comp Neurol 374:161-179. (Pubitemid 26357183)
57. Martin WD, Fletcher TF, BradleyWE. 1974. Innervation of feline perineal musculature. Anat Rec 180:15-30.
58. Mc Kenna KE, Nadelhaft I. 1986. The organization of the pudendal nerve in the male and female rat. J Comp Neurol 248:532-549. (Pubitemid 16073029)
59. Mc Kenna KE, Chung SK, McVary KT. 1991. A model for the study of sexual function in anaesthetized male and female rats. Am J Physiol 261:R1276-R1285.
60. McLachlan EM, Jänig W. 1983. The cell bodies of origin of sympathetic and sensory axons in some skin and muscle nerves of the cat hindlimb. J Comp Neurol 214:115-130. (Pubitemid 13162958)
61. Merighi A, Kar S, Gibson SJ, Ghidella S, Gobetto A, Peirone SM, Polak JM. 1990. The immunocytochemical distribution of seven peptides in the spinal cord and dorsal root ganglia of horse and pig. Anat Embryol 181:271-280. (Pubitemid 20153528)
62. Nakagawa S. 1980. Onuf's nucleus of the sacral cord in a south American monkey (Saimiri): its location and bilateral cortical input from area 4. Brain Res 191:337-344. (Pubitemid 10103910)
63. Newton BW, Romagnano MAA, Hamill RW. 1989. The ontogeny of substance P- and serotonin-like immunoreactivities in the sexually dimorphic cremaster nucleus of the rat spinal cord. Dev Brain Res 47:227-242.
64. Nickel R, Schummer A, Seiferle E. 1988. Trattato di anatomia degli animali domestici. Vol.IV, Milano: Casa editrice Ambrosiana.
65. Panu R, Bo Minelli L, Botti M, Gazza F, Acone F, Palmieri G. 2001. Peripheral ganglia supplying the genital smooth musculature in the female pig: an experimental study. J Anat 199:317-322. (Pubitemid 32827344)
66. Panu R, Bo Minelli L, Botti M, Gazza F, Acone F, Ragionieri L, Palmieri G. 2003. Localization of neurons projecting into the extrinsic penile smooth musculature of the pig: an experimental study on the retractor penis muscle. Anat Rec Part A 275:1102-1108.
67. Papka RE, Thompson BD, Schmidt HHHW. 1996. Identification of uterine-related sympathetic neurons in the rat inferior mesenteric ganglion: neurotransmitter content and afferent input. J Auton Nerv Syst 59:51-59.
68. Peshori KR, Erichsen JT, Collins III WF. 1995. Differences in the connectivity of the rat pudendal motor nuclei as revealed by retrograde transneuronal transport of wheat germ agglutinin. J Comp Neurol 353:119-128.
69. Roppolo JR, Nadelhaft I, de Groat WC. 1985. The organization of pudendal motoneurons and primary afferent projections in the spinal cord of the Rhesus monkey revealed by Horseradish Peroxidase. J Comp Neurol 234:475-488. (Pubitemid 15080932)
70. Sachs BD. 1982. Role of striated penile muscles in penile reflexes, copulation, and induction of pregnancy in the rat. J Reprod Fertil 66:433-443.
71. Saito M, Sone R, Ikeda M, Mano T. 1997. Sympathetic outflow to the skeletal muscle in humans increases during prolonged light exercise. J Appl Physiol 82:1237-1243. (Pubitemid 27172326)
72. Sato M, Mizuno N, Konishi A. 1978. Localization of motoneurons innervating perineal muscles: a HRP study in cat. Brain Res 140:149-154. (Pubitemid 8248396)
73. Schaller O. 1992. Illustrated veterinary anatomical nomenclature. Stuttgart Enke Iverlag. p 224.
74. Schrøder HD. 1980. Organization of the motoneurons innervating the pelvic muscles of the male rat. J Comp Neurol 192:567-587.
75. Schrøder HD. 1981 Onuf nucleus X: a morphological study of a human spinal nucleus. Anat Embryol 162:443-453. (Pubitemid 11060020)
76. Simmons MA. 1985 The complexity and diversity of synaptic transmission in the prevertebral sympathetic ganglia. Prog Neurobiol 24:43-93. (Pubitemid 15029506)
77. Sjöstrand NO. 1965. The adrenergic innervation of the vas deferens and the accessory male genital glands. Acta Physiol Scand 65:1-82.
78. Smolen AJ, Wright LL, Cunningham TJ. 1983. Neuron numbers in the superior cervical sympathetic ganglion of the rat: a critical comparison of methods for cell counting. J Neurocytol 12:739-750.
79. Sweeney TE, Sarelius IH. 1989. Arteriolar control of capillary cell flow in striated muscle. Circ Res 64:112-120.
80. Swindle MM, Moody DC, Philips LD. 1992. Swine as models in biomedical research. Ames: Iowa State University Press. pp 1-312.
81. Tang Y, Rampin O, Giuliano F, Ugolini G. 1999. Spinal and brain circuits to motoneurons of the bulbospongiosus muscle: retrograde transneuronal tracing with rabies virus. J Comp Neurol 414:167-192. (Pubitemid 29489901)
82. Thomas GD, Segal SS. 2004. Neural control of muscle blood flow during exercise. J Appl Physiol 97:731-738. (Pubitemid 38963148)
83. Thor KB, Morgan C, Nadelhaft I, Houston M, de Groat WC. 1989. Organization of afferent and efferent pathways in the pudendal nerve of the female cat. J Comp Neurol 288:263-279. (Pubitemid 19248757)
84. Timmermans J-P, Barbiers M, Scheuermann DW, Stach W, Adriaensen D, Mayer B, De Groodt-Lasseel MHA. 1993. Distribution pattern, neurochemical features and projections of nitrergic neurons in the pig small intestine. Ann Anat 176:515-525.
85. Ueyama T, Nomura S, Konishi A, Itoh K, Arakawa H. 1984. Central distribution of afferent and efferent components of the pudendal nerve in cat. J Comp Neurol 222:38-46. (Pubitemid 14180600)
86. Ulibarri C, Popper P, Micevych P. 1995. Motoneurons dorsolateral to the central canal innervate perineal muscles in the Mongolian gerbil. J Comp Neurol 356:225-237.
87. VanTeeffelen JWGE, Segal SS. 2003. Interaction between sympathetic nerve activation and muscle fibre contraction in resistance vessels of hamster retractor muscle. J Physiol 550:563-574.
88. Vercelli A, Cracco C. 1990. Effects of prepubertal castration on the spinal motor nucleus of the ischiocavernosus muscle of the rat. Cell Tissue Res 262:551-557.
89. Veronneau-Longueville F, Rampin O, Freund-Mercier M-J, Tang Y, Calas A, Marson L, McKenna KE, Stoeckel M-E, Benoit G, Giuliano F. 1999. Oxytocinergic innervation of autonomic nuclei controlling penile erection in the rat. Neuroscience 93:1437-1447. (Pubitemid 29397573)
90. Wasowicz K, Majewski M, Lakomy M. 1998. Distribution of neurons innervating the uterus of the pig. J Auton Nerv Syst 74:13-22. (Pubitemid 28517853)
91. Watanabe H, Yamamoto TY. 1978. Autonomic innervation of the muscles in the wall of the bladder and proximal urethra of male rats. J Anat 128:873-886. (Pubitemid 9208017)
92. Xu C, Giuliano F, Yaici ED, Conrath M, Trassard O, Benoit G, Vergè D. 2006. Identification of lumbar spinal neurons controlling simultaneously the prostate and the bulbospongiosus muscles in the rat. Neuroscience 138:561-573. (Pubitemid 43255565)
93. Xu C, Yaici ED, Conrath M, Blanchard P, Leclerc P, Benoit G, Vergè D, Giuliano F. 2005. Galanin and neurokinin-1 receptor immunoreactivity spinal neurons controlling the prostate and the bulbospongiosus muscle identified by transsynaptic labeling in the rat. Neuroscience 134:1325-1341. (Pubitemid 41207381)
94. Yamamoto T, Satomi H, Ise H, Takatama H, Takahashi K. 1978. Sacral spinal innervation of the rectal and vesical smooth muscles and the sphincteric striated muscles as demonstrated by the horseradish peroxidase method. Neurosci Lett 7:41-47. (Pubitemid 8265141)
95. Yucel S, Baskin LS. 2003. Neuroanatomy of the male uretra and perineum. BJU Int 92:624-630.