Skip to main content
Log in

Central distribution of efferent and afferent components of the pudendal nerve in rat

  • Original Articles
  • Published:
Anatomy and Embryology Aims and scope Submit manuscript

Summary

Central distribution of efferent and afferent components of the pudendal nerve was examined in the rat by the horseradish peroxidase (HRP) method after HRP application to the central cut end of the pudendal nerve. The pudendal motoneurons were located in the dorsolateral, dorsomedial and lateral groups at L5 and L6. Each of the dorsolateral and dorsomedial groups constituted a slender longitudinal cell column. Pudendal motoneurons in the lateral group were scattered at L5, rostrodorsally to the dorsolateral group. The neurons in the dorsolateral and lateral groups were labelled with HRP applied to the nerve branch innervating the ischiocavernosus and sphincter urethrae muscles. The neurons in the dorsomedial group were labelled with HRP applied to the branch supplying the sphincter ani externus and bulbospongiosus muscles. Some dendrites of pudendal motoneurons in the dorsomedial group extended to the contralateral dorsomedial group. These crossing dendrites were observed not only in male rats but also in female. The average number of the pudendal motoneurons in the dorsolateral and dorsomedial groups were larger in male rats than in female. A few neurons of the intermediolateral nucleus at upper L6 were also labelled with HRP applied to the dorsalis penis (clitoridis) nerve. Axon terminals of the pudendal nerve were distributed, bilaterally with an ipsilateral predominance, to the gracile nucleus, as well as to the dorsal horn and dorsal commissural gray from L4 to S2. A few labelled axons were seen in the intermediolateral nucleus at L6 and S1. Axon terminals from the dorsalis penis nerve were distributed more medially in the dorsal horn than those from the perinealis nerve.

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

Access this article

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

  • Abercrombie M (1946) Estimation of nuclear population from microtome sections. Anat Rec 94:239–247

    Google Scholar 

  • Breedlove SM, Arnold AP (1980) Hormone accumulation in a sexually dimorphic motor nucleus in the rat spinal cord. Science 210:564–566

    Google Scholar 

  • Breedlove SM, Arnold AP (1981) Sexually dimorphic motor nucleus in the rat lumbar spinal cord: response to adult hormone manipulation, absence in androgen-insensitive rats. Brain Res 225:297–307

    Google Scholar 

  • Breedlove SM, Arnold AP (1983) Sex differences in the pattern of steroid accumulation by motoneurons of the rat lumbar spinal cord. J Comp Neurol 215:211–216

    Google Scholar 

  • Breedlove SM, Jacobson CD, Gorski RA, Arnold AP (1982) Masculinization of the female rat spinal cord following a single neonatal injection of testosterone propionate but not estradiol benzoate. Brain Res 237:173–181

    Google Scholar 

  • Breedlove SM, Jordan CL, Arnold AP (1983) Neurogenesis of motoneurons in the sexually dimorphic spinal nucleus of the bulbocavernosus in the rats. Develop Brain Res 9:39–43

    Google Scholar 

  • Brown PB, Fuchs JL (1975) Somatotopic representation of hindlimb skin in cat dorsal horn. J Neurophysiol 38:1–9

    Google Scholar 

  • Cervero F, Connell L (1984) Distribution of somatic and visceral primary afferent fibers within the thoracic spinal cord of the cat. J Comp Neurol 230:88–93

    Google Scholar 

  • Ciriello J, Calaresu FR (1983) Central projections of afferent renal fibers in the rat: an anterograde transport study of horseradish peroxidase. J Auton Nerv Syst 8:273–285

    Google Scholar 

  • Charlton CG, Helke CJ (1985) Autoradiographic localization and characterization of spinal cord substance P binding sites: high densities in sensory, autonomic, phrenic, and Onuf's motor nucler. J Neurosci 5:1653–1661

    Google Scholar 

  • Culberson JL, Brown PB (1984) Projections of hindlimb dorsal roots to lumbosacral spinal cord of cat. J Neurophysiol 51:516–528

    Google Scholar 

  • Culberson JL, Haines DE, Kimmel KL, Brown PB (1979) Contralateral projections of primary afferent fibers to mammalian spinal cord. Exp Neurol 64:83–97

    Google Scholar 

  • De Araujo CG, Schmidt RA, Tanaglio EA (1982) Neural pathways to lower urinary tract identified by retrograde axonal transport of horseradish peroxidase. Urology 19:290–295

    Google Scholar 

  • DeGroat WC, Booth AM (1980) Physiology of the urinary bladder and urethra. Ann Intern Med 92:312–315

    Google Scholar 

  • DeGroat WC, Nadelhaft I, Milne RJ, Booth AM, Morgan C, Thor K (1981) Organization of the sacral parasympathetic reflex pathways to the urinary bladder and large intestine. J Auton Nerv Syst 3:135–160

    Google Scholar 

  • DeGroat WC, Kawatani M, Hisamitsu T, Lowe I, Morgan C, Roppolo J, Booth AM, Nadelhaft I, Kuo D, Thor K (1983) The role of neuropeptides in the sacral autonomic reflex pathways of the cat. J Auton Nerv Syst 7:339–350

    Google Scholar 

  • Dray A, Nunan L (1985) Opioid inhibition of reflex urinary bladder contractions: dissociation of supraspinal and spinal mechanisms. Brain Res 337:142–145

    Google Scholar 

  • Fishman RB, Breedlove SM (1985) The androgenic induction of spinal sexual dimorphism is independent of supraspinal afferents. Dev Brain Res 23:255–258

    Google Scholar 

  • Gibson SJ, Polak JM, Bloom SR, Wall PD (1981) The distribution of nine peptides in the rat spinal cord with special emphasis on the substantia gelatinosa and on the area around the central canal (lamina X). J Comp Neurol 201:65–79

    Google Scholar 

  • Gibson SJ, Polak JM, Allen JM, Adrian TE, Kelly JS, Bloom SR (1984) The distribution and origin of a novel brain peptide, neuropeptide Y, in the spinal cord of several mammals. J Comp Neurol 227:78–91

    Google Scholar 

  • Glazer EJ, Basbaum AI (1980) Leucine enkephalin: localization in and axoplasmic transport by sacral parasympathetic preganglionic neurons. Science 208:1479–1481

    Google Scholar 

  • Glazer EJ, Basbaum AI (1981) Immunohistochemical localization of leucine-enkephalin in the spinal cord of the cat: enkephalin-containing marginal neurons and pain modulation. J Comp Neurol 196:377–389

    Google Scholar 

  • Grant G, Ygge J (1981) Somatotopic organization of the thoracic spinal nerve in the dorsal horn demonstrated with transganglionic degeneration. J Comp Neurol 202:357–364

    Google Scholar 

  • Hayes KJ (1965) The so-called “levator ani” of the rat. Acta Endocrinol (Copenh) 48:337–347

    Google Scholar 

  • Honda CN, Lee CL (1985) Immunohistochemistry of synaptic input and functional characterization of neurons near the spinal central canal. Brain Res 343:120–128

    Google Scholar 

  • Hulsebosch CE, Coggeshall RE (1982) An analysis of the axon populations in the nerves to the pelvic viscera in the rat. J Comp Neurol 211:1–10

    Google Scholar 

  • Hunt SP, Emson PC, Gilbert R, Goldstein M, Kimmel JR (1981) Presence of avian pancreatic polypeptide-like immunoreactivity in catecholamine and methionine-enkaphalin-containing neurones within the central nervous system. Neurosci Lett 21:125–130

    Google Scholar 

  • Jordan CL, Breedlove SM, Arnold AP (1982) Sexual dimorphism and the influence of neonatal androgen in the dorsolateral motor nucleus of the rat lumbar spinal cord. Brain Res 249:309–314

    Google Scholar 

  • Jubelin B, Galeano C, Ladouceur D, Lemaire S, Elhilali MM (1984) Effect of enkephalin on the micturition cycle of the cat. Life Sci 34:2015–2027

    Google Scholar 

  • Katagiri T, Gibson SJ, Su HC, Polak JM (1986) Composition and central projections of the pudendal nerve in the rat investigated by combined peptide immunohistochemistry and retrograde flurorescent labelling. Brain Res 372:313–322

    Google Scholar 

  • Koeber HR, Brown PB (1980) Projections of two hindlimb cutaneous nerves to cat dorsal horn. J Neurophysiol 44:259–269

    Google Scholar 

  • Konishi A, Sato M, Mizuno N, Itoh K, Nomura S, Sugimoto T (1978) An electron microscope study of the areas of the Onuf's nucleus in the cat. Brain Res 156:333–338

    Google Scholar 

  • Konishi A, Itoh K, Sugimoto T, Yasui Y, Kaneko T, Takada M, Mizuno N (1985) Leucine-enkephalin-like immunoreactive afferent fibers to pudendal motoneurons in the cat. Neurosci Lett 61:109–113

    Google Scholar 

  • Kuo DC, DeGroat WC (1985) Primary afferent projections of the major splanchnic nerve to the spinal cord and gracile nucleus of the cat. J Comp Neurol 231:421–434

    Google Scholar 

  • Kuo DC, Nadelhaft I, Hisamitsu T, DeGroat WC (1983) Segmental distribution and central projections of renal afferent fibers in the cat studied by transganglionic transport of horseradish peroxidase. J Comp Neurol 216:162–174

    Google Scholar 

  • Kuo DC, Oravitz JJ, DeGroat WC (1984) Tracing of afferent and efferent pathways in the left inferior cardiac nerve of the cat using retrograde and transganglionic transport of horseradish peroxidase. Brain Res 321:111–118

    Google Scholar 

  • Kuru M (1965) Nervous control of micturition. Physiol Rev 45:425–494

    Google Scholar 

  • Kuzuhara S, Kanazawa I, Nakanishi T (1980) Topographical localization of the Onuf's nucleus innervating the rectal and vesical striated sphincter muscles: a retrograde fluorescent double labelling in cat and dog. Neurosci Lett 16:125–130

    Google Scholar 

  • Light AR, Perl ER (1979a) Reexamination of the dorsal root projection to the spinal dorsal horn including observations on the differential termination of coarse and fine fibers. J Comp Neurol 186:117–132

    Google Scholar 

  • Light AR, Perl ER (1979b) Spinal termination of functionally identified primary afferent neurons with slowly conducting myelinated fibers. J Comp Neurol 186:133–150

    Google Scholar 

  • Mannen T, Iwata M, Toyokura Y, Nagashima K (1977) Preservation of a certain motoneurone group of the sacral cord in amyotrophic lateral sclerosis: its clinical significance. J Neurol Neurosurg Psychiatr 40:464–469

    Google Scholar 

  • Mannen T, Iwata M, Toyokura Y, Nagashima K (1982) The Onuf's nucleus and the external anal sphincter muscles in amyotrophic lateral sclerosis and Shy-Drager syndrome. Acta Neuropathol (Berl) 58:255–260

    Google Scholar 

  • Matsushita M, Tanami T (1983) Contralateral termination of primary afferent axons in the sacral and caudal segments of the cat, as studied by anterograde transport of horseradish peroxidase. J Comp Neurol 220:206–218

    Google Scholar 

  • Mawe GM, Bresnahan JC, Beattie MS (1986) A light and electron microscopic analysis of the sacral parasympathetic nucleus after labelling primary afferent and efferent elements with HRP. J Comp Neurol 250:33–57

    Google Scholar 

  • McKenna KE, Nedelhaft I (1986) The organization of the pudendal nerve in the male and female rat. J Comp Neurol 248:532–549

    Google Scholar 

  • Mesulam M-M (1978) Tetramethyl benzidine for horseradish peroxidase neurohistochemistry: a non-carcinogenic blue reaction-product with superior sensitivity for visualizing neural afferents and efferents. J Histochem Cytochem 26:106–117

    Google Scholar 

  • Micevych PE, Coquelin A, Arnold AP (1986) Immunohistochemical distribution of substance P, serotonin, and methionine enkephalin in sexually dimorphic nuclei of the rat lumbar spinal cord. J Comp Neurol 248:235–244

    Google Scholar 

  • Morgan C, Nadelhaft I, DeGroat WC (1981) The distribution of visceral primary afferents from the pelvic nerve to Lissauer's tract and the spinal gray matter and its relationship to the sacral parasympathetic nucleus. J Comp Neurol 201:415–440

    Google Scholar 

  • Morgan C, DeGroat WC, Nadelhaft I (1986) The spinal distribution of sympathetic preganglionic and visceral primary afferent neurons that send axons into the hypogastric nerves of the cat. J Comp Neurol 243:23–40

    Google Scholar 

  • Nadelhaft I, Booth AM (1984) 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 226:238–245

    Google Scholar 

  • Nadelhaft I, Roppolo J, Morgan C, DeGroat WC (1983) Parasympathetic preganglionic neurons and visceral primary afferents in monkey spinal cord revealed following application of horseradish peroxidase to pelvic nerve. J Comp Neurol 216:36–52

    Google Scholar 

  • Nagashima T, Beppu H, Uono M, Yamada H (1979) Demonstration of neuronal localization in Onufrowicz's group-X in rabbit by double labelling method. Acta Histochem Cytochem (Japan) 12:409–415

    Google Scholar 

  • Nahin RL, Madsen AM, Giesler GJ Jr (1983) Anatomical and physiological studies of the gray matter surrounding the spinal cord central canal. J Comp Neurol 220:321–335

    Google Scholar 

  • 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

    Google Scholar 

  • Neuhuber W (1982) 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 164:413–425

    Google Scholar 

  • Neuhuber WL, Sandoz PA, Fryscak T (1986) The central projections of primary afferent neurons of greater splanchnic and intercostal nerves in the rat. A horseradish peroxidase study. Anat Embryol 174:123–144

    Google Scholar 

  • Núnez R, Gross GH, Sachs BD (1986) Origin and central projections of rat dorsal penile nerve: possible direct projection to autonomic and somatic neurons by primary afferents of nonmuscle origin. J Comp Neurol 247:417–429

    Google Scholar 

  • Onuf (Onufrowicz) B (1899) Notes on the arrangement and function of the cell groups in the sacral region of the spinal cord. J Nerv Ment Dis 26:498–504

    Google Scholar 

  • Onuf (Onufrowicz) B (1900) On the arrangement and function of the cell groups of the sacral region of the spinal cord in man. Arch Neurol Psychopathol 3:387–412

    Google Scholar 

  • Petras JM, Cummings JF (1978) Sympathetic and parasympathetic innervation of the urinary bladder and urethra. Brain Res 153:363–369

    Google Scholar 

  • Pomeranz B, Wall PD, Weber WV (1968) Cord cells responding to fine myelinated afferents from viscera, muscle and skin. J Physiol (Lond) 199:511–532

    Google Scholar 

  • Réthelyi M, Trevino DL, Perl ER (1979) Distribution of primary afferent fibers within the sacrococcygeal dorsal horn: an autoradiographic study. J Comp Neurol 185:603–622

    Google Scholar 

  • Romagnano MA, Hamill RW (1985) Spinal parasympathetic enkephalin fibers: patterns and projections. Brain Res 335:174–181

    Google Scholar 

  • Roppolo JR, Nadelhaft I, DeGroat 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 234:475–388

    Google Scholar 

  • Rose RD, Collins WF III (1985) Crossing dendrites may be a substrate for synchronized activation of penile motoneurons. Brain Res 337:373–377

    Google Scholar 

  • Sasek CA, Elde RP (1985) Distribution of neuropeptide Y-like immunoreactivity and its relationship to FMRF-amide-like immunoreactivity in the sixth lumbar and first sacral spinal cord segments of the rat. J Neurosci 5:1729–1739

    Google Scholar 

  • Sasek CA, Elde RP (1986) Coexistence of enkephalin and dynorphin immunoreactivities in neurons in the dorsal gray commissure of the sixth lumbar and first sacral cord segments in rat. Brain Res 381:8–14

    Google Scholar 

  • Sasek CA, Seybold JS, Elde RP (1984) The immunohistochemical localisation of nine peptides in the sacral parasympathetic nucleus and the dorsal grey commissure in rat spinal cord. Neuroscience 12:855–873

    Google Scholar 

  • Sato M, Mizuno N, Konishi A (1978) Localization of motoneurons innervating perineal muscles: a HRP study in cat. Brain Res 140:149–154

    Google Scholar 

  • Schrøder HD (1980) Organization of the motoneurons innervating the pelvic muscles of the male rat. J Comp Neurol 192:567–587

    Google Scholar 

  • Schrøder HD (1981) Onuf's nucleus X: a morphological study of a human spinal nucleus. Anat Embryol 162:443–453

    Google Scholar 

  • Schrøder HD (1984) Somatostatin in the caudal spinal cord: an immunohistochemical study of the spinal centers involved in the innervation of pelvic organs. J Comp Neurol 223:400–414

    Google Scholar 

  • Schrøder HD (1985) Anatomical and pathoanatomical studies on the spinal efferent systems innervating pelvic structures. 1. Organization of spinal nuclei in animals. 2. The nucleus X-pelvic motor system in man. J Auton Nerv Syst 14:23–48

    Google Scholar 

  • Senegelaub DR, Arnold AP (1986) Development and loss of early projections in a sexually dimorphic rat spinal nucleus. J Neurosci 6:1613–1620

    Google Scholar 

  • Smith CL (1983) The development and post-natal organization of primary afferent projections to the rat thoracic spinal cord. J Comp Neurol 220:29–43

    Google Scholar 

  • Smith CL (1986) Sensory neurons supplying touch domes near the body midlines project bilaterally in the thoracic spinal cord of rats. J Comp Neurol 245:541–552

    Google Scholar 

  • Streit P, Reubi JC (1977) A new and sensitive staining method for axonally transported horseradish peroxidase (HRP) in the pigeon visual system. Brain Res 126:530–537

    Google Scholar 

  • Taylor DCM, Korf H-W, Pierau Fr-K (1982) Distribution of sensory neurones of the pudendal nerve in the dorsal root ganglia and their projection to the spinal cord. Horseradish-peroxidase studies in the rat. Cell Tissue Res 226:555–564

    Google Scholar 

  • Thor KB, Roppolo JR, DeGroat WC (1983) Naloxone induced micturition in unanesthetized paraplegic cats. J Urol 129:202–205

    Google Scholar 

  • Ueyama T, Mizuno N, 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

    Google Scholar 

  • Ueyama T, Mizuno N, Takahashi O, Nomura S, Arakawa H, Matsushima R (1985a) Central distribution of efferent and afferent components of the pudendal nerve in macaque monkey. J Comp Neurol 232:248–556

    Google Scholar 

  • Ueyama T, Arakawa H, Mizuno N (1985b) Contralateral termination of pudendal nerve fibers in the gracile nucleus of the rat. Neurosci Lett 62:113–117

    Google Scholar 

  • Wall PD (1960) Cord cells responding to touch, damage, and temperature of skin. J Neurophysiol 23:197–210

    Google Scholar 

  • Wan XST, Trojanowski FQ, Gonatas JO, Liu CN (1982) Cytoarchitecture of the extranuclear and commissural dendrites of hypoglossal nucleus neurons as revealed by conjugates of horseradish peroxidase with cholera toxin. Exp Neurol 78:167–175

    Google Scholar 

  • Weiss HD (1972) The physiology of human penile erection. Ann Intern Med 76:793–799

    Google Scholar 

  • Yamamoto T, Satomi H, Ise H, Takatama H, Takahashi K (1978) Sacral spinal innervations of the rectal and vesical smooth muscles and the sphincter-ic striated muscles as demonstrated by the horseradish peroxidase method. Neurosci Lett 7:41–47

    Google Scholar 

  • Ygge J, Grant G (1983) The organization of the thoracic spinal nerve projection in the rat dorsal horn demonstrated with transganglionic transport of horseradish peroxidase. J Comp Neurol 216:1–9

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ueyama, T., Arakawa, H. & Mizuno, N. Central distribution of efferent and afferent components of the pudendal nerve in rat. Anat Embryol 177, 37–49 (1987). https://doi.org/10.1007/BF00325288

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00325288

Key words

Navigation