Skip to main content

Androgen-Dependent Plasticity of a Neuromuscular System

  • Chapter

Part of the book series: NATO ASI Series ((NSSA,volume 234))

Abstract

The perineal muscles and their spinal motoneurons are sexually dimorphic in adult mammals. The onset of this sexual dimorphism underlies the production of sex specific behaviors. In fact, in male rats the bulbocavernosus (BC), the ischiocavernosus (IC) and the levator ani (LA) muscles attach to the penis and participate in copulatory reflexes such as erection. In adult female rats these muscles are atrophied (Cihak et al., 1970) and made up of few muscle fibers (Tobin and Joubert, 1988). The spinal motor nuclei innervating perineal muscles in the rat are located in the lumbosacral spinal cord (Schroeder, 1980), being the homologous of Onuf’s nucleus in man (Onuf, 1900). In males two distinct neuronal columns are recognizable: a dorsolateral one, generally for the IC, the external vesical sphincter and the external anal sphincter, and a dorsomedial one, for the BC and the LA muscles overall (Schroeder, 1980). In females, these motor nuclei are made up of fewer and smaller motoneurons, mostly innervating the nondimorphic anal and vesical sphincters (McKenna and Nadelhaft, 1986).

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   39.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   54.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Araki, I., Harada, Y., and Kuno, M. (1991) Target-dependent Hormonal Control of Neuron Size in the Rat Spinal Nucleus of the Bulbocavernosus. J. Neurosci. 11:3025.

    PubMed  CAS  Google Scholar 

  • Bailce-Gordon, R.J., Breedlove, S.M., Bernstein, S., and Lichtman, J.W. (1990) Neuromuscular Junctions Shrink and Expand as Muscle Fiber Size is Manipulated, in vivo Observations in the Androgen-sensitive Bulbocavernosus Muscle of Mice. J. Neurosci. 10:2660.

    Google Scholar 

  • Balice-Gordon, R.J., and Lichtman, J.W. (1990) In vivo Visualization of the Growth of Pre-and Postsynaptic Elements of Neuromuscular Junctions in the Mouse. J. Neurosci. 10:894.

    PubMed  CAS  Google Scholar 

  • Breedlove, S.M. (1985) Hormonal Control of the Anatomical Specificity of Motoneuron-to-Muscle Innervation in Rats. Science 227:1357.

    Article  PubMed  CAS  Google Scholar 

  • Breedlove, S.M., and Arnold, A.P. (1980) Hormone Accumulation in a Sexually Dimorphic Motor Nucleus of the Rat Spinal Cord. Science 210:564.

    Article  PubMed  CAS  Google Scholar 

  • Breedlove, S.M., and Arnold, A.P. (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.

    Article  PubMed  CAS  Google Scholar 

  • Breedlove, S.M., and Arnold, A.P. (1983a) Hormonal Control of a Developing Neuromuscular System: 1. Complete Demasculinization of the Male Rat Spinal Nucleus of the Bulbocavernosus Using the Anti-androgen Flutamide. J. Neurosci. 3:417.

    PubMed  CAS  Google Scholar 

  • Breedlove, S.M., and Arnold, A.P. (1983b) Hormonal Control of a Developing Neuromuscular System: 11. Sensitive Periods for the Androgen-induced Masculinization of the Rat Spinal Nucleus of the Bulbocavernosus. J. Neurosci. 3:424.

    PubMed  CAS  Google Scholar 

  • Breedlove, S.M., Jacobson, C.D., Gorski, R.A., and Arnold, A.P. (1982) Masculinization of the Female Rat Spinal Cord Following a Single Neonatal Injection of Testosterone Propionate but not Estradiol Benzoate. Brain Res. 237:173.

    Article  PubMed  CAS  Google Scholar 

  • Breedlove, S.M., Jordan, C.L., and Arnold, A.P. (1983) Neurogenesis of Motoneurons in the Sexually Dimorphic Spinal Nucleus of the Bulbocavernosus in Rats. Devl. Brain Res. 9:39.

    Article  Google Scholar 

  • Cihak, R., Gutmann, E., and Hanzlikova, V. (1970) Involution and Hormone-induced Persistence of m. Sphincter (Levator) Ani in Female Rats. J. Anat. 106:93.

    PubMed  CAS  Google Scholar 

  • Collins, W.F. (1991) Passive Electrical Properties of Bulbospongiosus Motoneurons in Gonadally Intact and Castrated Adult Male Rats. Soc. Neurosci. Abstr. 16:1060.

    Google Scholar 

  • Cracco, C., and Vercelli A. (1991) Hormone-dependent Plasticity of the Motoneurons of the Ischiocavernosus Muscle: An Ultrastructural Study. In: Plasticity and Regeneration of the Nervous System, P.S. Timiras, A. Privat, E. Giacobini, J. Lauder and A. Vernadakis, eds Plenum Press, New York.

    Google Scholar 

  • Filogamo, G., and Robecchi, M.G. (1985) La tension mécanique régle le développement des ébouches musculaires. Bull. Ass. Anat. 69:241.

    CAS  Google Scholar 

  • Fishman, R.B., and Breedlove, S.M. (1985) The Androgenic Induction of Spinal Sexual Dimorphism is Independent of Supraspinal Afferents. Devl. Brain Res. 23:255.

    Article  CAS  Google Scholar 

  • Fishman, R.B., and Breedlove, S.M. (1987) Androgen Blockade of Bulbocavernosus Muscle Inhibit Testosterone-dependent Masculinization of Spinal Motoneurons in Newborn Female Rats. Soc. Neurosci. Abstr. 13:1520.

    Google Scholar 

  • Fishman, R.B., and Breedlove, S.M. (1988) Neonatal Androgen Maintains Sexually Dimorphic Muscles in the Absence of Innervation. Muscle and Nerve 11:553.

    Article  PubMed  CAS  Google Scholar 

  • Fishman, R.B., Chism, L., Firestone, G.L., and Breedlove, S.M. (1990) Evidence for Androgen Receptors in Sexually Dimorphic Perineal Muscles of Neonatal Male Rats. J. Neurobiol. 21:694.

    Article  PubMed  CAS  Google Scholar 

  • Forger, N.G., and Breedlove, S.M. (1987) Seasonal Variation in Mammalian Striated Muscle Mass and Motoneuron Morphology. J. Neurobiol. 18:155.

    Article  PubMed  CAS  Google Scholar 

  • Galavazi, G., and Szirmai, J.A. (1971) Cytomorphometry of Skeletal Muscle: The Influence of Age and Testosterone on the Rat m. Levator Ani. Z. Zellforsch. 121:507.

    Article  PubMed  CAS  Google Scholar 

  • Goldstein, L.A., Kurz, E.M., and Sengelaub, D.R. (1990) Androgen Regulation of Dendritic Growth and Retraction in the Development of a Sexually Dimorphic Spinal Nucleus. J. Neurosci. 10:935.

    PubMed  CAS  Google Scholar 

  • Gorski, R. and Arnold, A.P. (1984) Gonadal Steroid Induction of Structural Sex Differences in the Central Nervous System. Ann. Rev. Neurosci. 7:413.

    Article  PubMed  Google Scholar 

  • Hamburger, V., and Levi-Montalcini, R. (1949) Proliferation, Differentiation and Degeneration in the Spinal Ganglia of the Chick Embryo under Normal and Experimental Conditions. J. Exp. Zool. 111:457.

    Article  PubMed  CAS  Google Scholar 

  • Hanzlikova, V., and Gutmann, E. (1972) Effect of Foreign Innervation on the Androgen-sensitive Levator Ani Muscle of the Rat, Z. Zelfforsch. 135:165.

    Article  CAS  Google Scholar 

  • Hanzlikova, V., and Gutmann, E. (1974) The Absence of Androgen Sensitivity in the Grafted Soleus Muscle Innervated by the Pudendal Nerve. Cell Tissue Res. 154: 121.

    Article  PubMed  CAS  Google Scholar 

  • Henneman, E., Somjen, G., and Carpenter, D.O. (1965) Functional Significance of Cell Size in Spinal Motoneurons. J. Neurophvsiol. 28:560.

    CAS  Google Scholar 

  • Holliday, M., and Hamburger, V. (1976) Reduction of the Naturally Occurring Motor Neuron Loss by Enlargement of the Periphery. J. Comp. Neurol. 170:311.

    Article  Google Scholar 

  • Hughes, B.J., Bowen, J.M., Campion, D.R., and Bradley, W.E. (1982) Effect of Prepubertal Castration on Porcine Bulbospongiosus Muscle. Anat. Embryol. 168:51.

    Article  Google Scholar 

  • Jordan, C.L., Letinski, M.S., and Arnold, A.P. (1988) Synapse Elimination Occurs Late in the Hormone-sensitive Levator Ani Muscle of the Rat. J. Neurobiol. 19:335.

    Article  PubMed  CAS  Google Scholar 

  • Jordan, C.L., Letinski, M.S., and Arnold, A.P. (1990) Critical Period for the Androgenic Block of Neuromuscular Synapse Elimination. J. Neurobiol. 21:760.

    Article  PubMed  CAS  Google Scholar 

  • Joubert, Y., and Tobin C. (1989) Satellite Cell Proliferation and Increase in the Number of Myonuclei Induced by Testosterone in the Levator Ani Muscle of the Adult Female Rat. Devl. Biol. 131:550.

    Article  CAS  Google Scholar 

  • Krieg, M., and Voght, K.D. (1977) Biochemical Substrate of Androgenic Actions at a Cellular Level in Prostate, Bulbocavernosus and Levator Ani and in Skeletal Muscles. Acta Endocrinol. 85 (Suppl. 214):43.

    CAS  Google Scholar 

  • Kurz, E.M., Sengelaub, D.R., and Arnold, A.P. (1986) Androgen Regulate the Dendritic Length of Mammalian Motoneurons in Adulthood. Science 232:395.

    Article  PubMed  CAS  Google Scholar 

  • Lee Crews, L., and Wigston, D.J. (1990) The Dependence of Motoneurons on their Target Muscle during Postnatal Development of the Mouse. J. Neurosci. 10:1643.

    PubMed  CAS  Google Scholar 

  • Leedy, M.G., Beattie M.S., and Bresnahan, J.C. (1987) Testosterone-induced Plasticity of Synaptic Inputs to Adult Mammalian Motoneurons. Brain Res. 424:386.

    Article  PubMed  CAS  Google Scholar 

  • Manabe, T., Araki, I., Takahashi, T., and Kuno, M. (1991) Membrane Currents Recorded from Sexually Dimorphic Motoneurones of the Bulbocavernosus Muscle in Neonatal Rats. J. Physiol. 440:419.

    PubMed  CAS  Google Scholar 

  • Matsumoto, A., Micevych, P.E., and Arnold, A.P. (1988a) Androgen Synaptic Input to Motoneurons of the Adult Rat Spinal Cord. J. Neurosci. 8:4158.

    Google Scholar 

  • Matsumoto, A., Arnold, A.P., Zampighi, G.A., and Mycevych, P.E. (1988b) Androgenic Regulation of Gap Junctions Between Motoneurons in the Rat Spinal Cord. J. Neurosci. 8:4177.

    PubMed  CAS  Google Scholar 

  • Matsumoto, A., Arai, Y., Urano, A., and Hyodo, S. (1991) Androgen Regulates Gap Junction mRNA Expression in the Motoneurons of Lumbar Spinal Cords in Adult Male Rats. Soc. Neurosci. Abstr. 17:1319.

    Google Scholar 

  • McKenna, K., and Nadelhaft, I. (1986) The Organization of Pudendal Nerve in the Male and Female Rat. J. Comp. Neurol. 248:532.

    Article  PubMed  CAS  Google Scholar 

  • Mills, A., and Sengelaub, D.R. (1991) Development of Neuronal Number in Primary Afferents of a Sexually Dimorphic Neuromuscular System is Androgen-dependent. Soc. Neurosci. Abstr. 16:1318.

    Google Scholar 

  • Nordeen, E.J., Nordeen, K.W., Sengelaub, D.R., and Arnold, A.P. (1985) Androgens Prevent Normally Occurring Cell Death in a Sexually Dimorphic Spinal Nucleus. Science 229:671.

    Article  PubMed  CAS  Google Scholar 

  • Okado, N., and Oppenheim, R.W. (1984) Cell Death of Motoneurons in the Chick Embryo Spinal Cord: IX. The Loss of Motoneurons Following Removal of Afferent Inputs. J. Neurosci. 4:1639.

    PubMed  CAS  Google Scholar 

  • Onuf, B. (1900) On the Arrangement and Function of the Cell Groups in the Sacral Region of the Spinal Cord. Arch. Neurol. Psychopathol. 3:387.

    Google Scholar 

  • Oppenheim, R.W. (1991) Cell Death during Development of the Nervous System. Annu. Rev. Neurosci. 14:453.

    Article  PubMed  CAS  Google Scholar 

  • Rand, M.N., and Breedlove, S.M. (1987) Ontogeny of Funtional Innervation of Bulbocavernosus Muscles in Male and Female Rats. Devl. Brain Res. 33:150.

    Article  Google Scholar 

  • Schroeder, H.D. (1980) Organization of the Motoneurons Innervating the Pelvic Muscles of the Male Rat. J. Comp. Neurol. 192:567.

    Article  Google Scholar 

  • Sengelaub, D.R., and Arnold, A.P. (1986) Development and Loss of Early Projections in a Sexually Dimorphic Rat Spinal Nucleus. J. Neurosci. 6:1613.

    PubMed  CAS  Google Scholar 

  • Sengelaub, D.R., and Arnold, A.P. (1989) Hormonal Control of Neuron Number in Sexually Dimorphic Spinal Nuclei of the Rat: 1. Testosterone-regulated Death in the Dorsolateral Nucleus. J. Comp. Neurol. 280–622.

    Google Scholar 

  • Tanaka, H., and Landmesser, L.T. (1986) Cell Death of Lumbosacral Motoneurons in Chick, Quail and Chick-Quail Chimera Embryos: A Test of the Quantitative Matching Hypothesis of Neuronal Cell Death. J. Neurosci. 6:2889.

    PubMed  CAS  Google Scholar 

  • Tanaka, J., and Arnold, A.P. (1991) Androgenic Modulation of the Excitability of Lumbar Neurons in the Rat Bulbocavernosus Reflex. Soc. Neurosci. Abstr. 17:1319.

    Google Scholar 

  • Tobin, C., and Joubert, Y. (1988) The Levator Ani of the Female Rat: A Suitable Model for Studying the Effects of Testosterone on the Development of Mammalian Muscles. Biol. Struct. Morphoq. 1:28.

    CAS  Google Scholar 

  • Tobin, C., and Joubert, Y. (1991) Testosterone-induced Development of the Rat Levator Ani Muscle. Devl. Biol. 146:131.

    Article  CAS  Google Scholar 

  • Tucek, S., Kostirova, D., and Gutman, E. (1976) Testosterone-induced Changes of ChAT and ChE Activities in the Rat Levator Ani Muscle. J. Neurol. Sci. 27:353.

    Article  PubMed  CAS  Google Scholar 

  • Venable, J.H. (1966a) Constant Cell Populations in Normal, Testosterone-deprived and Testosterone-stimulated Levator Ani Muscle. Am. J. Anat. 119:263.

    Article  PubMed  CAS  Google Scholar 

  • Venable, J.H. (1966b) Morphology of Cells of Normal, Testosterone-deprived and Testosterone-stimulated Levator Ani Muscles. Am, J. Anat. 119:271.

    Article  CAS  Google Scholar 

  • Vercelli, A., and Cracco, C. (1989) Influence of Testosterone on the Development of the Ischiocavernosus Muscle of the Rat. Acta Anat. 134:177.

    Article  PubMed  CAS  Google Scholar 

  • Vercelli, A., and Cracco, C. (1990) Effects of Prepubertal Castration on the Spinal Motor Nucleus of the Ischiocavernosus Muscle of the Rat. Cell Tissue Res. 262:551.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1992 Springer Science+Business Media New York

About this chapter

Cite this chapter

Cracco, C., Vercelli, A. (1992). Androgen-Dependent Plasticity of a Neuromuscular System. In: Sharma, S.C., Goffinet, A.M. (eds) Development of the Central Nervous System in Vertebrates. NATO ASI Series, vol 234. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-3018-3_15

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-3018-3_15

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4613-6315-6

  • Online ISBN: 978-1-4615-3018-3

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics