Skip to main content
SpringerLink
Log in
Book cover

Molecular Aspects of Development and Aging of the Nervous System pp 245–259Cite as

The Ontogeny of Adrenergic Fibers in Rat Spinal Cord

  • Chapter

Part of the book series: Advances in Experimental Medicine and Biology ((AEMB,volume 265))

Abstract

Preganglionic neurons play a pivitol role in the integration of descending central signals involved in sympathetic and parasympathetic regulation. However, the number of neurotransmitter systems which converge in the preganglionic cell column has made study of the complex synaptology of the preganglionic neuron and the development of its innervation exceedingly difficult. Although many neurotransmitters have been identified in the region of preganglionic neurons, it was not until recently that the termination of phenotypically defined fibers was demonstrated on preganglionic neurons which project to identified sympathetic targets. This chapter reviews studies which have focused on the development and synaptology of one of these projections which arises in adrenergic neurons located in the medulla oblongata and which terminates in the thoracic region of spinal cord. Study of adrenergic neurons has been facilitated by the specific expression of the epinephrine-synthesizing enzyme, phenylethanolamine N-methyltransferase (PNMT), which distinguishes adrenergic neurons from other types of catecholamine-synthesizing cells. Study of this particular projection is interesting due to the implication of adrenergic neurons in a wide array of autonomic and endocrine functions including cardiovascular regulation (Saavedra et al., 1979; Ross et al., 1984b; Goodchild et al., 1984; Morrison et al., 1988), reproduction (Coen and Coombs, 1983; Sheaves et al., 1985; and the stress response (Saavedra and Torda, 1980; Mezey et al., 1984; Liposits et al., 1986 a,b).

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

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

  • Astier, B., Kitahama, K., Denoroy, L., Jouvet, M., Renoud B. (1987). Immunohistochemical evidence for the adrenergic medullary longitudinal bundle as a major ascending pathway to the locus coeruleus. Neuroscience Lett. 74 (2): 132–1.

    Article  Google Scholar 

  • Beato, K.K., Burke, W.J., Joh, T.H., and Haring, J.H. (1987). Cortical epinephrine projections demonstrated by retrograde tracing combined with tyrosine hydroxylase and phenylethanolamine N-methyltransferase immunocytochemistry. Soc. Neurosci. Abst. 13: 366–1

    Google Scholar 

  • Bernstein-Goral, H.L. (1988). The ontogeny of adrenergic fibers in rat spinal cord. Ph.D. Dissertation. State University of New York at Stony Brook.

    Google Scholar 

  • Bernstein-Goral, H., and Bohn, M.C. (1988). Ontogeny of adrenergic fibers in rat spinal cord in relationship to adrenal preganglionic neurons. J. Neurosci. Res. 21: 333–351.

    Google Scholar 

  • Bernstein-Goral, H., and Bohn, M.C. (1989). Phenylethanolamine N-methyltransferase(PNMT) immunoreactive terminals synapse on adrenal preganglionic neurons in the rat spinal cord. Neurosc. (in press).

    Google Scholar 

  • Black, I.B., Bloom, E.M., Hamill, R.W. (1976). Central regulation of sympathetic neuron development. Proc. Natl. Acad. Sci. USA 73 (10): 3575–3578.

    Article  Google Scholar 

  • Bohn, M.C. Goldstein, M., Black, I.B. (1981). Role of glucocorticoids in expression of the adrenergic phenotype in rat embryonic adrenal gland. Dev. Biol. 82: 1–10.

    Google Scholar 

  • Bohn, M.C., Goldstein, M., Black, I.B. (1986). Expression and development of phenylethanolamine N-methyltransferase (PNMT) in rat brain stem: studies with glucocorticoids. Dev. Biol. 114: 180–193.

    Article  Google Scholar 

  • Coen, C.W., Coombs, M.C. (1983). Effects of manipulating catecholamines on the incidence of the preovulatory surge of luteninizing hormone and ovulation in the rat: Evidence for a necessary involvement of hypothalamic adrenaline in the normal or midnight surge. Neurosci. 10: 187–206.

    Google Scholar 

  • Daikoku, S., Kinutani, M., Sako, M., (1977). Development of adrenal medullary cells in rats with reference to synaptogenesis. Cell Tiss. Res. 179: 77–86.

    Google Scholar 

  • Forehand, C.J. (1985). Density of somatic innervation on mammalian autonomic ganglion cells is inversely related to dendritic complexity and preganglionic convergence. J. Neurosci. 5 (12): 3403–3408.

    Google Scholar 

  • Foster, G.A., Schultzberg, M., Goldstein, M., Hökfelt T. (1985a). Differential ontogeny of three putative catecholamine cell types in the postnatal rat retina. Develop. Brain Res. 22: 187–196

    Google Scholar 

  • Foster, G.A., Schultzberg, M., Goldstein, M., Hökfelt, T. (1985b). Ontogeny of phenylethanolamine N-methyltransferase-and tyrosine hydoxylase-like immunoreactivity in presumptive adrenaline neurons of the foetal rat central nervous system. J. Comp. Neurol. 236: 348–381.

    Article  Google Scholar 

  • Foster G.A., Schultzberg, M., Dahl, D., Goldstein, M., Verhofstad, A.A.J. (1985c). Ephemeral existence of a single catecholamine synthetic enzyme in the olfactory placode and the spinal cord of the embryonic rat. Int. J. Devel. Neuroscience. 3 (6): 597–608.

    Article  Google Scholar 

  • Foster, G.A., Sundstrom, E., Helmer-Matyjek, E., Goldstein, M., Hökfelt T. (1987). Abundance in the embryonic brainstem of adrenaline during the absence of detectable tyrosine hydroxylase activity. J. Neurochem. 48: 202–207.

    Article  Google Scholar 

  • Gagner, J., Gauthier, S., Sourkes, T.L. (1983). Participation of spinal monoaminergic and cholinergic systems in the regulation of adrenal tyrosine hydoxylase. Neuropharm. 22: 45–53.

    Article  Google Scholar 

  • Gauthier, P., and Reader, T.A. (1982). Adrenomedullary secretory response to midbrain stimulation in rat: effects of depletion of brain catecholamines or serotonin. Can. J. Physiol. Pharmacol. 60; 1464–1474.

    Google Scholar 

  • Goodchild, A.K., Moon, E.A., Dampney, R.A.L., Howe, P.R.C. (1984). Evidence that adrenaline neurons in the rostral ventolateral medulla have a vasopressor function. Neuroscience Lett. 45: 267–272.

    Article  Google Scholar 

  • Guyenet, P., and Young, B. (1987). Projections of nucleus paragigantocellularis lateralis to locus coeruleus and other structures in rat. Brain Res. 406: 171–184.

    Article  Google Scholar 

  • Hamill, R.W., Bloom, E.M., Black, I.B. (1977). The effect of spinal cord transection on the development of cholinergic and adrenergic sympathetic neurons. Brain Res. 134: 269–278.

    Article  Google Scholar 

  • Hamill, R.W., Cochard, P., Black, I.B. (1983). Long-term effects of spinal transection on the development and function of sympathetic ganglia. Brain Res. 266: 21–27.

    Article  Google Scholar 

  • Hökfelt, T., Foster, G.A., Johansson, O., Schultzberg, M., Holets, V., Ju, G., Skagerberg, G., Palkovits, M. (1988). Central phenylethanolamine N-methyltransferaseimmunoreactive neurons: Distribution, projections, fine structure, ontogeny, coexisting peptides. In; Epinephrine in the Central Nervous System. (J. Stolk, D. Uprichard, K. Fuxe, eds.) Oxford U. Press. pp. 10–45.

    Google Scholar 

  • Hökfelt, T., Fuxe, K., Goldstein, M., Johansson, O. (1974). Immunohistochemical evidence for the existence of adrenaline neurons in the rat brain. Brain Res. 66: 235–251.

    Article  Google Scholar 

  • Hornby, P.J., and Piekut, D.T. (1987). Catecholamine distribution and relationship to magnocelluar neurons in the paraventricular nucleus of the rat. Cell Tiss. Res. 248 (2): 239–246.

    Google Scholar 

  • Howe, P.R.C., Costa, M., Furness, J.B., Chalmers, J.P. (1980). Simultaneus demonstration of phenylethanolamine N-methyltransferase immunofluorescent and catecholamine fluorescent nerve cell bodies in the rat medulla oblongata. Neurosci. 5: 2229–2238.

    Google Scholar 

  • Johnson, Jr., E.M., Caserta, M., Ross, L.L. (1977). Effects of destruction of the postganglionic sympathetic neurons in neonatal rats on development of choline acetyltransferase and survival of preganglionic cholinergic neurons. Brain Res. 136: 455–464.

    Article  Google Scholar 

  • Kaiser, K.P., Karten, H.J., Katz, B., and Bohn, M.C. (1987) Catecholaminergic horizontal and amacrine cells in the feret retina. J. Neurosci. 7: 3996–4007.

    Google Scholar 

  • Kalia, M., Woodward, D.J., Smith, W.K., Fuxe, K. (1985a). Rat medulla oblongata. IV. Topographical distribution of catecholaminergic neurons with quantitative three-dimensional computer reconstruction. J. Comp. Neurol. 233: 350–364.

    Google Scholar 

  • Kalia, M., Fuxe, K., Goldstein, M. (1985b). Rat medulla oblongata. III. Adrenergic (C1 amp; C2) neurons, nerve fibers and presumptive terminal processes. J.Comp. Neurol. 233: 333–349.

    Google Scholar 

  • Kirby, R.F., and McCarty, R. (1987). Ontogeny of functional sympathetic innervation to the heart and adrenal medulla in the preweanling rat. J. Autonom. Nerv. Syst. 19: 67–75.

    Google Scholar 

  • Kohno, J., Shinoda, K., Kawai, Y., Ohuchi, T., Ono, K., Shinotani, Y. (1988). Interaction between adrenergic fibers and intermediate cholinergic neurons in the rat spinal cord: A new double-immunostaining method for correlated light and electron microscopic observations. Neuroscience 25 (1): 113–212.

    Article  Google Scholar 

  • LaGamma, E.F., and Adler, J.H. (1988). Development of transynaptic regulation of adrenal enkephalin. Dev. Brain Res. 39: 177–182.

    Google Scholar 

  • Larramendi, L.M.H. (1969). Analysis of synaptogenesis in the cerebellum of the mouse. In: Neurobiology of cerebellar evolution and development, Amer. Med. Ass. Educ. amp; Res. Fdn., Chicago. pp. 803–843.

    Google Scholar 

  • Lau, C., Pylypiw, A., Ross, L. (1985). Development of serotonergic and adrenergic receptors in the rat spinal cord: effects of neonatal chemical lesions and hyperthyroidism. Dev. Brain Res. 19: 57–66.

    Google Scholar 

  • Lau, C., Ross, L.L., Whitmore, W.L., Slotkin, T.A. (1987). Regulation of adrenal chromaffin cell development by the central monoaminergic system: Differential control of norepinephine and epinephrine levels and secretory responses. Neurosci. 22 (3): 1067–1075.

    Article  Google Scholar 

  • Lawrence, J.M., Hamill, R.W., Cochard, P., Raisman, G., Black, I.B. (1981). Effects of spinal cord transection on synapse numbers and biochemical maturation in rat lumbar sympathetic ganglia. Brain Res. 212: 83–88.

    Article  Google Scholar 

  • Liposits, Zs., Phelix, C., Paull, W.K. (1986). Electron microscopic analysis of tyrosine hydroxylase, dopamine-B-hydroxylase and phenylethanolamine N-methyltransferase immunoreactive innervation of the hypothalamic paraventricular nucleus in the rat. Histochemistry 84: 105–120.

    Article  Google Scholar 

  • Liposits, Zs., Phelix, C., Paull, W.K. (1986). Adrenergic innervation of corticotropin releasing factor ( CRF)-synthesizing neurons in the hypothalamic paraventricular nucleus of the rat. Histochemistry 84: 201–205.

    Google Scholar 

  • Makhail, Y., and Mahran, Z. (1965). Innervation of the cortical and medullary portions of the adrenal gland of the rat during postnatal life. Anat. Rec. 152: 431–438.

    Google Scholar 

  • Mefford, I.N. (1988). Are there epinephrine neurons in rat brain? Brain Res. Reviews 12: 383–395.

    Article  Google Scholar 

  • Mezey, E., Kiss, J.L., Skirboll, L.R., Goldstein, M., Axelrod, J. (1984). Increase of corticotropin-releasing factor staining in rat paraventricular nucleus neurons by depletion of hypothalamic adrenaline Nature 310: 140–141.

    Google Scholar 

  • Milner, T.A., Morrison, S.F., Abate, C., Reis, D.J. (1988). Phenylethanolamine Nmethyltransferase-containing terminals synapse directly on sympathetic preganglionic neurons in the rat. Brain Res. 448: 205–222.

    Article  Google Scholar 

  • Morrison, S.F., Milner, T.A., Reis, D.J. (1988). Reticulospinal vasomotor neurons of the rat rostral ventrolateral medulla: Relationship to sympathetic nerve activity and the Cl adrenergic cell group. J. Neurosci. 8: 1286–1301.

    Google Scholar 

  • Nakamura, K., and Nakamura, K. (1978). Role of brainstem and spinal noradrenergic and adrenergic neurons in the development and maintenance of hypertension in spontaneously hypertensive rats. Naunyn-Schmiedeberg’s Arch. Pharmacol. 305: 127–133.

    Google Scholar 

  • Pieribone, V., Aston-Jones, G., Bohn, M.C. (1988). Most adrenergic afferents to locus coeruleus originate in the Cl ventrolateral medullary cell group: a fluorescent double labeling study. Neurosci. Lett. 85: 297–303.

    Google Scholar 

  • Pieribone, V.A., Aston-Jones, G., Bohn, M., Bernstein-Goral, H. (1987). Double labeling using flurogold reveals neurotransmitter identity of afferents to locus coeruleus. Soc. Neurosci. Abstr. 13: 14–58.

    Google Scholar 

  • Ross, C.A., Armstrong, D.A., Ruggiero, D.A., Pickel, V.M., Joh, T.H. Reis, D.J. (1981a). Adrenaline neurons in the rostral ventrolateral medulla innervate thoracic spinal cord: a combined immunocytochemical and retrograde transport demonstration. Neuroscience Lett. 25: 257–262.

    Google Scholar 

  • Ross, C.A., Ruggiero, D.A., Reis, D.J. (1981b). Projections to the spinal cord from neurons close to the ventral surface of the hindbrain in the rat. Neuroscience Lett. 25: 145–148.

    Article  Google Scholar 

  • Ross, C.A., Ruggiero, D.A., Meeley, M.P., Park, D.H., Joh, T.H., Reis, D.J. (1984a). A new group of neurons in hypothalamus containing phenylethanolamine Nmethyltransferase ( PNMT) but not tyrosine hydroxylase. Brain Res. 306: 349–353.

    Google Scholar 

  • Ross, C.A., Ruggiero, D.A., Park, D.H., Joh, T.H., Sved, A.F., Fernandez-Pardal, J., Saavedra, J.M., Reis, D.J. (1984b). Tonic vasomotor control by the rostral ventrolateral medulla: effects of electrical or chemical stimulation of the areas containing Cl adrenaline neurons on arterial pressure, heart rate and plasma catecholamines and vasopressin. J. Neuroscience 4 (2): 474–494.

    Google Scholar 

  • Ross, C.A., Ruggiero, D.A., Joh, T.H., Park, D.H., Reis, D.J. (1984c). Rostral ventrolateral medulla: selective projections to the thoracic autonomic cell column from the region containing Cl adrenaline neurons. J. Comp. Neurol. 228: 168–185.

    Google Scholar 

  • Ross, L.L., Smolen, A.J., Cherry, J. (1980). Spinal cord transection interferes with normal development of sympathetic preganglionic neurons. Soc. Neurosci. Abs. 6: 385.

    Google Scholar 

  • Ross, L.L., Smolen, A.J., Cherry, J. (1981). Supraspinal pathways regulate the development of the normal pattern and density of innervation of the adrenal medulla. Anat. Rec. 199: 127A.

    Google Scholar 

  • Ross, L.L., Pylypiw, A., Chmelewski. W. (1982). Development of catecholamines and adrenergic receptors in the rat spinal cord. Soc. Neurosci. Abstr. 8: 175.

    Google Scholar 

  • Ross, L.L., Smolen, A.J., McCarthy, L. (1983). Supraspinal pathways regulate the mitotic activity of adrenal medulla cells. Anat. Rec. 205: 167–168.

    Google Scholar 

  • Ruggiero, D.A., Ross, C.A., Anwar, M., Park, D.H., Joh, T.H. Reis D.J. (1985). Distribution of neurons containing phenylethanolamine N-methyltransferase in medulla and hypothalamus of the rat. J. Comp. Neurol. 239: 127–154.

    Article  Google Scholar 

  • Saavedra, J.M., Kvetnansky, R., Kopin, I.J. (1979). Adrenaline, noradrenaline, and dopamine levels in specific brainstem areas of acutely immobilized rats. Brain Res. 160: 271–280.

    Article  Google Scholar 

  • Saavedra, J.M., Torda, T. (1980). Increased brainstem and decreased hypothalamic adrenaline-forming enzyme after acute and repeated immobilization stress in the rat. Neuroendocrinol. 31: 142–146.

    Article  Google Scholar 

  • Sawchenko, P.E., and Swanson, L.W. (1982). Immunohistochemical identification of neurons in the paraventricular nucleus of the hypothalamus that project to the medulla or to the spinal cord in the rat. J. Comp. Neurol. 205: 260–272.

    Google Scholar 

  • Schafer, T., Schwab, M.E., Thoenen, H. (1983). Increased formation of preganglionic synapses and axons due to a retrograde trans-synaptic action of nerve growth factor in the rat sympathetic nervous system. J. Neurosci. 3 (7): 1501–1510.

    Google Scholar 

  • Schramm, L.P., Adair, J.R., Striblin, J.M., Gray, L.P. (1975). Preganglionic innervation of the adrenal gland of the rat: a study using horseradish peroxidase. Exp. Neurol. 49: 540–553.

    Google Scholar 

  • Schramm, L.P. Stribling, J.M., Adair, J.R. (1976). Developmental reorientation of sympathetic preganglionic neurons in the rat. Brain Res. 106: 166–171.

    Article  Google Scholar 

  • Seidler, F.J., and Slotkin, T.A. (1985). Adrenomedullary function in the neonatal rat: responses to acute hypoxia. J. Physiol. ( London ) 358: 1–16.

    Google Scholar 

  • Seidler, F.J., and Slotkin, T.A. (1986a). Non-neurogenic adrenal catecholamine release in the neonatal rat: exocytosis or diffusion? Dev. Brain Res. 28: 274–277.

    Article  Google Scholar 

  • Seidler, F.J., and Slotkin, T.A. (1986b). Ontogeny of adrenomedullary responses to hypoxia and hypoglycemia: Roll of splanchnic innervation. Brain Res. Bull. 16: 11–14.

    Google Scholar 

  • Sheaves, R., Laynes, R., and MacKinnon, C.B. (1985). Evidence that central epinephrine neurons participate in the control and regulation of neuroendocrine events during the estrous cycle. Endocrinol. 116: 542–546.

    Article  Google Scholar 

  • Smolen, A., and Raisman, G. (1980). Synapse formation in the rat superior cervical ganglion during normal development and after neonatal deafferentiation. Brain Res. 181: 315–323.

    Article  Google Scholar 

  • Smolen, A.J., and Beaston-Wimmer, P. (1986). Dendritic development in the rat superior cervical ganglion. Dev. Brain Res. 29: 245–252.

    Google Scholar 

  • Strack, A.M., Sawyer, W.B., Marubio, L.M., Loewy, A.D. (1988). Spinal origin of sympathetic preganglionic neurons in the rat. Brain Res. 455: 187–191.

    Article  Google Scholar 

  • Swanson, L.M., Sawchenko, P.E., Berod, A., Hartman, B.K., Helle, K.B., Van Orden, D.E. (1981). An immunohistochemical study of the organization of catecholaminergic cells and terminal fields in the paraventricular and supraoptic nuclei of the hypothalamus. J. Comp. Neurol. 196: 271–285.

    Google Scholar 

  • Teitelman, G., Baker, H., Joh, T.H., Reis, D.J. (1979). Appearance of catecholamine synthesizing enzymes during development of rat embryo sympathetic nervous system: Possible role of tissue environment. Proc. Natl. Acad. Sci. U.S.A. 76: 509–513.

    Article  Google Scholar 

  • Tucker, D.C., Saper, C.B., Ruggiero, D.A., Reis, D.J. (1987). Organization of central adrenergic pathways: I. Relationship of ventrolateral medullary projections to the hypothalamus and spinal cord. J. Comp. Neurol. 259: 591–603.

    Google Scholar 

  • Vaughn, J.E., Henrikson, C.K., Grieshaber, J.A. (1974). A quantitative study of synapses on motor neuron dendritic growth cones in developing mouse spinal cord. J. Cell Biol. 60: 664–672.

    Article  Google Scholar 

  • Vaughn, J.E., Sims, T., Nakashima, M. (1977). A comparison of the early developmental axodendritic and axosomatic synapses upon embryonic mouse spinal motor neurons. J. Comp. Neurol. 175: 79–100.

    Article  Google Scholar 

  • Verhofstad, A.A., Hökfelt, T., Goldstein, M., Steinbusch, H.W.M., Jooster, H.W.J (1979). Appearance of tyrosine hydroxylase, aromatic amino acid decarboxylase, dopamine B-hydroxylase and phenylethanolamine N-methyltransferase during the ontogenesis of the adrenal medulla. Cell Tissue Res. 200: 1–13.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Cell Biology, Georgetown University,School of Medicine, 3900 Reservoir Road, N.W., Washington, D.C., 20007, USA

    Holli Bernstein-Goral

  2. Department of Neurobiology and Anatomy, University of Rochester Medical Center, Rochester, NY, 14642, USA

    Martha Churchill Bohn

Authors
  1. Holli Bernstein-Goral
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martha Churchill Bohn
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. The University of North Carolina School of Medicine, Chapel Hill, North Carolina, USA

    Jean M. Lauder

  2. Institute of Biology, INSERM, Montpellier, France

    Alain Privat

  3. Southern Illinois University School of Medicine, Springfield, Illinois, USA

    Ezio Giacobini

  4. University of California, Berkeley, California, USA

    Paola S. Timiras

  5. University of Colorado School of Medicine, Denver, Colorado, USA

    Antonia Vernadakis

Rights and permissions

Reprints and permissions

Copyright information

© 1990 Springer Science+Business Media New York

About this chapter

Cite this chapter

Bernstein-Goral, H., Bohn, M.C. (1990). The Ontogeny of Adrenergic Fibers in Rat Spinal Cord. In: Lauder, J.M., Privat, A., Giacobini, E., Timiras, P.S., Vernadakis, A. (eds) Molecular Aspects of Development and Aging of the Nervous System. Advances in Experimental Medicine and Biology, vol 265. Springer, Boston, MA. https://doi.org/10.1007/978-1-4757-5876-4_23

Download citation

  • DOI: https://doi.org/10.1007/978-1-4757-5876-4_23

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4757-5878-8

  • Online ISBN: 978-1-4757-5876-4

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation