Skip to main content
SpringerLink
Log in

The Expression of Cholinergic and Adrenergic Properties by Autonomic Neurons in Tissue Culture

  • Chapter
Excitable Cells in Tissue Culture

Abstract

Both circumstance and paradox dictate that this chapter should center primarily on the autonomic adrenergic (sympathetic) neuron in tissue culture. The particular circumstance is the availability of a well-defined trophic factor, nerve growth factor (NGF), for this neuron, allowing its long-term culture isolated from all other tissues; no comparable factor has been characterized for neurons from other portions of the autonomic nervous system. The paradox is that adrenergic neurons in tissue culture have provided much new information on the development of cholinergic mechanisms: when taken for culture from the perinatal animal, the adrenergic neuron has the unexpected property of developing the ability to synthesize and release acetylcholine and to establish cholinergic interactions with adjacent neurons of its own type. Because of the intense interest in exploring the nature and mechanism of this transmitter shift, a substantial portion of recent work on the adrenergic neuron in culture is centered on these problems. The sympathetic neuron may also provide adrenergic Innervation to a variety of target tissues in culture and thus has been useful for the study of both adrenergic and cholinergic mechanisms.

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

Access this chapter

Log in via an institution
eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 16.99
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

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Aiken, J.W., and Reit, E.A., 1969, A comparison of the sensitivity to chemical stimuli of adrenergic and cholinergic neurons in the cat stellate ganglion, J. Pharmacol. Exp. Ther. 169:211.

    PubMed  CAS  Google Scholar 

  • Betz, W., 1976, The formation of synapses between chick embryo skeletal muscle and ciliary ganglia grown in vitro, J. Physiol. (Lond.) 254:63.

    CAS  Google Scholar 

  • Black, I.B., 1977, Regulation of the growth and development of sympathetic neurons in vivo, in: Progress in Clinical and Biological Research, Vol. 15, Cellular Neurobiology (Z. Hall, R. Kelly, and C.F. Fox, eds.), pp. 61–71, Alan R. Liss, New York.

    Google Scholar 

  • Blackman, J.G., Ginsborg, B.L., and Ray, C., 1963, Some effects of changes in ionic concentration on the action potential of sympathetic ganglion cells in the frog, J. Physiol. (Lond.) 167:374.

    CAS  Google Scholar 

  • Bray, D., 1970, Surface movements during the growth of single explanted neurons, Proc. Natl. Acad. Sci. USA 65:905.

    Article  PubMed  CAS  Google Scholar 

  • Bray, P., 1973, Branching patterns of individual sympathetic neurons in culture, J. Cell Biol. 56:702.

    Article  PubMed  CAS  Google Scholar 

  • Brown, D.A., and Fumagalli, L., 1977, Dissociation of α-bungarotoxin binding and receptor block in the rat superior cervical ganglion, Brain Res. 129:165.

    Article  PubMed  CAS  Google Scholar 

  • Bunge, M.B., 1973, Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture, J. Cell Biol. 56:713.

    Article  PubMed  CAS  Google Scholar 

  • Bunge, M.B., 1977, Initial endocytosis of peroxidase or ferritin by growth cones of cultured nerve cells, J. Neurocytol. 6:407.

    Article  PubMed  CAS  Google Scholar 

  • Bunge, R., Johnson, M., and Ross, C.D., 1978, Nature and nurture in development of the autonomic neuron, Science 199:1409.

    Article  PubMed  CAS  Google Scholar 

  • Bunge, R.P., Rees, R., Wood, P., Burton, H., and Ko, C.-P., 1974, Anatomical and physiological observations on synapses formed on isolated autonomic neurons in tissue culture, Brain Res. 66:401.

    Article  Google Scholar 

  • Burn, J.H., 1977, The function of acetylcholine released from sympathetic fibres, Clin. Exp. Pharmacol. Physiol. 4:59.

    Article  PubMed  CAS  Google Scholar 

  • Burn, J.H., and Rand, M.J., 1965, Acetylcholine in adrenergic transmission, in: Annual Review of Pharmacology (W.S. Cutting, R.H. Dreisbash, and H.W. Elliott, eds.), pp. 163-182, Annual Reviews, Palo Alto, California.

    Google Scholar 

  • Burnstock, G., 1976, Do some nerve cells release more than one transmitter? Neuroscience 1:239.

    Article  PubMed  CAS  Google Scholar 

  • Burnstock, G., 1978, Do some sympathetic neurons synthesize and release both noradrenaline and acetylcholine? Prog. Neurobiol. 10:1.

    Article  Google Scholar 

  • Burnstock, G., and Bell, C., 1974, Peripheral autonomic transmission, in: The Peripheral Nervous System (J.I. Hubbard, ed.), pp. 277–327, Plenum Press, New York.

    Chapter  Google Scholar 

  • Burnstock, G., and Costa, M., 1975, Adrenergic Neurons, Their Organization, Function and Development in the Peripheral Nervous System, Chapman and Hall, London.

    Google Scholar 

  • Burton, H., and Bunge, R.P., 1975, A comparison of the uptake and release of [3H] norephine-phrine in rat autonomic and sensory ganglia in tissue culture, Brain Res. 97:157.

    Article  PubMed  CAS  Google Scholar 

  • Campbell, G., 1970, Autonomic nervous supply to effector tissues, in: Smooth Muscle (E. Bülbring, A.F. Brading, A.W. Jones, and T. Tomita, eds.), pp. 451–495, The Williams & Wilkins Co., Baltimore.

    Google Scholar 

  • Carbonetto, S.T., and Fambrough, D.M., 1978, Rates of metabolism and site of insertion of a plasma membrane protein in rapidly growing neurons, Neurosci. Abstr. 4:510.

    Google Scholar 

  • Carbonetto, S.T., Fambrough, D.M., and Muller, K.J., 1977, α-Bungarotoxin binding to chick sympathetic neurons, Neurosci. Abstr. 3:454.

    Google Scholar 

  • Carbonetto, S.T., Fambrough, D.M., and Muller, K.J., 1978, Nonequivalence of α-bungarotoxin receptors and acetylcholine receptors in chick sympathetic neurons, Proc. Natl. Acad. Sci. USA 75:1016.

    Article  PubMed  CAS  Google Scholar 

  • Ceccarelli, B., Clementi, F., and Mantegazza, P., 1971, Synaptic transmission in the superior cervical ganglion of the cat after reinnervation by vagus fibres, J. Physiol. (Lond.) 216:87.

    CAS  Google Scholar 

  • Chamley, J., Mark, G., Campbell, G., and Burnstock, G., 1972, Sympathetic ganglia in culture. I. Neurons, Z. Zellforsch. Mikrosk. Anat. 135:287.

    Article  PubMed  CAS  Google Scholar 

  • Chamley, J., Campbell, G., and Burnstock, G., 1973, An analysis of the interactions between sympathetic nerve fibers and smooth muscle cells in tissue culture, Dev. Biol. 33:344.

    Article  PubMed  CAS  Google Scholar 

  • Chamley, J., Campbell, G., and Burnstock, G., 1974, Dedifferentiation, redifferentiation and bundle formation of smooth muscle cells in tissue culture: The influence of cell number and nerve fibres, J. Embryol. Exp. Morphol. 32:297.

    PubMed  CAS  Google Scholar 

  • Christ, D.D., and Nishi, S., 1971a, Site of adrenaline blockade in the superior cervical ganglion of the rabbit, J. Physiol. (Lond.) 213:107.

    CAS  Google Scholar 

  • Christ, D.D., and Nishi, S., 1971b, Effects of adrenaline on nerve terminals in the superior cervical ganglion of the rabbit, Br. J. Pharmacol. 41:331.

    PubMed  CAS  Google Scholar 

  • Chun, L.L.Y., and Patterson, P.H., 1977a, Role of nerve growth factor in the development of rat sympathetic neurons in vitro. I. Survival, growth, and differentiation of catecholamine production, J. Cell Biol. 75:694.

    Article  PubMed  CAS  Google Scholar 

  • Chun, L.L.Y., and Patterson, P.H., 1977b, Role of nerve growth factor in the development of rat sympathetic neurons in vitro. II. Developmental studies, J. Cell Biol. 75:705.

    Article  PubMed  CAS  Google Scholar 

  • Chun, L.L.Y., and Patterson, P.H., 1977c, Role of nerve growth factor in the development of rat sympathetic neurons in vitro. III. Effect on acetylcholine production, J. Cell Biol. 75:712.

    Article  PubMed  CAS  Google Scholar 

  • Claude, P., 1973, Electron microscopy of dissociated rat sympathetic neurons in culture, J. Cell Biol. 59:57a.

    Google Scholar 

  • Cochard, P., Goldstein, M., and Black, I.B., 1978, Ontogenetic appearance and disappearance of tyrosine hydroxylase and catecholamines in the rat embryo, Proc. Natl. Acad. Sci. USA 15:2986.

    Article  Google Scholar 

  • Coughlin, M.D., 1975, Target organ stimulation of parasympathetic nerve growth in the developing mouse submandibular gland, Dev. Biol. 43:140.

    Article  PubMed  CAS  Google Scholar 

  • Crain, S.M., 1968, Development of functional neuromuscular connections between separate explants of fetal mammalian tissues after maturation in culture, Anat. Rec. 160:466.

    Google Scholar 

  • Crain, S.M., 1976, Neurophysiologic Studies in Tissue Culture, Raven Press, New York.

    Google Scholar 

  • Dail, W.G., and Evan, A.P., 1978, Ultrastructure of adrenergic terminals and SIF cells in the superior cervical ganglion of the rabbit, Brain Res. 148:469.

    Article  PubMed  CAS  Google Scholar 

  • Dail, W.G., Jr., Evan, A.P., Jr., and Eason, H.R., 1975, The major ganglion in the pelvic plexus of the male rat: A histochemical and ultrastructural study, Cell Tissue Res. 159:49.

    Article  PubMed  CAS  Google Scholar 

  • Dennis, M.J., Harris, A.J., and Kuffler, S.W., 1971, Synaptic transmission and its duplication by focally applied ACh in parasympathetic neurons in the heart of the frog, Proc. R. Soc. Lond. B 177:509.

    Article  PubMed  CAS  Google Scholar 

  • Dichter, M.A., and Fischbach, G.D., 1977, The action potential of chick dorsal root ganglion neurones maintained in cell culture, J. Physiol. (Lond.) 267:281.

    CAS  Google Scholar 

  • Dreyfus, C.L., Bornstein, M.B., and Gershon, M.D., 1977a, Synthesis of serotonin by neurons of the myenteric plexus in situ and in organotypic tissue culture, Brain Res. 128:125.

    Article  PubMed  CAS  Google Scholar 

  • Dreyfus, C.L., Sherman, D.L., and Gershon, M.D., 1977b, Uptake of serotonin by intrinsic neurons of the myenteric plexus grown in organotypic tissue culture, Brain Res. 128:109.

    Article  PubMed  CAS  Google Scholar 

  • Dun, N., and Karczmar, A.G., 1977, The presynaptic site of action of norepinephrine in the superior cervical ganglion of guinea pig, J. Pharmacol. Exp. Ther. 200:328.

    PubMed  CAS  Google Scholar 

  • Dun, N.J., and Karczmar, A.G., 1978, Involvement of an interneuron in the generation of the slow inhibitory postsynaptic potential in mammalian sympathetic ganglia, Proc. Natl. Acad. Sci. USA 75:4029.

    Article  PubMed  CAS  Google Scholar 

  • Dun, N., and Nishi, S., 1974, Effects of dopamine on the superior cervical ganglion of the rabbit, J. Physiol. (Lond.) 239:155.

    CAS  Google Scholar 

  • Elfvin, L.-G., 1971, Ultrastructural studies on the synaptology of the inferior mesenteric ganglion of the cat, J. Ultrastruct. Res. 37:411.

    Article  PubMed  CAS  Google Scholar 

  • Eränkö, L., 1972, Ultrastructure of the developing sympathetic nerve cell and the storage of catecholamines, Brain Res. 46:159.

    Article  PubMed  Google Scholar 

  • Ferry, C.B., 1963, The sympathomimetic effect of acetylcholine on the spleen of the cat, J. Physiol. (Lond.) 167:487.

    CAS  Google Scholar 

  • Ferry, C.B., 1966, Cholinergic link hypothesis in adrenergic neuroeffector transmission, Physiol. Rev. 46:420.

    PubMed  CAS  Google Scholar 

  • Fujiwara, M., and Kurahashi, K., 1976, Cholinergic nature of the primary afferent vagus synapsed in cross anastomosed superior cervical ganglia, Life Sci. 19:1175.

    Article  PubMed  CAS  Google Scholar 

  • Furness, J.B., and Costa, M., 1974, The adrenergic Innervation of the gastrointestinal tract, Ergeb. Physiol. 69:1.

    CAS  Google Scholar 

  • Furshpan, E.J., MacLeish, P.R., O’Lague, P.H., and Potter, D.D., 1976, Chemical transmission between rat sympathetic neurons and cardiac myocytes developing in microcultures: Evidence for cholinergic, adrenergic, and dual-function neurons, Proc. Natl. Acad. Sci. USA 73:4225.

    Article  PubMed  CAS  Google Scholar 

  • Greengard, P., 1978, Cyclic Nucleotides, Phosphorylated Proteins, and Neuronal function, Raven Press, New York.

    Google Scholar 

  • Grillo, M.A., 1966, Electron microscopy of sympathetic tissues, Pharmacol. Rev. 18:387.

    PubMed  CAS  Google Scholar 

  • Harrison, R., 1910, The outgrowth of the nerve fiber as a mode of protoplasmic movement, J. Exp. Zool. 9:787.

    Article  Google Scholar 

  • Hashiguchi, T., Ushiyama, N.S., Kobayashi, H., and Libet, B., 1978, Does cyclic GMP mediate the slow excitatory synaptic potential in sympathetic ganglia? Nature 271:267.

    Article  PubMed  CAS  Google Scholar 

  • Hendry, I.A., 1977, Cell division in the developing sympathetic nervous system, J. Neurocytol. 6:299.

    Article  PubMed  CAS  Google Scholar 

  • Hild, W., and Tasaki, I., 1962, Morphological and physiological properties of neurons and glial cells in tissue culture, J. Neurophysiol. 25:277.

    PubMed  CAS  Google Scholar 

  • Hill, C.E., and Hendry, I.A., 1976, Differences in sensitivity to nerve growth factor of axon formation and tyrosine hydroxylase induction in cultured sympathetic neurons, Neuroscience 1:489.

    Article  PubMed  CAS  Google Scholar 

  • Hill, C.E., and Hendry, I.A., 1977, Development of neurons synthesizing noradrenaline, and acetylcholine in the superior cervical ganglion of the rat in vivo and in vitro, Neuroscience 2:741.

    Article  PubMed  CAS  Google Scholar 

  • Hill, C.E., Purves, R.D., Watanabe, H., and Burnstock, G., 1976, Specificity of Innervation of iris musculature by sympathetic nerve fibres in tissue culture, Pflügers Arch. 361:127.

    Article  PubMed  CAS  Google Scholar 

  • Hirst, G.D.S., and Spence, I., 1973, Calcium action potentials in mammalian peripheral neurons, Nature New Biol. 243:54.

    PubMed  CAS  Google Scholar 

  • Hooisma, J., Slaaf, D.N., Meeter, E., and Stevens, W.F., 1975, The Innervation of chick striated muscle fibers by the chick ciliary ganglion in tissue culture, Brain Res. 85:79.

    Article  PubMed  CAS  Google Scholar 

  • Horn, J.P., and McAfee, D.A., 1978, Norepinephrine antagonizes calcium-dependent potentials in rat sympathetic neurons, Neurosci. Abstr. 4:235.

    Google Scholar 

  • Jacobowitz, D., 1970, Catecholamine fluorescence studies of adrenergic neurons and chromaffin cells in sympathetic ganglia, Fed. Proc. 29:1929.

    PubMed  CAS  Google Scholar 

  • Jacobowitz, D.M., 1974, The peripheral autonomic system, in: The Peripheral Nervous System (J.I. Hubbard, ed.), pp. 87–110, Plenum Press, New York.

    Chapter  Google Scholar 

  • Jessen, K., McConnell, J., Purves, R., Burnstock, G., and Chamley-Campbell, J., 1978, Tissue culture of mammalian enteric neurons, Brain Res. 152:573.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, M., Ross, D., Meyers, M., Rees, R., Bunge, R.P., Wakshull, E., and Burton, H., 1976, Synaptic vesicle cytochemistry changes when cultured sympathetic neurons develop cholinergic interactions, Nature 262:308.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, J.I., Ross, C.D., Meyers, M., Spitznagel, E.L., and Bunge, R.P., 1980a, Morphological and biochemical studies on the development of cholinergic properties in cultured sympathetic neurons. I. Correlative changes in choline acetyltransferase and synaptic vesicle cytochemistry, J. Cell Biol. 84:680.

    Article  PubMed  CAS  Google Scholar 

  • Johnson, J.I., Ross, C.D., and Bunge, R.P., 1980b, Morphological and biochemical studies on the development of cholinergic properties in cultured sympathetic neurons. II. Dependence on postnatal age, J. Cell Biol. 84:692.

    Article  PubMed  CAS  Google Scholar 

  • Joö, F., Lever, J.D., Ivens, C., Mottram, D.R., and Presley, R., 1971, A fine structural and electron histochemical study of axon terminals in the rat superior cervical ganglion after acute and chronic preganglionic denervation, J. Anat. 110:181.

    PubMed  Google Scholar 

  • Katz, B., and Thesleff, S., 1957, A study of the “desensitization” produced by acetylcholine at the motor end plate, J. Physiol. (Lond.) 138:63.

    CAS  Google Scholar 

  • Kemplay, S.K., and Garrett, J.R., 1976, Effects of a heterologous cross-culture between the postganglionic sympathetic and the preganglionic parasympathetic nerve trunks of submandibular glands in cats, Cell Tissue Res. 167:197.

    Article  PubMed  CAS  Google Scholar 

  • Ko, C.-P., 1975, Electrophysiological Studies of Synaptic Transmission in Nerve Tissue Cultures of Rat Spinal Cord and Dissociated Superior Cervical Ganglion Neurons, Ph.D. Thesis, Washington University, St. Louis, Missouri.

    Google Scholar 

  • Ko, C.-P., Burton, H., and Bunge, R.P., 1976a, Synaptic transmission between rat spinal cord explants and dissociated superior cervical ganglion neurons in tissue culture, Brain Res. 117:437.

    Article  PubMed  CAS  Google Scholar 

  • Ko, C.-P., Burton, H., Johnson, M.I., and Bunge, R.P., 1976b, Synaptic transmission between rat superior cervical ganglion neurons in dissociated cell cultures, Brain Res. 117:461.

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi, H., Hashiguchi, T., and Ushiyama, N.S., 1978, Postsynaptic modulation of excitatory process in sympathetic ganglia by cyclic AMP, Nature 271:268.

    Article  PubMed  CAS  Google Scholar 

  • Koketsu, K., and Nishi, S., 1969, Calcium and action potentials of bullfrog sympathetic ganglion cells, J. Gen. Physiol. 53:608.

    Article  PubMed  CAS  Google Scholar 

  • Kuffler, S.W., and Yoshikami, D., 1975, The distribution of acetylcholine sensitivity at the postsynaptic membrane of vertebrate skeletal twitch muscles: Ionotophoretic mapping in the micron range, J. Physiol. (Lond.) 244:703.

    CAS  Google Scholar 

  • Landis, S.C., 1976, Rat sympathetic neurons and cardiac myocytes developing in micro-cultures: Correlation of the fine structure of endings with neurotransmitter function in single neurons, Proc. Natl. Acad. Sci. USA 73:4220.

    Article  PubMed  CAS  Google Scholar 

  • Landis, S.C., 1977, Morphological properties of the dendrites and axons of dissociated rat sympathetic neurons, Neurosci. Abstr. 3:525.

    Google Scholar 

  • Landis, S.C., MacLeish, P.R., Potter, D.D., Furshpan, E.J., and Patterson, P.H., 1976, Synapses formed between dissociated sympathetic neurons: The influence of conditioned medium, Neurosci. Abstr. 2:197.

    Google Scholar 

  • LeDouarin, N.M., and Teillet, M.A., 1974, Experimental analysis of the migration and differentiation of neuroblasts of the autonomic nervous system and of neuroectodermal mesenchymal derivatives, using a biological cell marking technique, Dev. Biol. 41:162.

    Article  CAS  Google Scholar 

  • LeDouarin, N.M., Renaud, D., Teillet, M.A., and LeDouarin, G., 1975, Cholinergic differentiation of presumptive adrenergic neuroblasts in interspecific chimeras after heterotropic transplantations, Proc. Natl. Acad. Sci. USA 72:728.

    Article  CAS  Google Scholar 

  • LeDouarin, N.M., Teillet, M.A., and LeLievre, C., 1977, Influence of the tissue environment on the differentiation of neural crest cells, in: Cell and Tissue Interactions (J. Lash and M. Burger, eds.), pp. 11–28, Raven Press, New York.

    Google Scholar 

  • LeDouarin, N.M., Teillet, M.A., Ziller, C., and Smith, J., 1978, Adrenergic differentiation of cells of the cholinergic ciliary and Remak ganglia in avian embryo after in vivo transplantation, Proc. Natl. Acad. Sci. USA 75:2030.

    Article  CAS  Google Scholar 

  • Levi, G., and Delorenzi, E., 1934, Transformazione degli elementi dei gangli spinali e simpatici cultivati in vitro, Arch. Ital. Anat. Embriol. 33:443.

    Google Scholar 

  • Levi-Montalcini, R., and Angeletti, P., 1963, Essential role of the nerve growth factor in the survival and maintenance of dissociated sensory and sympathetic nerve cells in vitro, Dev. Biol. 7:658.

    Article  Google Scholar 

  • Levi-Montalcini, R., Meyer, H., and Hamburger, V., 1954, In vitro experiments on the effects of mouse sarcomas 180 and 37 on the spinal and sympathetic ganglia of the chick embryo, Cancer Res. 14:49.

    PubMed  CAS  Google Scholar 

  • Lewis, W.H., and Lewis, M.R., 1912, The cultivation of sympathetic nerves from the intestine of chick embryos in saline solutions, Anat. Rec. 6:7.

    Article  Google Scholar 

  • Libet, B., 1975, The SIF cell as a functional dopamine-releasing interneuron in the rabbit superior cervical ganglion, in: SIF Cells: Structure and Function of the Small, Intensely Fluorescent Sympathetic Cells, Fogarty International Center Proceedings, No. 30 (O. Eränkö, ed.), pp. 163–177, U.S. Government Printing Office, Washington, D.C.

    Google Scholar 

  • Lichtman, J.W., 1977, The reorganization of synaptic connexions in the rat submandibular ganglion during postnatal development, J. Physiol. (Lond.) 273:155.

    CAS  Google Scholar 

  • Lichtman, J.W., Yip, J.W., and Purves, D., 1978, Segmentally selective Innervation of mammalian sympathetic ganglia: Relative roles of intraganglionic position and postganglionic targets, Neurosci. Abstr. 4:119.

    Google Scholar 

  • Mains, R.E., and Patterson, P.H., 1973a, Primary cultures of dissociated sympathetic neurons. I. Establishment of long-term growth in culture and studies of differentiated properties, J. Cell Biol. 59:329.

    Article  PubMed  CAS  Google Scholar 

  • Mains, R.E., and Patterson, P.H., 1973b, Primary cultures of dissociated sympathetic neurons. II. Initial studies on catecholamine metabolism, J. Cell Biol. 59:346.

    Article  PubMed  CAS  Google Scholar 

  • Mains, R.E., and Patterson, P.H., 1973c, Primary cultures of dissociated sympathetic neurons. III. Changes in metabolism with age in culture, J. Cell Biol. 59:361.

    Article  PubMed  CAS  Google Scholar 

  • Mark, G.E., Chamley, J.H., and Burnstock, G., 1973, Interactions between autonomic nerves and smooth and cardiac muscle cells in tissue culture, Dev. Biol. 32:194.

    Article  PubMed  CAS  Google Scholar 

  • Masurovsky, E., and Benitez, H., 1967, Apparent Innervation of chick cardiac muscle by sympathetic neurons in corganized culture, Anat. Rec. 157:285.

    Google Scholar 

  • Matsuda, Y., Yoshida, S., and Yonezawa, T., 1978, Tetrodotoxin sensitivity and Ca component of action potentials of mouse dorsal root ganglion cells cultured in vitro, Brain Res. 154:69.

    Article  PubMed  CAS  Google Scholar 

  • Matthews, M.B., and Raisman, G., 1969, The ultrastructure and somatic efferent synapses of small granule containing cells in the superior cervical ganglion, J. Anat. 105:255.

    PubMed  CAS  Google Scholar 

  • Matthews, M.R., 1974, Ultrastructure of ganglionic junctions, in: The Peripheral Nervous System (J.I. Hubbard, ed.), pp. 111–150, Plenum Press, New York.

    Chapter  Google Scholar 

  • Merrillees, N.C.R., 1968, The nervous environment of individual smooth muscle cells of the guinea pig vas deferens, J. Cell Biol. 37:794.

    Article  PubMed  CAS  Google Scholar 

  • Murray, M., and Stout, A., 1947, Adult human sympathetic ganglion cells cultivated in vitro, Am. J. Anat. 30:225.

    Article  Google Scholar 

  • Neale, E.A., MacDonald, R.L., and Nelson, P.G., 1978, Intracellular horseradish peroxidase injection for correlation of light and electron microscopic anatomy with synaptic physiology of cultured mouse spinal cord neurons, Brain Res. 152:265.

    Article  PubMed  CAS  Google Scholar 

  • Nishi, R., and Berg, D.K., 1977, Dissociated ciliary ganglion neurons in vitro: Survival and synapse formation, Proc. Natl. Acad. Sci. USA 74:5171.

    Article  PubMed  CAS  Google Scholar 

  • Nishi, R., and Berg, D.K., 1979, Survival and development of ciliary ganglion neurones grown alone in cell culture, Nature 277:232.

    Article  PubMed  CAS  Google Scholar 

  • Nishi, S., 1974, Ganglionic transmission, in: The Peripheral Nervous System (J.I. Hubbard, ed.), pp. 225–255, Plenum Press, New York.

    Chapter  Google Scholar 

  • Njå, A., and Purves, D., 1977a, Specific Innervation of guinea-pig superior cervical ganglion cells by preganglionic fibres arising from different levels of the spinal cord, J. Physiol. (Lond.) 264:565.

    Google Scholar 

  • Njå, A., and Purves, D., 1977b, Re-innervation of guinea-pig superior cervical ganglion cells by preganglionic fibres arising from different levels of the spinal cord, J. Physiol. (Lond.) 272:633.

    Google Scholar 

  • Njå, A., and Purves, D., 1978, Specificity of initial synaptic contacts made on guinea-pig superior cervical ganglion cells during regeneration of the cervical sympathetic trunk, J. Physiol. (Lond.) 281:45.

    Google Scholar 

  • Nurse, C.A., and O’Lague, P.H., 1975, Formation of cholinergic synapses between dissociated sympathetic neurons and skeletal myotubes of the rat in cell culture, Proc. Natl. Acad. Sci. USA 75:1955.

    Article  Google Scholar 

  • Obata, K., 1974, Transmitter sensitivities of some nerve and muscle cells in culture, Brain Res. 73:71.

    Article  PubMed  CAS  Google Scholar 

  • Okun, L.M., 1972, Isolated dorsal root ganglion neurons in culture: Cytological maturation and extension of electrically active processes, J. Neurobiol. 3:111.

    Article  PubMed  CAS  Google Scholar 

  • O’Lague, P.H., Obata, K., Claude, P., Furshpan, E.G., and Potter, D.D., 1974, Evidence for cholinergic synapses between dissociated rat sympathetic neurons in cell culture, Proc. Natl. Acad. Sci. USA 71:3602.

    Article  PubMed  Google Scholar 

  • O’Lague, P.H., MacLeish, P.R., Nurse, C.A., Claude, P., Furshpan, E.J., and Potter, D.D., 1976, Physiological and morphological studies on developing sympathetic neurons in dissociated cell culture, Cold Spring Harbor Symp. Quant. Biol. XL:399.

    Article  Google Scholar 

  • O’Lague, P.H., Potter, D.D., and Furshpan, E.J., 1978a, Studies on rat sympathetic neurons developing in cell culture. I. Growth characteristics and electrophysiological properties, Dev. Biol. 67:384.

    Article  PubMed  Google Scholar 

  • O’Lague, P.H., Furshpan, E.J., and Potter, D.D., 1978b, Studies on rat sympathetic neurons developing in cell culture. II. Synaptic mechanisms, Dev. Biol. 67:404.

    Article  PubMed  Google Scholar 

  • O’Lague, P.H., Potter, D.D., and Furshpan, E.G., 1978c, Studies on rat sympathetic neurons developing in cell culture. III. Cholinergic transmission, Dev. Biol. 67:424.

    Article  PubMed  Google Scholar 

  • Olson, M.I., and Bunge, R.P., 1973, Anatomical observations on the specificity of synapse formation in tissue culture, Brain Res. 59:19.

    Article  PubMed  CAS  Google Scholar 

  • Patterson, P.H., 1978, Environmental determination of autonomic neurotransmitter functions, Ann. Rev. Neurosci. 1:1.

    Article  PubMed  CAS  Google Scholar 

  • Patterson, P.H., and Chun, L.L.Y., 1974, The influence of non-neuronal cells on catecholamine and acetylcholine synthesis and accumulation in cultures of dissociated sympathetic neurons, Proc. Natl. Acad. Sci. USA 71:3607.

    Article  PubMed  CAS  Google Scholar 

  • Patterson, P.H., and Chun, L.L.Y., 1977a, The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. I. Effects of conditioned medium, Dev. Biol. 56:263.

    Article  PubMed  CAS  Google Scholar 

  • Patterson, P.H., and Chun, L.L.Y., 1977b, The induction of acetylcholine synthesis in primary cultures of dissociated rat sympathetic neurons. II. Developmental aspects, Dev. Biol. 60:473.

    Article  PubMed  CAS  Google Scholar 

  • Patterson, P.H., Reichardt, L.F., and Chun, L.L.Y., 1976, Biochemical studies on the development of primary sympathetic neurons in cell culture, Cold Spring Harbor Symp. Quant. Biol. XL:389.

    Article  Google Scholar 

  • Patterson, P.H., Chun, L.L.Y., and Reichardt, L.F., 1977, The role of non-neuronal cells in the development of sympathetically derived neurons, in: Progress in Clinical and Biological Research, Vol. 15, Cellular Neurobiology (Z. Hall, R. Kelly, and C.F. Fox, eds.), pp. 95–103, Alan R. Liss, New York.

    Google Scholar 

  • Perri, V., Sacchi, O., and Casella, C., 1970, Electrical properties and synaptic connections of the sympathetic neurons in the rat and guinea pig superior cervical ganglion, Pflügers Arch. 314:40.

    Article  PubMed  CAS  Google Scholar 

  • Phillis, J.W., 1970, The Pharmacology of Synapses, Wheaton and Co., Exeter.

    Google Scholar 

  • Purves, D., 1976, Competitive and non-competitive re-innervation of mammalian sympathetic neurones by native and foreign fibres, J. Physiol. (Lond.) 261:453.

    CAS  Google Scholar 

  • Purves, D., and Lichtman, J.S., 1978, Formation and maintenance of synaptic connections in autonomic ganglia, Physiol. Rev. 58:821.

    PubMed  CAS  Google Scholar 

  • Purves, D., and Njå, A., 1976, Effect of nerve growth factor on synaptic depression after axotomy, Nature 260:535.

    Article  PubMed  CAS  Google Scholar 

  • Purves, D., Lichtman, J.W., and Yip, J.W., 1978, Segmentally selective Innervation of mammalian sympathetic ganglia: Further evidence for the importance of postganglionic target position, Neurosci. Abstr. 4:124.

    Google Scholar 

  • Purves, R.D., Hill, D.E., Chamley, J.H., Mark, G.E., Fry, D.M., and Burnstock, G., 1974, Functional autonomic neuromuscular junctions in tissue culture, Pflügers Arch. 350:1.

    Article  PubMed  CAS  Google Scholar 

  • Raisman, G., Field, P.M., Östberg, A.-J.C., Iversen, L.L., and Zigmond, R.E., 1974, A quantitative ultrastructural and biochemical analysis of the process of reinnervation of the superior cervical ganglion in the adult rat, Brain Res. 71:1.

    Article  PubMed  CAS  Google Scholar 

  • Rees, R., and Bunge, R.P., 1974, Morphological and cytochemical studies of synapses formed in culture between isolated rat superior cervical ganglion neurons, J. Comp. Neurol. 157:1.

    Article  PubMed  CAS  Google Scholar 

  • Rees, R.P., Bunge, M.B., and Bunge, R.P., 1976, Morphological changes in the neuritic growth cone and target neuron during synaptic junction development in culture, J. Cell Biol. 68:240.

    Article  PubMed  CAS  Google Scholar 

  • Reichardt, L.F., and Patterson, P.H., 1977, Neurotransmitter synthesis and uptake by isolated sympathetic neurones in microcultures, Nature 270:147.

    Article  PubMed  CAS  Google Scholar 

  • Roper, S., 1976a, An electrophysiological study of chemical and electrical synapses on neurones in the parasympathetic cardiac ganglion of the mud puppy, Necturus maculosus: Evidence for intrinsic ganglionic Innervation, J. Physiol. (Lond.) 254:427.

    CAS  Google Scholar 

  • Roper, S., 1976b, The acetylcholine sensitivity of the surface membrane of multiply-innervated para-sympatehtic ganglion cells in the mudpuppy before and after partial denervation, J. Physiol. (Lond.) 254:455.

    CAS  Google Scholar 

  • Ross, D., and Bunge, R.P., 1976, Choline acetyltransferase in cultures of rat superior cervical ganglion, Neurosci. Abstr. 2:769.

    Google Scholar 

  • Ross, D., Johnson, M., and Bunge, R., 1977, Development of cholinergic characteristics in adrenergic neurones is age dependent, Nature 267:536.

    Article  PubMed  CAS  Google Scholar 

  • Sargent, P.B., and Dennis, M.J., 1977, Formation of synapses between parasympathetic neurones deprived of preganglionic Innervation, Nature 268:456.

    Article  PubMed  CAS  Google Scholar 

  • Shimada, Y., and Fischman, D., 1973, Morphological and physiological evidence for the development of functional neuromuscular junctions in vitro, Dev. Biol. 31:200.

    Article  PubMed  CAS  Google Scholar 

  • Silberstein, S., Johnson, D., Jacobowitz, D., and Kopin, I., 1971, Sympathetic reinnervation of the rat iris in organ culture, Proc. Natl. Acad. Sci. USA 68:1121.

    Article  PubMed  CAS  Google Scholar 

  • Sjöqvist, F., 1963, The correlation between the occurrence and localization of acetylcholinesterase-rich cell bodies in the stellate ganglion and the outflow of cholinergic sweat secretory fibers to the forepaw of the cat, Acta Physiol. Scand. 57:339.

    Article  PubMed  Google Scholar 

  • Szantroch, Z., 1933, Beobachtung an den Kulturen des Sympathetikus. Ergebnisse der Zuchtung des Remakschen Darmnerven, Arch. Exp. Zellforsch. 14:442.

    Google Scholar 

  • Tamarind, D.L., and Quilliam, J.P., 1971, Synaptic organization and other ultrastructural features of the superior cervical ganglion of the rat, kitten, and rabbit, Micron 2:204.

    Google Scholar 

  • Tashiro, N., and Nishi, S., 1972, Effects of alkali-earth cations on sympathetic ganglion cells of the rabbit, Life Sci. 11:941.

    Article  CAS  Google Scholar 

  • Thompson, W., Njå, A., and Purves, D., 1978, Effects of postganglionic axotomy on the regeneration of selective synaptic connections in the guinea-pig superior cervical ganglion, Neurosci. Abstr. 4:128.

    Google Scholar 

  • Tuttle, J., Ard, M., and Suszkiw, J., 1978, Neuronal survival and cat activity in dissociated cell cultures of ciliary ganglion, Neurosci. Abstr. 4:596.

    Google Scholar 

  • Uehara, Y., Campbell, G.R., and Burnstock, G., 1976, Muscle and its Innervation, Edward Arnold, London.

    Google Scholar 

  • Varon, S., and Raiborn, C., 1971, Excitability and conduction in neurons of dissociated ganglionic cell cultures, Brain Res. 30:83.

    Article  PubMed  CAS  Google Scholar 

  • Volle, R.L., 1969, Ganglionic transmission, Annu. Rev. Pharmacol. 9:135.

    Article  PubMed  CAS  Google Scholar 

  • Wakshull, E.M., 1978, Studies on the in Vitro Development of Rat Sympathetic Neurons, Ph.D. Thesis, Washington University, St. Louis, Missouri.

    Google Scholar 

  • Wakshull, E.M., Johnson, J.I., and Burton, H., 1978, Persistence of an amine uptake system in cultured rat sympathetic neurons which use acetylcholine as their transmitter, J. Cell Biol. 79:121.

    Article  PubMed  CAS  Google Scholar 

  • Wakshull, E.M., Johnson, M.I., and Burton, H., 1979a, Postnatal rat sympathetic neurons in culture. I. A comparison with embryonic neurons, J. Neurophysiol. 42:1410.

    PubMed  CAS  Google Scholar 

  • Wakshull, E.M., Johnson, M.I., and Burton, H., 1979b, Postnatal rat sympathetic neurons in culture. II. Synaptic transmission by postnatal neurons, J. Neurophysiol. 42:1426.

    PubMed  CAS  Google Scholar 

  • Walicke, P.A., Campenot, R.B., and Patterson, P.H., 1977, Determination of transmitter function by neuronal activity, Proc. Natl. Acad. Sci. USA 74:5767.

    Article  PubMed  CAS  Google Scholar 

  • Weight, F.F., 1971, Mechanisms of synaptic transmission, in: Neurosciences Research, Vol. 4 (S. Ehrenpreis and O.C. Solnitzky, eds.), pp. 1–27, Academic Press, New York.

    Google Scholar 

  • Weston, J., 1970, The migration and differentiation of neural crest cells, Adv. Morphol. 8:41.

    CAS  Google Scholar 

  • Williams, T.H., and Palay, S.L., 1969, Ultrastructure of the small neurons in the superior cervical ganglion, Brain Res. 15:17.

    Article  PubMed  CAS  Google Scholar 

  • Yamauchi, A., Lever, J.D., and Kemp, K.W., 1973, Catecholamine loading and depletion in the rat superior cervical ganglion: A formol fluorescence and enzyme histochemical study with numerical assessments, J. Anat. 114:271.

    PubMed  CAS  Google Scholar 

  • Yarowsky, P., and McAfee, D.A., 1977, Calcium dependent potentials in the rat superior cervical ganglion, Neurosci. Abstr. 3:25.

    Google Scholar 

  • Yip, J.W., Purves, D., and Lichtman, J.W., 1978, Segmentally selective Innervation of mammalian sympathetic ganglia: Comparative Innervation of cervical and thoracic ganglia, Neurosci. Abstr. 4:130.

    Google Scholar 

  • Yokota, R., and Yamauchi, A., 1974, Ultrastructure of the mouse superior cervical ganglion with particular reference to the pre-and postganglionic elements covering the soma of its principal neurons, Am. J. Anat. 140:281.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Anatomy and Neurobiology, Washington University School of Medicine, St. Louis, Missouri, 63130, USA

    Harold Burton & Richard P. Bunge

Authors
  1. Harold Burton
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Richard P. Bunge
    View author publications

    You can also search for this author in PubMed Google Scholar

Editor information

Editors and Affiliations

  1. Laboratory of Developmental Neurobiology, National Institute of Child Health and Human Development, National Institutes of Health, Bethesda, Maryland, 20205, USA

    Phillip G. Nelson

  2. Department of Physiology, Duke University Medical Center, Durham, North Carolina, 27710, USA

    Melvyn Lieberman

Rights and permissions

Reprints and permissions

Copyright information

© 1981 Plenum Press, New York

About this chapter

Cite this chapter

Burton, H., Bunge, R.P. (1981). The Expression of Cholinergic and Adrenergic Properties by Autonomic Neurons in Tissue Culture. In: Nelson, P.G., Lieberman, M. (eds) Excitable Cells in Tissue Culture. Springer, Boston, MA. https://doi.org/10.1007/978-1-4684-3803-1_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-4684-3803-1_1

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4684-3805-5

  • Online ISBN: 978-1-4684-3803-1

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics

Search

Navigation