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The Development of Primary Sensory Neurons

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The Primary Afferent Neuron

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Abstract

Primary sensory neurons originate from progenitor cells of ectodermal origin. These progenitors migrate to the sites of developing sensory ganglia where they differentiate. Sensory neurons are initially bipolar and extend two axonal processes in opposite directions towards their peripheral and central target fields. The innervation of these target fields is associated with a period of neuronal death during which superfluous neurons are eliminated followed by a period of modification and refinement of connections.

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References

  • Barde, Y. A., Edgar, D., and Thoenen, H., 1982, Purification of a new neurotrophic factor from mammalian brain, Embo J., 1:549–553

    PubMed  CAS  Google Scholar 

  • Baroffio, A., Dupin, E., and Le Douarin, N. M., 1988, Clone-forming ability and differentiation potential of migratory crest cells, Proc. Natl. Acad. Sci. USA, 85:5325–5329

    Article  PubMed  CAS  Google Scholar 

  • Bronner-Fraser, M., and Fraser, S. E., 1988, Cell lineage analysis reveals multipotency of some avian neural crest cells, Nature, 335:161–164

    Article  PubMed  CAS  Google Scholar 

  • D’Amico-Martel, A., and Noden, D. M., 1983, Contributions of placodal and neural crest cells to avian cranial peripheral ganglia, Am. J. Anat., 166:445–468

    Article  PubMed  Google Scholar 

  • Davies, A. M., 1986, The survival and growth of embryonic proprioceptive neurons is promoted by a factor present in skeletal muscle, Dev. Biol., 115:56–67

    Article  PubMed  CAS  Google Scholar 

  • Davies, A. M., 1987, Molecular and cellular aspects of patterning sensory neurone connections in the vertebrate nervous system, Development, 101:185–208

    PubMed  CAS  Google Scholar 

  • Davies, A. M., 1988, Role of neurotrophic factors in development, Trends Genetics, 4:139–143

    Article  CAS  Google Scholar 

  • Davies, A. M., 1989, Intrinsic differences in the growth rate of early nerve fibres related to target distance, Nature, 337:553–555

    Article  PubMed  CAS  Google Scholar 

  • Davies, A. M., Bandtlow, C., Heuman, R., Korsching, S., Rohrer, H., and Thoenen, H., 1987, Timing and site of nerve growth factor synthesis in developing skin in relation to innervation and expression of the receptor, Nature, 326:353–358

    Article  PubMed  CAS  Google Scholar 

  • Davies, A. M., and Lindsay, R. M., 1985, The avian cranial sensory ganglia in culture, Devl. Biol., 111:62–72

    Article  CAS  Google Scholar 

  • Davies, A. M., and Lumsden, A. G. S., 1984, Relation of target encounter and neuronal death to nerve growth factor responsiveness in the developing mouse trigeminal ganglion, J. Comp. Neurol., 253:13–24

    Article  Google Scholar 

  • Davies, A. M., Lumsden, A. G. S., and Rohrer, H., 1987, Neural crest-derived proprioceptive neurons express NGF receptors but are not supported by NGF in culture, Neuroscience, 20:37–46

    Article  PubMed  CAS  Google Scholar 

  • Davies, A. M., Thoenen, H., and Barde, Y. A., 1986, Different factors from the central nervous system and periphery regulate the survival of sensory neurones, Nature, 319:497–499

    Article  PubMed  CAS  Google Scholar 

  • Davies, A. M., Thoenen, H., and Barde, Y. A., 1986, The response of chick sensory neurons to brain-derived neurotrophic factor, J. Neurosci., 6:1897–1904

    PubMed  CAS  Google Scholar 

  • Davies, A. M., Thoenen, H., and Barde, Y. A., 1986, The response of chick sensory neurons to brain-derived neurotrophic factor, J. Neurosci., 6:1897–1904

    PubMed  CAS  Google Scholar 

  • Dodd, J., and Jessell, T. M., 1985, Lactoseries carbohydrates specify subsets of sensory dorsal root ganglion neurons projecting to the superficial dorsal horn of the rat spinal cord, J. Neurosci., 5:3278–3294

    PubMed  CAS  Google Scholar 

  • Dodd, J., and Jessell, T. M., 1986, Cell surface glycoconjugates and carbohydrate binding proteins: possible recognition signals in sensory neurone development, J. Exp. Biol., 124:225–238

    PubMed  CAS  Google Scholar 

  • Ernsberger, U., and Rohrer, H., 1988, Neuronal precursor cells in chick dorsal root ganglia: Differentiation and survival in vitro, Dev. Biol., 126:420–432

    Article  PubMed  CAS  Google Scholar 

  • Ferguson, B. A., 1983, Development of motor innervation of the chick following dorso-ventral limb bud rotations, J. Neurosci., 3:1760–1772

    PubMed  CAS  Google Scholar 

  • Gundersen, R., and Barrett, J. N., 1979, Neuronal chemotaxis: chick dorsal root axons turn towards high concentrations of nerve growth factor, Science, 206:1079–1080

    Article  PubMed  CAS  Google Scholar 

  • Harris, W. A., 1986, Homing behaviour of axons in the embryonic vertebrate brain, Nature, 320:266–269

    Article  PubMed  CAS  Google Scholar 

  • Hofer, M. M., and Barde, Y. A., 1988, Brain-derived neurotrophic factor prevents neuronal death in vivo, Nature, 331:261–262

    Article  PubMed  CAS  Google Scholar 

  • Honig, M. G., Lance-Jones, C., and Landmesser, L., 1986, The development of sensory projection patterns in embryonic chick hind limb under experimental conditions, Dev. Biol., 118:532–548

    Article  PubMed  CAS  Google Scholar 

  • Kalcheim, C., Barde, Y. A., Thoenen, H., and Le Douarin, N. M., 1987, In vivo effect of brain-derived neurotrophic factor on the survival of developing dorsal root ganglion cells, Embo J., 6:2871–2873

    PubMed  CAS  Google Scholar 

  • Kalcheim, C., and Le Douarin, N. M., 1986, Requirement of a neural tube signal for the differentiation of neural crest cells into dorsal root ganglia, Dev. Biol., 116:451–466

    Article  PubMed  CAS  Google Scholar 

  • Korsching, S., and Thoenen, H., 1985, Nerve growth factor supply for sensory neurons: site of origin and competition with the sympathetic nervous system, Neurosci. Lett., 39:1–4

    Article  Google Scholar 

  • Lance-Jones, C., and Landmesser, L., 1980, Motoneuron projection patterns in the chick hind limb following early partial spinal cord reversals, J. Physiol. (Lond.), 302:581–602

    CAS  Google Scholar 

  • Landmesser, L., 1984, The development of specific motor pathways in the chick embryo, Trends Neurosci., 7:336–339

    Article  Google Scholar 

  • Landmesser, L., and Honig, M. G., 1986, Altered sensory projections in the chick hind limb following early removal of motoneurons, Dev. Biol., 118:511–531

    Article  PubMed  CAS  Google Scholar 

  • Le Douarin, N. M., 1982, “The Neural Crest,” Cambridge University Press, London, New York.

    Google Scholar 

  • Le Douarin, N. M., 1984, A model for cell line divergence in the ontogeny of the peripheral nervous system, in: “Cellular and Molecular Biology of Neuronal Development,” I.B. Black, ed., Plenum, New York: 3–28

    Google Scholar 

  • Le Douarin, N. M., 1986, Cell line segregation during peripheral nervous system ontogeny, Science, 231:1515–1522

    Article  PubMed  Google Scholar 

  • Le Douarin, N. M., Fontaine-Perus, J., and Couly, G., 1986, Cephalic ectodermal placodes and neurogenesis, Trends Neurosci., 9:175–180

    Article  Google Scholar 

  • Levi-Montalcini, R., 1982, Developmental neurobiology and the natural history of nerve growth factor, A. Rev. Neurosci., 5:341–362

    Article  CAS  Google Scholar 

  • Levi-Montalcini, R., and Angeletti, P. U., 1968, Nerve growth factor, Physiol Rev., 48:534–569

    PubMed  CAS  Google Scholar 

  • Lindsay, R. M., and Rohrer, H., 1985, Placodal sensory neurons in culture: nodose ganglion neurons are unresponsive to NGF, lack NGF receptors but are supported by a liver-derived neurotrophic factor, Dev. Biol., 112:30–48

    Article  PubMed  CAS  Google Scholar 

  • Lindsay, R. M., Thoenen, H., and Barde, Y. A., 1985, Placode and neural crest-derived sensory neurons are responsive at early developmental stages to brain-derived neurotrophic factor. Dev. Biol., 112:319–328

    Article  PubMed  CAS  Google Scholar 

  • Lumsden, A. G. S., and Davies, A. M., 1983, Earliest sensory nerve fibres are guided to peripheral targets by attractants other than nerve growth factor, Nature, 306:786–788

    Article  PubMed  CAS  Google Scholar 

  • Lumsden, A. G. S., and Davies, A. M., 1986, Chemotropic effect of specific target epithelium in development of the mammalian nervous system, Nature, 323:538–539

    Article  PubMed  CAS  Google Scholar 

  • Lumsden, A. G. S., and Davies, A. M., 1987, Chemotropic influence of specific target epithelium on the growth of embryonic sensory neurites, in: “Epithelial-mesenchymal interactions in neural development,” J.R. Wolfe and J. Sievers, eds., NATO-ASI Series, H5:323–340

    Google Scholar 

  • McMahon, S. B., and Gibson, S., 1987, Peptide expression is altered when afferent nerves reinnervate inappropriate tissue, Neurosci. Lett., 73:9–15

    Article  PubMed  CAS  Google Scholar 

  • Menesini-Chen, M. G., Chen, J. S., and Levi-Montalcini, R., 1978, Sympathetic nerve fiber in growth in the central nervous system of neonatal rodents upon intracerebral NGF injections, Arch. Ital. Biol., 116:53–84

    PubMed  CAS  Google Scholar 

  • Narayanan, C. H., and Narayanan, Y., 1978, Determination of the embryonic origin of the mesencephalic nucleus of the trigeminal nerve in birds, J. Embryol. Exp. Morph., 43:85–105

    PubMed  CAS  Google Scholar 

  • Noden, D. M., 1978, The control of avian cephalic neural crest cytodifferentiation. II. Neural tissues, Dev. Biol., 67:313–329

    Article  PubMed  CAS  Google Scholar 

  • Oppenheim, R. W., 1981, Neuronal death and some related phenomena during neurogenesis: A selected historical review and progress report, in: “Studies in Developmental Biology,” W.M. Cowan, ed., Oxford University Press: 74–133

    Google Scholar 

  • Pearson, J., Johnson, E. M., and Brandeis, L., 1983, Effects of antibodies to nerve growth factor on intra uterine development of derivates of cranial neural crest and placode in the guinea pig, Dev. Biol., 96:32–36

    CAS  Google Scholar 

  • Regan, L., Dodd, J., Barondes, S., and Jessell, T. M., 1986, Selective expression of endogenous lactose-binding and lactoseries glycoconjugates in subsets of rat sensory neurons, Proc. Natl. Acad. Sci. USA, 83:2248–2252

    Article  PubMed  CAS  Google Scholar 

  • Roberts, W. J., and Elardo, S. M., 1986, Clustering of primary afferent fibers in peripheral nerve fascicles by sensory modality, Brain Res., 370:149–152

    Article  PubMed  CAS  Google Scholar 

  • Rush, R. A., 1984, Immunohistochemical localization of endogenous nerve growth factor, Nature, 312:364–367

    Article  PubMed  CAS  Google Scholar 

  • Rutishauser, U., and Jessell, T. M., 1988, Cell adhesion molecules in vertebrate neural development, Physiol Rev., 68:819–857

    PubMed  CAS  Google Scholar 

  • Schroeter, S., Pkrzywinski, J. A., and Tosney, K. W., 1988, Mesenchymal cell death delineates axon pathways in the hind limb and does so independently of neural interactions, Soc. Neurosci. Abst., 14:870

    Google Scholar 

  • Scott, S. A., 1982, The development of the segmental pattern of skin sensory innervation in embryonic chick hind limb, J. Physiol. (Lond.), 330:203–230

    CAS  Google Scholar 

  • Scott, S. A., 1986, Skin sensory innervation patterns in embryonic chick hind limb following dorsal root ganglion reversals, J. Neurobiol., 17:649–668

    Article  PubMed  CAS  Google Scholar 

  • Scott, S. A., 1988, Skin sensory innervation patterns in embryonic chick hind limbs deprived of motoneurons, Dev. Biol., 126:362–374

    Article  PubMed  CAS  Google Scholar 

  • Smith, C. L., and Frank, E., 1987, Peripheral specification of sensory neurons transplanted to novel locations along the neuraxis, J. Neurosci., 7:1537–1549

    PubMed  CAS  Google Scholar 

  • Smith, C. L., and Frank, E., 1988, Specifity of sensory projections to the spinal cord during development in bullfrogs, J. Comp. Neurol., 269:96–108

    Article  PubMed  CAS  Google Scholar 

  • Swanson, G. J., and Lewis, J. H., 1986, Sensory nerve routes in chick wing buds deprived of motor innervation, J. Embryol. Exp. Morph., 95:37–52

    PubMed  CAS  Google Scholar 

  • Thoenen, H., and Barde, Y. A., 1980, Physiology of nerve growth factor, Ann. Rev. Neurosci., 60:284–335

    Google Scholar 

  • Tosney, K. W., and Landmesser, L., 1984, Pattern and specifity of axonal outgrowth following varying degrees chick limb bud ablation, J. Neurosci., 4:2518–2527

    PubMed  CAS  Google Scholar 

  • Tosney, K. W., Watanabe, M., Landmesser, L., and Rutishauser, U., 1986, The distribution of N-CAM in the chick hind limb during axon outgrowth and synaptogenesis, Dev. Biol., 114:437–452

    Article  PubMed  CAS  Google Scholar 

  • Yip, H. K., and Johnson, E. M., 1984, Developing dorsal root ganglion neurons require trophic support from their central processes: Evidence for a role of retrogradely transported nerve growth factor from the central nervous system to the periphery, Proc. Natl. Acad. Sci. USA, 81:6245–6249

    Article  PubMed  CAS  Google Scholar 

  • Ziller, C., Fauquet, M., Kalcheim, C, Smith, J., and Le Douarin, N. M., 1987, Cell lineages in peripheral nervous system ontogeny: medium-induced modulation of neuronal phenotypic expression in neural crest cell cultures, Dev. Biol., 120:101–111

    Article  PubMed  CAS  Google Scholar 

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Author information

Authors and Affiliations

  1. Department of Anatomy, St. George’s Hospital Medical School, London, England

    Alun M. Davies

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  1. Alun M. Davies
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Editors and Affiliations

  1. Institute of Anatomy, University of Zurich-Irchel, Zurich, Switzerland

    Wolfgang Zenker  & Winfried L. Neuhuber  & 

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© 1990 Plenum Press, New York

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Davies, A.M. (1990). The Development of Primary Sensory Neurons. In: Zenker, W., Neuhuber, W.L. (eds) The Primary Afferent Neuron. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-0579-8_10

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  • DOI: https://doi.org/10.1007/978-1-4613-0579-8_10

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4612-7875-7

  • Online ISBN: 978-1-4613-0579-8

  • eBook Packages: Springer Book Archive

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