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Proliferation patterns of dorsal root ganglion neurons of cutaneous, muscle and visceral nerves in the rat

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Journal of Neurocytology

Abstract

In a previous study we provided evidence that dorsal root ganglion (DRG) neurons of different phenotypes have different birthdates. The present study aimed at determining if birthdates of DRG neurons are related to different types of peripheral nerves, namely cutaneous versus muscle, and somatic versus visceral. Pregnant rats were injected intraperitoneally with bromodeoxyuridine (BrdU) to label the neurons on one of the embryonic days E12–E16. When the progeny rats reached adulthood, a mixture of 1% B-fragment of cholera toxin and 1% isolectin B4 from Griffonia simplicifolia I was injected into the peripheral nerves, or a 5% Fluoro-Gold solution was applied to the transected end of the nerves. The saphenous and sural nerves were used as cutaneous nerves, the gastrocnemius nerve as a muscle nerve, the intercostal nerves T9–11 as somatic nerves and the greater splanchnic nerve as a visceral nerve. Cell size measurements were made of DRG neurons labeled from the two cutaneous nerves and the muscle nerve, as well as of neurons of the saphenous and gastrocnemius nerves labeled by BrdU at different embryonic stages. Most of the DRG neurons of the muscle and intercostal nerves were generated early, with peaks at E13, and those of the cutaneous and visceral afferent nerves later, with peaks at E14. The temporal differences were reflected in the cell size spectrum, the muscle nerve having a greater proportion of large neurons compared to the cutaneous nerves. The findings add to previous knowledge regarding the sequence of development of different DRG phenotypes.

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References

  • Altman, J. & Bayer, S. A. (1984) The development of the rat spinal cord. In Advances in Anatomy, Embryology and Cell Biology (edited by Beck, F., Hild, L. W., van Limborgh, J., Ortmann, R., Pauly, J. E. & Schiebler, T. H.) Vol. 85. Berlin: Springer Verlag.

    Google Scholar 

  • Harsh, C., Archibald, S. J. & Madison, R. D. (1991) Double-labeling of saphenous nerve neuron pools: A model for determining the accuracy of axon regeneration at the single neuron level. Journal of Neuroscience Methods 39, 123–130.

    PubMed  Google Scholar 

  • Johnson, G. D. & Nogueira Araujo, G. M. de C. (1981). Simple method of reducing fading of immunofluorescence during microscopy. Journal of Immunological Methods 43, 349–350.

    PubMed  Google Scholar 

  • Kitao, Y., Robertson, B., Kudo, M. & Grant, G. (1996) Neurogenesis of subpopulations of rat lumbar dorsal root ganglion neurons including neurons projecting to the dorsal column nuclei. Journal of Comparative Neurology 371, 249–257.

    PubMed  Google Scholar 

  • Lamotte, C. C., Kapadia, S. E. & Shapiro, C. M. (1991) Central projections of the sciatic, saphenous, median and ulnar nerves of the rat demonstrated by transganglionic transport of choleragenoid-HRP (B-HRP) and wheat germ agglutinin-HRP (WGA-HRP). Journal of Comparative Neurology 311, 546–562.

    PubMed  Google Scholar 

  • Lawson, S. N. (1992) Morphological and biochemical cell types of sensory neurons. In Sensory Neurons, Diversity, Development and Plasticity (edited by Scott, S. A.) pp. 27–59. New York, Oxford: Oxford University Press.

    Google Scholar 

  • Lawson, S. N. & Biscoe, T. J. (1979) Development of mouse dorsal root ganglia: An autoradiographic and quantitative study. Journal of Neurocytology 8, 265–274.

    PubMed  Google Scholar 

  • Lawson, S. N., Caddy, K. W. T. & Biscoe, T. J. (1974) Development of rat dorsal root ganglion neurons. Studies of birth dates and changes in mean cell diameter. Cell and Tissue Research 153, 399–413.

    PubMed  Google Scholar 

  • Marti, E., Gibson, S. J., Polak, J. M., Facer, P., Springall, D. R., van Aswegen, G., Aitchison, M. & Koltzenburg, M. (1987) Ontogeny of peptide-and amine-containing neurons in motor, sensory and autonomic regions of rat and human spinal cord, dorsal root ganglia, and rat skin. Journal of Comparative Neurology 266, 332–359.

    PubMed  Google Scholar 

  • Mirnics, K. & Koerber, H. R. (1995). Prenatal development of rat primary afferent fibers: I. Peripheral projections. Journal of Comparative Neurology 355, 589–600.

    PubMed  Google Scholar 

  • Noguchi, K., Kawai, Y., Fukuoka, T., Senba, E. & Miki, K. (1995) Substance P induced by peripheral nerve injury in primary afferent neurons and its effect on dorsal column nucleus neurons. Journal of Neuroscience 15, 7633–7643.

    PubMed  Google Scholar 

  • Nornes, H. O. & Das, G. D. (1974) Temporal pattern of neurogenesis in spinal cord of rat. I.Anautoradiographic study—Time and sites of origin and migration and settling patterns of neuroblasts. Brain Research 73, 121–138.

    PubMed  Google Scholar 

  • Perry, M. J. & Lawson, S. N. (1998) Differences in expression of oligosaccharides, neuropeptides, carbonic anhydrase and neurofilament in rat primary afferent neurons retrogradely labelled via skin, muscle or visceral nerves. Neuroscience 85, 293–310.

    PubMed  Google Scholar 

  • Rivero-MeliÁn, C. (1996) Organization of hindlimb nerve projections to the rat spinal cord: A choleragenoid horseradish peroxidase study.Journal of Comparative Neurology 364, 651–663.

    PubMed  Google Scholar 

  • Rivero-MeliÁn, C. & Grant, G. (1991) Choleragenoid horseradish peroxidase used for studying projections of some hindlimb cutaneous nerves and plantar foot afferents to the dorsal horn and Clarke's column in the rat. Experimental Brain Research 84, 125–132.

    Article  Google Scholar 

  • Robertson, B. & Grant, G. (1989) Immunocytochemical evidence for the localization of the GM1 ganglioside in carbonic anhydrase-containing and RT97immunoreactive rat primary sensory neurons. Journal of Neurocytology 18, 77–86.

    PubMed  Google Scholar 

  • Robertson, B., Perry, M. J. & Lawson, S. N. (1991) Populations of rat spinal primary afferent neurons with choleragenoid binding compared with those labelled by markers for neurofilament and carbohydrate groups: A quantitative immunocytochemical study. Journal of Neurocytology 20, 367–395.

    Article  Google Scholar 

  • Silverman, J. D. & Kruger, L. (1988) Lectin and neuropeptide labeling of separate populations of dorsal root ganglion neurons and associated nociceptor thin axons in rat testis and cornea whole-mount preparations. Somatosensory Research 5, 259–267.

    PubMed  Google Scholar 

  • Wang, H., Rivero-MeliÁn, C., Robertson, B. & Grant, G. (1994) Transganglionic transport and binding of the isolectin B4 from Griffonia simplicifolia I in rat primary sensory neurons. Neuroscience 62, 539–551.

    PubMed  Google Scholar 

  • Zheng, F. & Lawson, S. N. (1994) Immunocytochemical properties of rat renal afferent neurons in dorsal root ganglia: A quantitative study. Neuroscience 63, 295–306.

    PubMed  Google Scholar 

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Kitao, Y., Robertson, B., Kudo, M. et al. Proliferation patterns of dorsal root ganglion neurons of cutaneous, muscle and visceral nerves in the rat. J Neurocytol 31, 765–776 (2002). https://doi.org/10.1023/A:1025760116189

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