Hostname: page-component-77c89778f8-n9wrp Total loading time: 0 Render date: 2024-07-20T19:55:08.789Z Has data issue: false hasContentIssue false
  • English
  • Français

Stereological estimation of gap junction surface area per neuron in the developing nervous system of the invertebrate Mesocestoides corti

Published online by Cambridge University Press:  06 April 2009

A. J. Burns ,
C. V. Howard ,
J. M. Allen ,
D. Van Velsen  and
G. McKerr
A. J. Burns
Affiliation:
Department of Biological and Biomedical Sciences, University of Ulster, Coleraine, County Londonderry BT52 ISA, Northern Ireland, UK
C. V. Howard
Affiliation:
Department of Fetal and Infant Pathology, Royal Liverpool Children's Hospital, Myrtle Street, Liverpool L7 7DG, UK
J. M. Allen
Affiliation:
Department of Biological and Biomedical Sciences, University of Ulster, Coleraine, County Londonderry BT52 ISA, Northern Ireland, UK
D. Van Velsen
Affiliation:
Department of Fetal and Infant Pathology, Royal Liverpool Children's Hospital, Myrtle Street, Liverpool L7 7DG, UK
G. McKerr
Affiliation:
Department of Biological and Biomedical Sciences, University of Ulster, Coleraine, County Londonderry BT52 ISA, Northern Ireland, UK
Get access Rights & Permissions [Opens in a new window]

Summary

As a major morphological feature in establishing the form of the nervous system, it is recognized that neurons are initially overproduced, then naturally occurring cell death reduces the neuron number to the functional requirement. However, the mechanisms controlling the selective elimination of certain neurons during a general phase of cell death are not fully understood. One event that seems to be pivotal is the establishment of neural connections, the degree of which may be influential regarding the fate of specific neurons. However, little quantitative evidence is available to either support or refute this theory. In this current study, a Stereological measurement of gap junction per neuron was carried out within the invertebrate model system of the tapeworm metacestode Mesocestoides corti, which has previously been shown to overproduce neurons during the asexual reproduction stage of its life-cycle. Novel Stereological estimation methods with ‘ vertical sections’ indicated that prior to asexual division the cerebral ganglion possessed approximately 268 neurons, each with a gap junction surface area of 250 μm2. As division progressed, the neuron number increased to approximately 700, while the total surface area of gap junction remained statistically unchanged. As a result the surface area of gap junction per neuron decreased to 106 μm2, less than half that in the undividing stage. These results provide the first non-biased quantitative data regarding changes in the mean surface area of gap junction per neuron in a developing cerebral ganglion.

Keywords

stereologydevelopmentneuronal deathgap junctions
Type
Research Article
Information
Parasitology , Volume 111 , Issue 4 , November 1995 , pp. 505 - 513
Copyright
Copyright © Cambridge University Press 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Baddeley, A. J., Gunderson, H. J. G. & Cruz-Orive, L. M. (1986). Estimation of surface area from vertical sections. Journal of Microscopy 142, 259–76.CrossRefGoogle ScholarPubMed
Berg, D. (1984). New neuronal growth factors. Annual Review of Neurosciences 7, 149–90.CrossRefGoogle ScholarPubMed
Burns, A. J. (1993). Neuroanatomy and nerve cell recruitment within the asexually dividing tetrathyridium of Mesocestoides corti. D.Phil, thesis, University of Ulster, UK.Google Scholar
Changeaux, J. P. & Danchin, A. (1976). Selective stabilisation of developing synapses as a mechanism for the specification of neuronal networks. Nature, London 264, 705–12.CrossRefGoogle Scholar
Clarke, P. G. H. & Cowan, W. M. (1976). The development of the isthmo-optic tract in the chick, with special reference to the occurrence and correction of the developmental errors in the location and connections of isthmo-optic neurons. Journal of Comparative Neurology 167, 143–64.CrossRefGoogle Scholar
Coggeshall, R. E. (1992). A consideration of neural counting methods. Trends in Neurosciences 15, 9–13.CrossRefGoogle ScholarPubMed
Cowan, W. M., Fawcett, J. W., O'Leary, D. D. M. & Stanfield, B. B. (1984). Regressive events in neurogenesis. Science 225, 1258–65.CrossRefGoogle ScholarPubMed
Cowan, W. M. (1979). The development of the brain. Scientific American 241, 112–33.CrossRefGoogle ScholarPubMed
Cunningham, T. J. (1982). Naturally occurring neuron death and its regulation by developing neural pathways. International Review of Cytology 74, 163–86.CrossRefGoogle ScholarPubMed
Ellis, H. M. & Horvitz, H. R. (1986). Genetic control of programmed cell death in the nematode C. elegans. Cell 44, 817–29.CrossRefGoogle ScholarPubMed
Fahrbach, S. E. & Truman, J. W. (1987). Mechanisms for programmed cell death in the nervous system of a moth. In Selective Neuronal Death (ed. Bock, G. & O'Connor, M.) pp. 65–81. New York: Wiley.Google Scholar
Furber, S., Oppenheim, R. W. & Prevette, D. (1987). Naturally occurring neuron death in the ciliary ganglion of the chick embryo following removal of preganglionic input: evidence for the role of afferents in ganglion cell survival. Journal of Neuroscience 7, 1816–32.CrossRefGoogle ScholarPubMed
Gagliardini, V., Fernandez, P.-A., Lee, P. K. K., Drexler, H. C. A., Rotello, R. J., Fishman, M. C. & Yuan, J. (1994). Prevention of vertebrate neuronal death by the crmA gene. Science 263, 826–8.CrossRefGoogle ScholarPubMed
Greenwald, I. & Martinez-Arias, A. (1984). Programmed cell death in invertebrates. Trends in Neuroscience 12, 179–81.CrossRefGoogle Scholar
Gunderson, H. J. G. & Jensen, E. B. (1987). The efficiency of systematic sampling in stereology and its prediction. Journal of Microscopy 147, 229–63.CrossRefGoogle Scholar
Gunderson, H. J. G. (1986). Invited Review. Stereology of arbitrary particles. A review of unbiased number size estimators and the presentation of some new ones, in memory of William R. Thompson. Journal of Microscopy 143, 3–45.CrossRefGoogle Scholar
Hamburger, V. & Levi, Montalcini R. (1949). Proliferation, differentiation and degeneration in the spinal ganglia of chicks under normal and experimental conditions. Journal of Experimental Zoology 111, 457–502.CrossRefGoogle ScholarPubMed
Hamburger, V. & Oppenheim, R. W. (1982). Naturally occurring neuronal death in vertebrates. Neuroscience Comments 1, 38–55.Google Scholar
Hertzberg, E. L. & Johnston, R. G. (1988). Modern Cell Biology: Gap Junctions. New York: Liss.Google Scholar
Hollyday, M. & Hamburger, V. (1976). Reduction of the naturally occurring motoneuron loss by enlargement of the periphery. Journal of Comparative Neurology 170, 311–20.CrossRefGoogle ScholarPubMed
Horvitz, H. R., Ellis, H. M. & Sternberg, P. W. (1982). Programmed cell death in nematode development. Neuroscience Comments 1, 56–65.Google Scholar
Howard, C. V. (1990). Stereological techniques in biological electron microscopy. In Biophysical Electron Microscopy, (ed. Hawkes, P. W. & Valdre, V.) pp. 477–508. London: Academic Press.Google Scholar
Janson, A. M. & Møller, A. (1993). Chronic nicotine treatment counteracts nigral cell loss induced by a partial mesodiencephalic hemitransection: an analysis of the total number and mean volume of neurons and glia in substantia nigra of the male rat. Neuroscience 57, 931–41.CrossRefGoogle ScholarPubMed
Lance-Jones, C. (1982). Motoneuron cell death in the developing lumbar spinal cord of the mouse.Developments in Brain Research 4, 473–9.CrossRefGoogle Scholar
Landmesser, L. & Pilar, C. (1978). Interactions between neurons and their targets during in vivo synaptogenesis. Federation Proceedings 37, 2016–22.Google ScholarPubMed
Levi-Montalcini, R. (1982). Developmental neurobiology and the natural history of nerve growth factor. Annual Review of Neurosciences 5, 341–62.CrossRefGoogle ScholarPubMed
Linden, R. (1994). The survival of the developing neurons: a review of afferent control. Neuroscience 58, 671–82.CrossRefGoogle ScholarPubMed
Møller, A., Strange, P. & Gunderson, H. J. G. (1990). Efficient estimation of cell volume and number using the nucleator and disector. Journal of Microscopy 159, 61–71.CrossRefGoogle ScholarPubMed
Mudge, A. (1993). Motor neurons find their factors. Nature, London 363, 213–14.CrossRefGoogle ScholarPubMed
Oppenheim, R. W. (1991). Cell death during development of the nervous system. Annual Review of Neuroscience 14, 453–501.CrossRefGoogle ScholarPubMed
Pakkenburg, B. & Gunderson, H. J. G. (1988). Total number of neurons and glial cells in human brain nuclei estimated by the disector and fractionator. Journal of Microscopy 150, 1–20.CrossRefGoogle Scholar
Purves, D. (1988). Body and Brain, A Trophic Theory of Neural Connections. Cambridge, Mass: Harvard.Google Scholar
Raff, M. C., Barres, B. A., Burne, J. F., Coles, H. S., Ishizaki, Y. & Jacobsom, M. D. (1993). Programmed cell death and the control of cell survival: lessons from the nervous system. Science 262, 695–700.CrossRefGoogle ScholarPubMed
Specht, D. & Voge, M. (1965). Asexual multiplication of Mesocestoides tetrathyridia in laboratory animals. Journal of Parasitology 51, 268–72.CrossRefGoogle ScholarPubMed
Sterio, D. C. (1984). The unbiased estimation of number and sizes of arbitrary particles using the disector. Journal of Microscopy 134, 127–36.CrossRefGoogle ScholarPubMed
Sulston, J. E., Schierenberg, E., White, J. G. & Thornson, J. N. (1983). The embryonic cell lineage of the nematode Caenorhabditis elegans. Developmental Biology 100, 64–119.CrossRefGoogle ScholarPubMed
Thoenene, H. (1991). The changing scene of neurotrophic factors. Trends in Neurosciences 14, 165–70.CrossRefGoogle Scholar
Truman, J. W. & Schwartz, L. M. (1982). Programmed death in the nervous system of a moth. Trends in Neurosciences 5, 270–2.CrossRefGoogle Scholar
Weibel, E. R. (1981). Statistical Methods. Practical Methods for Biological Morphometry, Vol. 1. New York: Academic Press.Google Scholar
West, M. J., Coleman, P. D. & Flood, D. G. (1988). Estimating the number of granule cells in the dentate gyrus with the disector. Brain Research 448, 167–72.CrossRefGoogle ScholarPubMed
Yaegashi, H., Howard, C. V., McKerr, G. & Burns, A. J. (1993). Stereological estimation of the total number of neurons in the asexually dividing tetrathyridium of Mesocestoides corti. Parasitology 106, 177–83.CrossRefGoogle Scholar