Skip to main content
SpringerLink
Log in

Age-related fine structural changes in axons and synapses during deafferentation of the rat pyriform cortex: a possible basis for plasticity

  • Published:
Journal of Neurocytology

Summary

The purpose of this study was to compare the sequence of axonal and synaptic alterations following deafferentating lesions at selected postnatal ages and relate these changes to synaptic organization in the olfactory cortex. Rats received unilateral olfactory bulb ablation at 21/2, 6, 9 and 13 days of age and were studied at survivals of 12 h to 30 days. At least three clearly different forms of acute degeneration were seen; flocculent, granular and dense with the granular form an intermediate form. The proportion of granular and especially dense degeneration increases after six days of age as does the presence of glia. The denser the type of degeneration, the greater the retention of remnants of this form of synaptic degeneration at deafferented postsynaptic sites. This as well as the increased presence of glia after six days may be important factors in the limitation of plastic reorganization or reinnervation in more mature individuals. The youngest operated animals show rapid vacating of the receptor site, relative absence of glia and striking evidence of competitive reoccupation of deafferented sites.

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

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Bakay, R. A. E. &Westrum, L. E. (1982) Age-related ultrastructural changes in synaptic degeneration in olfactory cortex. A basis for plasticity.Society for Neurosciences Abstracts 8, 639.

    Google Scholar 

  • Benes, F. M., Parks, T. N. &Rubel, E. W. (1977) Rapid dendritic atrophy following deafferentation: An EM morphometric analysis.Brain Research 122, 1–13.

    PubMed  Google Scholar 

  • Caviness, V. S., Korde, M. G. &Williams, R. S. (1977) Cellular events induced in the molecular layer of pyriform cortex by ablation of the olfactory bulb in the mouse.Brain Research 134, 13–34.

    PubMed  Google Scholar 

  • Chen, S. &Hillman, D. E. (1982) Plasticity of the parallel fiber-Purkinje cell synapse by spine takeover and new synapse formation in the adult rat.Brain Research 240, 205–20.

    PubMed  Google Scholar 

  • Cotman, C. W. (1978) (editor)Neuronal Plasticity. New York: Raven Press.

    Google Scholar 

  • Cotman, C. W., Nieto-Sampedro, M. &Harris, E. W. (1981) Synaptic replacement in the nervous system of adult vertebrates.Physiological Reviews 61, 684–785.

    PubMed  Google Scholar 

  • Grain, B., Cotman, C. W., Taylor, D. &Lynch, G. (1973) A quantitative electron microscopic study of synaptogenesis in the dentate gyrus of the rat.Brain Research 63, 195–204.

    PubMed  Google Scholar 

  • Friedman, B. &Price, J. L. (1978) Age dependent reactions of olfactory cortex to deafferentation.Society for Neurosciences Abstracts 4, 1501.

    Google Scholar 

  • Friedman, B. &Price, J. L. (1981) Establishment of normal synaptic density in deafferented olfactory cortex.Brain Research 223, 146–51.

    PubMed  Google Scholar 

  • Gall, C. &Lynch, G. (1978) Rapid axon sprouting in the neonatal rat hippocampus.Brain Research 153, 357–62.

    PubMed  Google Scholar 

  • Gall, C., McWilliams, R. &Lynch, G. (1980) Accelerated rates of synaptogenesis by sprouting afferents in the immature hippocampal formation.Journal of Comparative Neurology 193, 1047–61.

    PubMed  Google Scholar 

  • Gentschev, T. &Sotelo, C. (1973) Degenerative patterns in the ventral cochlear nucleus of the rat after primary deafferentation. An ultrastructural study.Brain Research 62, 37–60.

    PubMed  Google Scholar 

  • Ghetti, B., Horoupian, D. S. &Wisniewski, H. M. (1975) Acute and long-term transneuronal response of dendrites of lateral geniculate neurons following transection of the primary visual afferent pathway.Advances in Neurology 12, 401–24.

    PubMed  Google Scholar 

  • Grafe, M. R. (1983) Developmental factors affecting regeneration in the central nervous system: Early but not late formed mitral cells reinnervate olfactory cortex after neonatal tract section.Journal of Neuroscience 3, 617–30.

    PubMed  Google Scholar 

  • Gramsbergen, A. &Ijkema-Paassen, J. (1982) CNS plasticity after hemicerebellectomy in the young rat. Quantitative relations between aberrant and normal cerebello-rubral projections.Neuroscience Letters 33, 129–34.

    PubMed  Google Scholar 

  • Haberly, L. B. &Price, J. L. (1978) Association and commissural fiber systems of the olfactory cortex of the rat.Journal of Comparative Neurology 178, 711–40.

    PubMed  Google Scholar 

  • Heimer, L. (1968) Synaptic distribution of centripetal and centrifugal nerve fibers in the olfactory system of the rat. An experimental anatomical study.Journal of Anatomy 103, 403–32.

    Google Scholar 

  • Heimer, L. &Kalil, R. (1978) Rapid transneuronal degeneration and death of cortical neurons following removal of the olfactory bulb in adult rats.Journal of Comparative Neurology 178, 559–609.

    PubMed  Google Scholar 

  • Heimer, L. &Peters, A. (1968) An electron microscopic study of a silver stain for degenerating boutons.Brain Research 8, 337–46.

    PubMed  Google Scholar 

  • Hitzemann, R. J. &Johnson, D. A. (1983) Developmental changes in synaptic membrane lipid composition and fluidity.Neurochemical Research 8, 121–36.

    PubMed  Google Scholar 

  • Jeanmonod, D., Rice, F. L. &Van Der Loos, H. (1981) Mouse somatosensory cortex: alterations in the barrelfield following receptor injury at different early postnatal ages.Neuroscience 6, 1503–33.

    PubMed  Google Scholar 

  • Kalil, K. &Reh, T. (1979) Regrowth of severed axons in the neonatal central nervous system: establishment of normal connections.Science 205, 1158–61.

    PubMed  Google Scholar 

  • Kalil, K. &Reh, T. (1982) A light and electron microscopic study of regrowing pyramidal tract fibers.Journal of Comparative Neurology 211, 265–75.

    PubMed  Google Scholar 

  • Kjerulf, T., O'neal, J., Calvin, W., Loeser, J. &Westrum, L. (1973) Deafferentation effects in lateral cuneate nucleus of the cat: Correlation of structural alterations with firing pattern changes.Experimental Neurology 39, 86–102.

    PubMed  Google Scholar 

  • Laemle, L. K. &Labriola, A. R. (1982) Retinocollicular projections in the neonatal rat: An anatomical basis for plasticity.Developmental Brain Research 3, 317–22.

    Google Scholar 

  • Lenn, N. J. (1978) Effect of neonatal deafferentation on synaptogenesis in the rat interpeduncular nucleus.Journal of Comparative Neurology 181, 99–116.

    Google Scholar 

  • Leong, S. K. (1976) An experimental study of the cortico-fugal system following cerebral lesions in albino rats.Experimental Brain Research 26, 235–47.

    Google Scholar 

  • Leong, S. K. (1978) Plasticity of cerebellar efferents after neonatal lesions in albino rats.Neuroscience Letters 7, 281–9.

    Google Scholar 

  • Leong, S. K. (1980) A qualitative electron microscopic study of the corticopontine projections after neonatal cerebellar hemispherectomy.Brain Research 194, 299–310.

    PubMed  Google Scholar 

  • Leonard, C. M. (1975) Developmental changes in olfactory bulb projections revealed by degeneration argyrophilia.Journal of Comparative Neurology 162, 467–86.

    PubMed  Google Scholar 

  • Lund, R. D. (1978)Development and Plasticity of the Brain. New York: Oxford University Press.

    Google Scholar 

  • Lund, R. D. &Lund, J. S. (1971) Modifications of synaptic patterns in the superior colliculus of the rat during development and following deafferentation.Vision Research Supplement 3, 281–98.

    Google Scholar 

  • Lund, R. &Westrum, L. E. (1966) Neurofibrils and the Nauta method.Science 151, 1397–99.

    PubMed  Google Scholar 

  • Lynch, G., Stanfield, B. &Cotman, C. W. (1972) Developmental differences in post-lesion axonal growth in the hippocampus.Brain Research 59, 155–68.

    Google Scholar 

  • Mathers, L. H., Jr (1977) Effects of neonatal deafferentation on the superficial laminae of the superior colliculus.Brain Research 126, 19–30.

    PubMed  Google Scholar 

  • Mathers, L. H., Jr &Ostrach, L. H. (1979) A critical period in the development of tectal neurons in the chick, as revealed by early enucleation.Brain Research 170, 219–30.

    PubMed  Google Scholar 

  • Matthews, D. A., Cotman, C. &Lynch, G. (1976) An electron microscopic study of lesion-induced synaptogenesis in the dentate gyrus of the adult rat. II. Reappearance of morphologically normal synaptic contacts.Brain Research 115, 23–41.

    PubMed  Google Scholar 

  • McWilliams, R. &Lynch, G. (1979) Terminal proliferation in the partially deafferented dentate gyrus: Time courses for the appearance and removal of degeneration and the replacement of lost terminals.Journal of Comparative Neurology 187, 191–8.

    PubMed  Google Scholar 

  • Mugnaini, E. &Friedrich, V. L. (1981) Electron microscopy: Identification and study of normal and degenerating neural elements by electron microscopy. In:Neuroanatomical Tract-Tracing Methods (edited byHeimer, L. andRobards, M. J.), pp. 377–406, New York: Plenum Press.

    Google Scholar 

  • Perry, V. H. &Cowey, A. (1982) A sensitive period for ganglion cell degeneration and the formation of aberrant retino-fugal connections following tectal lesions in rats.Neuroscience 7, 583–94.

    PubMed  Google Scholar 

  • Price, J. L. (1973) An autoradiographic study of complimentary laminar patterns of termination of afferent fibers to the olfactory cortex.Journal of Comparative Neurology 150, 87–108.

    PubMed  Google Scholar 

  • Price, J. L., Moxley, G. F. &Schwob, J. E. (1976) Development and plasiticity of complimentary afferent systems to the olfactory cortex.Experimental Brain Research Supplement 1, 148–54.

    Google Scholar 

  • Ralston, H. J. III &Ralston, D. D. (1979) The distribution of dorsal root axons in lamina I, II and III of the macaca spinal cord. A quantitative electron microscopic study.Journal of Comparative Neurology 184, 643–84.

    PubMed  Google Scholar 

  • Rothblat, L. A. &Hayes, L. L. (1982) Age-related changes in the distribution of visual callosal neurons following monocular enucleation in the rat.Brain Research 246, 146–9.

    PubMed  Google Scholar 

  • Rustioni, A. &Sotelo, C. (1974) Some effects of chronic deafferentation on the ultrastructuré of the nucleus gracilis of the cat.Brain Research 73, 527–33.

    PubMed  Google Scholar 

  • Sampedro, M. N., Bussineau, C. M. &Cotman, C. W. (1982) Turnover of brain postsynaptic densities after selective deafferentation: Detection by means of an antibody to antigen PSD-95.Brain Research 251, 211–20.

    PubMed  Google Scholar 

  • Schneider, G. E. (1981) Early lesions and abnormal neuronal connections.Trends in Neurosciences 4, 187–92.

    Google Scholar 

  • Schwob, J. E. &Price, J. L. (1978) The cortical projection of the olfactory bulb: Development in fetal and neonatal rats correlated with quantitative variations in adult rats.Brain Research 151, 369–74.

    PubMed  Google Scholar 

  • Singh, S. C. (1977) The development of olfactory and hippocampal pathways in the brain of the rat.Anatomy and Embryology 151, 183–99.

    PubMed  Google Scholar 

  • Somogyi, J., Hamori, J. &Silakov, V. L. (1982) Free postsynaptic sites in the lateral geniculate nucleus of adult cats following chronic decortication.Cell and Tissue Research 225, 437–42.

    PubMed  Google Scholar 

  • Spacek, J. (1982) ‘Tree’ postsynaptic-like densities in normal adult brain: Their occurrence, distribution, structure and association with subsurface cisterns.Journal of Neurocytology 11, 693–706.

    PubMed  Google Scholar 

  • Steward, O. (1982) Events within the sprouting neuron and the denervated neuropil during lesion-induced synaptogenesis. In:Changing Concepts of the Nervous System (edited byMorrison, A. R. andStrick, P. L.), pp. 33–48. New York: Academic Press.

    Google Scholar 

  • Steward, O. (1983) Alterations in polyribosomes associated with dendritic spines during reinnervation of the dentate gyrus of the adult rat.Journal of Neuroscience 3, 177–88.

    PubMed  Google Scholar 

  • Swenson, R. S. &Castro, A. J. (1982) Plasticity of mesodiencephalic projections to the inferior olive following neonatal hemicerebellectomy in rats.Brain Research 244, 169–72.

    PubMed  Google Scholar 

  • Tsukahara, N. (1981) Synaptic plasticity in the mammalian central nervous system.Annual Review of the Neurosciences 4, 351–79.

    Google Scholar 

  • Walberg, F. (1972) Further studies on silver impregnation of normal and degenerating boutons. A light and electron microscopic investigation of a filamentous degenerating system.Brain Research 36, 353–69.

    PubMed  Google Scholar 

  • Weber, E. D. &Stelzner, D. J. (1980) Synaptogenesis in the intermediate gray region of the lumbar spinal cord in the postnatal rat.Brain Research 185, 17–37.

    PubMed  Google Scholar 

  • Westrum, L. E. (1969) Electron microscopy of degeneration in the lateral olfactory tract and the prepyriform cortex of the rat.Zeitschift für Zellforschung 98, 157–87.

    Google Scholar 

  • Westrum, L. E. (1973) Early forms of terminal degeneration in the spinal trigeminal nucleus following rhizotomy.Journal of Neurocytology 2, 189–215.

    PubMed  Google Scholar 

  • Westrum, L. E. (1974) Electron microscopy of deafferentation in the spinal trigeminal nucleus.Advances in Neurology 4, 53–60.

    Google Scholar 

  • Westrum, L. E. (1975a) Axonal patterns in olfactory cortex after olfactory bulb removal in newborn rats.Experimental Neurology 47, 442–7.

    PubMed  Google Scholar 

  • Westrum, L. E. (1975b) Electron microscopy of synaptic structures in olfactory cortex of early postnatal rats.Journal of Neurocytology 4, 713–32.

    PubMed  Google Scholar 

  • Westrum, L. E. (1980) Alterations in axons and synapses of olfactory cortex following olfactory bulb lesions in newborn rats.Anatomy and Embryology 160, 153–72.

    PubMed  Google Scholar 

  • Westrum, L. E. &Miller, E. (1979) Synapse development in olfactory cortex.Society for Neurosciences Abstracts 5, 611.

    Google Scholar 

  • White, L. E., Jr (1965) Olfactory bulb projections in the rat.Anatomical Record 152, 465–80.

    Google Scholar 

Download references

Author information

Author notes

  1. R. A. E. Bakay

    Present address: Department of Neurosurgery, Emory University, Atlanta, Georgia, USA

Authors and Affiliations

  1. Department of Neurological Surgery, University of Washington, 98195, Seattle, Washington, USA

    R. A. E. Bakay

  2. Department of Biological Structure, University of Washington, 98195, Seattle, Washington, USA

    L. E. Westrum

Authors
  1. R. A. E. Bakay
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. L. E. Westrum
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bakay, R.A.E., Westrum, L.E. Age-related fine structural changes in axons and synapses during deafferentation of the rat pyriform cortex: a possible basis for plasticity. J Neurocytol 13, 743–765 (1984). https://doi.org/10.1007/BF01148492

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01148492

Keywords

Search

Navigation