Cell and Tissue Research

, Volume 214, Issue 2, pp 303–321 | Cite as

The temporo-spatial course of degeneration after cutting cortico-cortical connections in adult rats

  • J. R. Wolff
  • S. Eins
  • M. Holzgraefe
  • L. Záborszky


Adult albino rats received callosotomies or lesions in the paracingular cortex. Between 12 h and 3 months after injury the structure and topography of the degeneration products were studied by light- and electron-microscopy. The degeneration process was quantified by television-image analysis applied to sections prepared according to a new technique that stains reliably degenerating terminals and lysosomes (Gallyas et al. 1980). All types of cortico-cortical connections show a multiphasic degeneration process: During a precursor stage a small number of dense bodies and mitochondrial granules are stained. These and the few early degenerating axon terminals are much more diffusely distributed than the large number of terminals that degenerate during the following period. The terminal degeneration shows a biphasic time course. One maximum appears at 2–7 days post operation, which corresponds to the well known direct consequence of axotomy. The second peak at 10–20 days post operation could be caused by transneuronal reorganization of the cortical connectivity. Terminal degeneration always begins along the borders between cortical regions and areas, but it may change its laminar and columnar distribution pattern during the second phase. The degeneration products that are phagocytosed by astrocytes seem to be removed by intracellular transport to their perivascular endfeet. The degeneration process ends with fiber degeneration which, especially in laminae I and VI, may form a separate peak after 20 days or more.

Key words

Cortico-cortical connections Degeneration Time course Rat 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Akers RM, Killackey HP (1978) Organization of cortico-cortical connections in the parietal cortex of the rat. J Comp Neurol 181:513–538Google Scholar
  2. Beresford WA (1965) A discussion on retrograde changes in nerve fibres. In: Singer M, Schadé JP (eds) Degeneration patterns in the nervous system. Progr Brain Res 14:33–56Google Scholar
  3. Billardon M, Sicart F, Badoz J, Chapelle J, Taurel L (1970) Analyse des courbes d'absorption et de dichroisme circulaire magnétique: Application aux ions Pb2+ et Ag dans les halogénures alcalius. J Physiol (Paris) 31:219–225Google Scholar
  4. Cajal S, Ramón y (1959) Degeneration and regeneration of the nervous system (RM May, transi). Reprinted by Hafner, New York, p 396Google Scholar
  5. Cammermeyer J (1962) An evaluation of the significance of the “dark” neuron. Ergeb Anat Entwickl Gesch 36:1–61Google Scholar
  6. Cole M (1968) Retrograde degeneration of axon and soma in the nervous system. In: Bourne GH (ed) Structure and function of the nervous system. 1:269–300Google Scholar
  7. Colonnier M, Gray EG (1962) In: Breese SS (ed) Degeneration in the cerebral cortex. 5th Int Congr for Electron Microscopy, Acad Press NYGoogle Scholar
  8. Cook RD, Wiśniewski HM (1973) The role of oligodendroglia and astroglia in Wallerian degeneration of the optic nerve. Brain Res 61:191–206Google Scholar
  9. Creutzfeldt OD, Garey LJ, Kuroda R, Wolff JR (1977) The distribution of degenerating axons after small lesions in the intact and isolated cortex of the cat. Exp Brain Res 27:419–440Google Scholar
  10. Demênes D, Fuentes C, Marty R (1974) The kinetic processes of axonal degeneration in the central nervous system: A short-term experimental study in the corpus callosum of the rat. Acta Neuropathol 29:311–323Google Scholar
  11. Eager RP (1970) Selective staining of degenerating axons in the central nervous system by a simplified silver method: spinal cord projections to external cuneate and inferior olivary nuclei in the cat. Brain Res 22:137–141Google Scholar
  12. Fink RP, Heimer L (1967) Two methods for selective silver impregnation of degenerating axons and their synaptic endings in the central nervous system. Brain Res 4:369–374Google Scholar
  13. Friede RL, Martinez AJ (1970) Analysis of axon-sheath relations during early Wallerian degeneration. Brain Res 19:199–212Google Scholar
  14. Gallyas F, Wolff JR, Böttcher H, Záborszky L (1980) A reliable and sensitive method to locate terminal degeneration and lysosomes in the CNS. Stain Technol (in press)Google Scholar
  15. Glickstein M, Whitteridge D (1976) Degeneration of layer III pyramidal cells in area 18 following destruction of callosal input. Brain Res 104:148–157Google Scholar
  16. Grant G (1970) Neuronal changes central to the site of axon transection. A method for the identification of retrograde changes in perikarya, dendrites and axons by silver impregnation. In: Nauta WJH, Ebbesson SOE (eds) Contemporary Research Methods in Neuroanatomy, Springer NY, pp 173–185Google Scholar
  17. Griffiths GW (1979) Transport of glial cell acid phosphatase by endoplasmic reticulum into damaged axons. J Cell Sci 36:361–389Google Scholar
  18. Griffiths GW, Boschek CB (1976) Rapid degeneration of visual fibers following retinal lesions in the dipteran compound eye. Neurosci Letters 3:253–258Google Scholar
  19. Hasan M, Glees P, Spoerri PE (1974) Dissolution and removal of neuronal lipofuscin following dimethylaminoethyl p-chlorophenoxyacetate administration to guinea pigs. Cell Tissue Re 150:369–375Google Scholar
  20. Hassler R, Wagner A (1965) Experimentelle und morphologische Befunde über die vierfache corticale Projektion des visuellen Systems. Proc 8th Int Congr Neurol, Vol III, 77–96Google Scholar
  21. Holzgraefe M, Wolff JR (1977) A device for dark field microphotography at low magnification. J Microsc 111 Pt 2:225–227Google Scholar
  22. Jones EG, Powell TPS (1970) An electron microscopic study of terminal degeneration in the neocortex of the cat. Phil Trans R Soc Lond B 257:29–43Google Scholar
  23. Joseph BS (1973) Somatofugal events in Wallerian degeneration: a conceptual overview. Brain Res 59:1–18Google Scholar
  24. Joseph BS, Whitlock DG (1972) The spatio-temporal course of Wallerian degeneration within the CNS of toad (Bufo marinus) as defined by the Nauta silver method. Brain Behav Evol 5:1–17Google Scholar
  25. Kreutzberg GW, Tóth L, Kaiya H (1975) Acetylcholinesterase as a marker for dendritic transport and dendritic secretion. In: Kreutzberg GW (ed) Advances in Neurology 12, Physiology and Pathology of Dendrites. Raven Press NY, pp 269–281Google Scholar
  26. Krieg WJS (1946) Connections in the cerebral cortex. J Comp Neurol 84:221–323Google Scholar
  27. Lassek AM, Hard WL (1946) The pyramidal tract. The relation of axonal diameters to the rate of degeneration as revealed by the acid phosphatase method in monkey. J Neuropathol 5:374–379Google Scholar
  28. Lent R, Rocha-Miranda CE (1974) Survival times and patterns of degeneration in the visual system of the opossum. Brain Res 72:294–299Google Scholar
  29. Lund JS, Lund RD (1970) The termination of callosal fibres in the paravisual cortex of the rat. Brain Res 17:25–45Google Scholar
  30. Lynch G, Rose G, Gall C, Cotman CW (1975) The response of the dentate gyrus to partial deafferentation. In: Santini M (ed) Golgi Centennial Symposium. Raven Press NY, pp 305–317Google Scholar
  31. Makarov FN (1968) Commissural connections of visual cortex (fields 17,18,19) in cat. Arkh Anat Histol Embryol 55:48–54Google Scholar
  32. Nauta HJW, Butler A, Jane J (1973) Some observations on axonal degeneration resulting from superficial lesions of the cerebral cortex. J Comp Neurol 150:349–360Google Scholar
  33. Powell TPS, Cowan WM (1964) A note on retrograde fiber degeneration. J Anat (Lond) 98:579–585Google Scholar
  34. Richards W, Kalil R (1974) Dissociation of retinal fibers by degeneration rate. Brain Res 72:288–293Google Scholar
  35. Sanides F (1972) Representation in the cerebral cortex and its areal lamination patterns. In: Bourne GH (ed) Structure and Function of Nervous Tissue. Academic Press, New York London, Vol 5, pp 329–453Google Scholar
  36. Schneider GE (1968) Retinal projections characterized by differential rate of degeneration revealed by silver impregnation. Anat Rec 160:423, AbstrGoogle Scholar
  37. Sloper JJ, Powell TPS (1978) Observations on the process of degeneration of the afferent connections to the sensory motor cortex of the monkey. Neuroscience 3:1031–1044Google Scholar
  38. Tigges JW, Spatz W, Tigges M (1974) Efferent cortico-cortical fiber connections of area 18 in the squirrel monkey (Saimiri). J Comp Neurol 158:219–236Google Scholar
  39. Vaccarezza OL, Reader TA, Pasqualini E, Pecci-Saavedra J (1970) Temporal course of synaptic degeneration in the lateral geniculate nucleus. Exp Neurol 28:277–285Google Scholar
  40. van Crevel H, Verhaart WJC (1963) The rate of secondary degeneration in the central nervous system. I. The pyramidal tract of the cat. J Anat London 97:429–449. II. The optic nerve of the cat. J Anat London 97:451–464Google Scholar
  41. Vial JD (1955) The influence of axon length on the course of Wallerian degeneration of the motor end plates. Acta Physiol Lat Americ 5:95–103Google Scholar
  42. Walberg F (1963) Role of normal dendrites in removal of degenerating terminal boutons. Exp Neurol 8:112–124Google Scholar
  43. Walberg F (1965) An electron microscopic study of terminal degeneration in the inferior olive of the cat. J Comp Neurol 125:205–222Google Scholar
  44. Waxman SG, Swadlow HA (1976) Ultrastructure of visual callosal axons in the rabbit. Exp Neurol 53:115–127Google Scholar
  45. Wise SP, Jones EG (1976) The organization and postnatal development of the commissural projection of the rat somato-sensory cortex. J Comp Neurol 168:313–344Google Scholar
  46. Wolff JR (1977) Morphology of the extravascular space in brain in comparison to other tissues. Bibl Anat 15:210–212. Lewis DH (ed)Google Scholar
  47. Wolff JR, Záborszky L (1979) On the normal arrangement of fibres and terminals and limits of plasticity in the callosal system of the rat. In: Steele Russel J, van Hof WM, Berlucchi G (eds) Structure and function of cerebral commissures. The Macmillan Press Ltd, London and Basingstoke, pp 147–154Google Scholar
  48. Wolff JR, Rajan KT, Noack W (1974) The fate and fine structure of fragments of blood vessels in CNS tissue cultures. Cell Tissue Res 156:89–102Google Scholar

Copyright information

© Springer-Verlag 1981

Authors and Affiliations

  • J. R. Wolff
    • 1
    • 2
  • S. Eins
    • 1
    • 2
  • M. Holzgraefe
    • 1
    • 2
  • L. Záborszky
    • 1
    • 2
  1. 1.Department of NeurobiologyMax-Planck-Institut für biophysikalische ChemieGöttingenFederal Republic of Germany
  2. 2.Department of AnatomyUniversity of GöttingenGöttingenFederal Republic of Germany

Personalised recommendations