Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1978 Apr;277:395–408. doi: 10.1113/jphysiol.1978.sp012280

Mechanisms of functional recovery and regeneration after spinal cord transection in larval sea lamprey.

M E Selzer
PMCID: PMC1282397  PMID: 650547

Abstract

1. Large sea lamprey larvae, close to metamorphosis, regained swimming coordination after several weeks following complete spinal cord transection. Recovery was much faster when animals were kept at 23 than at 12 degrees C. 2. The behavioural recovery involved a regenerative mechanism in the spinal cord, since stimulation of the head resulted in tail curling, even when all tissue other than spinal cord and notocord was stripped away for several cm above and below the transection. 3. Following complete behavioural recovery, stimulation of the rostral cord evoked electrical signals recorded from the cord dorsum for only 10 mm below the transection. 4. Dorsal cells and giant interneurones, which normally project to the brain, could not be antidromically activated across the transection zone. However, giant interneurones could be activated polysynaptically by descending volleys. 5. Twelve of eighteen large reticulospinal axons followed in serial sections regenerated across the glial-ependymal scar, but branched abnormally and migrated away from their customary locations. They became smaller, and were finally lost within 4 mm of the centre of the transection zone. 6. These data suggest that behavioural recovery does not involve long axon tract regeneration. An alternate hypothesis, that short distance sprouting of axons across the transection zone may result in synapse formation with propriospinal interneurones which relay the necessary information, is discussed.

Full text

PDF
397

Images in this article

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baylor D. A., Nicholls J. G. Patterns of regeneration between individual nerve cells in the central nervous system of the leech. Nature. 1971 Jul 23;232(5308):268–270. doi: 10.1038/232268a0. [DOI] [PubMed] [Google Scholar]
  2. Bernstein J. J., Bernstein M. E. Effect of glial-ependymal scar and teflon arrest on the regenerative capacity of goldfish spinal cord. Exp Neurol. 1967 Sep;19(1):25–32. doi: 10.1016/0014-4886(67)90004-0. [DOI] [PubMed] [Google Scholar]
  3. Birse S. C., Bittner G. D. Regeneration of giant axons in earthworms. Brain Res. 1976 Sep 3;113(3):575–581. doi: 10.1016/0006-8993(76)90058-5. [DOI] [PubMed] [Google Scholar]
  4. CLEMENTE C. D. REGENERATION IN THE VERTEBRATE CENTRAL NERVOUS SYSTEM. Int Rev Neurobiol. 1964;6:257–301. doi: 10.1016/s0074-7742(08)60771-0. [DOI] [PubMed] [Google Scholar]
  5. Cass D. T., Sutton T. J., Mark R. F. Competition between nerves for functional connexions with axolotl muscles. Nature. 1973 May 25;243(5404):201–203. doi: 10.1038/243201a0. [DOI] [PubMed] [Google Scholar]
  6. Frank E., Jansen J. K., Rinvik E. A multisomatic axon in the central nervous system of the leech. J Comp Neurol. 1975 Jan 1;159(1):1–13. doi: 10.1002/cne.901590102. [DOI] [PubMed] [Google Scholar]
  7. GAZE R. M. Regeneration of the optic nerve in Xenopus laevis. Q J Exp Physiol Cogn Med Sci. 1959 Jul;44:290–308. doi: 10.1113/expphysiol.1959.sp001402. [DOI] [PubMed] [Google Scholar]
  8. Hoy R. R., Bittner G. D., Kennedy D. Regeneration in crustacean motoneurons: evidence for axonal fusion. Science. 1967 Apr 14;156(3772):251–252. doi: 10.1126/science.156.3772.251. [DOI] [PubMed] [Google Scholar]
  9. Jacobson M., Gaze R. M. Selection of appropriate tectal connections by regenerating optic nerve fibers in adult goldfish. Exp Neurol. 1965 Dec;13(4):418–430. doi: 10.1016/0014-4886(65)90128-7. [DOI] [PubMed] [Google Scholar]
  10. Jansen J. K., Nicholls J. G. Regeneration and changes in synaptic connections between individual nerve cells in the central nervous system of the leech. Proc Natl Acad Sci U S A. 1972 Mar;69(3):636–639. doi: 10.1073/pnas.69.3.636. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Mark R. F. Matching muscles and motoneurones. A review of some experiments on motor nerve regeneration. Brain Res. 1969 Jul;14(2):245–254. doi: 10.1016/0006-8993(69)90108-5. [DOI] [PubMed] [Google Scholar]
  12. Marotte L. R., Mark R. F. The mechanism of selective reinnervation of fish eye muscle. I. Evidence from muscle function during recovery. Brain Res. 1970 Apr 1;19(1):41–51. doi: 10.1016/0006-8993(70)90235-0. [DOI] [PubMed] [Google Scholar]
  13. Martin A. R., Wickelgren W. O. Sensory cells in the spinal cord of the sea lamprey. J Physiol. 1971 Jan;212(1):65–83. doi: 10.1113/jphysiol.1971.sp009310. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Pettegrew R. K., Windle W. F. Factors in recovery from spinal cord injury. Summarized transactions of a conference held May 24-25, 1976, in Granville, Ohio, under the auspices of Denison University and Help Them Walk Again Foundation. Exp Neurol. 1976 Dec;53(3):815–829. doi: 10.1016/0014-4886(76)90157-6. [DOI] [PubMed] [Google Scholar]
  15. Rovainen C. M., Johnson P. A., Roach E. A., Mankovsky J. A. Projections of individual axons in lamprey spinal cord determined by tracings through serial sections. J Comp Neurol. 1973 May 15;149(2):193–202. doi: 10.1002/cne.901490205. [DOI] [PubMed] [Google Scholar]
  16. Rovainen C. M. Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). I. Müller and Mauthner cells. J Neurophysiol. 1967 Sep;30(5):1000–1023. doi: 10.1152/jn.1967.30.5.1000. [DOI] [PubMed] [Google Scholar]
  17. Rovainen C. M. Physiological and anatomical studies on large neurons of central nervous system of the sea lamprey (Petromyzon marinus). II. Dorsal cells and giant interneurons. J Neurophysiol. 1967 Sep;30(5):1024–1042. doi: 10.1152/jn.1967.30.5.1024. [DOI] [PubMed] [Google Scholar]
  18. Rovainen C. M. Regeneration of Müller and Mauthner axons after spinal transection in larval lampreys. J Comp Neurol. 1976 Aug 15;168(4):545–554. doi: 10.1002/cne.901680407. [DOI] [PubMed] [Google Scholar]
  19. Rovainen C. M. Synaptic interactions of identified nerve cells in the spinal cord of the sea lamprey. J Comp Neurol. 1974 Mar 15;154(2):189–206. doi: 10.1002/cne.901540206. [DOI] [PubMed] [Google Scholar]
  20. Rovainen C. M. Synaptic interactions of reticulospinal neurons and nerve cells in the spinal cord of the sea lamprey. J Comp Neurol. 1974 Mar 15;154(2):207–223. doi: 10.1002/cne.901540207. [DOI] [PubMed] [Google Scholar]
  21. WINDLE W. F. Regeneration of axons in the vertebrate central nervous system. Physiol Rev. 1956 Oct;36(4):427–440. doi: 10.1152/physrev.1956.36.4.427. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of Physiology are provided here courtesy of The Physiological Society

RESOURCES