Skip to main content
Log in

Reformation of specific synaptic connections by regenerating sensory axons in the spinal cord of the bullfrog

  • Published:
Neurochemical Pathology

Abstract

The regrowth of sensory axons into the spinal cord of juvenile bullfrogs was studied after disruption of these fibers in the dorsal root. Within 9 d after the root had been frozen, regenerating sensory axons had reached the spinal cord, as revealed by labeling with horseradish peroxidase. Growth into the spinal cord, however, was much slower. Even several months after denervation, very few fibers had reestablished any of their normal longitudinal projections within the dorsal funiculus. Eventually, however, sensory axons grew across the region and into the dorsal horn. Intracellular recordings from motoneurons revealed that these axons made functional reconnections with spinal neurons. Muscle sensory axons established direct, monosynaptic inputs to motoneurons, whereas cutaneous fibers innervated these neurons polysynaptically. Moreover, sensory afferents from a particular muscle distinguished among different classes of motoneurons, just as in normal frogs. Thus, specific synaptic pathways can be reestablished by regenerating sensory axons if they can reach their appropriate target region within the spinal cord.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Baker R. E. and Richter A. P. J. (1977) Development of dorsal root III afferent fibres in postmetamorphic juveniles of the frogDiscoglossus pictus.Neuroscience 2, 271–273.

    Article  PubMed  CAS  Google Scholar 

  • Bohn R. C. and Stelzner D. J. (1980) Denervation of nonoptic brain areas along the course of the optic tract does not affect the success of optic nerve regeneration in frogs.J. Comp. Neurol. 190, 763–779.

    Article  PubMed  CAS  Google Scholar 

  • David S. and Aguayo A. J. (1981) Axon elongation into peripheral nervous system “bridges” after central nervous system injury in adult rats.Science 214, 931–933.

    Article  PubMed  CAS  Google Scholar 

  • Davis M. R. and Constantine-Paton M. (1983) Hyperplasia in the spinal sensory system of the frog. I. Plasticity in the most caudal dorsal root ganglion.J. Comp. Neurol. 221, 444–452.

    Article  PubMed  CAS  Google Scholar 

  • Ecker A. (1889) The Anatomy of the Frog, G. Haslam (transl.). Clarendon, Oxford, UK.

    Google Scholar 

  • Farel P. B. (1971) Long-lasting habituation in spinal frogs.Brain Res. 33, 405–417.

    Article  PubMed  CAS  Google Scholar 

  • Frank E. and Westerfield M. (1982) Synaptic organization of sensory and motor neurons innervating triceps brachii muscles in the bullfrog.J. Physiol. (Lond.)324, 479–494.

    CAS  Google Scholar 

  • Frank E., Harris W. A., and Kennedy M. B. (1980) Lysophosphatidyl choline facilitates labelling of CNS projections with horseradish peroxidase.J. Neurosci. Methods 2, 183–189.

    Article  PubMed  CAS  Google Scholar 

  • Frank E., Jhaveri S., and Sah D. W. Y. (1982) Regeneration of sensory-motor synapses in the spinal cord.Soc. Neurosci. Abstr. 8, 916.

    Google Scholar 

  • Friedman B. and Aguayo A. J. (1985) Injured neurons in the olfactory bulb of the adult rat grow axons along grafts of peripheral nerves.J. Neurosci. 5, 1616–1625.

    PubMed  CAS  Google Scholar 

  • Gaze R. M. and Jacobson M. (1963) A study of the retinotectal projection during regeneration of the optic nerve in the frog.Proc. Roy. Soc. (Lond.)157, 420–448.

    Article  Google Scholar 

  • Gaze R. M. and Keating M. J. (1970) Further studies on the restoration of the contralateral retinotectal projection following regeneration of the optic nerve in the frog.Brain Res. 21, 183–195.

    Article  PubMed  CAS  Google Scholar 

  • Itoh K., Konishi A., Nomura S., Mizuno N., Nakamura Y., and Sugimoto T. (1979) Application of coupled oxidation reaction to electron microscopic demonstration of horseradish peroxidase: Cobalt-glucose oxidase method.Brain Res. 175, 341–346.

    Article  PubMed  CAS  Google Scholar 

  • Jhaveri S. and Frank E. (1983) Central projections of the brachial nerve in bull-frogs: Muscle and cutaneous afferents project to different regions of the spinal cord.J. Comp. Neurol. 221, 304–312.

    Article  PubMed  CAS  Google Scholar 

  • Katzenstein M. B. and Bohn R. C. (1984) Regeneration of transected dorsal root ganglion cell axons into the spinal cord of adult frogs (Xenopus laevis).Brain Res. 300, 188–191.

    Article  PubMed  CAS  Google Scholar 

  • Lichtman J. W. and Frank E. (1984) Physiological evidence for specificity of synaptic connections between individual sensory and motor neurons in the brachial spinal cord of the bullfrog.J. Neurosci. 4, 1745–1753.

    PubMed  CAS  Google Scholar 

  • Lichtman J. W., Jhaveri S., and Frank E. (1984) Anatomical basis of specific connections between sensory axons and motor neurons in the bullfrog’s brachial spinal cord.J. Neurosci. 4, 1754–1763.

    PubMed  CAS  Google Scholar 

  • Liuzzi F. J. and Lasek R. J. (1983) Regeneration of sensory and motor axons into the spinal cord of the adult frog. A study using dorsal-to-dorsal and ventral-to-dorsal anastomoses.Soc. Neurosci. Abstr. 9, 695.

    Google Scholar 

  • Liuzzi F. J. and Lasek R. J. (1984) Electron microscopy of HRP injury-filled regenerated axons in the adult frog spinal cord.Soc. Neurosci. Abstr. 10, 1086.

    Google Scholar 

  • Liuzzi F. J. and Lasek R. J. (1985) Regeneration of lumbar dorsal root axons into the spinal cord of adult frogs (Rana pipiens), an HRP study.J. Comp. Neurol. 232, 456–465.

    Article  PubMed  CAS  Google Scholar 

  • Perkins C. S., Carlstedt T., Mizuno K., and Aguayo A. J. (1980) Failure of regenerating dorsal root axons to regrow into the spinal cord.Can. J. Neurol. Sci. 7, 323–325.

    Google Scholar 

  • Piatt J. and Piatt M. (1958) Transection of the spinal cord in the adult frog.Anat. Rec. 131, 81–95.

    Article  PubMed  CAS  Google Scholar 

  • Purves D. and Hadley R. D. (1985) Changes in the dendritic branching of adult mammalian neurons revealed by repeated imagingin situ.Nature 315, 404–406.

    Article  PubMed  CAS  Google Scholar 

  • Sah D. W. Y. and Frank E. (1984) Regeneration of sensory-motor synapses in the spinal cord of the bullfrog.J. Neurosci. 4, 2784–2791.

    PubMed  CAS  Google Scholar 

  • Silver J. (1985) The changing astrocyte: Its role in CNS axon tract development, in regenerative failure, and during induced regeneration upon transplantation.VIIth Biennial Conference on Regeneration in the Central Nervous System, National Spinal Cord Injury Association, Abstract.

  • Straznicky K. and Gaze R. M. (1971) The growth of the retina inXenopus laevis: An autoradiographic study.J. Embryol. Exp. Morph. 26, 67–79.

    PubMed  CAS  Google Scholar 

  • Taylor C. P., Krnjevic K., and Ropert N. (1984) Facilitation of CA3 pyramidal cell firing by electrical fields generated antidromically.Neuroscience 11, 101–109.

    Article  PubMed  CAS  Google Scholar 

  • Westerfield M. and Frank E. (1982) Specificity of electrical coupling among neurons innervating forelimb muscles of the adult bullfrog.J. Neurophysiol. 48, 904–913.

    PubMed  CAS  Google Scholar 

  • Zakon H. and Capranica R. R. (1981) Reformation of organized connections in the auditory system after regeneration of the eighth nerve.Science 213, 242–244.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Frank, E., Sah, D.W. Reformation of specific synaptic connections by regenerating sensory axons in the spinal cord of the bullfrog. Neurochemical Pathology 5, 165–185 (1986). https://doi.org/10.1007/BF02842934

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF02842934

Index Entries

Navigation