Skip to main content
The Journal of Physiology logoLink to The Journal of Physiology
. 1974 Oct;242(2):289–305. doi: 10.1113/jphysiol.1974.sp010708

Persistent modification of synaptic interactions between sensory and motor nerve cells following discrete lesions in the central nervous system of the leech

J K S Jansen Jr, K J Muller, J G Nicholls
PMCID: PMC1330668  PMID: 4376167

Abstract

We have examined changes that develop in the synaptic interactions of sensory and motor nerve cells following surgical lesions to the central nervous system of the leech. In one type of operation an individual ganglion was isolated from the rest of the nervous system by severing all the incoming and outgoing fibres. During the next few weeks, marked changes appeared in synaptic interactions.

1. In chronically isolated ganglia inhibitory potentials were recorded in the motoneurone which raises the skin into ridges (the AE cell) following impulses in sensory neurones that respond to pressure (P) or noxious (N) stimuli. In contrast the same AE cell in ganglia taken from normal animals shows excitatory synaptic potentials when the P or N sensory cells are stimulated.

2. Another altered synaptic interaction in ganglia isolated by lesions was that between sensory cells responding to touch and a motoneurone that supplies longitudinal muscles (L cell). Instead of the pure, electrical coupling potential seen normally, a large, additional chemically mediated excitatory potential was also apparent.

3. Some of the changes in synaptic interactions were not restricted to synapses within the isolated ganglion, but appeared gradually over the following year in successive ganglia along the length of the ventral nerve cord.

4. Indirect evidence suggests that the altered synaptic potentials that became conspicuous after operations are also present but smaller and obscured in normal animals.

5. It is concluded that some synapses in the leech nervous system are more readily changed than others by cutting the connectives. Furthermore, these changes influence in a predictable manner the way in which the animal behaves in response to mechanical stimuli.

Full text

PDF
292

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. Chemical and electrical synaptic connexions between cutaneous mechanoreceptor neurones in the central nervous system of the leech. J Physiol. 1969 Aug;203(3):591–609. doi: 10.1113/jphysiol.1969.sp008881. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. 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]
  3. COGGESHALL R. E., FAWCETT D. W. THE FINE STRUCTURE OF THE CENTRAL NERVOUS SYSTEM OF THE LEECH, HIRUDO MEDICINALIS. J Neurophysiol. 1964 Mar;27:229–289. doi: 10.1152/jn.1964.27.2.229. [DOI] [PubMed] [Google Scholar]
  4. Galun R., Kindler S. H. Chemical specificity of the feeding response in Hirudo medicinalis (L.). Comp Biochem Physiol. 1966 Jan;17(1):69–73. doi: 10.1016/0010-406x(66)90008-9. [DOI] [PubMed] [Google Scholar]
  5. Jansen J. K., Lomo T., Nicolaysen K., Westgaard R. H. Hyperinnervation of skeletal muscle fibers: dependence on muscle activity. Science. 1973 Aug 10;181(4099):559–561. doi: 10.1126/science.181.4099.559. [DOI] [PubMed] [Google Scholar]
  6. 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]
  7. Kandel E. R., Spencer W. A. Cellular neurophysiological approaches in the study of learning. Physiol Rev. 1968 Jan;48(1):65–134. doi: 10.1152/physrev.1968.48.1.65. [DOI] [PubMed] [Google Scholar]
  8. Kuffler S. W., Dennis M. J., Harris A. J. The development of chemosensitivity in extrasynaptic areas of the neuronal surface after denervation of parasympathetic ganglion cells in the heart of the frog. Proc R Soc Lond B Biol Sci. 1971 Apr 27;177(1049):555–563. doi: 10.1098/rspb.1971.0047. [DOI] [PubMed] [Google Scholar]
  9. Lomo T., Rosenthal J. Control of ACh sensitivity by muscle activity in the rat. J Physiol. 1972 Mar;221(2):493–513. doi: 10.1113/jphysiol.1972.sp009764. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. MILEDI R. The acetylcholine sensitivity of frog muscle fibres after complete or partial devervation. J Physiol. 1960 Apr;151:1–23. [PMC free article] [PubMed] [Google Scholar]
  11. Muller K. J., Nicholls J. G. Different properties of synapses between a single sensory neurone and two different motor cells in the leech C.N.S. J Physiol. 1974 Apr;238(2):357–369. doi: 10.1113/jphysiol.1974.sp010529. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Nicholls J. G., Baylor D. A. Specific modalities and receptive fields of sensory neurons in CNS of the leech. J Neurophysiol. 1968 Sep;31(5):740–756. doi: 10.1152/jn.1968.31.5.740. [DOI] [PubMed] [Google Scholar]
  13. Nicholls J. G., Purves D. A comparison of chemical and electrical synaptic transmission between single sensory cells and a motoneurone in the central nervous system of the leech. J Physiol. 1972 Sep;225(3):637–656. doi: 10.1113/jphysiol.1972.sp009961. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Nicholls J. G., Purves D. Monosynaptic chemical and electrical connexions between sensory and motor cells in the central nervous system of the leech. J Physiol. 1970 Aug;209(3):647–667. doi: 10.1113/jphysiol.1970.sp009184. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Purves D., McMahan U. J. The distribution of synapses on a physiologically identified motor neuron in the central nervous system of the leech. An electron microscope study after the injection of the fluorescent dye procion yellow. J Cell Biol. 1972 Oct;55(1):205–220. doi: 10.1083/jcb.55.1.205. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Stuart A. E. Physiological and morphological properties of motoneurones in the central nervous system of the leech. J Physiol. 1970 Aug;209(3):627–646. doi: 10.1113/jphysiol.1970.sp009183. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Wiesel T. N., Hubel D. H. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol. 1965 Nov;28(6):1029–1040. doi: 10.1152/jn.1965.28.6.1029. [DOI] [PubMed] [Google Scholar]
  18. Yoon M. Reversibility of the reorganization of retinotectal projection in goldfish. Exp Neurol. 1972 Jun;35(3):565–577. doi: 10.1016/0014-4886(72)90128-8. [DOI] [PubMed] [Google Scholar]

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

RESOURCES