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Evidence for Activity-Dependent Modulation of Sensory-Terminal Excitability in Spindles by Glutamate Release From Synaptic-Like Vesicles

  • Robert W. Banks
  • Guy S. Bewick
  • Brian Reid
  • Christine Richardson
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 508)

Abstract

Sensory terminals of muscle spindles and similar mechanosensory neurons contain large numbers of 50 nm, “synaptic-like” vesicles (SLVs), about whose role very little is known. Using fluorescence microscopy, immunocytochemistry and electrophysiological recording, we present evidence that SLVs undergo a recycling process, and that they release glutamate that has an autogenic excitatory effect on mechanosensory transduction, probably involving a metabotropic receptor linked to phospholipase D. The rate of recycling of SLVs is activity dependent, at least in part, as shown by an increased rate of destaining of preparations labelled with FM 143 during high-frequency, small-amplitude vibration. Immunogold labelling showed levels of glutamate-like reactivity in the sensory terminals at least as great as in probable la presynaptic terminals in the spinal cord. Exogenously applied glutamate has an excitatory effect on the spindle’s response to stretch, which is blocked by 3,5-dihydroxyphenylglycine.

Keywords

Muscle Spindle Spike Count Spider Venom Sensory Terminal Lumbrical Muscle 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

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References

  1. Adal, M. N., 1969, The fine structure of the sensory region of cat muscle spindlesJournal of Ultrastructure Research26,332–354.PubMedCrossRefGoogle Scholar
  2. Albani-Torregrossa, S., Attucci, S., Marinozzi, M., Pellicciari, R., Moroni, F. & Pellegrini-Giampietro, D. E., 1999, Antagonistic pharmacology of metabotropic glutamate receptors coupled to phospholipase D activation in adult rat hippocampus: focus on (2R,1’S,2’R,3’S)-2-(2’-carboxy-3’-phenylcyclopropyl)glycine versus 3,5-dihydroxyphenylglycineMolecular Pharmacology55, 699–707.PubMedGoogle Scholar
  3. Banks, R. W., and Barker, D., 2002, The muscle spindle, in:Myology3rd edition, A. G. Engel and C. FranziniArmstrong, eds., McGraw-Hill, New York, in press.Google Scholar
  4. Betz, W. J., Mao, F., and Bewick, G. S., 1992, Activity-dependent fluorescent staining and destaining of living vertebrate motor nerve terminalsJournal of Neuroscience12, 363–375.PubMedGoogle Scholar
  5. de Camilli, P., Vitadello, M., Canevini, M. P., Zanoni, R, Jahn R., and Gorio, A., 1988, The synaptic vesicle proteins synapsin I and synaptophysin (protein P38) are concentrated both in efferent and afferent nerve endings of the skeletal muscleJournal of Neuroscience8, 1625–1631.PubMedGoogle Scholar
  6. Engberg, I., Tarnawa, I., Durand, J., and Ouardouz, M., 1993, An analysis of synaptic transmission to motoneurons in the cat spinal cord using a new selective receptor blockerActa Physiologica Scandinavica148, 97–100.PubMedCrossRefGoogle Scholar
  7. Exton, J. H., 1997, Phospholipase D: enzymology, mechanisms of regulation, and functionPhysiological Reviews, 77, 303–320.Google Scholar
  8. Hammond, C., 2001Cellular and Molecular Neurobiology2nd edition, Academic Press, London, pp. 314–326.Google Scholar
  9. Hunt, C. C., Wilkinson, R. S., and Fukami, Y., 1978, Ionic basis of the receptor potential in primary endings of mammalian muscle spindles, Journal of General Physiology, 71, 683–698.PubMedCrossRefGoogle Scholar
  10. Mizote, M., and Takano, K., 1985, The response of cat muscle spindle primary endings to FM muscle vibration during fusimotor stimulation or following local injection of tetanus toxin, in: The Muscle Spindle, I. A. Boyd, and M. H. Gladden, eds. Macmillan, Basingstoke, pp. 365–369.Google Scholar
  11. Queiroz, L. S., and Duchen, L. W., 1982, Effects of Latrodectus spider venoms on sensory and motor nerve terminals of muscle spindles, Proceedings of the Royal Society of London. Series B: Biological Sciences, 216, 103–110.CrossRefGoogle Scholar
  12. Storm-Mathisen, J., Leknes, A. K., Bore, A. T., Vaaland, J. L., Edminson, P., Haug, F.-M. S., and Ottersen, O. P., 1983, First visualization of glutamate and GABA in neurones by immunocytochemistry, Nature, 301, 517–520.PubMedCrossRefGoogle Scholar
  13. Walmsley, B., and Bolton, P. S., 1994, An in vivo pharmacological study of single group Ia fibre contacts with motoneurones in the cat spinal cord, Journal of Physiology, 481, 731–741.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Robert W. Banks
    • 1
  • Guy S. Bewick
    • 2
  • Brian Reid
    • 2
  • Christine Richardson
    • 1
  1. 1.University of DurhamDurhamUK
  2. 2.University of AberdeenAberdeenUK

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