Summary
The effects of the venom of the spider Latrodectus mactans hasselti on the superior cervical ganglion were studied in the guinea pig. Under anaesthesia the ganglion was bathed in venom solution for 15 min. Shortly afterwards animals salivated profusely and later developed unilateral ptosis and enophthalmos. Postoperative survival times ranged from 15 min to 10 weeks. Electron microscopy showed acute swelling of preganglionic cholinergic nerve terminals, followed by degeneration with separation of synapses. Other ganglionic elements appeared to be undamaged, although after detachment of synapses the dendritic postsynaptic specializations were reduced in number. Recovery was very rapid; axon growth cones were identifiable at 18 h and synapse reformation was well established by 2 weeks. With longer survival times there was progressive restoration of normal morphology such that by 8 weeks regeneration appeared complete. These experiments indicate that the preganglionic cholinergic nerve terminals are selectively affected by Latrodectus venom and have a considerable capacity for appropriate regeneration.
Similar content being viewed by others
References
Al-Khafaji, F. A. H., Anderson, P. N., Mitchell, J. &Mayor, D. (1983) The permeability of autonomic ganglia to horseradish peroxidase.Journal of Anatomy 137, 675–82.
Black, I. B., Chikaraishi, D. M. &Lewis, E. J. (1985) Trans-synaptic increase in RNA coding for tyrosine hydroxylase in a rat sympathetic ganglion.Brain Research 339, 151–3.
Bray, G. M. &Aguayo, A. J. (1974) Regeneration of peripheral unmyelinated nerves. Fate of the axonal sprouts which develop after injury.Journal of Anatomy 117, 517–29.
Bunge, M. B. (1973) Fine structure of nerve fibers and growth cones of isolated sympathetic neurons in culture.Journal of Cell Biology 56, 713–35.
Byrne, G. C. &Pemberton, P. J. (1983) Red-back spider (Latrodectus mactans hasselti) envenomation in a neonate.Medical Journal of Australia 2, 665–6.
Chmouliovsky, M., Dunant, Y., Graf, J., Straub, R. W. &Rufener, C. (1972) Inhibition of creatine phosphokinase activity and synaptic transmission by black widow spider venom.Brain Research 44, 289–93.
Dail, W. G. &Barton, S. (1983) Structure and organization of mammalian sympathetic ganglia. InAutonomic Ganglia (edited byElfvin, L.-G.), pp. 3–26. New York: John Wiley.
Deitch, J. A. &Rubel, E. W. (1984) Afferent influences on brain stem auditory nuclei of the chicken: time course and specificity of dendritic atrophy following deafferentation.Journal of Comparative Neurology 229, 66–79.
Duchen, L. W., Gomez, S. &Queiroz, L. S. (1981) The neuromuscular junction of mouse after black widow spider venom.Journal of Physiology 316, 279–91.
Dun, N. J. (1983) Peptide hormones and transmission in sympathetic ganglia. InAutonomic Ganglia (edited byElfvin, L.-G.), pp. 345–66. New York: John Wiley.
Dyck, P. J. &Hopkins, A. P. (1972) Electron microscopic observations on degeneration and regeneration of unmyelinated nerve fibres.Brain 95, 223–34.
Einhorn, V. F. &Hamilton, R. C. (1973) Transmitter release by red back spider venom.Journal of Pharmacy and Pharmacology 25, 824–6.
Elfvin, L.-G. (1963a) The ultrastructure of the superior cervical sympathetic ganglion of the cat I. The structure of ganglion cell processes as studied by serial sections.Journal of Ultrastructure Research 8, 403–40.
Elfvin, L.-G. (1963b) The ultrastructure of the superior cervical sympathetic ganglion of the cat II. The structure of the preganglionic fibers and the synapses as studied by serial sections.Journal of Ultrastructure Research 8, 441–76.
Flecknell, P. A. &Mitchell, M. (1984) Midazolam and fentanyl-fluanisone: assessment of anaesthetic effects in laboratory rodents and rabbits.Laboratory Animals 18, 143–6.
Forehand, C. J. (1985) Density of somatic innervation on mammalian autonomic ganglion cells is inversely related to dendritic complexity and preganglionic convergence.Journal of Neuroscience 5, 3403–8.
Fritz, L. C., Tzeng, M.-C. &Mauro, A. (1980) Different components of black widow spider venom mediate transmitter release at vertebrate and lobster neuromuscular junctions.Nature 283, 486–7.
Frontali, N. (1972) Catecholamine-depleting effect of black widow spider venom on iris nerve fibres. Brain Research37, 146–80.
Frontali, N., Ceccarelli, B., Gorio, A., Mauro, A., Siekevitz, P., Tzeng, M.-C. &Hurlbut, W. P. (1976) Purification from black widow spider venom of a protein factor causing the depletion of synaptic vesicles at neuromuscular junction.Journal of Cell Biology 68, 462–79.
Gabella, G. (1976)Structure of the Autonomic Nervous System, pp. 3–45. London: Chapman and Hall.
Gorio, A. &Mauro, A. (1979) Reversibility and mode of action of black widow spider venom on the vertebrate neuromuscular junction.Journal of General Physiology 73, 245–63.
Hamilton, R. C. &Robinson, P. M. (1973) Disappearance of small vesicles from adrenergic nerve endings in the rat vas deferens caused by red back spider venom.Journal of Neurocytology 2, 465–9.
Hamori, J., Láng, E. &Simon, L. (1968) Experimental degeneration of the preganglionic fibers in the superior cervical ganglion of the cat. An electron microscope study.Zeitschrift für Zellforschung und mikroskopische Anatomic 90, 37–52.
Heuser, J. E. &Reese, T. S. (1973) Evidence of recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction.Journal of Cell Biology 57, 315–44.
Hume, R. I. &Purves, D. (1981) Geometry of neonatal neurones and the regulation of synapse elimination.Nature 293, 469–71.
Hunt, C. C. &Nelson, P. G. (1965) Structural and functional changes in the frog sympathetic ganglion following cutting of the presynaptic nerve fibres.Journal of Physiology 177, 1–20.
Hurlbut, W. P. &Ceccarelli, B. (1979) Use of black widow spider venom to study the release of neurotransmitters. InNeurotoxins: Tools in Neurobiology (edited byCeccarelli, B. &Clementi, F.), pp. 87–115. New York: Raven Press.
Maehlen, J. &Nj↠, A. (1982) The effects of electrical stimulation on sprouting after partial denervation of guinea-pig sympathetic ganglion cells.Journal of Physiology 322, 151–66.
Maretic, Z. (1978) Epidemiology of envenomation, symptomatology, pathology and treatment. InHandbook of Experimental Pharmacology, Vol. 48,Arthropod Venoms. (edited byBellini, S.), pp. 185–212. Berlin: Springer-Verlag.
Maretic, Z. &Jelasic, F. (1953) Uber den Einfluss des toxins der spinneLatrodectus tredecimguttatus auf das nervensystem.Acta tropica 10, 209–24.
Matthews, M. R. (1983) The ultrastructure of junctions in the sympathetic ganglia of mammals. InAutonomic Ganglia (edited byElfvin, L.-G.), pp. 27–66. New York: John Wiley.
Matthews, M. R. &Nelson, V. H. (1975) Detachment of structurally intact nerve endings from chromatolytic neurones of rat superior cervical ganglia during the depression of synaptic transmission induced by postganglionic axotomy.Journal of Physiology 245, 91–135.
McLachlan, E. M. (1974) The formation of synapses in mammalian sympathetic ganglia reinnervated with preganglionic or somatic nerves.Journal of Physiology 237, 217–42.
Njå, A. &Purves, D. (1977) Re-innervation of guinea-pig superior cervical ganglia by preganglionic fibres arising from different levels of the spinal cord.Journal of Physiology 272, 633–51.
Njå, A. &Purves, D. (1978a) The effects of nerve growth factor and its antiserum on synapses in the superior cervical ganglion of the guinea-pig.Journal of Physiology 277, 53–75.
Njå, A. &Purves, D. (1978b) Specificity of initial synaptic contacts made on guinea-pig superior cervical ganglion cells during regeneration of the cervical sympathetic trunk.Journal of Physiology 281, 45–62.
Östberg, A. J. C., Raisman, G., Field, P. M., Iverson, L. L. &Zigmond, R. E. (1976) A quantitative comparison of the formation of synapses in the rat superior cervical sympathetic ganglion by its own and foreign nerves.Brain Research 107, 445–70.
Purves, D. (1976) Competitive and non-competitive reinnervation of mammalian sympathetic neurons by and foreign fibers.Journal of Physiology 261, 453–75.
Queiroz, L. S. &Duchen, L. W. (1982) Effects ofLatrodectus spider venoms on sensory and motor nerve terminals of muscle spindles.Proceedings of the Royal Society of London, Series B 216, 103–10.
Quilliam, J. D. &Tamarind, J. P. (1972) Electron microscopy of degenerative changes in decentralized rat superior cervical ganglia.Micron 3, 454–72.
Raisman, G., Field, P. M., Östberg, A. J. C., Iversen, L. L. &Zigmond, R. E. (1974) A quantitative ultrastructural and biochemical analysis of the process of reinnervation of the superior cervical ganglion in the adult rat.Brain Research 71, 1–16.
Ramsay, D. A. &Matthews, M. R. (1985) Denervationinduced formation of adrenergic synapses in the superior cervical sympathetic ganglion of the rat and the enhancement of this effect by postganglionic axotomy.Neuroscience 16, 997–1026.
Rouiller, C. H., Nicolescu, P., Orci, L. &Rufener, C. (1971) The effect of anoxia on the ultrastructure of the superior cervical ganglion of the ratin vitro.Virchoivs Archives (Abteilung B. Zellpathologie) 7, 269–92.
Schafer, T., Schwab, M. E. &Thoenen, H. (1983) Increased formation of preganglionic synapses and axons due to a retrograde trans-synaptic action of nerve growth factor in the rat sympathetic nervous system.Journal of Neuroscience 3, 1501–10.
Smolen, A. J., Beaston-Wimmer, P., Wright, L. L., Lindley, T. &Cader, C. (1985) Neurotransmitter synthesis, storage, and turnover in neonatally deafferented sympathetic neurons.Developmental Brain Research 23, 211–18.
Sugimoto, T. &Gobel, S. (1984) Dendritic changes in the spinal dorsal horn following transection of a peripheral nerve.Brain Research 321, 199–208.
Thomas, P. K. (1963) The connective tissue of peripheral nerve: an electron microscope study.Journal of Anatomy 97, 35–44.
Tzeng, M.-C. &Siekevitz, P. (1978) The effect of the purified major protein factor (α-latrotoxin) of black widow spider venom on the release of acetylcholine and norepinephrine from mouse cerebral cortex slices.Brain Research 139, 190–6.
Voyvodic, J. T. (1987) Development and regulation of dendrites in the rat superior cervical ganglion.Journal of Neuroscience 7, 904–12.
Wiener, S. (1961) Red back spider bite in Australia. An analysis of 167 cases.Medical Journal of Australia 2, 44–9.
Wiley, R. G., Spencer, C. &Pysh, J. J. (1987) Time course and frequency dependence of synaptic vesicle depletion and recovery in electrically stimulated sympathetic ganglia.Journal of Neurocytology 16, 359–72.
Wisniewski, H. M., Ghetti, B. &Horoupian, D. S. (1972) The fate of synaptic membranes of degenerating optic nerve terminals and their role in the mechanism of trans-synaptic changes.Journal of Neurocytology 1, 297–310.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Daniel, S.E. Degeneration and regeneration in the superior cervical sympathetic ganglion afterLatrodectus venom. J Neurocytol 18, 407–421 (1989). https://doi.org/10.1007/BF01190843
Received:
Revised:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01190843