Skip to main content
Log in

The Critical Role of Intracellular Calcium in the Mechanisms of Plasticity of Common Snail Defensive Behavior Command Neurons LPl1 and RPl1 in Nociceptive Sensitization

  • Published:
Neuroscience and Behavioral Physiology Aims and scope Submit manuscript

Abstract

Studies on semi-intact common snail preparations addressed the involvement of intracellular calcium in changes in the excitability and responses to sensory stimuli of defensive behavior command neurons LPl1 and RPl1 during the acquisition of nociceptive sensitization. Application of sensitizing stimuli to the heads of control snails led to depolarization of neuron membranes, increases in neuron excitability, and depression of the responses of neurons to sensory stimuli during the short-term stage, and marked facilitation of responses in the long-term stage of sensitization. Acquisition of sensitization during profound hyperpolarization of neurons led to suppression of the increase in excitability, along with depression of responses to chemical stimulation of the head in the short- and long-term stages of sensitization. Neuron responses to tactile stimulation of the head and foot showed synaptic facilitation, similar to that seen in neurons of control animals. Acquisition of sensitization during intracellular injection of the calcium chelators EGTA and BAPTA led to suppression of synaptic facilitation in the responses of neurons to both chemical and tactile stimulation. In these conditions, membrane excitability increased to a greater extent than in neurons of control animals. The results of these experiments suggest that changes in responses to sensory stimulation in sensitized snails are associated with postsynaptic calcium-dependent mechanisms of plasticity in neurons LPl1 and RPl1.

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

  1. P. M. Balaban and I. S. Zakharov, Learning and Development: A Common Basis for Two Phenomena [in Russian], Nauka, Moscow (1992).

    Google Scholar 

  2. N. A. Beregovoi, Kh. L. Gainutdinov, O. G. Safronova, and M. B. Shtark, “Electrophysiological and neurochemical studies of long-term sensitization in the common snail,” Byull. Éksperim. Biol. Med., 106, No. 9, 259 (1988).

    Google Scholar 

  3. N. I. Bravarenko, P. M. Balaban, and E. N. Sokolov, “Organization of the sensory input of the command neuron system,” Zh. Vyssh. Nerv. Deyat., 32, No. 1, 94 (1982).

    Google Scholar 

  4. T. Kh. Gainutdinova, V. V. Andrianov, and Kh. L. Gainutdinov, “The effects of 5,6-dihydroxytryptamine on membrane and threshold potentials in command neurons in long-term sensitization in the common snail,” Dokl. Ros. Akad. Nauk., 361, No. 2, 268 (1998).

    Google Scholar 

  5. V. D. Goncharuk, S. A. Kozyrev, and V. P. Nikitin, “Acquisition of sensitization in the common snail: morphofunctional correlates in defensive behavior command neurons,” Neirofiziologiya, 1, No. 2, 150 (1993).

    Google Scholar 

  6. T. N. Grechenko, “Characteristics of the formation of conditioned responses in isolated LPa3 neurons in the common snail,” Zh. Vyssh. Nerv. Deyat., 39, No. 6, 1170 (1989).

    Google Scholar 

  7. L. N. Grechenko, “Protein metabolism in the formation of a defensive reflex in mollusks,” Zh. Vyssh. Nerv. Deyat., 42, No. 6, 1221 (1992).

    Google Scholar 

  8. L. N. Grechenko and G. V. Vasil'ev, “Possible molecular-cellular mechanisms regulating gene expression in learning,” Ros. Fiziol. Zh. im. I. M. Sechenova, 85, No. 1, 48 (1999).

    Google Scholar 

  9. T. L. D'yakonova, “The role of cAMP in supporting the plastic properties of the electrically excitable neuron membranes,” Zh. Vyssh. Nerv. Deyat., 37, No. 1, 106 (1987).

    Google Scholar 

  10. T. L. D'yakonova and T. M. Turpaev, “Plasticity of the electrically excitable neuron membrane: possible role of calcium ions,” Dokl. Akad. Nauk SSSR, 271, No. 5, 1261 (1983).

    Google Scholar 

  11. V. A. Dyatlov, “Receptors for ionotropic transmitters in common snail neurons: ionic nature and mechanisms of regulation of functions and topography,” Zh. Vyssh. Nerv. Deyat., 43, No. 5, 969 (1993).

    Google Scholar 

  12. N. I. Kononenko, “The effects of intracellular injections of cyclic adenosine monophosphate on the calcium current in identified common snail neurons,” Neirofiziologiya, 14, No. 3, 290 (1982).

    Google Scholar 

  13. O. A. Maksimova and P. M. Balaban, Neuronal Mechanisms of the Plasticity of Behavior [in Russian], Nauka, Moscow (1983).

    Google Scholar 

  14. A. Yu. Malyshev, N. I. Bravarenko, A. S. Pivovarov, and P. M. Balaban, “The effects of serotonin levels on postsynaptically induced potentiation of snail neuron responses,” Zh. Vyssh. Nerv. Deyat., 47, No. 3, 553 (1997).

    Google Scholar 

  15. V. P. Nikitin, “A transient stage of long-term synaptic facilitation in defensive behavior command neurons in sensitized snails,” Ros. Fiziol. Zh. im. I. M. Sechenova, 85, No. 1, 35 (1999).

    Google Scholar 

  16. V. P. Nikitin and S. A. Kozyrev, “Dynamics of defensive and feeding reactions in the acquisition of sensitization in the common snail,” Zh. Vyssh. Nerv. Deyat., 41, No. 3, 478 (1991).

    Google Scholar 

  17. V. P. Nikitin and S. A. Kozyrev, “Action of protein synthesis inhibitors on the neuronal mechanisms of sensitization in the common snail,” Neirofiziologiya, 25, No. 2, 109 (1993).

    Google Scholar 

  18. V. P. Nikitin and S. A. Kozyrev, “The effects of cAMP on the excitability and responses of defensive behavior command neurons evoked by sensory stimuli in the common snail,” Ros. Fiziol. Zh. im. I. M. Sechenova, 85, No. 2, 237 (1999).

    Google Scholar 

  19. V. P. Nikitin, S. A. Kozyrev, and M. O. Samoilov, “Conditioning and sensitization in the common snail: neurophysiological and metabolic characteristics,” Zh. Vyssh. Nerv. Deyat., 42, No. 6, 1260 (1992).

    Google Scholar 

  20. V. P. Nikitin, S. A. Kozyrev, and A. V. Shevelkin, “NMDA glutamate receptor antagonists have selective influences on the synaptic mechanisms of nociceptive sensitization in the snail,” Zh. Vyssh. Nerv. Deyat., 50, No. 3, 601 (2000).

    Google Scholar 

  21. V. P. Nikitin, M. O. Samoilov, and S. A. Kozyrev, “Mechanisms of the acquisition of sensitization in the common snail: involvement of calcium and calmodulin,” Zh. Vyssh. Nerv. Deyat., 42, No. 6, 1250 (1992).

    Google Scholar 

  22. T. P. Norekyan and D. B. Logunov, “Comparison of the plasticity of the monosynaptic inputs of command neurons in the common snail with the plastic properties of the chemoreceptor membrane during the process of rhythmic stimulation,” Neirofiziologiya, 17, No. 2, 279 (1985).

    Google Scholar 

  23. A. S. Pivovarov, “Cholinoreceptors of common snail neurons: identification, plasticity, and its regulation by opioids and second messengers,” Zh. Vyssh. Nerv. Deyat., 42, No. 6, 1271 (1992).

    Google Scholar 

  24. E. N. Sokolov, Neuronal Mechanisms of Memory and Learning [in Russian], Nauka, Moscow (1981).

    Google Scholar 

  25. A. V. Shevelkin, V. P. Nikitin, S. A. Kozyrev, et al., “Serotonin imitates several of the neuronal effects of nociceptive sensitization in the common snail,” Zh. Vyssh. Nerv. Deyat., 47, No. 3, 532 (1997).

    Google Scholar 

  26. L. E. Tsitolovskii, “Integrative activity of nerve cells during recording of memory traces,” Usp. Fiziol. Nauk., 17, No. 2, 83 (1986).

    Google Scholar 

  27. J. X. Bao, E. R. Kandel, and R. D. Hawkins, “Involvement of presynaptic and postsynaptic mechanisms in a cellular analog of classical conditioning of Aplysia sensory-motor neuron synapses in isolated cell culture,” J. Neurosci., 18, No. 1, 458 (1998).

    Google Scholar 

  28. Y. D. Bogdanov, P. M. Balaban, D. A. Poteryaev, et al, “Putative neuropeptides and an EF-hand motif region are encoded by a novel gene expressed in the four giant interneurons of the terrestrial snail,” Neurosci., 85, 637 (1998).

    Google Scholar 

  29. X. Y. Lin and D. L. Glanzman, “Long-term potentiation of Aplysia sensorimotor synapses in cell culture: regulation by postsynaptic voltage,” Proc. Roy. Soc. B. Biol. Sci., 255, No. 1343, 113 (1994).

    Google Scholar 

  30. R. C. Malenka and R. A. Nicoll, “Long-term potentiation – a decade of progress?” Science, 285, No. 5435, 1870 (1999).

    Google Scholar 

  31. M. L. Mayer and G. L. Westbrook, “The physiology of excitatory amino acids in the vertebrate central nervous system,” Progr. Neurobiol., 28, 197 (1987).

    Google Scholar 

  32. G. G. Murphy and D. L. Glanzman, “Enhancement of sensorimotor connections by conditioning-related stimulation in Aplysia depends upon postsynaptic Ca2+,” Proc. Natl. Acad. Sci. USA, 93, No. 18, 9931 (1996).

    Google Scholar 

  33. L. E. Trudeau and V. F. Castellucci, “Postsynaptic modifications in long-term facilitation in Aplysia: upregulation of excitatory amino acid receptors,” J. Neurosci., 15, No. 2, 1275 (1995).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Nikitin, V.P., Kozyrev, S.A. The Critical Role of Intracellular Calcium in the Mechanisms of Plasticity of Common Snail Defensive Behavior Command Neurons LPl1 and RPl1 in Nociceptive Sensitization. Neurosci Behav Physiol 33, 513–519 (2003). https://doi.org/10.1023/A:1023423519777

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1023423519777

Keywords

Navigation