Skip to main content
Log in

Effects induced by an actin-polymerizing peptide in goldfish mauthner neurons

  • Published:
Neurophysiology Aims and scope

Abstract

In goldfishes, we studied (i) manifestations of functional activity of Mauthner neurons (MNs) reflected in motor behavior and (ii) changes in 3-D morphometry (ratio of volumes) and ultrastructure of MNs after applications of an actin-polymerizing peptide obtained from scorpion venom and after vestibular rotational stimulations (trainings) inducing natural modification of functions of the MNs (adaptation). In MNs subjected to application of the peptide, the increase in the functional resistance and morphological stability caused by long-lasting stimulation directly depended on the dose of the applied peptide or on the effectiveness of trainings, whereas in intact and control MNs such stimulation resulted in significant decreases in the activity and volumes of these cells. At the ultrastructure level, both applications of the peptide and trainings caused the formation of extensive bundles of actin filaments (“stress-fibers”) in the cytoplasm of MNs and led to an increase in the dimension of desmosome-like contacts (DLCs) in afferent synapses. At chemical synapses, the effect looked like a reciprocal decrease in the length of the active zones (a structural sign of long-term depression, LTD), while at mixed synapses this was manifested in an increase in the number of fibrillar bridges in the gaps of DLCs (a structural sign of long-term potentiation, LTP). The data obtained allow us to hypothesize that LTD of the efficacy of transmission through chemical synapses is involved in the formation of the adaptation state of the MNs and that polymerization of actin in the cytoplasm and DLCs underlies the mechanism of LTD and adaptation. The development of ultrastructural manifestations of LTP at mixed synapses after polymerization of actin by the peptide, which is related to a reciprocal increase in the efficacy of “mixed” afferent inputs, explains the maintenance of a high integral level of activity of the MNs, despite a drop in the functional activity of “ chemical” afferent inputs. Therefore, the actin cytoskeleton plays a clearly significant role in the maintenance of the balance of excitation at the neuronal level.

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. D. A. Moshkov, Adaptation and Ultrastructure of the Neuron [in Russian], Nauka, Moscow (1985).

    Google Scholar 

  2. D. A. Moshkov, L. L. Pavlik, N. R. Tiras, et al. “Ultrastructural changes in mixed synapses of Mauthner neurons related to long-term potentiation and natural modification of the motor function,” Neurophysiology, 35, No. 5, 361–370 (2003).

    Article  Google Scholar 

  3. N. R. Tiras and D. A. Moshkov, “A behavioral and ultrastructural study of the effect of application of colchicine on Mauthner neurons of the goldfish Carassius auratus,” Zh. Évol. Biokhim. Fiziol., 14, No. 5, 486–491 (1978).

    PubMed  CAS  Google Scholar 

  4. D. A. Moshkov, N. R. Tiras, and M. E. Saxon, “Phalloidin changes the synaptic contact ultrastructure,” Naturwissenschaften, 67, 194–195 (1980).

    Article  PubMed  CAS  Google Scholar 

  5. E. N. Bezgina, L. L. Pavlik, G. Z. Mikhailova, et al., “Morphofunctional effects of applications of glutamate and dopamine on the goldfish Mauthner neurons,” Neurophysiology, 38, No. 4, 320–330 (2006).

    Article  Google Scholar 

  6. A. E. Pereda, A. Triller, H. Korn, et al., “Dopamine enhances both electrotonic coupling and chemical excitatory postsynaptic potentials at mixed synapses,” Proc. Natl. Acad. Sci. USA, 89, 12088–12092 (1992).

    Google Scholar 

  7. D. A. Moshkov, N. F. Mukhtasimova, L. L. Pavlik, et al., “In vitro long-term potentiation of electrotonic responses of goldfish Mauthner cells is accompanied by ultrastructural changes at afferent mixed synapses,” Neuroscience, 88, No. 3, 591–605 (1998).

    Article  Google Scholar 

  8. L. L. Pavlik, N. R. Tiras, N. F. Mukhtasimova, et al., “Involvement of actin in electrotonic transmission through mixed synapses of goldfish Mauthner neurons,” Morfologiya, 123, No. 1, 41–47 (2003).

    CAS  Google Scholar 

  9. G. Z. Mikhailova, N. R. Tiras, E. E. Grigor’yeva, et al., “Rotational stimulation-related changes of the motor asymmetry in the goldfish,” Neurophysiology, 37, Nos. 5/6, 379–387 (2005).

    Article  Google Scholar 

  10. D. A. Moshkov, N. R Tiras, and V. V. Potemkin, “Effect of phalloidin and long-lasting sensory stimulation on ultrastructure of the goldfish Mauthner neurons,” Tsitologiya, 26, No 12, 1351–1356 (1984).

    Google Scholar 

  11. L. L. Pavlik, N. R. Tiras, D. A. Moshkov, “Actin in Mauthner neurons of the goldfish after treatment with phalloidin and adaptation to long-lasting natural stimulation,” Tsitologiya, 39, No. 12, 1109–1115 (1997).

    CAS  Google Scholar 

  12. N. R. Tiras, I. B. Mikheeva, D. A. Moshkov, et al., “Scorpion venom contains physiologically active compounds influencing the state of neuronal actin,” Dokl. Akad. Nauk SSSR, 368, No. 3, 416–419 (1999).

    CAS  Google Scholar 

  13. I. B. Mikheeva, N. R. Tiras, D. A. Moshkov, et al., “Desmosome-like contacts as targets for the action of scorpion venom,” Tsitologiya, 42, No. 7, 635–646 (2000).

    CAS  Google Scholar 

  14. N. R. Tiras, I. B. Mikheeva, P. I. Pakhotin, and D. A. Moshkov, “Morphofunctional studies of adapted Mauthner neurons of the goldfish under conditions of long-lasting incubation of the medulla,” Morfologiya, 122, No. 6, 19–24 (2002).

    CAS  Google Scholar 

  15. N. R. Tiras, I. B. Mikheeva, et al., “Morphofunctional modifications of incubated Mauthner neurons of the goldfish under the influence of peptides from scorpion venom,” Morfologiya, 123, No. 3, 40–45 (2003).

    CAS  Google Scholar 

  16. V. Jaravin, D. Nolde, M. Reibarkh, et al., “Three-dimentional structure of toxin osk1_from Orthochirus scrobiculosus scorpion venom,” Biochemistry, 36, No. 6, 1223–1232 (1997).

    Article  Google Scholar 

  17. N. R. Tiras, S. N. Udal’tsov, G. Z. Mikhailova, and D. A. Moshkov, “Identification of peptides from scorpion venom that interact with actin using electron microscopy,” Biol. Membr., 20, No. 1, 73–77 (2003).

    Google Scholar 

  18. N. R. Tiras, I. B. Mikheeva, D. A. Moshkov, et al., “Mauthner neurons of fishes as the test-object for screening of toxins of Arthropoda,” Dokl. Akad. Nauk SSSR, 364, No. 1, 121–125 (1999).

    Google Scholar 

  19. G. Z. Mikhailova, N. R. Tiras, V. D. Pavlik, et al., “Morphological parameters of Mauthner neurons of goldfishes with modified asymmetry of motor behavior,” Neurophysiology, 38, No. 1, 15–26 (2006).

    Article  Google Scholar 

  20. G. Z. Mikhailova, V. D. Pavlik, N. R. Tiras, et al., “Correlations of the dimensions of Mauthner neurons with the preference of goldfishes to turn rightward or leftward,” Morfologiya, 127, No. 2, 16–19 (2005).

    CAS  Google Scholar 

  21. L. L. Pavlik, N. R. Tiras, I. B. Shodina, and D. A. Moshkov, “Modifications of the actin cytoskeleton in goldfish Mauthner neurons after long-lasting stimulation,” Tsitologiya, 39, No. 7, 546–551 (1997).

    Google Scholar 

  22. N. R. Tiras, G. V. Zherdev, and D. A. Moshkov, “Ultrastructure of Mauthner cells in fish adapted to long-term vestibular stimulation and effect of ethanol,” J. Neural Plastic., 6, No. 4, 91–102 (1999).

    Article  CAS  Google Scholar 

  23. E. Lee, E. A. Shelden, and D. A. Knecht, “Formation of F-actin aggregates in cells treated with actin stabilizing drugs,” Cell Motil. Cytoskeleton, 39, 122–123 (1998).

    Article  PubMed  CAS  Google Scholar 

  24. N. R. Tiras, L. L. Pavlik, and D. A. Moshkov, “Detection of actin and the peculiarities of organization of the cytoskeleton of goldfish Mauthner neurons,” Tsitologiya, 32, No 4, 352–358 (1990).

    CAS  Google Scholar 

  25. N. R. Tiras, L. L. Pavlik, and D. A. Moshkov, “Alterations in the cytoskeleton of the goldfish Mauthner cells under various pharmacological treatments,” Acta Histochem., 41, 249–256 (1992).

    CAS  Google Scholar 

  26. N. R. Tiras, I. B. Mikheeva, D. A. Moshkov, et al., “Venom from black Central Asia scorpion defends Mauthner neurons from the injuring action of long-lasting stimulation,” Morfologiya, 113, 100–104 (1998).

    CAS  Google Scholar 

  27. N. R. Tiras and D. A. Moshkov, “Ultrastructure of afferent inhibitory and excitatory synapses of Mauthner neurons,” Tsitologiya, 29, No. 3, 288–294 (1987).

    Google Scholar 

  28. L. A. Kashapova, D. A. Moshkov, and E. N. Bezgina, “Active zones and plasticity of motor nerve terminals,” in: Plasticity of Motoneuronal Connections, Elsevier Sci. Publ. BV, Amsterdam (1991), pp. 163–173.

    Google Scholar 

  29. D. K. Ryugo, M. M. Wu, and T. Pongstaporn, “Activity-related features of synapse morphology: a study of endbulbs of Held,” J. Comp. Neurol., 365, No. 3, 141–158 (1996).

    Article  PubMed  CAS  Google Scholar 

  30. B. Geiger, Z. Avnur, T. Volberg, and T. Volk, “Molecular domains of adherent junctions,” in: The Cell in Contacts. Adhesions and Junctions as Morphogenetic Determinants, John Wiley and Sons, New York (1985), pp. 461–489.

    Google Scholar 

  31. X. D. Yang and D. S. Faber, “Initial synaptic efficacy influences induction and expression of long-term changes in transmission,” Proc. Natl. Acad. Sci. USA, 88, 4299–4303 (1992).

    Article  Google Scholar 

  32. K. S. Raevskii and V. P. Georgiev, Transmitter Amino Acids: Neuropharmacological and Neurochemical Aspects [in Russian], Meditsina, Moscow (1986).

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to N. R. Tiras, G. Z. Mikhailova or D. A. Moshkov.

Additional information

Neirofiziologiya/Neurophysiology, Vol. 38, Nos. 5/6, pp. 389–401, September–December, 2006.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Tiras, N.R., Mikhailova, G.Z. & Moshkov, D.A. Effects induced by an actin-polymerizing peptide in goldfish mauthner neurons. Neurophysiology 38, 327–337 (2006). https://doi.org/10.1007/s11062-006-0067-1

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11062-006-0067-1

Keywords

Navigation