Skip to main content
SpringerLink
Log in

Neuronal analysis of hunting behavior of the pteropod molluscClione limacina

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

Abstract

The neurons of the cerebral ganglia controlling the movements of the hunting apparatus of the predatory pelagic pteropod mollusc, Clione limacina, are described in detail. A large group of high-threshold, electrically interconnected neurons, A, was identified, the impulse activity of which leads to the opening of the skin folds and the forward ejection of the hunting tentacles of the clione. Group B neurons which exhibit a constant background activity and which receive powerful inhibitory inputs from the A cells, conversely, induce the contraction and the withdrawal of the hunting tentacles into the head. The third group, are the C neurons, the impulse activity of which leads to the drawing together of the skin folds covering the hunting apparatus. The effect of such mediators as serotonin, dopamine, and gamma aminobutyric acid acid on the identified neurons was investigated. Serotonin depolarizes both A and B neurons, but the activation of the hunting apparatus appears to be an integrated effect: the activated A neurons inhibit the B neurons due to powerful IPSP, interrupting the direct excitatory effect of serotonin. Dopamine in various concentrations exerts the opposite effect: at low concentrations only B cells are activated and the tentacles are withdrawn into the head; at high concentrations the A neurons begin to operate; these neurons inhibit the B cells and activate the hunting apparatus. GABA exerts an integral, well-coordinated effect on the neurons controlling the movements of the hunting apparatus, and effect which is directed toward the activation of hunting behavior: it depolarizes-activates A neurons and hyperpolarizes-inhibits B and C neurons.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  1. Yu. I. Varshavskii, I. M. Gel'fand, T. G. Delyagina, E. S. Meyzerov, et al., “Certain mechanisms of the control of locomotion in the pteropod mollusc Clione limacina,”Zh. Obshch. Biologii,48, No. 3, 325–339 (1987).

    Google Scholar 

  2. Yu. M. Burmistrov, “The circulation of the nerve impulse in the system of lateral giant axons of the crayfish,”Biofizika,10, 90–97 (1965).

    Google Scholar 

  3. N. P. Wagner,Invertebrates of the White Sea, Vol. 1 [in Russian], Saint-Petersburg, (1885).

  4. E. A. Kabotyanskii and D. A. Sakharov, “Neuronal correlates of serotonin-dependent behavior of the pteropod mollusc clione,”Zh. Vyssh. Nerv. Deyat.,40, No. 4, 739–753 (1990).

    Google Scholar 

  5. N. M. Litvinova and G. N. Orlovskii, “Alimentary behavior of the pteropod molluscClione limacina,”Byul. MOIP. Old. Biol.,90, No. 4, 73–77 (1985).

    Google Scholar 

  6. T. P. Norekyan, I. S. Zakharov, and P. M. Balaban, “Neurophysiological mechanisms of change in the reaction to defensive stimuli during the activation of alimentary behavior in the pteropod molluscClione limacina,”Dokl. AN SSSR,302, No. 2, 491–494 (1988).

    Google Scholar 

  7. D. A. Sakharov and E. A. Kabotyanskii, “The integration of behavior of a pteropod mollusc by dopamine and serotonin,”Zh. Obshch. Biol.,47, No. 2, 234–245 (1986).

    Google Scholar 

  8. A. A. Ukhtomskii,The Doctrine of the Dominant, in:Collected Works, Vol. 1 [in Russian], Leningrad (1950).

  9. Zh. P. Shuranova and Yu. M. Burmistrov,The Neurophysiology of the Crayfish [in Russian], Nauka, Moscow (1988).

    Google Scholar 

  10. G. Chapman, “The hydrostatic skeleton in the invertebrates,”Biol. Rev. of the Cambridge Philos. Society,33 (3), 338–371 (1985).

    Google Scholar 

  11. B. Dale, “Blood pressure and its hydraulic function inHelix pomatia L.,”J. Exptl. Biol.,59, No. 2, 477–490 (1973).

    Google Scholar 

  12. B. Dale, “Extrusion, retraction and respiratory movements inHelix pomatia in relation to distribution and circulation of the blood,”J. Zool.,173, No. 3, 427–439 (1974).

    Google Scholar 

  13. B. Granzow and S. B. Kater, “Identified higher-order neurons controlling the feeding motor program ofHelisoma,”Neuroscience,2, 1049–1063 (1977).

    Google Scholar 

  14. E. A. Kabotyanski and D. A. Sakharov, “Monoamine-dependent behavioral states in the pteropod mollusc Clione limacina,” in:Neurobiology of Invertebrates: Transmitters, Modulators, and Receptors, Vol. 36, J. Salanki and S. Roza (eds.), Symposia Biologica Hungarica, Budapest (1988), pp. 463–477.

  15. I. Kupfermann and K. R. Weiss, “The role of serotonin in arousal of feeding behavior ofAplysia,” in:Serotonin Neurotransmission and Behavior, Cambridge (1981), pp. 255–287.

  16. C. M. Lalli, “Structure and function of the buccal apparatus ofClione limacina (Phipps) with a review of feeding in gymnosomatous pteropods,”J. Exptl. Marine Biol. Ecology,4, 101–118 (1970).

    Google Scholar 

  17. C. M. Lalli and R. W. Gilmer,Pelagic Snails. The Biology of Holoplanktonic Gastropod Mollusks, Stanford University Press (1989).

  18. Ch. M. Lent, “Serotonin: a chemical mediator of feeding behavior in leeches,” in:Signal Molecules and Mechanisms of Animal Behavior. Abstracts. Symposium, Pushchino (1989), p. 36.

  19. T. P. Norekyan and I. S. Zakharov, “Effects of serotonin on pleural and pedal neurons, involved in inhibitory control of locomotion in Clione,” in:Signal Molecules and Mechanisms of Animal Behavior. Abstracts. Symposium, Pushchino (1989), p. 44.

  20. G. Rao, C. A. Barnes and B. L. McNaughton, “Intracellular fluorescent staining with carboxylflourescein: a rapid and reliable method for quantifying dye-coupling in mammalian central nervous system,”J. Neurosci. Methods,16, No. 2, 251–263 (19860.

    Google Scholar 

  21. J. E. Richmond, A. D. Murphy, A. G. M. Bulloch, and K. Lukowiak, “Evidence of an excitatory effect of GABA on feeding patterned motor activity ofHelisoma trivolvis,”Soc. Neurosci. Abstr.,12, Part 2, 792 (1986).

    Google Scholar 

  22. D. Sakharov, “Integrative function of serotonin common to distantly related invertebrate animals,” in:The Early Brain, H. Gustafsson and M. Reuter (eds.), Academi Press, Abo (1990), pp. 73–88.

    Google Scholar 

  23. R. A. Satterlie and A. N. Spencer, “Swimming in the pteropod mollusc,Clione limacina. II. Physiology,”J. Exptl. Biol.,116, No. 1, 205–222 (1985).

    Google Scholar 

  24. E. S. Vizi,Non-Synaptic Interactions between Neurons: Modulation of Neurochemical Transmission, Wiley a. Sons, New York (1984).

    Google Scholar 

  25. K. R. Weiss and I. Kupfermann, “Serotoninergic neuronal activity and arousal of feeding inAplysia californica,”Soc. Neurosci. Symp.,3, 66–89 (1977).

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Institute of Higher Nervous Activity and Neurophysiology, Russian Academy of Sciences, Moscow

    T. P. Norekyan & R. Satterlie

  2. Arizona State University, Tempe, USA

    T. P. Norekyan & R. Satterlie

  3. “Friday Harbor” Biostation, Washington University, USA

    T. P. Norekyan & R. Satterlie

Authors
  1. T. P. Norekyan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. R. Satterlie
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Translated from Zhurnal Vyssnei Nervnoi Deyatel'nosti imeni I. P. Pavlova, Vol. 41, No. 5, pp. 982–997, September–October, 1991.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Norekyan, T.P., Satterlie, R. Neuronal analysis of hunting behavior of the pteropod molluscClione limacina . Neurosci Behav Physiol 23, 11–23 (1993). https://doi.org/10.1007/BF01182633

Download citation

  • Received:

  • Revised:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF01182633

Keywords

Search

Navigation