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Control of spatial orientation in a mollusc

Nature volume 393, pages 172–175 (1998)Cite this article

Abstract

The main function of postural nervous mechanisms in different species, from mollusc to man, is to counteract the force of gravity and stabilize body orientation in space1,2,3. Here we investigate the basic principles of postural control in a simple animal model, the marine mollusc Clione limacina. When swimming, C. limacina maintains its vertical orientation because of the activity of the postural neuronal network. Driven by gravity-sensing organs (statocysts), the network causes postural corrections by producing tail flexions. To understand how this function occurs, we studied network activity by using a new method. We used an in vitro preparation that consisted of the central nervous system isolated with the statocysts. Output signals from the network (electrical activity of tail motor neurons) controlled an electrical motor which rotated the preparation in space. We analysed the activity of individual neurons involved in postural stabilization under opened or closed feedback loop. When we closed this artificial feedback loop, the network stabilized the vertical orientation of the preparation. This stabilization is based on the tendency of the network to minimize the difference between the activities of the two antagonistic groups of neurons, which are driven by orientation-dependent sensory inputs.

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Figure 1: Postural reactions in C.limacina and principal elements of the postural network.
Figure 2: Methods for in vitro investigations of the postural network.
Figure 3: Responses of motor neurons and interneurons to manual rotation of the preparation (opened feedback loop).
Figure 4: Activity of motor neurons from the LTN and RTN, recorded under the conditions of closed feedback loop.
Figure 5: Activity of the postural network depends on temperature.
Figure 6: Temperature-dependent reconfiguration of the postural network.

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References

  1. Orlovsky, G. N. Gravistatic postural control in simpler systems. Curr. Opin. Neurobiol. 1, 612–627 (1991).

    Article  Google Scholar 

  2. Macpherson, J. M., Deliagina, T. G. & Orlovsky, G. N. in Neurons, Networks, and Motor Behavior (eds Stein, P. S. G., Grillner, S., Selverston, A. I. & Stuart, D. G.) 257–267 (MIT Press, Cambridge, 1997).

    Google Scholar 

  3. Horak, F. B. & Macpherson, J. M. in Handbook of Phsyiology: Integration of Motor, Circulatory, Respiratory and Metabolic Control during Exercise (eds Shepard, J. & Rowell, L.) 1–39 (Oxford Univ. Press, 1995).

    Google Scholar 

  4. Arshavsky, Y. I., Beloozerova, I. N., Orlovsky, G. N., Panchin, Y. V. & Pavlova, G. A. Control of locomotion in marine mollusc Clione limacina. 1. Efferent activity during actual and fictitious swimming. Exp. Brain Res. 58, 255–262 (1985).

    PubMed  Google Scholar 

  5. Arshavsky, Y. I.et al. in Simpler Nervous Systems (eds Sakharov, D. A. & Winlow, W.) 290–316 (Manchester Univ. Press, UK, 1991).

    Google Scholar 

  6. Satterlie, R. A., LaBarbera, M. & Spencer, A. N. Swimming in the pteropod mollusc Clione limacina. 1. Behavior and morphology. J. Exp. Biol. 116, 189–204 (1985).

    Google Scholar 

  7. Panchin, Y. V., Arshavsky, Y. I., Deliagina, T. G., Popova, L. B. & Orlovsky, G. N. Control of locomotion of marine mollusk Clione limacina. IX. Neuronal mechanisms of spatial orientation. J. Neurophys. 73, 1924–1936 (1995).

    Article  CAS  Google Scholar 

  8. Alkon, D. L. Responses of hair cells to statocyst rotation. J. Gen. Physiol. 66, 507–530 (1975).

    Article  CAS  Google Scholar 

  9. Janse, C. Sensory system involved in gravity orientation in pulmonate snail Lymnaea stagnalis. J. Comp. Physiol. A 145, 311–319 (1982).

    Article  Google Scholar 

  10. Tsirulis, T. P. The fine structure of the statocyst in the pteropod mollusk Clione limacina. J. Evol. Biochem. Physiol. 10, 181–188 (1974).

    CAS  Google Scholar 

  11. Panchin, Y. V., Arshavsky, Y. I., Deliagina, T. G., Popova, L. B. & Orlovsky, G. N. Control of locomotion in marine mollusk Clione limacina. VIII. Cerebropedal neurons. J. Neurophys. 73, 1912–1923 (1995).

    Article  CAS  Google Scholar 

  12. Arshavsky, Y. I., Deliagina, T. G. & Orlovsky, G. N. Patttern generation. Curr. Opin. Neurobiol. 6, 781–789 (1997).

    Article  Google Scholar 

  13. Marder, E. & Calabrese, R. L. Principles of rhythmic motor pattern generation. Physiol. Rev. 76, 687–717 (1996).

    Article  CAS  Google Scholar 

  14. Selverston, A. I., Panchin, Y. V., Arshavsky, Y. I. & Orlovsky, G. N. in Neurons, Networks, and Motor Behavior (eds Stein, P. S. G., Grillner, S., Selverston, A. I. & Stuart, D. G.) 105–117 (MIT Press, Cambridge, 1997).

    Google Scholar 

  15. Panchin, Y. V. Cellular mechanisms for the temperature sensitive spatial orientation in Clione. Neuroreport 8, 3345–3348 (1997).

    Article  CAS  Google Scholar 

  16. Harris-Warrick, R. M. & Marder, E. Modulation of neural networks for behavior. Annu. Rev. Neurosci. 14, 39–57 (1991).

    Article  CAS  Google Scholar 

  17. Selverston, A. I. Neuromodulatory control of rhythmic behaviors in invertebrates. Int. Rev. Cytol. 147, 1–24 (1993).

    Article  CAS  Google Scholar 

  18. Selverston, A. I. Modulation of circuits underlying rhythmic behaviors. J. Comp. Physiol. A 176, 139–147 (1995).

    Article  Google Scholar 

  19. Arshavsky, Y. I.et al. Pharmacologically induced elements of the hunting and feeding behavior in the pteropod mollusk Clione limacina. 1. Effects of physostigmine. J. Neurophys. 69, 522–532 (1993).

    Article  CAS  Google Scholar 

  20. Deliagina, T. G. Vestibular compensation in lampreys: impairment and recovery of equlibrium control during locomotion. J. Exp. Biol. 200, 1459–1471 (1997).

    CAS  PubMed  Google Scholar 

  21. Deliagina, T. G., Popova, L. B. & Grant, G. The role of tonic vestibular input for postural control in rats. Arch. Ital. Biol. 135, 239–261 (1997).

    CAS  PubMed  Google Scholar 

  22. Hensler, K. in Neurobiology of Sensory Systems (eds Naresh Singh, R. & Strausfeld, N. J.) 531–554 (Plenum, New York, 1989).

    Book  Google Scholar 

  23. Hensler, K. & Rowell, C. H. F. Control of optomotor responses by descending deviation detector neurons in intact flying locust. J. Exp. Biol. 149, 191–205 (1990).

    Google Scholar 

  24. Takahata, M., Yoshino, M. & Hisada, M. Neuronal mechanisms underlying crayfish steering behaviour as an equilibrium response. J. Exp. Biol. 114, 599–617 (1985).

    Google Scholar 

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Acknowledgements

We thank Ö. Ekeberg, A. Büschges and O. Bloom for comments on the manuscript. This work was supported by the grants from the HHMI (to T.G.D.), Royal Swedish Academy of Sciences (to T.G.D. and G.N.O.) and Swedish Medical Research Council (to T.G.D.).

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Authors and Affiliations

  1. Department of Neuroscience, The Nobel Institute of Neurophysiology, Karolinska Institutet, Stockholm, S-171 77, Sweden

    Tatiana G. Deliagina & Grigori N. Orlovsky

  2. AN Belozersky Institute of Physico-Chemical Biology, Moscow State University, Moscow, 119 899, Russia

    Tatiana G. Deliagina & Grigori N. Orlovsky

  3. Institute of Neurobiology, University of Purerto Rico, San Juan, PR00901, USA

    Yuri I. Arshavsky

  4. Institute of Information Transmission Problems, Russian Academy of Sciences, Moscow, 101447, Russia

    Yuri I. Arshavsky

Authors
  1. Tatiana G. Deliagina
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  2. Yuri I. Arshavsky
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  3. Grigori N. Orlovsky
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Correspondence to Tatiana G. Deliagina.

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Deliagina, T., Arshavsky, Y. & Orlovsky, G. Control of spatial orientation in a mollusc. Nature 393, 172–175 (1998). https://doi.org/10.1038/30251

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