Insulin and Memory in Lymnaea

Abstract

The pond snail, Lymnaea stagnalis, is capable of learning conditioned taste aversion (CTA) and consolidating this CTA into long-term memory (LTM). The DNA microarray experiments showed that some of molluscan insulin-related peptides (MIPs) were up-regulated in snails exhibiting CTA-LTM. On the other hand, the electrophysiological experiments showed that application of secretions from the MIPscontaining cells evoked long-term potentiation (LTP) at the synapses between the cerebral giant cell (a key interneuron for CTA) and the B1 motoneuron (a buccal motoneuron). We thus hypothesized that MIPs and MIP receptors play an important role at the synapses, probably underlying the CTA-LTM consolidation process. To examine this hypothesis, we applied the antibody, which recognizes the binding site of mammalian insulin receptors and is thought to cross-react MIP receptors, to the Lymnaea CNS. Our present data showed that an application of the antibody for insulin receptors to the isolated CNS blocked LTP, and that an injection of the antibody into the Lymnaea abdominal cavity inhibited LTM consolidation, but not CTA formation.

References

  1. 1.

    Azami, S., Wagatsuma, A., Sadamoto, H., Hatakeyama, D., Usami, T., Fujie, M., Koyanagi, R., Azumi, K., Fujito, Y., Lukowiak, K., Ito, E. (2006) Altered gene activity correlated with long-term memory formation of conditioned taste aversion in Lymnaea. J. Neurosci. Res. 84, 1610–1620.

    CAS  Article  Google Scholar 

  2. 2.

    Benjamin, P. R., Rose, R. M., Slade, C. T., Lacy, M. G. (1979) Morphology of identified neurones in the buccal ganglia of Lymnaea stagnalis. J. Exp. Biol. 80, 119–135.

    Google Scholar 

  3. 3.

    Elliott, C. J., Vehovszky, A. (2000) Comparative pharmacology of feeding in molluscs. Acta Biol. Hung. 51, 153–163.

    CAS  PubMed  Google Scholar 

  4. 4.

    Hajali, V., Mohaddes, G., Babri, S. H. (2009) Intracerebroventricular insulin improves spatial learning and memory in male Wistar rats. Behav. Neurosci. 123, 1309–1314.

    CAS  Article  Google Scholar 

  5. 5.

    Ito, E., Kobayashi, S., Kojima, S., Sadamoto, H., Hatakeyama, D. (1999) Associative learning in the pond snail, Lymnaea stagnalis. Zool. Sci. 16, 711–723.

    Article  Google Scholar 

  6. 6.

    Jonas, E. A., Knox, R. J., Kaczmarek, L. K., Schwartz, J. H., Solomon, D. H. (1996) Insulin receptor in Aplysia neurons: characterization, molecular cloning, and modulation of ion currents. J. Neurosci. 16, 1645–1658.

    CAS  Article  Google Scholar 

  7. 7.

    Kawai, R., Kobayashi, S., Fujito, Y., Ito, E. (2011) Multiple subtypes of serotonin receptors in the feeding circuit of a pond snail. Zool. Sci. 28, 517–525.

    CAS  Article  Google Scholar 

  8. 8.

    Kojima, S., Yamanaka, M., Fujito, Y., Ito, E. (1996) Differential neuroethological effects of aversive and appetitive reinforcing stimuli on associative learning in Lymnaea stagnalis. Zool. Sci. 13, 803–812.

    Article  Google Scholar 

  9. 9.

    Kojima, S., Nakamura, H., Nagayama, S., Fujito, Y., Ito, E. (1997) Enhancement of an inhibitory input to the feeding central pattern generator in Lymnaea stagnalis during conditioned taste-aversion learning. Neurosci. Lett. 230, 179–182.

    CAS  Article  Google Scholar 

  10. 10.

    Li, K. W., Geraerts, W. P., Joosse, J. (1992) Purification and sequencing of molluscan insulin-related peptide II from the neuroendocrine light green cells in Lymnaea stagnalis. Endocrinology 130, 3427–3432.

    CAS  Article  Google Scholar 

  11. 11.

    Li, K. W., Geraerts, W. P., Ebberink, R. H., Joosse, J. (1992) Purification and sequencing of molluscan insulin-related peptide I (MIP I) from the neuroendocrine light green cells of Lymnaea stagnalis. Mol. Cell. Endocrinol. 85, 141–150.

    CAS  Article  Google Scholar 

  12. 12.

    Li, K. W., Geraerts, W. P., van Loenhout, H., Joosse, J. (1992) Biosynthesis and axonal transport of multiple molluscan insulin-related peptides by the neuroendocrine light green cells of Lymnaea stagnalis. Gen. Comp. Endocrinol. 87, 79–86.

    CAS  Article  Google Scholar 

  13. 13.

    McCrohan, C. R., Benjamin, P. R. (1980) Synaptic relationships of the cerebral giant cells with motoneurones in the feeding system of Lymnaea stagnalis. J. Exp. Biol. 85, 169–186.

    CAS  Google Scholar 

  14. 14.

    Meester, I., Ramkema, M. D., van Minnen, J., Boer, H. H. (1992) Differential expression of four genes encoding molluscan insulin-related peptides in the central nervous system of the pond snail Lymnaea stagnalis. Cell Tissue Res. 269, 183–188.

    CAS  Article  Google Scholar 

  15. 15.

    Nakamura, H., Kobayashi, S., Kojima, S., Urano, A., Ito, E. (1999) PKA-dependent regulation of synaptic enhancement between a buccal motor neuron and its regulatory interneuron in Lymnaea stagnalis. Zool. Sci. 16, 387–394.

    CAS  Article  Google Scholar 

  16. 16.

    Roovers, E., Vincent, M. E., van Kesteren, E., Geraerts, W. P., Planta, R. J., Vreugdenhil, E., van Heerikhuizen, H. (1995) Characterization of a putative molluscan insulin–related peptide receptor. Gene 162, 181–188.

    CAS  Article  Google Scholar 

  17. 17.

    Rose, R. M., Benjamin, P. R. (1979) The relationship of the central motor pattern to the feeding cycle of Lymnaea stagnalis. J. Exp. Biol. 80, 137–163.

    CAS  PubMed  Google Scholar 

  18. 18.

    Sakakibara, M. (2006) Comparative study of visuo-vestibular conditioning in Lymnaea stagnalis. Biol. Bull. 210, 298–307.

    Article  Google Scholar 

  19. 19.

    Sanna, P. P., Cammalleri, M., Berton, F., Simpson, C., Lutjens, R., Bloom, F. E., Francesconi, W. (2002) Phosphatidylinositol 3–kinase is required for the expression but not for the induction or the maintenance of long-term potentiation in the hippocampal CA1 region. J. Neurosci. 22, 3359–3365.

    CAS  Article  Google Scholar 

  20. 20.

    Smit, A. B., Geraerts, P. M., Meester, I., van Heerikhuizen, H., Joosse, J. (1991) Characterization of a cDNA clone encoding molluscan insulin-related peptide II of Lymnaea stagnalis. Eur. J. Biochem. 199, 699–703.

    CAS  Article  Google Scholar 

  21. 21.

    Smit, A. B., Thijsen, S. F., Geraerts, W. P., Meester, I., van Heerikhuizen, H., Joosse, J. (1992) Characterization of a cDNA clone encoding molluscan insulin-related peptide V of Lymnaea stagnalis. Brain Res. Mol. Brain Res. 14, 7–12.

    CAS  Article  Google Scholar 

  22. 22.

    Smit, A. B., van Marle, A., van Elk, R., Bogerd, J., van Heerikhuizen, H., Geraerts, W. P. (1993) Evolutionary conservation of the insulin gene structure in invertebrates: cloning of the gene encoding molluscan insulin-related peptide III from Lymnaea stagnalis. J. Mol. Endocrinol. 11, 103–113.

    CAS  Article  Google Scholar 

  23. 23.

    Smit, A. B., Spijker, S., van Minnen, J., Burke, J. F., De Winter, F., van Elk, R., Geraerts, W. P. (1996) Expression and characterization of molluscan insulin-related peptide VII from the mollusc Lymnaea stagnalis. Neuroscience 70, 589–596.

    CAS  Article  Google Scholar 

  24. 24.

    Straub, V. A., Staras, K., Kemenes, G., Benjamin, P. R. (2002) Endogenous and network properties of Lymnaea feeding central pattern generator interneurons. J. Neurophysiol. 88, 1569–1583.

    Article  Google Scholar 

  25. 25.

    Straub, V. A., Grant, J., O’Shea, M., Benjamin, P. R. (2007) Modulation of serotonergic nurotransmission by nitric oxide. J. Neurophysiol. 97, 1088–1099.

    CAS  Article  Google Scholar 

  26. 26.

    Sugai, R., Azami, S., Shiga, H., Watanabe, T., Sadamoto, H., Kobayashi, S., Hatakeyama, D., Fujito, Y., Lukowiak, K., Ito, E. (2007) One-trial conditioned taste aversion in Lymnaea: good and poor performers in long-term memory acquisition. J. Exp. Biol. 210, 1225–1237.

    Article  Google Scholar 

  27. 27.

    Tomioka, M., Adachi, T., Suzuki, H., Kunitomo, H., Schafer, W. R., Iino, Y. (2006) The insulin/PI 3-kinase pathway regulates salt chemotaxis learning in Caenorhabditis elegans. Neuron 51, 613–625.

    CAS  Article  Google Scholar 

  28. 28.

    Wagatsuma, A., Sugai, R., Chono, K., Azami, S., Hatakeyama, D., Sadamoto, H., Ito, E. (2004) The early snail acquires the learning. comparison of scores for conditioned taste aversion between morning and afternoon. Acta Biol. Hung. 55, 149–155.

    Article  Google Scholar 

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Correspondence to E. Ito.

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Presented during the 12th ISIN Symposium on Invertebrate Neurobiology, August 31–September 4, 2011, Tihany, Hungary.

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Ito, E., Okada, R., Sakamoto, Y. et al. Insulin and Memory in Lymnaea. BIOLOGIA FUTURA 63, 194–201 (2012). https://doi.org/10.1556/ABiol.63.2012.Suppl.2.25

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Keywords

  • Conditioned taste aversion
  • insulin
  • long-term potentiation
  • long-term memory
  • mollusc