Advertisement

Acta Biologica Hungarica

, Volume 55, Issue 1–4, pp 149–155 | Cite as

The Early Snail Acquires the Learning. Comparison of Scores for Conditioned Taste Aversion Between Morning and Afternoon

  • Akiko Wagatsuma
  • Rio Sugai
  • K. Chono
  • Sachiyo Azami
  • D. Hatakeyama
  • Hisayo Sadamoto
  • E. ItoEmail author
Open Access
Article

Abstract

The pond snail Lymnaea stagnalis acquires conditioned taste aversion (CTA) and maintains its memory for more than a. month. Snails in our laboratory were cultured at 20 °C on a. 12: 12 light-dark cycle (light from 7 am to 7 pm). To examine the hours during which snails acquire CTA effectively, we trained some snails in the morning and others in the afternoon, and then compared their scores. CTA developed in both cases, but scores were significantly better in the morning than in the afternoon. To elucidate the cause of this difference in scores, we observed the voluntary activity of snails and found the circadian rhythm reflected in the snails’ free-movement distances; distances at the circadian time 0–12 (daytime) were significantly longer than those at the circadian time 12–24 (nighttime). This rhythm was kept up for at least 3 days, even in constant darkness. In conclusion, L. stagnalis should be trained in the morning to acquire associative learning, possibly because of its greater propensity to roam about at that time as opposed to the afternoon.

Keywords

Associative learning circadian rhythm Lymnaea 

References

  1. 1.
    Benjamin, P. R., Staras, K., Kemenes, G. (2000) A. systems approach to the cellular analysis of associative learning in the pond snail Lymnaea. Learn. Mem. 7, 124–131.Google Scholar
  2. 2.
    Chono, K., Fujito, Y., Ito, E. (2002) Non-ocular dermal photoreception in the pond snail Lymnaea stagnalis. Brain Res. 951, 107–112.CrossRefGoogle Scholar
  3. 3.
    Copping, J., Syed, N. I., Winlow, W. (2000) Seasonal plasticity of synaptic connections between identified neurones in Lymnaea. Acta Biol. Hung. 51, 205–210.Google Scholar
  4. 4.
    Fernandez, R. I., Levenson, J., Nunez-Regueiro, M., Cleary, L., Eskin, A. (2001) Circadian regulation of long-term sensitization in Aplysia. Soc. Neurosci. Abs. Abstr. 644.10.Google Scholar
  5. 5.
    Hatakeyama, D., Ito, E. (1999) Three-dimensional reconstruction and mapping of serotonin-like immunoreactive neurons in the central nervous system of the pond snail, Lymnaea stagnalis, with the confocal laser scanning microscope. Bioimages 7, 1–12.Google Scholar
  6. 6.
    Hatakeyama, D., Ito, E. (2000) Distribution and developmental changes in GABA-like immunoreactive neurons in the central nervous system of pond snail, Lymnaea stagnalis. J. Comp. Neurol. 418, 310–322.Google Scholar
  7. 7.
    Hatakeyama, D., Ito, I., Kojima, S., Fujito, Y., Ito, E. (2000) Complement receptor 3-like immunore-activity in the light green cells and the canopy cells of the pond snail, Lymnaea stagnalis. Brain Res. 865, 102–106.Google Scholar
  8. 8.
    Hattar, S., Lyons, L. C., Eskin, A. (2002) Circadian regulation of a. transcription factor, ApC/EBP, in the eye of Aplysia californica. J. Neurochem. 83, 1401–1411.Google Scholar
  9. 9.
    Ito, E., Kobayashi, S., Kojima, S., Sadamoto, H., Hatakeyama, D. (1999) Associative learning in the pond snail, Lymnaea stagnalis. Zool. Sci. 16, 711–723.Google Scholar
  10. 10.
    Kemenes, I., Kemenes, G., Andrew, R. J., Benjamin, P. R., O’Shea, M. (2002) Critical time-window for NO-cGMP-dependent long-term memory formation after one-trial appetitive conditioning. J. Neurosci. 22, 1414–1425.CrossRefGoogle Scholar
  11. 11.
    Kobayashi, S., Kojima, S., Yamanaka, M., Sadamoto, H., Nakamura, H., Fujito, Y., Kawai, R., Sakakibara, M., Ito, E. (1998) Operant conditioning of escape behavior in the pond snail, Lymnaea stagnalis. Zool. Sci. 15, 683–690.Google Scholar
  12. 12.
    Kobayashi, S., Sadamoto, H., Ogawa, H., Kitamura, Y., Oka, K., Tanishita, K., Ito, E. (2000) Nitric oxide generation around buccal ganglia accompanying feeding behavior in the pond snail, Lymnaea stagnalis. Neurosci. Res. 38, 27–34.CrossRefGoogle Scholar
  13. 13.
    Kobayashi, S., Ogawa, H., Fujito, Y., Ito, E. (2000) Nitric oxide suppresses fictive feeding response in Lymnaea stagnalis. Neurosci. Lett. 285, 209–212.CrossRefGoogle Scholar
  14. 14.
    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.Google Scholar
  15. 15.
    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.CrossRefGoogle Scholar
  16. 16.
    Kojima, S., Kobayashi, S., Yamanaka, M., Sadamoto, H., Nakamura, H., Fujito, Y., Kawai, R., Sakakibara, M., Ito, E. (1998) Sensory preconditioning for feeding response in the pond snail, Lymnaea stagnalis. Brain Res. 808, 113–115.CrossRefGoogle Scholar
  17. 17.
    Kojima, S., Ogawa, H., Kouuchi, T., Nidaira, T., Hosono, T., Ito, E. (2000) Neuron-independent Ca2+ signaling in glial cells of snail’s brain. Neuroscience 100, 893–900.CrossRefGoogle Scholar
  18. 18.
    Kojima, S., Hosono, T., Fujito, Y., Ito, E. (2001) Optical detection of neuromodulatory effects of conditioned taste aversion in the pond snail Lymnaea stagnalis. J. Neurobiol. 49, 118–128.Google Scholar
  19. 19.
    Levenson, J., Byrne, J. H., Eskin, A. (1999) Levels of serotonin in the hemolymph of Aplysia are modulated by light/dark cycles and sensitizing training. J. Neurosci. 19, 8094–8103.CrossRefGoogle Scholar
  20. 20.
    Lukowiak, K., Syed, N. (1999) Learning, memory and a. respiratory central pattern generator. Comp. Biochem. Physiol. A. 124, 265–274.CrossRefGoogle Scholar
  21. 21.
    Lukowiak, K., Sangha, S., McComb, C., Varshney, N., Rosenegger, D., Sadamoto, H., Scheiben-stock, A. (2003) Associative learning and memory in Lymnaea stagnalis: how well do they remember? J. Exp. Biol. 206, 2097–2103.CrossRefGoogle Scholar
  22. 22.
    Nakamura, FL, Ito, I., Kojima, S., Fujito, Y., Suzuki, FL, Ito, E. (1999) Histological characterization of lip and tentacle nerves in Lymnaea stagnalis. Neurosci. Res. 33, 127–136.Google Scholar
  23. 23.
    Nakamura, H., Kojima, S., Kobayashi, S., Ito, I., Fujito, Y., Suzuki, H., Ito, E. (1999) Physiological characterization of lip and tentacle nerves in Lymnaea stagnalis. Neurosci. Res. 33, 291–298.Google Scholar
  24. 24.
    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.Google Scholar
  25. 25.
    Ono, M., Kawai, R., Horikoshi, T., Yasuoka, T., Sakakibara, M. (2002) Associative learning acquisition and retention depends on developmental stage in Lymnaea stagnalis. Neurobiol. Learn. Mem. 78, 53–64.Google Scholar
  26. 26.
    Sadamoto, H., Hatakeyama, D., Kojima, S., Fujito, Y., Ito, E. (1998) Histochemical study on the relation between NO-generative neurons and central circuitry for feeding in the pond snail, Lymnaea stagnalis. Neurosci. Res. 32, 57–63.CrossRefGoogle Scholar
  27. 27.
    Sadamoto, H., Yamanaka, M., Hatakeyama, D., Nakamura, H., Kojima, S., Yamashita, M., Ito, E. (2000) Developmental study of anatomical substrate for conditioned taste aversion in Lymnaea stagnalis. Zool. Sci. 17, 141–148.Google Scholar
  28. 28.
    Sadamoto, H., Sato, H., Kobayashi, S., Murakami, J., Aonuma, H., Ando, H., Fujito, Y., Hamano, K., Awaji, M., Lukowiak, K., Urano, A., Ito, E. (2004) CREB in the pond snail Lymnaea stagnalis. Cloning, gene expression and function in identifiable neurons of the central nervous system. J. Neurobiol. 58, 455–466.CrossRefGoogle Scholar
  29. 29.
    Yamanaka, M., Sadamoto, H., Hatakeyama, D., Nakamura, H., Kojima, S., Kimura, T., Yamashita, M., Urano, A., Ito, E. (1999) Developmental changes in conditioned taste aversion in Lymnaea stagnalis. Zool. Sci. 16, 9–16.Google Scholar
  30. 30.
    Yamanaka, M., Hatakeyama, D., Sadamoto, H., Kimura, T., Ito, E. (2000) Development of key neurons for learning stimulates learning ability in Lymnaea stagnalis. Neurosci. Lett. 278, 113–116.Google Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2004

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  • Akiko Wagatsuma
    • 1
  • Rio Sugai
    • 1
  • K. Chono
    • 1
  • Sachiyo Azami
    • 1
  • D. Hatakeyama
    • 1
  • Hisayo Sadamoto
    • 2
  • E. Ito
    • 1
    • 2
    Email author
  1. 1.Division of Biological Sciences, Graduate School of ScienceHokkaido UniversitySapporoJapan
  2. 2.Division of Innovative Research, Creative Research Initiative “Sousei” (CRIS)Hokkaido UniversitySapporoJapan

Personalised recommendations