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Taste discrimination in conditioned taste aversion of the pond snail Lymnaea stagnalis
Abstract
SUMMARY: Conditioned taste aversion (CTA) in the pond snail Lymnaea stagnalis has been widely used as a model for gaining an understanding of the molecular and behavioral mechanisms underlying learning and memory. At the behavioral level, however, it is still unclear how taste discrimination and CTA interact. We thus examined how CTA to one taste affected the feeding response induced by another appetitive food stimulus. We first demonstrated that snails have the capacity to recognize sucrose and carrot juice as distinct appetitive stimuli. We then found that snails can become conditioned(i.e. CTA) to avoid one of the stimuli and not the other. These results show that snails can distinguish between appetitive stimuli during CTA, suggesting that taste discrimination is processed upstream of the site where memory consolidation in the snail brain occurs. Moreover, we examined second-order conditioning with two appetitive stimuli and one aversive stimulus. Snails acquired second-order conditioning and were still able to distinguish between the different stimuli. Finally, we repeatedly presented the conditional stimulus alone to the conditioned snails, but this procedure did not extinguish the long-term memory of CTA in the snails. Taken together, our data suggest that CTA causes specific, irreversible and rigid changes from appetitive stimuli to aversive ones in the conditioning procedure.
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“and in the pond snail Lymnaea stagnalis second order conditioning of simple taste discrimination was observed (Sugai et al. 2006; for more tests see Benjamin and Kemenes 2010)”
From Unlimited Associative Learning and the origins of consciousness: a primer and some predictions (2020) · cites this paper as Sugai et al. 2006
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Cites
Context, time, and memory retrieval in the interference paradigms of Pavlovian learning
Bouton, M. E. (1993) · Psychological Bulletin · doi:10.1037/0033-2909.114.1.80 · Cited by 1,896
Behavioral Regulation of the Milieu Interne in Man and Rat
García, J., Hankins, W. G., & Rusiniak, K. W. (1974) · Science · doi:10.1126/science.185.4154.824 · Cited by 1,124
Conditioned Aversion to Saccharin Resulting from Exposure to Gamma Radiation
García, J., Kimeldorf, D. J., & Koelling, R. A. (1955) · Science · doi:10.1126/science.122.3160.157 · Cited by 1,011
A General Theory of Aversion Learning a
García, J., Lasiter, P. S., Bermúdez‐Rattoni, F., & Deems, D. A. (1985) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1985.tb27060.x · Cited by 409
Invertebrate Learning and Memory: From Behavior to Molecules
Carew, T. J., & Sahley, C. L. (1986) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.09.030186.002251 · Cited by 403
An analysis of associative learning in a terrestrial mollusc
Sahley, C. L., Rudy, J. W., & Gelperin, A. (1981) · Journal of Comparative Physiology A · doi:10.1007/bf00612791 · Cited by 259
A Systems Approach to the Cellular Analysis of Associative Learning in the Pond Snail LymnaeaPreprint
Benjamin, P. R., Staras, K., & Kemenes, G. (2000) · Learning & Memory · doi:10.1101/lm.7.3.124 · Cited by 167
Sangha, S., Scheibenstock, A., Morrow, R., & Lukowiak, K. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-30-09842.2003 · Cited by 109
Self-citationFulton, D. J., Kemenes, I., Andrew, R., & Benjamin, P. R. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.03970.x · Cited by 102
Sadamoto, H., Sato, H., Kobayashi, S., Murakami, J., Aonuma, H., Ando, H., Fujito, Y., Hamano, K., Awaji, M., Lukowiak, K., et al. (2003) · Journal of Neurobiology · doi:10.1002/neu.10296 · Cited by 94
Self-citationKojima, S., Nanakamura, H., Nagayama, S., et al. (1997) · Neuroscience Letters · doi:10.1016/s0304-3940(97)00507-7 · Cited by 87
Kojima, S., Yamanaka, M., Fujito, Y., et al. (1996) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.13.803 · Cited by 85
Self-citationAssociative learning and memory inLymnaea stagnalis: how well do they remember?
Lukowiak, K., Sangha, S., McComb, C., et al. (2003) · Journal of Experimental Biology · doi:10.1242/jeb.00374 · Cited by 79
Self-citationContext Learning and the Effect of Context on Memory Retrieval in LymnaeaPreprint
Haney, J. J., & Lukowiak, K. (2001) · Learning & Memory · doi:10.1101/lm.34701 · Cited by 75
Self-citationAssociative Learning in the Pond Snail, Lymnaea stagnalis
Ito, E., Kobayashi, S., Kojima, S., et al. (1999) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.16.711 · Cited by 69
Self-citationWagatsuma, A., Sadamoto, H., Kitahashi, T., Lukowiak, K. D., Urano, A., & Ito, E. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01625 · Cited by 67
Self-citationRibeiro, M. J., Serfözö, Z., Papp, A., Kemenes, I., O’Shea, M., Yin, J. C. P., Benjamin, P. R., & Kemenes, G. (2003) · European Journal of Neuroscience · doi:10.1046/j.1460-9568.2003.02856.x · Cited by 67
Impairing Forgetting by Preventing New Learning and Memory.
Sangha, S., Scheibenstock, A., Martens, K., Varshney, N., Cooke, R., & Lukowiak, K. (2005) · Behavioral Neuroscience · doi:10.1037/0735-7044.119.3.787 · Cited by 67
Self-citationBoosting intermediate-term into long-term memory
Parvez, K., Stewart, O., Sangha, S., & Lukowiak, K. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01545 · Cited by 64
Self-citationJones, N. G., Kemenes, I., Kemenes, G., & Benjamin, P. R. (2003) · Current Biology · doi:10.1016/s0960-9822(03)00380-4 · Cited by 53
Central localization of plasticity involved in appetitive conditioning in LymnaeaPreprint
Straub, V. A., Styles, B. J., Ireland, J. S., et al. (2004) · Learning & Memory · doi:10.1101/lm.77004 · Cited by 53
Kobayashi, S., Sadamoto, H., Ogawa, H., et al. (2000) · Neuroscience Research · doi:10.1016/s0168-0102(00)00136-x · Cited by 52
Self-citationHatakeyama, D., Sadamoto, H., Watanabe, T., Wagatsuma, A., Kobayashi, S., Fujito, Y., Yamashita, M., Sakakibara, M., Kemenes, G., & Ito, E. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.12.009 · Cited by 52
Self-citationWagatsuma, A., Sugai, R., Chono, K., Azami, S., Hatakeyama, D., Sadamoto, H., & Ito, E. (2004) · Acta Biologica Hungarica · doi:10.1556/abiol.55.2004.1-4.18 · Cited by 50
Self-citationSadamoto, H., Hatakeyama, D., Kojima, S., et al. (1998) · Neuroscience Research · doi:10.1016/s0168-0102(98)00066-2 · Cited by 47
Self-citationPhysiological characterization of lip and tentacle nerves in Lymnaea stagnalis
Nakamura, H., Kojima, S., Kobayashi, S., et al. (1999) · Neuroscience Research · doi:10.1016/s0168-0102(99)00020-6 · Cited by 41
Operant conditioning of an in vitro CNS-pneumostome preparation of Lymnaea
McComb, C., Rosenegger, D. G., Varshney, N., Kwok, H. Y., & Lukowiak, K. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.02.002 · Cited by 41
Self-citationKojima, S., Hosono, T., Fujito, Y., et al. (2001) · Journal of Neurobiology · doi:10.1002/neu.1069 · Cited by 40
Self-citationSensory preconditioning for feeding response in the pond snail, Lymnaea stagnalis
Kojima, S., Kobayashi, S., Yamanaka, M., et al. (1998) · Brain Research · doi:10.1016/s0006-8993(98)00823-3 · Cited by 38
Electrophysiological Responses to Light of Neurons in the Eye and Statocyst of Lymnaea stagnalis
Sakakibara, M., Aritaka, T., Iizuka, A., et al. (2004) · Journal of Neurophysiology · doi:10.1152/jn.00692.2004 · Cited by 38
Nitric oxide suppresses fictive feeding response in Lymnaea stagnalis
Kobayashi, S., Ogawa, H., Fujito, Y., et al. (2000) · Neuroscience Letters · doi:10.1016/s0304-3940(00)01079-x · Cited by 38
Self-citationConditioned taste aversion with sucrose and tactile stimuli in the pond snail Lymnaea stagnalis
Kawai, R., Sunada, H., Horikoshi, T., & Sakakibara, M. (2004) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2004.06.003 · Cited by 37
Nakamura, H., Kobayashi, S., Kojima, S., et al. (1999) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.16.387 · Cited by 37
Fujie, S., Yamamoto, T., Murakami, J., Hatakeyama, D., Shiga, H., Suzuki, N., & Ito, E. (2004) · Journal of Neurobiology · doi:10.1002/neu.20046 · Cited by 32
Self-citationHatakeyama, D., Fujito, Y., Sakakibara, M., & Ito, E. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0965-8 · Cited by 32
Self-citationDevelopmental Changes in Conditioned Taste Aversion in Lymnaea stagnalis
Yamanaka, M., Sadamoto, H., Hatakeyama, D., et al. (1999) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.16.9 · Cited by 32
Self-citationJuvenileLymnaeaventilate,learn and remember differently than do adultLymnaea
McComb, C., Varshney, N., & Lukowiak, K. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01544 · Cited by 31
Self-citationSakura, M., Kabetani, M., Watanabe, S., et al. (2004) · Neuroscience Letters · doi:10.1016/j.neulet.2004.08.025 · Cited by 30
Ito, I., Kimura, T., Watanabe, S., et al. (2004) · Journal of Neurobiology · doi:10.1002/neu.10328 · Cited by 22
Sadamoto, H., Azami, S., & Ito, E. (2004) · Acta Biologica Hungarica · doi:10.1556/abiol.55.2004.1-4.20 · Cited by 20
Self-citationIto, I., Watanabe, S., Kimura, T., et al. (2003) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.20.1337 · Cited by 15
Hatakeyama, D., Sadamoto, H., & Ito, E. (2004) · Acta Biologica Hungarica · doi:10.1556/abiol.55.2004.1-4.19 · Cited by 14
Self-citationIto, I., Watanabe, S., Kimura, T., et al. (2003) · ZOOLOGICAL SCIENCE · doi:10.2108/zsj.20.1327 · Cited by 13
Calexcitin‐like immunoreactivity in the pond snail Lymnaea stagnalis
Hatakeyama, D., Inamura, S., Ito, E., et al. (2004) · Neuroscience Research Communications · doi:10.1002/nrc.20017 · Cited by 7
Self-citation
Research works printed but not linked: 1
- Mackintosh, N. J. (1974). Extinction. In The Physiology of Animal Learning. pp.405-483. London: Academic Press.
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Unlimited Associative Learning and the origins of consciousness: a primer and some predictions
Birch, J., Ginsburg, S., & Jablonka, E. (2020) · Biology & Philosophy · doi:10.1007/s10539-020-09772-0 · Cited by 149
“For example, gastropod molluscs show rapid avoidance learning (Siegel and Jarvik 1974), and in the pond snail Lymnaea stagnalis second order conditioning of simple taste discrimination was observed (Sugai et al. 2006; for more tests see Benjamin and Kemenes 2010), but we are not aware of experiments testing for discri…”
Background
Metadata
- Authors
- Sugai, R., Shiga, H., Azami, S., Watanabe, T., Sadamoto, H., Fujito, Y., Lukowiak, K., & Ito, E.
- Affiliations
- Hokkaido University (JP)
- Sapporo Medical University (JP)
- University of Calgary (CA)
- Corresponding author
- Ito, Etsuro
- Venue
- Journal of Experimental Biology
- Publisher
- The Company of Biologists
- Published
- 2006-03-01
- Volume
- 209
- Issue
- 5
- Pages
- 826-833
- ISSN
- 0022-0949 (ISSN-L)
- 1477-9145
- OpenAlex
- W2149412668
- Cited by
- 57
- References
- 44
- Citations by year
- 2026: 1 · 2025: 1 · 2024: 3 · 2023: 3 · 2022: 2 · 2021: 4 · 2020: 4 · 2019: 3 · 2018: 1 · 2017: 3 · 2016: 2 · 2015: 3 · 2014: 2 · 2013: 8 · 2012: 1
- FWCI
- 1.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Journal of Experimental Biology (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Agricultural and Biological Sciences › Animal Science and Zoology › Mollusks and Parasites Studies
- Keywords
- conditioned taste aversion, Lymnaea stagnalis, taste discrimination, second-order conditioning, appetitive stimuli, memory consolidation, learning and memory, memory extinction, feeding behavior, sucrose, carrot juice
- MeSH terms
- Animals, Conditioning, Psychological, Lymnaea, Taste, Time Factors
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