The DOI matches its Crossref record; 40 of the 40 references it cites were found in a registry or an index.
Learning Performance of Normal and Mutant Drosophila after Repeated Conditioning Trials with Discrete Stimuli
Open accessAbstract
A new olfactory conditioning procedure is described using short training trials with discrete presentation of conditioned stimuli (CS) and unconditioned stimuli (US). A short odor presentation along with a single-shock stimulus produced modest but reliable and reproducible learning. Multiple trials presented sequentially improved performance with increasing trial number. Trial spacing had a significant impact on performance. Two trials presented with a short intertrial interval (ITI) produced no improvement over a single trial; two trials with a 15 min ITI significantly boosted performance. This effect required two associative trials, because substituting one of the trials with the CS alone, US alone, or an unpaired CS–US failed to boost performance. The increase in initial performance with two trials decayed within 15 min after training. Thus, the effect is short-lived. The utility of using a battery of tests, including a single short trial, two massed trials, and two spaced trials, to investigate parameters of memory formation in several mutants was demonstrated.
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In the citing paper
“Spaced training also leads to improved memory in invertebrates, such as the mollusk Aplysia californica11–14, Drosophila melanogaster15,16 and bees17, and in rodents18,19 and non-human primates20,21.”
From The right time to learn: Mechanisms and optimization of spaced learning (2016) · cites this paper as [15]
In the citing paper
“The spacing effect has been well demonstrated in Drosophila (Tully et al., 1994; Beck et al., 2000; Ho et al., 2007).”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Beck et al., 2000
In the citing paper
“In Drosophila, the spacing effect is well defined phenomenologically (Tully et al., 1994; Beck et al., 2000) and it is used as a behavioral strategy to induce protein synthesis-dependent LTM.”
From The Phosphatase SHP2 Regulates the Spacing Effect for Long-Term Memory Induction (2009) · cites this paper as Beck et al., 2000
Citations
Cites
Classical conditioning and retention in normal and mutantDrosophila melanogaster
Tully, T., & Quinn, W. G. (1985) · Journal of Comparative Physiology A · doi:10.1007/bf01350033 · Cited by 1,189
Classical conditioning and brain systems: the role of awareness
Clark, R. E., & Squire, L. R. (1998) · Science · doi:10.1126/science.280.5360.77 · Cited by 1,138
Goldstone, R. L. (1998) · Annual Review of Psychology · doi:10.1146/annurev.psych.49.1.585 · Cited by 973
Genetic dissection of consolidated memory in Drosophila
Tully, T., Preat, T., Boynton, S. C., & Del Vecchio, M. (1994) · Cell · doi:10.1016/0092-8674(94)90398-0 · Cited by 924
Associative Odor Learning in Drosophila Abolished by Chemical Ablation of Mushroom Bodies
de Belle, J. S., & Heisenberg, M. (1994) · Science · doi:10.1126/science.8303280 · Cited by 797
A Critical Period for Macromolecular Synthesis in Long-Term Heterosynaptic Facilitation in Aplysia
Montarolo, P. G., Goelet, P., Castellucci, V. F., Morgan, J., Kandel, E. R., & Schacher, S. (1986) · Science · doi:10.1126/science.3775383 · Cited by 769
Martin, K. C., Casadio, A., Zhu, H., Yaping, E., Rose, J. C., Chen, M., Bailey, C. H., & Kandel, E. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80484-5 · Cited by 740
Learning and memory in the honeybee
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Behavioral studies of Pavlovian conditioning
Rescorla, R. A. (1988) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.11.030188.001553 · Cited by 715
dunce, a mutant of Drosophila deficient in learning.
Dudai, Y., Jan, Y. N., Byers, D., Quinn, W. G., & Benzer, S. (1976) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.73.5.1684 · Cited by 619
Research works printed but not linked: 2
- Jellies JA (1981) Associative olfactory conditioning in Drosophila melanogaster and memory retention through metamorphosis. Master thesis (Illinois State University).
- 10.1016/0896-6273(93)90178-T · DOI
Cited by
Sorted by citations
Suh, G. S. B., Wong, A. M., Hergarden, A. C., Wang, J. W., Simon, A. F., Benzer, S., Axel, R., & Anderson, D. J. (2004) · Nature · doi:10.1038/nature02980 · Cited by 563
OLFACTORY MEMORY FORMATION INDROSOPHILA: From Molecular to Systems Neuroscience
Davis, R. L. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135651 · Cited by 543
Self-citationThe Role of Drosophila Mushroom Body Signaling in Olfactory Memory
McGuire, S. E., Le, P. T., & Davis, R. L. (2001) · Science · doi:10.1126/science.1062622 · Cited by 457
Self-citationInvited Review: Intermittent hypoxia and respiratory plasticity
Mitchell, G. S., Baker, T. L., Nanda, S. A., Fuller, D. D., Zabka, A. G., Hodgeman, B. A., Bavis, R. W., Mack, K. J., & Olson, E. B. (2001) · Journal of Applied Physiology · doi:10.1152/jappl.2001.90.6.2466 · Cited by 394
Kim, Y.-C., Lee, H.-G., & Han, K. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.1167-07.2007 · Cited by 365
Metadata
- Authors
- Beck, C. D. O., Schroeder, B., & Davis, R. L.
- Affiliations
- Baylor College of Medicine (US)
- ORCID
- Davis, Ronald L.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2000-04-15
- Volume
- 20
- Issue
- 8
- Pages
- 2944-2953
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6772219
- OpenAlex
- W1603963294
- Cited by
- 120
- References
- 38
- Citations by year
- 2026: 3 · 2025: 1 · 2024: 6 · 2023: 5 · 2022: 4 · 2021: 11 · 2020: 9 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 8 · 2015: 6 · 2014: 2 · 2013: 4 · 2012: 6
- FWCI
- 0.90
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (R01NS019904, NS-19904, R37NS019904)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurobiology and Insect Physiology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- olfactory conditioning, Drosophila, associative learning, intertrial interval, memory formation, learning performance, mutant analysis
- MeSH terms
- Alleles, Animals, Conditioning, Operant, Drosophila, Electric Stimulation, Learning, Memory, Mutation, Phenotype, Smell, Time Factors
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