Distinct molecular underpinnings of Drosophila olfactory trace conditioning
Open accessAbstract
Trace conditioning is valued as a simple experimental model to assess how the brain associates events that are discrete in time. Here, we adapted an olfactory trace conditioning procedure in Drosophila melanogaster by training fruit flies to avoid an odor that is followed by foot shock many seconds later. The molecular underpinnings of the learning are distinct from the well-characterized simultaneous conditioning, where odor and punishment temporally overlap. First, Rutabaga adenylyl cyclase (Rut-AC), a putative molecular coincidence detector vital for simultaneous conditioning, is dispensable in trace conditioning. Second, dominant-negative Rac expression, thought to sustain early labile memory, significantly enhances learning of trace conditioning, but leaves simultaneous conditioning unaffected. We further show that targeting Rac inhibition to the mushroom body (MB) but not the antennal lobe (AL) suffices to achieve the enhancement effect. Moreover, the absence of trace conditioning learning in D1 dopamine receptor mutants is rescued by restoration of expression specifically in the adult MB. These results suggest the MB as a crucial neuroanatomical locus for trace conditioning, which may harbor a Rac activity-sensitive olfactory “sensory buffer” that later converges with the punishment signal carried by dopamine signaling. The distinct molecular signature of trace conditioning revealed here shall contribute to the understanding of how the brain overcomes a temporal gap in potentially related events.
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There is evidence of a simple form of trace conditioning on olfactory stimuli in honey bees and fruit flies, though it is hard to be sure that the conditioned stimulus has really gone by the time the unconditioned stimulus has arrived.
“There is also evidence of a simple form of trace conditioning on olfactory stimuli, though it is hard to be sure, with olfactory stimuli, that the conditioned stimulus has really gone by the time the unconditioned stimulus has arrived (Shuai et al. 2011; Szyszka et al. 2011; Dylla et al. 2013, 2017).”
From Unlimited Associative Learning and the origins of consciousness: a primer and some predictions (2020) · cites this paper as Shuai et al. 2011
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- Authors
- Shuai, Y., Hu, Y., Qin, H., Campbell, R. A. A., & Zhong, Y.
- Affiliations
- Cold Spring Harbor Laboratory (US)
- Tsinghua University (CN)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2011-11-28
- Volume
- 108
- Issue
- 50
- Pages
- 20201-20206
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3250181
- OpenAlex
- W1967353273
- Cited by
- 45
- References
- 53
- Citations by year
- 2026: 2 · 2025: 6 · 2024: 2 · 2023: 4 · 2022: 4 · 2021: 4 · 2020: 3 · 2019: 2 · 2018: 1 · 2017: 2 · 2016: 3 · 2015: 3 · 2014: 2 · 2013: 3 · 2012: 4
- FWCI
- 1.19
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- Funders
- U.S. Department of Defense (W81XWH)
- National Institutes of Health (W81XWH)
- National Key Research and Development Program of China
- National Institute of Neurological Disorders and Stroke (R01NS064331)
- 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 › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Keywords
- Drosophila melanogaster, Rac GTPase, mushroom body, antennal lobe, dopamine D1 receptor, coincidence detection, memory consolidation
- MeSH terms
- Animals, Conditioning, Psychological, Drosophila melanogaster, Memory, Mutation, Odorants, Olfactory Pathways, Receptors, Dopamine, rac GTP-Binding Proteins, Mushroom Bodies
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
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