Mind the Gap: Olfactory Trace Conditioning in Honeybees
Open accessAbstract
Trace conditioning is a form of classical conditioning, where a neutral stimulus (conditioned stimulus, CS) is associated with a following appetitive or aversive stimulus (unconditioned stimulus, US). Unlike classical delay conditioning, in trace conditioning there is a stimulus-free gap between CS and US, and thus a poststimulus neural representation (trace) of the CS is required to bridge the gap until its association with the US. The properties of such stimulus traces are not well understood, nor are their underlying physiological mechanisms. Using behavioral and physiological approaches, we studied appetitive olfactory trace conditioning in honeybees. We found that single-odor presentation created a trace containing information about odor identity. This trace conveyed odor information about the initial stimulus and was robust against interference by other odors. Memory acquisition decreased with increasing CS–US gap length. The maximum learnable CS–US gap length could be extended by previous trace-conditioning experience. Furthermore, acquisition improved when an additional odor was presented during the CS–US gap. Using calcium imaging, we tested whether projection neurons in the primary olfactory brain area, the antennal lobe, contain a CS trace. We found odor-specific persistent responses after stimulus offset. These post-odor responses, however, did not encode the CS trace, and perceived odor quality could be predicted by the initial but not by the post-odor response. Our data suggest that olfactory trace conditioning is a less reflexive form of learning than classical delay conditioning, indicating that odor traces might involve higher-level cognitive processes.
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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 Szyszka et al. 2011
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Paoli, M., Wystrach, A., Ronsin, B., & Giurfa, M. (2024) · eLife · doi:10.7554/elife.93789.1.sa3
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- Authors
- Szyszka, P., Demmler, C., Oemisch, M., Sommer, L., Biergans, S., Birnbach, B., Silbering, A. F., & Galizia, C. G.
- Affiliations
- University of Konstanz (DE)
- Corresponding author
- Szyszka, Paul
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2011-05-18
- Volume
- 31
- Issue
- 20
- Pages
- 7229-7239
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6622586
- OpenAlex
- W2171206703
- Cited by
- 79
- References
- 62
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 11 · 2023: 5 · 2022: 4 · 2021: 4 · 2020: 5 · 2019: 2 · 2018: 4 · 2017: 4 · 2016: 3 · 2015: 2 · 2014: 9 · 2013: 9 · 2012: 5
- FWCI
- 3.57
- 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)
- KOPS (University of Konstanz) (submittedVersion)
- Funders
- Deutsche Forschungsgemeinschaft
- 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 › Sensory Systems › Olfactory and Sensory Function Studies
- Keywords
- Apis mellifera, classical conditioning, antennal lobe, projection neurons, odor identity, odor quality, memory acquisition, delay conditioning, olfactory learning
- MeSH terms
- Animals, Bees, Conditioning, Classical, Learning, Odorants, Reaction Time, Smell, Olfactory Receptor Neurons
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