Trace conditioning in insects—keep the trace!

Dylla, Kristina V.; Galili, Dana S.; Szyszka, Paul; Lüdke, Alja

doi:10.3389/fphys.2013.00067

Cited by 57Neurobiology and Insect Physiology ResearchMemory and Neural MechanismsNeuroscience and Neuropharmacology Research

Trace conditioning in insects—keep the trace!

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Dylla, Kristina V., Galili, Dana S., Szyszka, Paul, Lüdke, Alja·2013·Frontiers in Physiology

DOI 10.3389/fphys.2013.00067PMC PMC3750952

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Abstract

Trace conditioning is a form of associative learning that can be induced by presenting a conditioned stimulus (CS) and an unconditioned stimulus (US) following each other, but separated by a temporal gap. This gap distinguishes trace conditioning from classical delay conditioning, where the CS and US overlap. To bridge the temporal gap between both stimuli and to form an association between CS and US in trace conditioning, the brain must keep a neural representation of the CS after its termination-a stimulus trace. Behavioral and physiological studies on trace and delay conditioning revealed similarities between the two forms of learning, like similar memory decay and similar odor identity perception in invertebrates. On the other hand differences were reported also, like the requirement of distinct brain structures in vertebrates or disparities in molecular mechanisms in both vertebrates and invertebrates. For example, in commonly used vertebrate conditioning paradigms the hippocampus is necessary for trace but not for delay conditioning, and Drosophila delay conditioning requires the Rutabaga adenylyl cyclase (Rut-AC), which is dispensable in trace conditioning. It is still unknown how the brain encodes CS traces and how they are associated with a US in trace conditioning. Insects serve as powerful models to address the mechanisms underlying trace conditioning, due to their simple brain anatomy, behavioral accessibility and established methods of genetic interference. In this review we summarize the recent progress in insect trace conditioning on the behavioral and physiological level and emphasize similarities and differences compared to delay conditioning. Moreover, we examine proposed molecular and computational models and reassess different experimental approaches used for trace conditioning.

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Within-stimulus competition in trace conditioning of the rabbit’s nictitating membrane response
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(1998) · doi:10.1002/(sici)1098-1063(1998)8:6

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“…temporal durability of compound percepts based on back and forth (reentrant) signaling is the basis of working memory (Wang, 2001) and of trace conditioning (in which there is a temporal gap between the US and the CS; Solomon et al., 1986; Woodruff-Pak and Disterhoft, 2008; Dylla et al., 2013).”
Background
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Scientific Arguments against Free Will
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Dedication
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Epigraph
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Frontispiece
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The Philosophy of Free Will
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The Neuroscience of Free Will
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The Basic Questions
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Introduction
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Notes
Tse, P. U. (2024) · doi:10.1093/oso/9780198876953.002.0008
Copyright Page
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Other minds
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Who is Conscious?
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Introduction
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Unconscious minds
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Where are we now?
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It’s hard not to be a Dualist
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Other minds without words
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Trace conditioning: insights from invertebrate models on bridging the temporal gap
Rivi, V., Ponkshe, A., Lukowiak, K. D., & Batabyal, A. (2026) · Biology Letters · doi:10.1098/rsbl.2026.0022

Reviewed by:
Dylla, K. V., Galili, D. S., Szyszka, P., Lüdke, A., Pyza, E. M., Skoulakis, E. M. C., Centre Alexander Fleming, Steven, J., & Belle, D. (2013)
Self-citation
Trace conditioning: insights from invertebrate models on bridging the temporal gap
Rivi, V., Ponkshe, A., Lukowiak, K. D., & Batabyal, A. (2026) · Biology Letters · doi:10.1098/rsbl.2026.0022
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Differential mechanisms underlie trace and delay conditioning in Drosophila
Grover, D., Chen, J., Xie, J. L., Li, J., Changeux, J., & Greenspan, R. J. (2022) · Nature · doi:10.1038/s41586-022-04433-6 · Cited by 63 · see citing works
Distinct molecular underpinnings of Drosophila olfactory trace conditioning
Shuai, Y., Hu, Y., Qin, H., Campbell, R. A. A., & Zhong, Y. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1107489109 · Cited by 45 · see citing works

Authors: Dylla, K. V., Galili, D. S., Szyszka, P., & Lüdke, A.
Affiliations: Max Planck Society (DE)
University of Konstanz (DE)
Corresponding author: Lüdke, Alja
ORCID: Galili, Dana S.
Szyszka, Paul
Lüdke, Alja
Venue: Frontiers in Physiology
Publisher: Frontiers Media SA
Published: 2013
Volume: 4
Pages: 67-67
ISSN: 1664-042X (ISSN-L)
DOI: 10.3389/fphys.2013.00067
PMC: PMC3750952
OpenAlex: W2071422380
Cited by: 57
References: 110
Citations by year: 2026: 1 · 2025: 17 · 2024: 18 · 2023: 1 · 2022: 3 · 2021: 5 · 2020: 2 · 2019: 1 · 2018: 2 · 2017: 3 · 2016: 1 · 2015: 1 · 2014: 1 · 2013: 1
FWCI: 0.65
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: Frontiers in Physiology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
KOPS (University of Konstanz) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
Max Planck Digital Library (submittedVersion)
MPG.PuRe (Max Planck Society) (submittedVersion)
Funders: International Max Planck Research School for Environmental, Cellular and Molecular Microbiology
Minerva Foundation
Bundesministerium für Bildung und Forschung (01GQ0931)
Universität Konstanz
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: trace conditioning, delay conditioning, associative learning, insects, time gap, memory decay, hippocampus, Drosophila, computational models of learning, memory encoding

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Trace conditioning in insects—keep the trace!

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