Trace Conditioning and the Hippocampus: The Importance of Contiguity
Open accessAbstract
Trace conditioning, a form of classical conditioning in which the presentation of the conditioned stimulus (CS) and the unconditioned stimulus (US) is separated in time by an interstimulus interval, requires an intact hippocampus. In contrast, classical conditioning procedures in which the CS and US are not separated by an interstimulus interval (i.e., delay conditioning procedures) typically do not (Solomon et al., 1986). However, why trace conditioning is dependent on the hippocampus is unknown. Several theories suggest that it is specifically the discontiguity between the CS and US in trace conditioning that critically engages the hippocampus. However, there are other explanations that do not depend on discontiguity. To determine whether the lack of contiguity renders trace conditioning hippocampal dependent, we designed a “contiguous trace conditioning” (CTC) paradigm in which CS–US contiguity is restored by re-presenting the CS simultaneously with the US. Although rats with excitotoxic lesions of the hippocampus could not learn a standard trace fear-conditioning paradigm, lesioned rats trained on CTC showed significant conditioning, at levels similar to those with sham surgeries. Importantly, lesioned rats trained solely with simultaneous CS–US presentations did not demonstrate conditioning. Together, these data suggest that rats with hippocampal lesions can form a memory of a trace CS–US association when contiguity is restored. Therefore, the dependence of traditional trace paradigms on the hippocampus can be attributed to the absence of temporal contiguity.
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Hippocampal damage impairs trace conditioning in humans, rabbits and rats.
“For example, hippocampal damage impairs trace conditioning in humans, rabbits and rats (Bangasser et al. 2006; Raybuck and Lattal 2014; McEchron et al. 1998; Moyer et al. 2015).”
From Unlimited Associative Learning and the origins of consciousness: a primer and some predictions (2020) · cites this paper as Bangasser et al. 2006
The Results section reports that hippocampal lesions prevented standard trace fear conditioning in rats. The References list rabbit studies, but the passages do not establish impairment in rabbits; the discussion instead notes that H.M. learned trace conditioning despite hippocampal damage, possibly after prior delay training. The paper therefore does not support the claim across all three species as stated. (LLM, conf=0.86)
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- Authors
- Bangasser, D. A., Waxler, D. E., Santollo, J., & Shors, T. J.
- Affiliations
- Rutgers, The State University of New Jersey (US)
- Corresponding author
- Shors, Tracey J.
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-08-23
- Volume
- 26
- Issue
- 34
- Pages
- 8702-8706
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC3289537
- OpenAlex
- W1990588924
- Cited by
- 185
- References
- 31
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 16 · 2023: 10 · 2022: 7 · 2021: 10 · 2020: 12 · 2019: 7 · 2018: 8 · 2017: 8 · 2016: 7 · 2015: 8 · 2014: 9 · 2013: 15 · 2012: 9
- FWCI
- 4.53
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Science Foundation (0444364)
- National Institute of Mental Health (R01MH059740, MH-59970, MH-59740, R01MH059970)
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
- Keywords
- trace conditioning, hippocampus, delay conditioning, hippocampal lesions, excitotoxic lesions, fear conditioning, associative memory, temporal contiguity
- MeSH terms
- Animals, Brain Diseases, Conditioning, Classical, Fear, Hippocampus, Male, Time Factors, Rats, Sprague-Dawley, Rats
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