Cited by 239Memory and Neural MechanismsNeural and Behavioral Psychology StudiesMemory Processes and Influences

Neural Substrates Mediating Human Delay and Trace Fear Conditioning

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Knight, David C., Cheng, Dominic T., Smith, Christine N., Stein, Elliot A., Helmstetter, Fred J.·2004·The Journal of Neuroscience

Abstract

Previous functional magnetic resonance imaging (fMRI) studies with human subjects have explored the neural substrates involved in forming associations in Pavlovian fear conditioning. Most of these studies used delay procedures, in which the conditioned stimulus (CS) and unconditioned stimulus (UCS) coterminate. Less is known about brain regions that support trace conditioning, a procedure in which an interval of time (trace interval) elapses between CS termination and UCS onset. Previous work suggests significant overlap in the neural circuitry supporting delay and trace fear conditioning, although trace conditioning requires recruitment of additional brain regions. In the present event-related fMRI study, skin conductance and continuous measures of UCS expectancy were recorded concurrently with whole-brain blood oxygenation level-dependent (BOLD) imaging during direct comparison of delay and trace discrimination learning. Significant activation was observed within the visual cortex for all CSs. Anterior cingulate and medial thalamic activity reflected associative learning common to both delay and trace procedures. Activations within the supplementary motor area (SMA), frontal operculum, middle frontal gyri, and inferior parietal lobule were specifically associated with trace interval processing. The hippocampus displayed BOLD signal increases early in training during all conditions; however, differences were observed in hippocampal response magnitude related to the accuracy of predicting UCS presentations. These results demonstrate overlapping patterns of activation within the anterior cingulate, medial thalamus, and visual cortex during delay and trace procedures, with additional recruitment of the hippocampus, SMA, frontal operculum, middle frontal gyrus, and inferior parietal lobule during trace conditioning. These data suggest that the hippocampus codes temporal information during trace conditioning, whereas brain regions supporting working memory processes maintain the CS-UCS representation during the trace interval.

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Crossref · 10.1523/jneurosci.0433-03.2004

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Authors
Knight, D. C., Cheng, D. T., Smith, C. N., Stein, E. A., & Helmstetter, F. J.
Affiliations
  • University of Wisconsin–Milwaukee (US)
  • National Institutes of Health (US)
  • Medical College of Wisconsin (US)
Venue
The Journal of Neuroscience
Published
2004-01-07
Volume
24
Issue
1
Pages
218-228
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
OpenAlex
W2144116954
Cited by
239
References
73
Citations by year
2026: 7 · 2025: 3 · 2024: 3 · 2023: 4 · 2022: 6 · 2021: 10 · 2020: 7 · 2019: 6 · 2018: 4 · 2017: 7 · 2016: 13 · 2015: 11 · 2014: 22 · 2013: 26 · 2012: 13
FWCI
6.22
Type
journal article
Language
en
Open access
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • National Institute of Mental Health (R01MH060668, F31MH011722, MH060668, MH11722)
  • National Institute on Drug Abuse (R01DA009465, DA 09465)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Neural and Behavioral Psychology Studies
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
Keywords
fear conditioning, trace conditioning, delay conditioning, classical conditioning, neural correlates, hippocampus, supplementary motor area, frontal operculum, inferior parietal lobule, anterior cingulate cortex, medial thalamus, visual cortex, working memory, temporal coding
MeSH terms
Adolescent, Adult, Brain, Conditioning, Classical, Electric Conductivity, Electric Stimulation, Electroshock, Fear, Female, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Neurons, Time Factors

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