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Cited by 171Memory and Neural MechanismsNeural and Behavioral Psychology StudiesMemory Processes and Influences

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Context conditioning and extinction in humans: differential contribution of the hippocampus, amygdala and prefrontal cortex

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Lang, Simone, Kroll, Alexander, Lipinski, Slawomira J., Wessa, Michèle, Ridder, Stephanie, Christmann, Christoph, Schad, Lothar R., Flor, Herta·2009·European Journal of Neuroscience
DOI 10.1111/j.1460-9568.2009.06624.xPMC PMC2695154
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Abstract

Functional magnetic resonance imaging was used to investigate the role of the hippocampus, amygdala and medial prefrontal cortex (mPFC) in a contextual conditioning and extinction paradigm provoking anxiety. Twenty-one healthy persons participated in a differential context conditioning procedure with two different background colours as contexts. During acquisition increased activity to the conditioned stimulus (CS+) relative to the CS- was found in the left hippocampus and anterior cingulate cortex (ACC). The amygdala, insula and inferior frontal cortex were differentially active during late acquisition. Extinction was accompanied by enhanced activation to CS+ vs. CS- in the dorsal anterior cingulate cortex (dACC). The results are in accordance with animal studies and provide evidence for the important role of the hippocampus in contextual learning in humans. Connectivity analyses revealed correlated activity between the left posterior hippocampus and dACC (BA32) during early acquisition and the dACC, left posterior hippocampus and right amygdala during extinction. These data are consistent with theoretical models that propose an inhibitory effect of the mPFC on the amygdala. The interaction of the mPFC with the hippocampus may reflect the context-specificity of extinction learning.

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Crossref · 10.1111/j.1460-9568.2009.06624.x

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Figures

Fig. 1 Schematic representation of the acquisition phase of the experiment. As can be seen, the colours are presented gradually until they reach their maximal spectrum. During habituation CS and US were presented in random order. During conditioning, the context changed gradually from orange to orange and blue to blue and orange. If the same colour was repeated (i.e. from blue to blue), the colour gradually changed from blue to black and from black to blue. In our example, the blue context represents the CS+ that was paired in the acquisition phase with a threat stimulus and later extinguished. Note that the onset of threat stimulus was unpredictable, i.e. it was given at varying intervals after context onset. During extinction no US was delivered. Within extinction, the colours were presented with clear on- and offsets, separated by a black screen.
Fig. 1 Schematic representation of the acquisition phase of the experiment. As can be seen, the colours are presented gradually until they reach their maximal spectrum. During habituation CS and US were presented in random order. During conditioning, the context changed gradually from orange to orange and blue to blue and orange. If the same colour was repeated (i.e. from blue to blue), the colour gradually changed from blue to black and from black to blue. In our example, the blue context represents the CS+ that was paired in the acquisition phase with a threat stimulus and later extinguished. Note that the onset of threat stimulus was unpredictable, i.e. it was given at varying intervals after context onset. During extinction no US was delivered. Within extinction, the colours were presented with clear on- and offsets, separated by a black screen.CC BY · PubMed Central
Fig. 2 Skin conductance response (SCR; means and standard errors of the means) to the CS+unpaired vs. CS− for the four phases (habituation, first and second acquisition phase, and extinction) during differential context conditioning (a). (b–d) Self-report data (means and standard errors of the means) for arousal (b), valence (c), and CS–US contingency (d). *P < 0.05, **P < 0.01, ***P < 0.001.
Fig. 2 Skin conductance response (SCR; means and standard errors of the means) to the CS+unpaired vs. CS− for the four phases (habituation, first and second acquisition phase, and extinction) during differential context conditioning (a). (b–d) Self-report data (means and standard errors of the means) for arousal (b), valence (c), and CS–US contingency (d). *P < 0.05, **P < 0.01, ***P < 0.001.CC BY · PubMed Central
Fig. 3 Neural activation and percent signal changes for the single conditioning phases (Hab = habituation; Acq1 = early acquisition phase; Acq2 = late acquisition phase; Ext = extinction) to CS+ vs. CS− for (a) the left posterior hippocampus, (b) the left dorsal hippocampus (during late acquisition), (c) the left amygdala and (d) the right dorsal anterior cingulate cortex (dACC; BA32). *Significant CS+/CS− differentiation.
Fig. 3 Neural activation and percent signal changes for the single conditioning phases (Hab = habituation; Acq1 = early acquisition phase; Acq2 = late acquisition phase; Ext = extinction) to CS+ vs. CS− for (a) the left posterior hippocampus, (b) the left dorsal hippocampus (during late acquisition), (c) the left amygdala and (d) the right dorsal anterior cingulate cortex (dACC; BA32). *Significant CS+/CS− differentiation.CC BY · PubMed Central
Fig. 4 T-maps for extinction showing significant coupling between (a) BA32 (seed region) and (b) left posterior hippocampus [MNI coordinate (−27, −24, −9) and (−24, −18, −12), P < 0.05, FDR-corrected for ROI] and (c) right amygdala [MNI coordinate (18, 0, −15), P < 0.05, FDR-corrected for ROI]. (d) Regression line between signal changes to CS+ vs. CS− in BA32 (seed region) and right amygdala (target region). BA, Brodmann area; L, left; R, right.
Fig. 4 T-maps for extinction showing significant coupling between (a) BA32 (seed region) and (b) left posterior hippocampus [MNI coordinate (−27, −24, −9) and (−24, −18, −12), P < 0.05, FDR-corrected for ROI] and (c) right amygdala [MNI coordinate (18, 0, −15), P < 0.05, FDR-corrected for ROI]. (d) Regression line between signal changes to CS+ vs. CS− in BA32 (seed region) and right amygdala (target region). BA, Brodmann area; L, left; R, right.CC BY · PubMed Central

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  1. Rescorla R.A., 1972, Classical conditioning II: current theory and research, 64

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Metadata

Authors
Lang, S., Kroll, A., Lipinski, S. J., Wessa, M., Ridder, S., Christmann, C., Schad, L. R., & Flor, H.
Affiliations
Heidelberg University (DE)
ORCID
Venue
European Journal of Neuroscience
Publisher
Wiley
Published
2009-02
Volume
29
Issue
4
Pages
823-832
ISSN
  • 0953-816X (ISSN-L)
  • 1460-9568
DOI
10.1111/j.1460-9568.2009.06624.x
PMC
PMC2695154
OpenAlex
W1991878909
Cited by
171
References
72
Citations by year
2026: 2 · 2025: 1 · 2024: 8 · 2023: 3 · 2022: 7 · 2021: 8 · 2020: 10 · 2019: 11 · 2018: 18 · 2017: 12 · 2016: 15 · 2015: 11 · 2014: 16 · 2013: 16 · 2012: 10
FWCI
5.32
Type
journal article
Language
en
Open access
Licence
onlinelibrary.wiley.com/termsAndConditions#vor (vor, 5 d)
Locations
  • European Journal of Neuroscience (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
Deutsche Forschungsgemeinschaft
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
contextual conditioning, extinction learning, hippocampus, amygdala, medial prefrontal cortex, anterior cingulate cortex, anxiety, contextual learning, hippocampal-amygdala interaction, neuronal connectivity
MeSH terms
Adult, Amygdala, Cerebral Cortex, Conditioning, Psychological, Cues, Electric Stimulation, Extinction, Psychological, Female, Galvanic Skin Response, Hippocampus, Humans, Magnetic Resonance Imaging, Male, Neural Pathways, Photic Stimulation, Regression Analysis, Prefrontal Cortex, Young Adult

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