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Cited by 295Memory and Neural MechanismsMemory Processes and InfluencesStress Responses and Cortisol

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Stressed Memories: How Acute Stress Affects Memory Formation in Humans

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Henckens, Marloes J. A. G., Hermans, Erno J., Pu, Zhenwei, Joëls, Marian, Fernández, Guillén·2009·The Journal of Neuroscience
DOI 10.1523/jneurosci.1184-09.2009PMC PMC6664979
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Abstract

Stressful, aversive events are extremely well remembered. Such a declarative memory enhancement is evidently beneficial for survival, but the same mechanism may become maladaptive and culminate in mental diseases such as posttraumatic stress disorder (PTSD). Stress hormones are known to enhance postlearning consolidation of aversive memories but are also thought to have immediate effects on attentional, sensory, and mnemonic processes at memory formation. Despite their significance for our understanding of the etiology of stress-related mental disorders, effects of acute stress at memory formation, and their brain correlates at the system scale, remain elusive. Using an integrated experimental approach, we probed the neural correlates of memory formation while participants underwent a controlled stress induction procedure in a crossover design. Physiological (cortisol level, heart rate, and pupil dilation) and subjective measures confirmed acute stress. Remarkably, reduced hippocampal activation during encoding predicted stress-enhanced memory performance, both within and between participants. Stress, moreover, amplified early visual and inferior temporal responses, suggesting that hypervigilant processing goes along with enhanced inferior temporal information reduction to relay a higher proportion of task-relevant information to the hippocampus. Thus, acute stress affects neural correlates of memory formation in an unexpected manner, the understanding of which may elucidate mechanisms underlying psychological trauma etiology.

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Crossref · 10.1523/jneurosci.1184-09.2009

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Figures

Figure 1 Experimental design. IAPS pictures (Lang et al., 1999) were encoded during fMRI scanning in either a stressful or a neutral control condition generated by short movie clips. Psychological and physiological measures were obtained to monitor the effectiveness of stress induction. Memory was tested 24 h later in a cued recall test. S, Saliva sample; P, PANAS questionnaire (Watson et al., 1988).
Figure 1 Experimental design. IAPS pictures (Lang et al., 1999) were encoded during fMRI scanning in either a stressful or a neutral control condition generated by short movie clips. Psychological and physiological measures were obtained to monitor the effectiveness of stress induction. Memory was tested 24 h later in a cued recall test. S, Saliva sample; P, PANAS questionnaire (Watson et al., 1988).CC-BY-NC-SA · From the PDF
Figure 2 Physiological effects of stress. A , B , The stress induction procedure increased (area under the curve) cortisol levels (expressed as percentage of baseline) (45-135 min) ( A ) and reduced mean phasic pupil dilation (expressed as ratio of baseline diameter) after the initial light reflex ( B ). Significance refers to the observed within-subject effects, and the error bars represent SEM of the between-subject variance. * p < 0.05.
Figure 2 Physiological effects of stress. A , B , The stress induction procedure increased (area under the curve) cortisol levels (expressed as percentage of baseline) (45-135 min) ( A ) and reduced mean phasic pupil dilation (expressed as ratio of baseline diameter) after the initial light reflex ( B ). Significance refers to the observed within-subject effects, and the error bars represent SEM of the between-subject variance. * p < 0.05.CC-BY-NC-SA · From the PDF
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Figure 4 Stress modulated the subsequent memory effect in the right hippocampus. A , Statistical parametric map, here thresholded at p < 0.001 (uncorrected) for visualization purposes, revealed a negative stress induction by subsequent memory effect interaction ( x = 28). B , Signal differences between subsequently remembered and forgotten trials separately depicted for the stress induction and control condition, based on averaged parameter estimates of the total volume of the anatomically defined hippocampus,revealedanegativesubsequentmemoryeffectduringstress. C , The observed stress-induced decrease in hippocampal responses predicted the stress-related improvement in memory performance across subjects. Error bars represent SEM of the between-subjects variance.
Figure 4 Stress modulated the subsequent memory effect in the right hippocampus. A , Statistical parametric map, here thresholded at p < 0.001 (uncorrected) for visualization purposes, revealed a negative stress induction by subsequent memory effect interaction ( x = 28). B , Signal differences between subsequently remembered and forgotten trials separately depicted for the stress induction and control condition, based on averaged parameter estimates of the total volume of the anatomically defined hippocampus,revealedanegativesubsequentmemoryeffectduringstress. C , The observed stress-induced decrease in hippocampal responses predicted the stress-related improvement in memory performance across subjects. Error bars represent SEM of the between-subjects variance.CC-BY-NC-SA · From the PDF

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  1. 10.1017/S0048577298001991 · DOI

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Metadata

Authors
Henckens, M. J. A. G., Hermans, E. J., Pu, Z., Joëls, M., & Fernández, G.
Affiliations
  • Radboud University Nijmegen (NL)
  • University of Amsterdam (NL)
Corresponding author
Henckens, Marloes J. A. G.
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2009-08-12
Volume
29
Issue
32
Pages
10111-10119
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.1184-09.2009
PMC
PMC6664979
OpenAlex
W2158213171
Cited by
295
References
64
Citations by year
2026: 8 · 2025: 12 · 2024: 21 · 2023: 16 · 2022: 9 · 2021: 21 · 2020: 17 · 2019: 27 · 2018: 17 · 2017: 23 · 2016: 23 · 2015: 12 · 2014: 16 · 2013: 24 · 2012: 14
FWCI
7.90
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
  • UvA-DARE (University of Amsterdam) (publishedVersion, other-oa)
  • Radboud Repository (Radboud University) (submittedVersion)
  • Radboud Repository (Radboud University) (submittedVersion, other-oa)
  • Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
Funders
Nederlandse Organisatie voor Wetenschappelijk Onderzoek (918.66.613)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Memory Processes and Influences
  • Life Sciences › Neuroscience › Behavioral Neuroscience › Stress Responses and Cortisol
Keywords
acute stress, memory formation, post-traumatic stress disorder, hippocampal activation, memory encoding, stress hormones, cortisol, stress induction, visual cortex, inferior temporal cortex, hypervigilance, neural correlates of memory, psychological trauma
MeSH terms
Adult, Brain Mapping, Heart Rate, Hippocampus, Humans, Hydrocortisone, Magnetic Resonance Imaging, Male, Pattern Recognition, Visual, Photic Stimulation, Pupil, Surveys and Questionnaires, Mental Recall, Saliva, Stress, Psychological, Temporal Lobe, Cross-Over Studies, Young Adult

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