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Articles, Behavioral/Systems/Cognitive

Stressed Memories: How Acute Stress Affects Memory Formation in Humans

Marloes J. A. G. Henckens, Erno J. Hermans, Zhenwei Pu, Marian Joëls and Guillén Fernández
Journal of Neuroscience 12 August 2009, 29 (32) 10111-10119; DOI: https://doi.org/10.1523/JNEUROSCI.1184-09.2009
Marloes J. A. G. Henckens
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Erno J. Hermans
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Zhenwei Pu
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Marian Joëls
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Guillén Fernández
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    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).

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    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.

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    Figure 3.

    Brain regions affected by stress induction and memory (y = −72, −59). A, Stress induction increased responsiveness within the primary visual cortex and right inferior temporal region, centered on the fusiform gyrus. B, Positive (in red) subsequent memory effects in large inferior temporal and superior parietal regions and negative (in blue) subsequent memory effects in posterior midline structures comprising the cuneus and the lingual gyrus. C, Conjunctions of positive effects of stress induction with positive (in red) or negative (in blue) subsequent memory effects. These figures show that enhanced recruitment of the primary visual cortex after stress induction was detrimental to memory formation. In contrast, stress-enhanced inferior temporal activation proved beneficial. All statistical parametric maps are thresholded at p < 0.001, uncorrected, using minimum statistic/global null methods for conjunction effects, for visualization purposes. For formal statistical tests, see Table 1.

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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, revealed a negative subsequent memory effect during stress. 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.

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    Table 1.

    Brain regions revealing significant main, interaction, or conjunction effects

    RegionCoordinatesPeak T score
    xyz
    Main effect of subsequent memory
        Remembered > forgotten
            Middle occipital gyrus, L−26−68366.64***
            Middle occipital gyrus, R30−68387.39***
            Inferior temporal gyrus, L−46−62−67.94***
            Inferior temporal gyrus, R54−56−108.69***
            Fusiform gyrus, L−34−32−204.46++
            Fusiform gyrus, R34−32−224.15++
            Inferior parietal lobule, L−44−44566.63***
            Inferior parietal lobule, R36−52565.31**
            Inferior frontal gyrus, L−503468.47***
            Inferior frontal gyrus, R526226.21***
    543865.93***
        Forgotten > remembered
            Cuneus, L−4−90244.86*
            Cuneus, R16−64348.46***
            Lingual gyrus, L−16−62−45.74**
            Middle frontal gyrus, R3834345.04*
    2852224.87*
    Main effect of stress
        Stress > control
            Superior occipital gyrus, L−8−9485.09*
            Superior occipital gyrus, R16−92204.99*
            Lingual gyrus, R8−72−25.86***
            Fusiform gyrus, L−36−66−163.88+
            Fusiform gyrus, R28−70−65.28*
    28−50−24.88*
            Inferior temporal gyrus, R46−48−184.06++
    Stress by SME interaction (negative)
        Hippocampus, R28−26−84.29++
        Forgotten > remembered during stress
            Hippocampus, R28−26−85.01*
    Stress by SME conjunction
        Remembered > forgotten and stress > control
            Inferior temporal gyrus, R48−52−63.20†
        Stress > control and forgotten > remembered
            Lingual gyrus, L−8−76−64.21++
    −20−62−43.68+
    • ↵The peak x, y, z coordinates are given in MNI152 standard space coordinates. L and R denote left and right. SME, Subsequent memory effect.

    • ↵*p < 0.05 whole-brain corrected;

    • ↵**p < 0.01 whole-brain corrected;

    • ***p < 0.001 whole-brain corrected; +p < 0.05 small volume corrected; ++p < 0.01 small volume corrected, †p < 0.05 small volume corrected (r = 10 mm) centered on the maximum of the main contrast.

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The Journal of Neuroscience: 29 (32)
Journal of Neuroscience
Vol. 29, Issue 32
12 Aug 2009
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Stressed Memories: How Acute Stress Affects Memory Formation in Humans
Marloes J. A. G. Henckens, Erno J. Hermans, Zhenwei Pu, Marian Joëls, Guillén Fernández
Journal of Neuroscience 12 August 2009, 29 (32) 10111-10119; DOI: 10.1523/JNEUROSCI.1184-09.2009

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Stressed Memories: How Acute Stress Affects Memory Formation in Humans
Marloes J. A. G. Henckens, Erno J. Hermans, Zhenwei Pu, Marian Joëls, Guillén Fernández
Journal of Neuroscience 12 August 2009, 29 (32) 10111-10119; DOI: 10.1523/JNEUROSCI.1184-09.2009
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