Stressed memories: how acute stress affects memory formation in humans

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.

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 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 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.

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.