Learning under stress impairs memory formation

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Abstract

Converging lines of evidence indicate that stress either before or after learning influences memory. Surprisingly little is known about how memory is affected when people learn while they are stressed. Here, we examined the impact of learning under stress in 48 healthy young men and women. Participants were exposed to stress (socially evaluated cold pressor test) or a control condition while they learned emotional words and neutral words that were either conceptually associated with or unrelated to the stressor. Memory was assessed in free recall and recognition tests 24 h after learning. Learning under stress reduced both free recall and recognition performance, irrespective of the emotionality and the stress context relatedness of the words. While the effect of stress was comparable in men and women, women outperformed men in the free recall test. These findings show a memory impairing effect of learning under stress in humans and challenge some assumptions of current theories about the impact of stress around the time of learning on memory formation.

Introduction

Stress and the hormones and neurotransmitters released in response to stress, such as glucocorticoids and catecholamines, shape memory processes. The nature of these effects is time-dependent. Stress prior to learning can facilitate or reduce memory (Elzinga et al., 2005, Payne et al., 2006, Schwabe, Bohringer, et al., 2008). Stress immediately after learning enhances memory (Cahill et al., 2003, Roozendaal, 2000, Wolf, 2008) whereas stress shortly before testing has mainly detrimental effects on memory (Buchanan et al., 2006, de Quervain et al., 1998, Schwabe and Wolf, 2009a).

A recent model (Joels, Pu, Wiegert, Oitzl, & Krugers, 2006) explains these seemingly discrepant effects of stress by the biphasic effects of stress hormones, in particular glucocorticoids (GC; cortisol in humans, corticosterone in rodents). GC exert their effects via rapid non-genomic or delayed genomic pathways (de Kloet, Karst, & Joels, 2008). Joels and colleagues (2006) argue that early stress responses, including corticotropin releasing factor (CRF), noradrenaline and rapid GC actions favor attentional processes and the encoding of relevant information. Delayed genomic GC actions, however, would suppress neuronal activity and therefore reduce the processing of new information. Thus, it is assumed that stress enhances memory when it is experienced in the context and around the time of learning; stress out of the learning context is supposed to impair memory. Support for this model comes mainly from rodent studies. For instance, rats trained at a relatively low temperature of 19 °C, i.e. under very stressful conditions, in the Morris water maze showed better acquisition and retention rates compared to rats trained at 25 °C (Sandi, Loscertales, & Guaza, 1997). Moreover, synaptic plasticity in the rodent hippocampus is enhanced when high corticosterone concentrations coincide with repetitive stimulation while synaptic plasticity is impaired when corticosterone is administered before or after stimulation (Diamond et al., 2007, Kim and Diamond, 2002, Wiegert et al., 2006).

Comparable evidence from humans is largely missing. Only two very recent studies aimed to test the assumptions of the model by Joels and colleagues (2006) in humans (Smeets et al., 2007, Smeets et al., 2009). In these studies, participants were exposed to psychosocial stress shortly before they learned words that were either related or unrelated to the stressor. Corroborating the assumptions of Joels et al. (2006), stressed participants remembered more stressor-related words than non-stressed controls. In these studies learning took place after a 15-min stressor, i.e. when cortisol concentrations were already elevated. Whether learning under stress, i.e. at the onset of stress, when catecholamines and CRF rise but cortisol concentrations are not yet increased may enhance subsequent memory in humans is unknown.

In the present experiment, we examined the impact of stress during learning on memory performance. To this end, we presented participants information while they were exposed to stress (socially evaluated cold pressor test) or a control condition. The presented information varied in its emotionality from neutral to positive and negative because previous studies suggested that emotional material is particularly sensitive to the effects of stress (Buchanan et al., 2006, Kuhlmann et al., 2005). Furthermore, we presented material that was related to the stress context. Memory was assessed 24 h after learning. According to the model by Joels and colleagues (2006), it can be predicted that learning under stress enhances memory, in particular for stress context-related information.

Section snippets

Participants and general procedure

Forty-eight healthy young men and women recruited at the Ruhr-University Bochum participated in this study (16 men, 32 women; age: M = 23.6 years, range 19–39 years; body-mass-index (BMI): M = 22.4 kg/m2, range 18–28 kg/m2). Twenty women were taking oral contraceptives. Exclusion criteria were checked in a standardized interview and comprised smoking, any medical illness within the prior 3 weeks, current or lifetime psychopathology, current treatment with psychotropic medications, β-blockers or

Subjective and physiological stress responses

Participants’ subjective assessments, blood pressure and cortisol changes indicated the successful stress induction by the SECPT.

Discussion

Earlier human studies examined changes in memory when participants were stressed before learning, after learning or before retention testing (Joels et al., 2006, Wolf, in press). To our knowledge, the present study is the first that assessed the impact of learning under stress, i.e. at the onset of the stress response. Our results show profound memory impairment in participants that were stressed during learning. Learning under stress reduced both free recall and recognition performance by more

Acknowledgments

This work was supported by DFG grant SCHW1357/2-1. We thank Sarah Schuster, Emine Nebi and Mathias Winnicki for their assistance during data collection.

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