Elsevier

Biological Psychology

Volume 89, Issue 3, March 2012, Pages 539-544
Biological Psychology

Sex differences in emotional memory consolidation: The effect of stress-induced salivary alpha-amylase and cortisol

https://doi.org/10.1016/j.biopsycho.2011.12.006Get rights and content

Abstract

This study examined sex differences in the emotional memory consolidation, and the impact of stress-induced cortisol and salivary alpha amylase responses on emotional memory recall. Following baseline salivary measures, 39 healthy women and 41 men viewed 20 neutral and 20 negative arousing images, and then underwent either a cold pressor stress test or control condition, followed by further salivary measures. Participants returned two days later for a free recall test. The stress condition induced greater cortisol response, and negative images were better recalled than neutral. Whereas women displayed greater recall of negative images under stress than men, they recalled fewer negative images in the control condition. Stress-induced cortisol predicted recall of negative images in women, and neutral images in men. This suggests there is an enhanced consolidation of negative images under stress in women that may be a potential mechanism for the greater female prevalence for developing anxiety disorders.

Highlights

► Negative images were better recalled than neutral images. ► Women under stressful conditions recalled greater negative images than men. ► Women under non-stressful conditions recalled fewer negative images than men. ► Stress-induced cortisol predicted negative image recall in men. ► Stress-induced cortisol predicted negative and neutral image recall in women.

Introduction

An outstanding question in psychiatry is why women are particularly vulnerable to developing anxiety disorders. Epidemiologic studies show that women develop anxiety disorders such as Generalized Anxiety Disorder, Posttraumatic Stress Disorder (PTSD), Specific Phobia and Panic Disorder at twice the rate of men (Kessler et al., 2005). Recently, researchers have postulated that biological mechanisms may contribute to the female prevalence for anxiety (Cahill, 2006).

Many anxiety disorders (in particular PTSD) are characterized by intrusive images and distressing memories (Brewin et al., 2010). Recent theoretical models converge in proposing that visually processed memories are associated with greater arousal (Brewin et al., 2010), which may lead to greater memory consolidation and recall (McGaugh, 2004). A prevailing model of emotional memory suggests that high levels of stress hormones (noradrenaline and cortisol) released at the time of encoding result in an overconsolidation of emotional memories (McGaugh, 2004). Therefore, a potential biological mechanism underlying the female prevalence for anxiety disorders may be greater consolidation of emotional memories, leading to increased intrusive memories.

Empirical support for the memory modulation hypothesis arises from findings that emotional memories are recalled better than neutral memories (Anderson et al., 2006, McGaugh, 2004). Direct pharmacological manipulation of the noradrenergic system via post training amygdala infusions of noradrenergic agonists, antagonists and a combination of the two have provided compelling evidence for the role of the noradrenergic system in memory consolidation in both rats and humans (Cahill and Van Stegeren, 2003, LaBar, 2007, McGaugh, 2004, O’Carroll et al., 1999, Southwick et al., 2002). There is also compelling evidence for a role of glucocorticoids and their interaction with noradrenaline in mediating memory consolidation in rats and humans (Roozendaal et al., 2006, Kukolja et al., 2008).

Women have been found to have better recall of emotional memories than men (Bloise and Johnson, 2007, Davis, 1999, Canli et al., 2002). In line with the memory modulation hypothesis (McGaugh, 2004), there is also evidence to suggest that this enhanced ability for emotional memory is mediated by arousal in women. A recent study examined a biomarker of endogenous noradrenaline (salivary alpha amylase (sAA) in response to negative arousing images, and found that 21 of the 24 noradrenergic responders were women and that noradrenergic response was associated with greater negative memory recall (Segal and Cahill, 2009). Although this is initial evidence of a greater noradrenergic response in women, several other studies examining salivary alpha amylase to negative arousing images (but not emotional memory) have failed to find stress-induced sex differences (Takai et al., 2007, Van Stegeren et al., 2006, Van Stegeren et al., 2008), and baseline alpha amylase levels have been reported as higher in men (Van Stegeren et al., 2008). A potential reason for this inconsistency is variability in controlling for oral contraceptive use and menstrual phase in women (Van Stegeren et al., 2008). Although alpha amylase has been shown to increase emotional images and physical stressors (Van Stegeren et al., 2008), no studies have examined sex differences in alpha amylase response to physical stressors. Recent animal evidence in response to acute physical restraint stress reveals greater activation of locus coerulus neurons (the main noradrenergic nucleus in the brain) in female rats compared to males (Curtis et al., 2006, Valentino et al., 2011), and there appear greater dendritic branches on locus coerulus neurons in female rats (Bangasser et al., 2011). Consistently, a recent functional magnetic resonance imaging (fMRI) study reported greater activation in dorsal brainstem and midbrain regions (in regions containing ascending noradrenergic signals) in females following trauma compared to males (Felmingham et al., 2010). Therefore, further research is required to examine sex differences in noradrenergic (via salivary alpha amylase) response to stress in humans who are not taking oral contraceptives.

Studies of sex differences in the relationship of stress-induced cortisol and memory also yield inconsistent findings. Although greater cortisol response to acute stress has been found in men (Kirschbaum et al., 1999, Cornelisse et al., 2011), these studies failed to control for menstrual phase in women and did not control for oral contraceptive use. Position in the menstrual cycle has been shown to have a potent effect on cortisol response (Kirschbaum et al., 1999), and cortisol ha been shown to affect memory retrieval in naturally cycling women, but not in those taking hormonal contraception (Kuhlmann and Wolf, 2005). When controlling for menstrual phase, recent evidence reveals an association between cortisol and recall of negative images in the mid-luteal phase of the menstrual cycle (which is associated with greater glucocorticoid release) but not the early or late follicular phases (Andreano et al., 2008).

In summary, there is preliminary evidence that women display greater noradrenergic responses to stress, and have greater emotional memory recall than men. There is also an association between glucocorticoid release in the mid-luteal phase of the menstrual cycle and emotional memory recall in women. Accordingly, the greater female prevalence for developing anxiety disorders may be at least partially explained by a greater release of stress hormones, and thus greater memory consolidation and recall of emotional memories. The aim of the current study was to test this hypothesis by comparing salivary alpha amylase and cortisol responses following a stressor (compared to a control condition) presented immediately after encoding negative and neutral images in a sample of naturally cycling women. It was predicted that women would have greater delayed recall of threat images (but not neutral) compared to men, and that this would be mediated by salivary alpha amylase and cortisol responses to stress.

Section snippets

Participants

80 healthy undergraduate psychology students (41 women, 39 men) were recruited for the study as part of course credit. Participants were aged 18–40 years, had no history of psychiatric disorders, substance abuse, or traumatic brain injury, and were not taking psychoactive medications. Female participants had no menstrual irregularities and were not taking hormonal contraceptives. Women and men were randomly assigned to a stress (Cold Pressor Stess Test (CPS) or control (warm water) condition.

Demographic and ratings data

Table 1 presents demographic and clinical data for men and women in the CPS and control groups. Separate 2 (sex) × 2 (condition) ANOVAs revealed no significant differences in age, or DASS depression and anxiety scores between the groups in each condition. Four women were in the mid-luteal phase of the menstrual cycle in each of the CPS and control conditions. There were no significant differences in the ratings data (valence or arousal) between women and men in the different conditions. Negative

Discussion

This study addressed the critical but unexplored question of why women develop anxiety disorders at twice the rate of men. Specifically, we examined the role of a potential biological mechanism for this female vulnerability: enhanced consolidation of negative memories in women. The key finding was that women displayed greater recall of negative images under the stress condition than men, but recalled fewer negative images in the control condition. Post-stress increases in cortisol significantly

Acknowledgment

This project was funded by an ARC Discovery grant (DP0881814).

References (35)

  • A.H. Van Stegeren et al.

    Salivary alpha amylase and cortisol responses to different stress tasks: impact of sex

    International Journal of Psychophysiology

    (2008)
  • B. Wang et al.

    Gender differences in the effects of post-learning emotion on consolidation of item memory and source memory

    Neurobiology of Learning and Memory

    (2010)
  • A.K. Anderson et al.

    Emotional memories are not all created equal: evidence for selective memory enhancement

    Learning and Memory

    (2006)
  • J.M. Andreano et al.

    Glucocorticoid release and memory consolidation in men and women

    Psychological Science

    (2006)
  • S.M. Bloise et al.

    Memory for emotional and neutral information: gender and individual differences in emotional sensitivity

    Memory

    (2007)
  • C.R. Brewin et al.

    Intrusive images in psychological disorders: characteristics, neural mechanisms, and treatment implications

    Psychological Review

    (2010)
  • L. Cahill

    Why sex matters for neuroscience

    Nature Reviews Neuroscience

    (2006)
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