Elsevier

Psychoneuroendocrinology

Volume 80, June 2017, Pages 80-91
Psychoneuroendocrinology

Arousal amplifies biased competition between high and low priority memories more in women than in men: The role of elevated noradrenergic activity

https://doi.org/10.1016/j.psyneuen.2017.02.022Get rights and content

Highlights

  • Arousal enhanced competition effects in memory in women with high noradrenergic activity.

  • Men did not show such arousal-biased competition effects in memory.

  • Under high noradrenergic activity, arousal impaired distracter recognition in women.

  • Under high noradrenergic activity, arousal enhanced distracter recognition in men.

  • Memory selectivity was greater in naturally cycling women with high NE/low sex hormones.

Abstract

Recent findings indicate that emotional arousal can enhance memory consolidation of goal-relevant stimuli while impairing it for irrelevant stimuli. According to one recent model, these goal-dependent memory tradeoffs are driven by arousal-induced release of norepinephrine (NE), which amplifies neural gain in target sensory and memory processing brain regions. Past work also shows that ovarian hormones modulate activity in the same regions thought to support NE’s effects on memory, such as the amygdala, suggesting that men and women may be differentially susceptible to arousal’s dual effects on episodic memory. Here, we aimed to determine the neurohormonal mechanisms that mediate arousal-biased competition processes in memory. In a competitive visuo-attention task, participants viewed images of a transparent object overlaid on a background scene and explicitly memorized one of these stimuli while ignoring the other. Participants then heard emotional or neutral audio-clips and provided a subjective arousal rating. Hierarchical generalized linear modeling (HGLM) analyses revealed that greater pre-to-post task increases in salivary alpha-amylase (sAA), a biomarker of noradrenergic activity, was associated with significantly greater arousal-enhanced memory tradeoffs in women than in men. These sex-dependent effects appeared to result from phasic and background noradrenergic activity interacting to suppress task-irrelevant representations in women but enhancing them in men. Additionally, in naturally cycling women, low ovarian hormone levels interacted with increased noradrenergic activity to amplify memory selectivity independently of emotion-induced arousal. Together these findings suggest that increased noradrenergic transmission enhances preferential consolidation of goal-relevant memory traces according to phasic arousal and ovarian hormone levels in women.

Introduction

Emotionally arousing events form some of our most vivid and enduring memories (LaBar and Cabeza, 2006, Sharot et al., 2004). Yet arousal does more than simply enhance memory of emotional stimuli; it modulates processing of all information perceived during, shortly before, or shortly after an arousing event. Across experimental conditions, emotional stimuli can either enhance or impair memory for nearby neutral stimuli (Anderson et al., 2006, Bocanegra and Zeelenberg, 2009, Kensinger et al., 2007, Knight and Mather, 2009, Mather, 2007, Mather and Sutherland, 2011).

A reliable finding in the emotion-cognition literature is that foreground emotionally arousing objects often elicit a tradeoff by yielding enhanced object memory but impaired memory for neutral background scenes (Kensinger et al., 2007, Mather, 2007, Waring and Kensinger, 2011). Relatedly, when eyewitnesses to a crime recall their experience, they often remember the weapon itself − the source of arousal − at the cost of memory for the perpetrator’s face, a phenomenon known as the “weapon focus effect” (Steblay, 1992). Memory tradeoffs are also commonly observed when emotional and neutral memoranda compete nearby in time. For instance, several studies demonstrate that emotional images or words induce retrograde amnesia for preceding neutral stimuli (Hurlemann et al., 2005, Hurlemann et al., 2007, Knight and Mather, 2009, Strange et al., 2003). The adaptive significance of such arousal-related tradeoffs is that processing of seemingly inconsequential information is suppressed to allocate limited mental resources to processing the emotional object, which is likely to have greater motivational significance than nearby neutral information.

Recent studies, however, indicate that arousal can enhance rather than impair memory for neutral information when those stimuli have priority, such as goal relevance (Lee et al., 2015, Sakaki et al., 2014). The arousal-biased competition (ABC) model proposes that a momentary surge of arousal amplifies the effects of top-down attention, such that processing goal-relevant information is enhanced at the expense of processing distracting information (Mather and Sutherland, 2011). This framework builds upon the idea of biased competition in the brain, whereby − by virtue of their motivational relevance or perceptual salience − prioritized stimuli outcompete less salient information for limited mental resources to gain representation and reach awareness (Desimone and Duncan, 1995).

Increasing evidence supports ABC’s predictions that emotional arousal enhances the effects of goal relevance in memory. For example, seeing an emotional image can enhance memory for a preceding goal-relevant neutral object, while impairing memory for a subsequent less-attended neutral object (Sakaki et al., 2014). Likewise, hearing an emotional versus neutral sound suppresses memory consolidation for a neutral scene paired with a salient foreground object that was seen just beforehand (Ponzio and Mather, 2014). Based on these findings, it seems that emotional arousal amplifies competitive processes more generally, leading to “winner-take-more” and “loser-take-less” effects in memory regardless of whether priority is determined by emotional factors or not.

Presently, most brain-based models fail to account for the arousal’s dual effects on cognition. To address how arousal interacts with priority in the brain, the glutamate amplifies noradrenergic effects (GANE) model posits that activity-dependent increases in norepinephrine (NE) enable arousal to enhance already highly activated, prioritized mental representations even further (Mather et al., in press). According to GANE, the brain’s primary excitatory neurotransmitter, glutamate, serves as a flexible marker of priority. When arousal is induced, elevated glutamate levels corresponding with high priority (e.g., goal-relevant) stimuli spill over from the synaptic gap to interact with nearby NE axons and stimulate additional local NE release; in turn, local elevations of NE at these synapses engage low-binding-affinity β-adrenoreceptors that up-regulate glutamate release even further. In addition to enhancing the activation strength of important representations, the engagement of β-adrenoreceptors on nearby glutamate terminals triggers synaptic plasticity processes, thereby promoting the storage of “winning” mental representations into memory. Elsewhere, the predominantly inhibitory effects of NE release prevail where lower priority, “losing” representations fail to engage this positive glutamate-NE feedback loop. Together these dichotomous influences of NE on local regional activity amplify the gain on competition between high and lower priority representations, providing a neuromechanism by which arousal optimizes selectivity in perception and memory.

The GANE model helps reconcile and extend previous influential theories of how NE modulates episodic memory by highlighting the role of priority in regulating different memory outcomes. For instance, GANE aligns with models positing that NE biases attention (Markovic et al., 2014) and memory consolidation (McGaugh and Roozendaal, 2002, McGaugh, 2013) to favor emotional or affectively salient information over neutral information (Markovic et al., 2014). More recently, it was demonstrated that increasing NE levels with isometric handgrip in young women enhances selective memory for negative emotional stimuli (Nielsen et al., 2015), suggesting that NE release enhances memory selectivity even when sympathetic arousal is manipulated externally. Thus, the dominance of emotional stimuli in perception and memory may be due both to the prioritization they acquire through their motivational relevance (e.g., reward or punishment) as well as the presence of elevated NE.

Building upon these ideas, the GANE model proposes that the beneficial mnemonic effects of NE released under arousal are not unique to emotional stimuli but rather apply to any prioritized stimulus, including goal-relevant neutral stimuli. Consistent with this, one recent study showed that elevated levels of noradrenergic activity, indexed by salivary alpha-amylase (sAA), are positively associated with retrograde memory enhancements for goal-relevant neutral stimuli encountered prior to an emotional event (Clewett et al., 2017). Arousal-related NE release may also amplify competition in memory consolidation (e.g. Ponzio and Mather, 2014).

Another important consideration is how NE might affect memory consolidation differently in men and women given ample evidence of sex-dependent effects of emotional arousal on episodic memory. At the behavioral level, women show even stronger memory enhancements for emotional versus neutral stimuli and tend to recall emotional material more quickly and more vividly than men (Hamann, 2005, Hamann and Canli, 2004). Young women who show greater increases in salivary biomarkers of noradrenergic activity exhibit retrograde memory enhancement for high priority neutral images preceding something emotional (Clewett et al., 2017). Women also exhibit greater emotion-induced retrograde amnesia for inconspicuous neutral words preceding an emotional versus neutral oddball word, an effect that is β-adrenoreceptor-dependent (Strange et al., 2003).

Other work suggests that such sex differences in emotion-related memory consolidation may arise due interactions between NE released under arousal and background levels of sex steroid hormones. For instance, sex steroid hormone levels have been shown to modulate emotional memory enhancements both in the presence and absence of stress, such that higher levels of sex hormones lead to stronger emotional memory enhancements (Andreano et al., 2008, Ertman et al., 2011). There are also indications that estradiol potentiates NE release (Bangasser et al., 2016) and, along with progesterone, alters the responsivity of the amygdala and hippocampus − key regions that are regulated by NE and that support emotional memory consolidation (McIntyre et al., 2012) − to emotional images (Andreano and Cahill, 2010). However, there is also evidence of contradictory mnemonic effects of sex steroid hormones under arousal. For example, Nielsen et al. (2015) found that the memory-biasing effects of handgrip-induced increases in NE only occurred in women with lower estradiol and progesterone levels at encoding. Wegerer et al. (2014) also revealed that low levels of estradiol are associated with stronger intrusive memories for emotional materials (Wegerer et al., 2014). Together these data suggest that GANE effects may differ between young women and men due to fluctuating sex steroid hormone levels influencing the consolidation of prioritized information either independently or via interactions with NE release.

The goal of the present study was to determine whether noradrenergic activity, as indexed by salivary alpha-amylase (Ditzen et al., 2014), amplifies the effects of top-down priority in cognition, such that memory for goal-relevant neutral images is enhanced at the expense of memory for competing neutral distracters in men and women as predicted by GANE. Alternatively, other models would predict that emotional events disrupt ongoing cognitive selection processes due to NE re-allocating limited attention and mental resources towards processing emotionally salient stimuli (Bouret and Sara, 2005, Markovic et al., 2014). From this alternative perspective, encountering something emotional should always result in prioritization of the emotionally salient stimuli and thus attenuate processing of neutral stimuli irrespective of their goal relevance. In addition, given the mixed findings on the effects of sex steroid hormones, we examined whether there were significant sex-dependent effects of tonic noradrenergic activity and phasic arousal on the selective consolidation of neutral episodic memories. Based on prior emotion-cognition research, we were particularly interested in whether estradiol and progesterone altered the strength of NE’s effects on memory in young women.

Section snippets

Participants

One hundred and two healthy young adults were recruited from the University of Southern California Psychology Subject Pool to participate in this experiment. All participants provided written informed consent approved by the University of Southern California Institutional Review Board and were awarded course credits for their participation. All eligible individuals had normal or normal-to-corrected vision and hearing. Female participants were either using hormonal contraception or naturally

Sound arousal and distraction ratings

Mean distraction ratings for the sounds did not significantly differ between men (M = 3.26, SD = 1.16) and women (M = 3.40, SD = 1.67; p > 0.05). Mean subjective arousal ratings for the sounds also did not significantly differ between men and women in any of the three pre-defined valence categories. However, there was a robust main effect of Valence on subjective arousal ratings, F(2,56) = 773.89, p < 0.001, ηp2 = 0.97, such that participants perceived negative sounds (M = 7.11, SD = 0.66) as being significantly

Discussion

Given the broad and diffuse release of NE under arousal, the noradrenergic system is ideally positioned to modulate any on-going cognitive selection process when emotional events occur. Yet, although it is well established that NE released under arousal helps strengthen emotional memories (McGaugh and Roozendaal, 2002), there has been less examination of whether NE can also bias memory in favor of prioritized, goal-relevant neutral information. Our results supported this prediction, revealing

Conclusion

Years of research demonstrate that emotional arousal can enhance or impair cognitive processing. But, until recently, we lacked a unifying brain-based model to account for such dual effects. Our results support the recent hypothesis that NE released under arousal enhances the gain on competition between goal-relevant and distracting neutral information in memory (Mather et al., in press). Thus, beyond simply enhancing emotional memories, NE appears to amplify selectivity in memory consolidation

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    This project was funded by federal NIH grants R01AG038043 (M.M.), R01AG025340 (M.M.), a grant from the European Commission (FP7-PEOPLE-2013-CIG; M.S.), a University of Southern California Endowed Fellowship (D.C.), and federal NIA grant F32AG047840 (S.N.).

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