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. Author manuscript; available in PMC: 2023 Feb 28.
Published in final edited form as: Brain Cogn. 2018 Dec 12;133:94–105. doi: 10.1016/j.bandc.2018.11.009

Enhancing memory with stress: Progress, challenges, and opportunities

Elizabeth V Goldfarb 1
PMCID: PMC9972486  NIHMSID: NIHMS1871097  PMID: 30553573

Abstract

Stress can strongly influence what we learn and remember, including by making memories stronger. Experiments probing stress effects on hippocampus-dependent memory in rodents have revealed modulatory factors and physiological mechanisms by which acute stress can enhance long-term memory. However, extending these findings and mechanisms to understand when stress will enhance declarative memory in humans faces important challenges. This review synthesizes human and rodent studies of stress and memory, examining translational gaps related to measurements of declarative memory and stress responses in humans. Human studies diverge from rodent research by assessing declarative memories that may not depend on the hippocampus and by measuring peripheral rather than central stress responses. This highlights opportunities for future research across species, including assessing stress effects on hippocampal-dependent memory processes in humans and relating peripheral stress responses to stress effects on the function of memory-related brain regions in rodents. Together, these investigations will facilitate the translation of stress effects on memory function from rodents to humans and inform interventions that can harness the positive effects of stress on long-term memory.

Keywords: stress, glucocorticoids, memory, hippocampus, human, rodent

1. Introduction

Stress responses are fundamentally adaptive and enable us to face stressful events. These responses can also prepare us for future challenges by helping us remember stressful experiences (McGaugh, 2015). The goal of this review is to discuss insights regarding circumstances under which stress improves memory and highlight translational challenges related to measurements of memory and stress across species, with a focus on understanding the positive effects of acute stress on declarative memory in humans.

Acute stress is known to both enhance and impair cognitive function. One major area of progress in the human stress literature has been in characterizing the negative effects of stress (for a recent meta-analysis on stress-induced impairments in working memory and cognitive flexibility, see Shields, Sazma, & Yonelinas, 2016). In the domain of long-term memory, there is substantial experimental evidence demonstrating that exposure to acute stress before attempting to retrieve information impairs memory performance (reviewed in Gagnon & Wagner, 2016). However, there are also circumstances under which acute stress can greatly enhance memory (Joels, Pu, Wiegert, Oitzl, & Krugers, 2006; Roozendaal, 2002). Such mnemonic boosts may contribute to the strong trauma memories that characterize posttraumatic stress disorder, leading to proposed clinical interventions of blocking the trauma-induced stress response in order to attenuate these memories (D. de Quervain, Schwabe, & Roozendaal, 2017).

The enhancing effects of acute stress on memory extend beyond extreme cases of traumatic events. Across species, even mild to moderate laboratory stressors can improve memory. For example, stress leads rodents to show better memory for information including mazes (Conboy & Sandi, 2010; Diamond, Campbell, Park, Halonen, & Zoladz, 2007; Sandi, Loscertales, & Guaza, 1997) and object-location associations (Roebuck, Liu, Lins, Scott, & Howland, 2018), while humans show enhanced memory for words (McCullough & Yonelinas, 2013; Schwabe, Bohringer, Chatterjee, & Schachinger, 2008) and pictures (Cahill, Gorski, & Le, 2003; Henckens, Hermans, Pu, Joels, & Fernandez, 2009; Payne et al., 2007; Payne et al., 2006). This raises the possibility that, under the right conditions, even the pervasive stressors of everyday life could be leveraged to facilitate memory.

After defining stress and considering general mechanisms by which stress may enhance memory, this review highlights conditions shown in rodents to potentiate the enhancing effects of acute stress on hippocampal memory. The review then shifts to discuss translational challenges related to how declarative memory and stress responses are assessed in human research. Specifically, rodent and human studies diverge in whether they measure memories that crucially depend on the hippocampus, with rodent studies frequently measuring hippocampal-dependent (spatial) memories and human studies often measuring declarative memory for individual items, which instead depends on parts of the medial temporal lobe cortex. In addition, rodent studies can measure stress responses centrally by directly testing the effects of stress hormones on target tissue, whereas human studies are limited to peripheral assays.

Exploring the measurements of declarative memory and stress responses in humans reveals challenges for generalizing the conditions under which stress enhances rodent memory to predict when stress will facilitate human declarative memory. It also suggests fruitful next steps for both the human and nonhuman animal fields to understand the positive impact of acute stress on declarative memory.

1.1. What is acute stress?

To understand how acute stress influences memory, it is helpful to separate the triggering event (stressor) from the reaction to that event (stress response; also discussed in Lupien, Maheu, Tu, Fiocco, & Schramek, 2007). A stressor poses a potential threat to the homeostasis of an organism, and we frequently encounter mild or moderate stressors in daily life. Research in humans has employed methods including retrospective self-report questionnaires (e.g., Goldfarb, Shields, Daw, Slavich, & Phelps, 2017) or daily prompts (e.g., Connolly & Alloy, 2018) to investigate the relationship between such real-world stressors and memory. To probe the effects of acute stress (as opposed to prolonged, or chronic, exposure to stressors), researchers commonly expose participants to an experimental manipulation in the laboratory that is designed to act as a stressor. Effective stressors (i.e., those that are more likely to produce a stress response) are characterized as novel, unpredictable, and uncontrollable (Mason, 1968). In humans, effective stressors often involve a social-evaluative component, in which the participant receives negative social feedback which can threaten the participant’s social esteem or social status (S. S. Dickerson & Kemeny, 2004). To provide a concrete sense of how such conditions are created for human participants, descriptions of common laboratory stressors are shown in Table 1.

Table 1.

Common laboratory stressors in human research

Stressor Description Example reference
Physiological
Cold pressor test (CPT) Submerge arm in bucket of ice water (0-4°C) for three minutes Lovallo (1975)
CO2 test Inhale mixture of CO2 (35%) and O2 through mouthpiece Kaye et al. (2004)
Psychological
Trier social stress test (TSST) Prepare for, then perform speech and mental arithmetic in front of judgmental audience Kirschbaum, Pirke, and Hellhammer (1993)
Personalized imagery script Listen to and re-experience personalized imagery script describing real-life stressful event Sinha (2009)
Aversive image exposure View stream of highly negative and arousing IAPS pictures (Center for the Study of Emotion and Attention (CSEA-NIMH), 1999) Goldstein et al. (2005)
Aversive film clips View clips from movie with highly aversive content (extreme violence) Qin, Hermans, van Marle, Luo, and Fernandez (2009)
Cognitive
Trier mental challenge test Solve increasingly difficult mental arithmetic tasks under time pressure Pruessner, Hellhammer, and Kirschbaum (1999)
Star mirror tracing task Trace star-shaped figure as quickly and accurately as possible while viewing its reversed image. Under time pressure, receive negative feedback for errors Matthews, Woodall, and Allen (1993)
Paced auditory serial addition task (PASAT) Add sequential number pairs, retaining second number for use in subsequent pair. Numbers presented at increasingly fast pace Gronwall (1977)
Hybrid
Threat of shock Anticipate that shocks may be delivered through attached electrodes Grillon, Ameli, Woods, Merikangas, and Davis (1991)
Socially evaluated cold pressor test (SECPT) Submerge arm in bucket of ice water (0-4°C) for up to three minutes while observed by experimenter and videotaped for analysis of facial expressions Schwabe, Haddad, and Schachinger (2008)
Maastricht acute stress test (MAST) After preparation period, alternate submerging hand in bucket of ice water (2°C) for random intervals with performing mental arithmetic and receiving negative feedback. Videotaped to analyze facial expressions throughout Smeets et al. (2012)
Montreal imaging stress task (MIST) Perform challenging mental arithmetic under time pressure with negative feedback, shown unfavorable comparison to “average” performance Dedovic et al. (2005)
“Cognitive challenge” Perform challenging tasks under time pressure while receiving negative feedback from physician in white laboratory coat Bremner et al. (2003)

By administering stressors in the laboratory, researchers can standardize the experience across participants, control when the stressor occurs, and consistently measure the stress response. The stress response includes cognitive, affective, and physiological processes, with the field of stress and cognition largely focusing on two major parts of the physiological stress response. These include the immediate activation of the sympatho-adrenomedullary axis, leading to the rapid release of adrenaline and noradrenaline from the adrenal medulla, as well as the activation of the hypothalamic-pituitary-adrenal (HPA) axis, triggering the relatively slower release of glucocorticoids from the adrenal cortex (reviewed in Joels, Sarabdjitsingh, & Karst, 2012; Lupien et al., 2007; Ulrich-Lai & Herman, 2009). Adrenaline does not readily cross the blood-brain barrier and appears to act on memory processes through binding peripheral β-adrenoceptors and triggering the production of central adrenergic agents (Osborne, Pearson-Leary, & McNay, 2015; Roozendaal & McGaugh, 2011). In contrast, glucocorticoids (cortisol in humans and corticosterone in rodents) are small, lipophilic, and easily cross the blood-brain barrier. Once in the brain, glucocorticoids have been shown to bind to two major types of receptors, namely high-affinity mineralocorticoid (MR) and low-affinity glucocorticoid (GR) receptors (Reul & de Kloet, 1985).

Measuring the stress response (Section 3.2) is critical to understanding the effects of stress on cognitive processes like memory. For example, even if the stressor varies substantially across species (e.g., a human performing mental arithmetic and a rodent smelling a predator odor), these events each trigger a measurable stress response. Furthermore, even within a species, there is a great deal of variability in how individuals respond to a stressor (Mason, 1968). Quantifying the stress response thus enables researchers to compare and generalize how different components of this response modulate memory. In a complementary approach, pharmacological experiments testing the influence of different parts of the stress response have directly administered adrenergic or glucocorticoid agents (early examples in rodents: Gold & Van Buskirk, 1975; Sandi et al., 1997; humans: D. J. de Quervain, Roozendaal, Nitsch, McGaugh, & Hock, 2000; O’Carroll, Drysdale, Cahill, Shajahan, & Ebmeier, 1999), or blocked the adrenergic or glucocorticoid components of endogenous stress responses (rodent: D. J. de Quervain, Roozendaal, & McGaugh, 1998; Maroun & Akirav, 2008; human: Maheu, Joober, & Lupien, 2005; Nielson & Jensen, 1994). Together, these experimental approaches have provided key insights into the circumstances under which acute stress facilitates memory.

2. How could acute stress enhance memory?

Broadly speaking, acute stress is thought to influence memory through the actions of glucocorticoid and adrenergic agents on the neural networks that support memory processes. The positive effects of acute stress on memory have been shown to crucially involve glucocorticoid responses. For example, injections of corticosterone enhanced recognition and spatial memory in rodents (Roozendaal, Okuda, Van der Zee, & McGaugh, 2006; Sandi et al., 1997) and oral doses of cortisol enhanced declarative memory in humans (Abercrombie, Kalin, Thurow, Rosenkranz, & Davidson, 2003; Buchanan & Lovallo, 2001; Kuhlmann & Wolf, 2006). On the other side, blocking glucocorticoid synthesis during a stressful encoding experience prevented the enhancing effect of stress on later spatial memory in rodents (Conboy & Sandi, 2010) and diminished emotion-induced enhancement of subjective recollection in humans (Antypa, Vuilleumier, & Rimmele, 2018).

How might these physiological stress responses facilitate memory? The discovery that the hippocampus, a critical region for memory, retains high concentrations of glucocorticoids (McEwen, Weiss, & Schwartz, 1969), led to tremendous interest in studying this region to understand the neurobiological mechanisms underlying the diverse effects of stress on memory. Subsequent studies revealed that MR and GR receptors are each highly expressed in the hippocampus, suggesting that the function of this region would be particularly sensitive to stress hormones (Joels et al., 2012; Osborne et al., 2015). Although the field is not yet at a point to directly map cellular actions of stress hormones to behavioral consequences of stress (Joels, Karst, & Sarabdjitsingh, 2018), several effects of glucocorticoids on hippocampal function are consistent with enhancing effects of stress on memory, as will be discussed in more detail below (Section 2.1).

In addition to acting directly on the hippocampus, stress hormones may enhance memory by indirectly modulating hippocampal function. One major locus for these modulatory actions is the amygdala (particularly the basolateral nucleus, BLA). Research in rodents has demonstrated that the BLA broadly modulates hippocampal plasticity (Ikegaya, Saito, & Abe, 1994, 1995), is itself sensitive to stress hormones (Di et al., 2016; Karst, Berger, Erdmann, Schutz, & Joels, 2010), and mediates the effects of agents such as adrenaline, noradrenaline, and glucocorticoids on hippocampal memory (reviewed in Roozendaal & McGaugh, 2011). For example, the enhancing effects of BLA stimulation on hippocampal signaling (specifically in the dentate gyrus) were blocked by administering a GR antagonist (Vouimba, Yaniv, & Richter-Levin, 2007) or the glucocorticoid synthesis inhibitor metyrapone (Akirav & Richter-Levin, 2002). In addition, bilateral BLA lesions have been shown to block both impairing effects of acute stress and GR agonists (Kim, Lee, Han, & Packard, 2001; Roozendaal, Griffith, Buranday, De Quervain, & McGaugh, 2003), as well as enhancing effects of intrahippocampal glucocorticoid injections (Roozendaal & McGaugh, 1997) on spatial memory processes. Supporting the importance of these amygdala-hippocampal interactions, humans who encoded information in a stressful context showed both improved declarative memory and enhanced amygdala-hippocampal connectivity (as measured by functional neuroimaging, or fMRI) immediately after encoding (de Voogd, Klumpers, Fernandez, & Hermans, 2017). Finally, the amygdala also appears to play an important role in memory enhancement by supporting the interaction between glucocorticoids and adrenergic agents (Quirarte, Roozendaal, & McGaugh, 1997; reviewed in Roozendaal, McEwen, & Chattarji, 2009).

These direct and indirect effects of stress on hippocampal function are often cited to explain how stress influences declarative memory in humans (e.g., Cadle & Zoladz, 2015; Elzinga, Bakker, & Bremner, 2005; Kirschbaum, Wolf, May, Wippich, & Hellhammer, 1996). This is based on the memory system taxonomy in which declarative memory depends on the hippocampus (Squire, 2004). Although it is beyond the scope of this review, it is worth noting that the neural mechanisms underlying beneficial effects of stress on memory are likely to vary based on the information being remembered (Schwabe, 2017). For example, many studies have shown that stress can influence memory for associations between stimuli and responses (Goldfarb & Phelps, 2017). These memories critically involve the dorsolateral striatum (Packard & McGaugh, 1996), and can be enhanced via injections of corticosterone into this region (Quirarte et al., 2009; Siller-Perez, Serafin, Prado-Alcala, Roozendaal, & Quirarte, 2017). Other types of memory may be enhanced through direct actions of stress hormones on regions including prefrontal cortex (PFC; e.g., Barsegyan, Mackenzie, Kurose, McGaugh, & Roozendaal, 2010; reviewed in McEwen, Nasca, & Gray, 2016), insular cortex (Miranda, Quirarte, Rodriguez-Garcia, McGaugh, & Roozendaal, 2008), and nucleus accumbens (Wichmann, Fornari, & Roozendaal, 2012).

Despite these positive effects of glucocorticoids, acute stress does not always enhance memory. Even under carefully controlled experimental conditions in rodents, the effects of acute stress on memory are complex and varied. This has led to the discovery of conditions, or factors, that help determine whether a stressor will enhance or impair memory. A central challenge for the field, which is the focus of this review, concerns how to generalize these modulatory factors and their underlying neural mechanisms from rodents to humans.

2.1. When acute stress benefits memory: Key modulatory factors

Several key factors that modulate acute stress effects on memory in rodents are described in Table 2. For example, rats who learned a water maze during a stressor (cold water; leading to glucocorticoid release) had better memory for the maze than rats who learned without the stressor (Sandi et al., 1997). However, in another water maze experiment, rats exposed to a stressor 30–60 minutes before encoding (restraint and tailshocks, which also induce glucocorticoid release) had worse memory than non-stressed counterparts (Kim et al., 2001). Such findings demonstrate the crucial importance of stressor timing in determining whether stress will enhance or impair memory.

Table 2.

Factors influencing whether acute stress enhances memory

Key factor Memory enhanced if… For further reading
Stressor
 Dosage Moderate (not very low or high) Sandi and Pinelo-Nava (2007)
 Timing (relative to encoding) Close to encoding Diamond et al. (2007)
 Timing (memory phase) Prior to consolidation Roozendaal (2002)
 Stress ligand receptor MR Vogel, Fernandez, Joels, and Schwabe (2016)
Learned information
 Emotional content of memoranda Emotionally salient Roozendaal et al. (2009)
 Relationship to stressor Related Joels et al. (2006)
Participant
 Sex Varied (depends on oral contraceptives and menstrual phase) Merz and Wolf (2017)

Research in rodents has facilitated both behavioral evidence for these modulatory factors and potential neurobiological mechanisms by which these modulators may operate. For example, the benefits of stress for remembering emotionally salient information may be driven by an interaction between glucocorticoids and the adrenergic response that results from encoding emotionally salient information (for review, see Roozendaal & McGaugh, 2011). Habituating rodents to objects, and thus decreasing the emotional salience of these objects, blocked the enhancing effects of corticosterone on memory (Okuda, Roozendaal, & McGaugh, 2004). Likewise, blocking the adrenergic response during encoding prevented the enhancements in inhibitory avoidance or recognition memory that would have resulted from post-encoding dexamethasone (a synthetic glucocorticoid), GR-receptor agonists, or corticosterone (Quirarte et al., 1997; Roozendaal et al., 2006). In contrast, inducing an adrenergic response during encoding facilitated this enhancement (Roozendaal et al., 2006). Demonstrating the importance of the interaction between these agents, blocking the corticosterone response attenuated the positive effects of post-encoding adrenaline on cue conditioning memory (Roozendaal, Carmi, & McGaugh, 1996).

The modulatory factor of emotional salience may play a similar role in humans, as several studies have found that the enhancing effects of stress are limited to salient memoranda (pre-encoding: Payne et al., 2007; Payne et al., 2006; post-encoding: Cahill et al., 2003; Goldfarb, Tompary, Davachi, & Phelps, 2018; Kim et al., 2001; Smeets, Otgaar, Candel, & Wolf, 2008). As in rodents, this effect may operate through the interaction between adrenergic and glucocorticoid responses. Participants who had an adrenergic response during encoding also had improved declarative memory with oral cortisol, but those who did not show an adrenergic response did not demonstrate this benefit (S. K. Segal et al., 2014). In another study, although co-administration of yohimbine (promoting an adrenergic response) and hydrocortisone did not enhance memory more than hydrocortisone alone, the combination did change the neural circuits engaged during encoding (van Stegeren, Roozendaal, Kindt, Wolf, & Joels, 2010).

Another well-studied modulatory factor is the timing of stressor exposure relative to the onset of encoding. Specifically, if the stressor occurs near the time of encoding, memory will be enhanced. For example, rats exposed to a stressor immediately before learning a water maze had enhanced memory 24 hours later, whereas if the stressor began 30 minutes before encoding memory was not enhanced (Diamond et al., 2007) or was even impaired (Park, Zoladz, Conrad, Fleshner, & Diamond, 2008). Memory was also enhanced if the stressor was part of the learning experience (Conboy & Sandi, 2010; Salehi, Cordero, & Sandi, 2010; Sandi et al., 1997). This modulatory factor has been incorporated into several theoretical models of stress effects on memory, including the convergence in space and time model (Joels et al., 2006), the temporal dynamics model (Diamond et al., 2007), and the memory formation/memory storage model (Schwabe, Joels, Roozendaal, Wolf, & Oitzl, 2012). Remembering events that occurred near the time of the stressor may help an organism respond more adaptively to such events in the future. In contrast, events that occurred long after (or long before) the stressor are unlikely to be useful for future stressor encounters and may even compete for storage with more relevant events, leading these distal memories to be impaired (for further discussion, see Cadle & Zoladz, 2015).

One biological mechanism proposed to explain differing stress effects over time is grounded in the influence of glucocorticoids on hippocampal long-term potentiation (LTP). This form of synaptic plasticity has been implicated in learning and memory processes (Xiong & Krugers, 2015). Crucially, the timing of glucocorticoid effects on hippocampal LTP appears to mirror the timing of stressor effects on memory. First, just as memory was enhanced if encoding occurred during or soon after stressor exposure, LTP was enhanced if in vitro stimulation of hippocampal slices occurred during or soon after exposure to stress hormones. In a seminal experiment, Karst and colleagues stimulated mouse hippocampal slices and measured evoked excitatory postsynaptic currents (EPSPs) in the CA1 subregion. The frequency of miniature EPSPs (mEPSPs) were markedly and transiently increased when these slices were bathed in stress levels of corticosterone during stimulation (Karst et al., 2005; replicated in Olijslagers et al., 2008). Stimulation during corticosterone exposure also transiently enhanced the frequency of mEPSPs in the dentate gyrus subregion of the hippocampus (Pasricha, Joels, & Karst, 2011). Second, as with stressor-induced memory enhancements, a longer delay between corticosterone exposure and in vitro stimulation did not lead to enhanced LTP. Summarizing across studies, Joëls and colleagues noted that CA1 neurons showed reduced responses to stimulation beginning about 20 minutes following corticosterone exposure (Joels et al., 2012). For example, in vitro stimulation within 10 minutes of corticosterone exposure led to increased field EPSPs, but corticosterone administered 30 minutes before stimulation did not (Wiegert, Joels, & Krugers, 2006). In another experiment, stimulation 5 minutes after exposure to aldosterone (which binds MR receptors) led to increased LTP in the ventral hippocampus, whereas stimulation 30 minutes after hormone exposure did not (Maggio & Segal, 2012; for differences in stress effects on dorsal and ventral hippocampus, see M. Segal, Richter-Levin, & Maggio, 2010). Together, these experiments demonstrate that stress hormones act on a cellular process associated with learning and memory within the hippocampus following a temporal pattern that corresponds to the effects of stress hormones on memory performance.

Similar behavioral patterns of stress effects over time have been reported in humans. A recent meta-analysis showed that the timing of pre-encoding stressor exposure significantly predicted the effects of stress on declarative memory, with longer delays associated with impaired memory (Shields, Sazma, McCullough, & Yonelinas, 2017). As with rodents, stressors enhanced declarative memory if they were experienced shortly before (Hoscheidt, LaBar, Ryan, Jacobs, & Nadel, 2014; Luo et al., 2018; Payne et al., 2007) or during encoding (Henckens et al., 2009; Wiemers, Sauvage, Schoofs, Hamacher-Dang, & Wolf, 2013). Enabling direct comparisons of stress effects over time, two studies used the same memory assessments but exposed participants to a stressor either immediately or 30 minutes before encoding. Participants with a 30-minute delay between stress and encoding had worse free recall, whereas those exposed to stress immediately before learning had better free recall (Zoladz et al., 2011). Similarly, a 30-minute delay led to a negative correlation between cortisol and picture recognition, but no delay led to a positive correlation between cortisol and picture recognition (Quaedflieg, Schwabe, Meyer, & Smeets, 2013).

Despite the similarity of time-dependent stress effects on rodent and human memory, there are significant challenges in translating the underlying neural mechanism. First, the behavioral evidence in rodents is grounded in effects of stress on hippocampus-dependent tasks (mazes), and one compelling biological mechanism involves actions of stress hormones on the hippocampal plasticity. However, the behavioral evidence in humans comes from declarative memory assays that may not be hippocampal-dependent (discussed further in Section 3.1). Second, this biological mechanism relies on elevated levels of glucocorticoids in the hippocampus at the time of stimulation. Yet the assays of glucocorticoids in human research are necessarily peripheral, not central (Section 3.2). These challenges will be explored in the following sections.

3. Challenges in translating stress and memory findings in rodents to humans

The above section summarizes compelling evidence supporting predictions about when acute stress will enhance human memory. Unfortunately, designing an experiment in humans that capitalizes on the memory-boosting potential of stress remains challenging. For example, exposing participants to a moderate stressor close to the time that they learn emotionally arousing material should facilitate memory for this information. Yet some studies using these conditions in humans have reported no significant stress effects (Domes, Heinrichs, Rimmele, Reichwald, & Hautzinger, 2004; Wirkner, Weymar, Low, & Hamm, 2013) or even impaired memory (Schwabe & Wolf, 2010). Likewise, although enhancing effects of stress have been shown to be limited to emotionally salient rather than neutral memoranda for rodents and humans, human studies have also reported the opposite (Preuss & Wolf, 2009; Rimmele, Domes, Mathiak, & Hautzinger, 2003; Shermohammed, Davidow, Somerville, & Murty, 2018; Trammell & Clore, 2014). These discrepancies may be due to differences between the assessments of declarative memory used in human research compared to the assessments of spatial (hippocampal-dependent) memory used in rodent research. Furthermore, even when the effects of stress on memory appear qualitatively similar, it may not be appropriate to extrapolate the neurobiological mechanism proposed in rodents. Considering the assessments of memory and stress response in human experiments reveals the source of some of these challenges and highlights critical areas for future research.

3.1. Measurements of memory in humans

The majority of experiments assessing the influence of acute stress on declarative memory in humans operationalize memory using recognition and/or free recall for individual items (for pre-encoding stress examples, see Domes et al., 2004; Payne et al., 2007; Payne et al., 2006; Quaedflieg et al., 2013; Schwabe & Wolf, 2010; Wirkner et al., 2013; Zoladz et al., 2011; Zoladz et al., 2013). In a typical design (Domes et al., 2004), participants study a list of words. After a delay of at least 24 hours, they write down all the words that they can remember (free recall). They then complete a recognition test in which they are shown a list of words and indicate which are “old” (previously studied) or “new” (not previously studied).

Generalizing findings from hippocampal tasks in rodents to such memory tasks in humans can be problematic, yet the findings from these human experiments have made important contributions to the field of stress and memory. They have revealed that stress effects on human memory vary based on factors including whether the stressor occurs before consolidation or retrieval (Domes et al., 2004; Smeets et al., 2008) and the magnitude of the stress-induced cortisol response (Buchanan, Tranel, & Adolphs, 2006). As discussed earlier (Section 2.1), research in humans has also emphasized the importance of the affective content of the learned information and the delay between the stressor and encoding in modulating the direction of stress effects on subsequent memory. Nonetheless, these memory tasks present challenges for extending modulators of stress effects on memory from rodents to humans.

These challenges stem from evidence that distinct neural systems support different types of memories. Many studies examining the influence of acute stress on item recognition use stress effects on hippocampal function to motivate their designs and explain their findings. However, there is evidence that item recognition does not depend on an intact hippocampus (unless recognition judgments based on familiarity and recollection are explicitly separated; see Yonelinas, Aly, Wang, & Koen, 2010 and below for further discussion). Patients with selective hippocampal lesions had relatively spared item recognition (A. R. Mayes, Holdstock, Isaac, Hunkin, & Roberts, 2002; Turriziani, Fadda, Caltagirone, & Carlesimo, 2004; but see (Stark, Bayley, & Squire, 2002), and fMRI studies have demonstrated that hippocampal signal during encoding were not associated with successful item recognition (Davachi, Mitchell, & Wagner, 2003; Rugg et al., 2012; Staresina & Davachi, 2008). Instead, several lines of evidence, including single unit recordings, lesions, and fMRI, have shown that the perirhinal cortex (a nearby medial temporal lobe region) is critical for item recognition (reviewed in Brown & Aggleton, 2001; Davachi, 2006).

To extend findings regarding stress effects on hippocampal memory from rodents to humans, there is a need for human experiments that probe the effects of stress on memory processes that have been shown to depend on the hippocampus. This need may be partially addressed by assessing free recall. The involvement of the hippocampus in free recall has been demonstrated through studies of patients with selective hippocampal lesions (reviewed in Yonelinas et al., 2010) and fMRI studies (B. C. Dickerson et al., 2007; Staresina & Davachi, 2006; Strange, Otten, Josephs, Rugg, & Dolan, 2002). However, there are some concerns associated with using free recall to assess the influence of stress on hippocampal memory. First, although many memory retrieval tasks involve the PFC, free recall appears to particularly tax top-down attentional processes mediated by the PFC (discussed in Gagnon & Wagner, 2016). This creates a challenge for interpreting the mechanism underlying pre-retrieval stress effects, as acute stress may influence performance by impairing PFC function (Arnsten, 2009). This ambiguity in the target of stress effects is also apparent at a cognitive level, as free recall involves both a search process to generate the item as well as an assessment of the strength of that memory in order to decide that the item has been recalled. Either of these processes may be modulated by stress (discussed in McCullough & Yonelinas, 2013; Yonelinas, Parks, Koen, Jorgenson, & Mendoza, 2011). Second, there is no analog of a free recall task for nonhuman animals that would facilitate direct translation of acute stress findings (Yonelinas et al., 2010). Finally, free recall can be supported by both recollection and familiarity processes (Kragel & Polyn, 2016), which have been successfully isolated (and shown to differentially involve the hippocampus) in other tasks.

More recently, researchers have begun to use paradigms that separately assess recollection and familiarity, or associative and item memory, to investigate the influence of stress on these memory for these different types of information. Recollection refers to the retrieval of details and context of a particular encoding experience, whereas familiarity indicates the rapid sense that something was previously encountered, but without contextual details. The hippocampus has been shown to play a critical role in recollection and not familiarity (reviewed in Eichenbaum, Yonelinas, & Ranganath, 2007; Yonelinas et al., 2010; but see Merkow, Burke, & Kahana, 2015). These processes can be dissociated using item recognition tests in which participants are asked to indicate whether they “remember” (i.e., have recollective memory, or can reinstate specific details) or “know” (i.e., have a general sense of familiarity) that they have previously encountered the item. Using such subjective judgments presents challenges for assessing the influence of stress, as negative emotional arousal has been associated with participants reporting that they “remember” even when objective memory accuracy was impaired for contextual and associative details (Rimmele, Davachi, Petrov, Dougal, & Phelps, 2011). Another approach involves participants indicating if they “recollect” the item (sure the item was old and can remember details) or, if not, rate how confident they are that they recognize the item (1 = sure the item is new, 5 = sure the item is old). With these confidence ratings, receiver operating characteristics (ROC) curves are generated by plotting hits (items correctly identified as old) against misses (items incorrectly identified as new), with the intercept indicating recollection and the symmetry and curvature indicating familiarity (discussed further in Eichenbaum et al., 2007; Yonelinas et al., 2010). These assessments enable researchers to directly compare the influence of stress on these two memory processes (although with the subjectivity caveat noted above).

Measuring associative (in comparison to item-level) memory enables researchers to directly probe the influence of stress on a core hippocampal computation, namely the formation of associations between items or between items and contexts. Both the binding of information and context model (Diana, Yonelinas, & Ranganath, 2007) and the dual-process model (Davachi, 2006) posit that the hippocampus integrates item-level information (from perirhinal cortex) with context information (from parahippocampal cortex) in memory. Some theories (e.g., domain dichotomy) further stipulate that hippocampal processes are specifically involved in non-unitized representations and when associating items from different domains (A. Mayes, Montaldi, & Migo, 2007; Montaldi & Mayes, 2010). The critical role of the hippocampus in forming associations, even in the absence of conscious awareness (e.g., Chun & Phelps, 1999; Goldfarb, Chun, & Phelps, 2016; Hannula & Ranganath, 2009; Summerfield, Lepsien, Gitelman, Mesulam, & Nobre, 2006) forms a key component of processing-based models of multiple memory systems (Henke, 2010). The neuroanatomical distinction between memory for items and associations has been supported by studies of patients with amnesia (Giovanello, Verfaellie, & Keane, 2003) and selective hippocampal lesions (A. R. Mayes et al., 2004; Turriziani et al., 2004), who had intact item recognition but showed impaired associative memory, or showed a disproportionate impairment in associative relative to item memory (Hannula et al., 2015; but see Stark et al., 2002). The dissociation between hippocampal involvement in associative memory and perirhinal involvement in item memory has also been supported using fMRI (Davachi et al., 2003; Libby, Hannula, & Ranganath, 2014; Staresina & Davachi, 2008). Thus, measuring associative and item memory also enables the comparison of stress effects on hippocampal and non-hippocampal processes.

Recent experiments comparing the influence of acute stress on these processes have yielded an important insight: stress has distinct effects on these different types of memory. We used a within-subject design in which participants encoded pairs of negative words and neutral pictures. After a 24 hour delay, we assessed their item (word recognition) and associative (recognition of image studied with word) memory (Goldfarb et al., 2018). Each participant completed this task with no stress exposure, and was also exposed to acute stress at different memory phases (pre-encoding, post-encoding, and pre-retrieval), enabling us to control for baseline differences in memory performance. This design enabled us to test whether stressor timing (across memory phases), identified as a key modulator of stress effects in rodents (Table 2), would similarly modulate different types of declarative memory in humans. Within the same participants, we found that pre-encoding stress enhanced associative (but not item) memory, whereas post-encoding stress enhanced item (but not associative) memory for stimuli rated as highly arousing. Other researchers have examined stressor timing using tasks that separate familiarity and recollection. Similar to our finding of enhanced associative memory with pre-encoding stress, recollection (but not familiarity) for information encountered during a stressor was enhanced (Wiemers et al., 2013), although a recent study found that pre-encoding stress led to a negative correlation between cortisol and familiarity for arousing items (Wiemers, Hamacher-Dang, Yonelinas, & Wolf, 2018). In addition, consistent with our finding that post-encoding stress enhanced item memory, post-encoding stress enhanced familiarity (but not recollection) in males (McCullough & Yonelinas, 2013). These studies also revealed that the modulatory factor of stressor dosage had distinct effects on memory for different types of information. Although stressor dosage (measured as magnitude of endogenous cortisol response) modulated the effects of stress on both item/familiarity and associative/recollection memory, the shape of this association differed. Specifically, there was a linear relationship to item/familiarity and curvilinear relationship to associative/recollection memory (although the shape of this curvilinear relationship needs further investigation; Goldfarb et al., 2018; McCullough, Ritchey, Ranganath, & Yonelinas, 2015). Together, these studies have begun to reveal the scope of stress effects on declarative memory in humans and demonstrate the importance of studying the influence of stress on memory for different types of information.

3.1.1. How do assays of declarative memory influence the translation of positive stress effects?

Many experiments probing the effects of acute stress on human declarative memory measure memory for individual items, a type of memory that does not crucially depend on the hippocampus. Using tasks that query hippocampal-dependent memory in humans will be necessary to test whether the conditions and neural mechanisms that lead stress to enhance hippocampal-dependent memory in rodents (Table 2) generalize to humans.

Recent experiments have shown that the effects of stress on item memory differ from effects of stress on hippocampal-dependent processes, like recollection or associative memory. Thus, it cannot be assumed that all declarative memories will be enhanced under the same stress conditions that promote (frequently spatial) memory in rodents. This discrepancy creates an opportunity to ask how these conditions will modulate different types of declarative memory. For example, studies in rodents have shown that the emotional content of the memoranda modulates stress effects, with selectively enhanced memory for arousing information (Section 2.1). However, this modulatory factor may play distinct roles for stress effects on different types of human declarative memory. A large body of research has demonstrated that emotionality itself has distinct effects on memory for items and associations (Bisby & Burgess, 2013; Madan, Caplan, Lau, & Fujiwara, 2012; Madan, Fujiwara, Caplan, & Sommer, 2017; Mather, 2007). To date, whether the interactions between stress and emotionality vary between item and associative memory remains unclear. Supporting a similar role across memory tests, we found that enhancing effects of acute stress (pre- and post-encoding) on item and associative memory were limited to highly arousing stimuli (Goldfarb et al., 2018). In contrast, others have reported that stress (post-encoding) similarly influenced familiarity for negative and neutral stimuli, but did not significantly impact recollection for either type of stimuli (McCullough & Yonelinas, 2013). Thus, testing how the key factors described in Table 2 modulate stress effects across memory tests will be crucial to understand how stress facilitates human declarative memory.

Finally, although item recognition may not rely on the hippocampus, this form of memory is clearly susceptible to both enhancing (Hoscheidt et al., 2014; Payne et al., 2007) and impairing (Domes et al., 2004; Schwabe & Wolf, 2014) effects of acute stress. As studies in nonhuman animals have not directly examined the acute actions of stress hormones on the cortical medial temporal lobe regions that support item recognition, the neurobiological mechanism(s) underlying the influence of acute stress on this type of memory remain unclear. We cannot assume that these memory processes are modulated by the same mechanism that has been proposed to explain stress effects on hippocampal memory. As mentioned earlier (Section 2), there is growing evidence that acute stress can influence different types of memories through actions on diverse brain regions. Just as human research needs to assess hippocampal-dependent memory processes to generalize hippocampal-based cellular mechanisms, there is a need for rodent and in vitro studies to further characterize stress effects on the neural networks that are homologues of those that support human declarative memory.

3.2. Measurements of the stress response

Given the importance of the timing and dosage of the stress response in modulating stress effects on memory (Table 2), the assumptions involved in quantifying the stress response in humans require scrutiny. Human research is almost always limited to peripheral assays of cortisol and adrenergic responses in heart rate, saliva, blood, or urine. This presents less of a challenge for interpreting stress-induced adrenergic responses, as these also act peripherally (Roozendaal & McGaugh, 2011; although see Bosch, Veerman, de Geus, & Proctor, 2011 for limitations of these adrenergic assays). However, it presents a significant concern for understanding how cortisol influences cognition. Interpreting the functional role of peripheral cortisol changes is predicated on the assumption that this response accurately reflects changes in central (brain) cortisol, particularly in the brain region(s) supporting the cognitive task. This assumption has been tested in nonhuman animal studies, where levels of stress hormones can be directly assessed in neural tissue. One technique that has proven useful is in vivo microdialysis, in which probes are inserted into a target tissue and allow repeated sampling of extracellular glucocorticoid levels while the animal is conscious and freely moving (Linthorst, Flachskamm, Barden, Holsboer, & Reul, 2000). If blood is sampled at similar times and analyzed for glucocorticoids, this method enables direct comparison between peripheral and central stress-induced changes in glucocorticoid levels.

Before reviewing the results of these comparisons, it is worth briefly discussing what types of glucocorticoids are measured using these different assays. The total level of glucocorticoids in blood plasma is the sum of bound glucocorticoids, which are attached to binding proteins (including cortisol binding globulin, CBG), and free, or not bound, glucocorticoids. The extracellular glucocorticoids measured through microdialysis, as well as the glucocorticoids in saliva, are both free, although there is evidence that some salivary cortisol is bound (discussed in Levine, Zagoory-Sharon, Feldman, Lewis, & Weller, 2007). The functional roles of total, bound, and free glucocorticoids are not entirely clear. Although the “free hormone hypothesis” posits that only free cortisol is bioactive and available to move into cells, there is evidence that bound cortisol may also play this role (Levine et al., 2007).

As most human studies of stress and memory measure salivary cortisol, it is first necessary to consider the relationship between levels of cortisol in saliva and plasma before exploring the association between plasma and brain. Several studies have reported strong correlations between salivary and total plasma cortisol (Jung et al., 2014; Petrowski, Wintermann, Schaarschmidt, Bornstein, & Kirschbaum, 2013) as well as between salivary and (computed) free plasma cortisol (Hellhammer, Wust, & Kudielka, 2009; Levine et al., 2007). However, this does not imply that salivary cortisol can be categorically assumed to reflect levels in plasma. First, the strength of the saliva/plasma correlation can vary widely across individuals (Levine et al., 2007). Second, the relationship between salivary and plasma cortisol is no longer linear at very high levels. This is likely due to saturation of CBG; once CBG is saturated, any increases in cortisol beyond that saturation threshold (caused, for example, by acute stress exposure) cannot be bound by CBG, and thus will lead to inflated estimations of (free) cortisol increases in saliva (Hellhammer et al., 2009). Third, levels of cortisol in saliva are estimated to only be about 50–70% of cortisol levels in plasma (Levine et al., 2007). These observations emphasize the importance of accounting for baseline levels of cortisol in analyses of stress-induced cortisol effects. They also raise questions about the appropriateness of distinguishing stress “responders” from “non-responders” (a common practice in the human stress and memory literature) based on the magnitude of changes in salivary cortisol alone. For example, many studies employ the criteria of 1.5 nmol/l baseline-peak increase in salivary cortisol, a cutoff determined by analysis of a large cohort of humans exposed to the TSST (Miller, Plessow, Kirschbaum, & Stalder, 2013). However, it is not clear how this numerical cut-off for increases in salivary cortisol corresponds to changes in cortisol levels in plasma or, critically, the target neural tissue. It is possible that cutoffs based on salivary cortisol could be too lenient (i.e., if salivary cortisol increases were higher than detectable changes in the brain) or too strict (i.e., if increases in brain cortisol could influence activity even below “responder”-level changes in salivary cortisol).

Having discussed the relationship between saliva and plasma, we can now compare plasma and extracellular brain corticosterone. Both plasma and extracellular microdialysis assays (mostly in the hippocampus, but occasionally in PFC, amygdala, and caudate-putamen) reveal increases in corticosterone in response to stress exposure (Bouchez et al., 2012; Bray et al., 2016; Dominguez et al., 2014; Dorey, Pierard, Chauveau, David, & Beracochea, 2012; Droste et al., 2008; Garrido, de Blas, Del Arco, Segovia, & Mora, 2012). One key difference between central and peripheral assays concerns their ability to detect variability in the magnitude of the stress response. For example, rats exposed to 4 weeks of exercise had larger stress-induced corticosterone increases in plasma compared to sedentary rats (Droste, Chandramohan, Hill, Linthorst, & Reul, 2007), but there was no detectable difference in the hippocampus (Droste, Collins, Lightman, Linthorst, & Reul, 2009). Similarly, older rats had significantly higher stress-induced corticosterone increases than younger rats in (total) plasma, but the groups did not differ significantly in the hippocampus or PFC (Garrido et al., 2012). These discrepant findings led the authors to propose mechanisms by which corticosterone “access-to-brain” might be restrained (discussed further in Droste et al., 2009; Garrido et al., 2012). In the opposite direction, rats in withdrawal from amphetamine had significantly higher stress-induced corticosterone increases than controls in the ventral hippocampus, but no differences were observed in plasma (total, free, or bound corticosterone; Bray et al., 2016). As chronic use of addictive substances is associated with dysregulated HPA axis responses (discussed in Goldfarb & Sinha, 2018), this latter pattern may be specific to substance-using populations, but is important to consider for studies examining stress effects on cognition in human substance users. Together, these findings demonstrate variability in magnitude of central and peripheral glucocorticoid responses and underscore the need for caution when interpreting the functional role of peripheral glucocorticoid responses.

Comparing plasma and brain corticosterone also brings to light variability in the time course of the central and peripheral glucocorticoid response to stress. As discussed earlier (Section 2), the timing of stressor exposure relative to encoding plays a key role in modulating the effects of stress on memory. Thus, understanding when stressor-induced elevations in corticosterone are detectable in the brain, and whether this corresponds to peripheral measures, should facilitate the design of experiments that maximize the enhancing effects of stress. In one key experiment, Droste and colleagues concurrently sampled corticosterone in plasma and hippocampal dialysate before, during, and after exposure to a 15-minute forced swim stressor (Droste et al., 2008). Sampling with a high degree of temporal resolution (every 10 minutes pre- and post-stressor, and every 5 minutes during the stressor), they found that hippocampal corticosterone levels peaked around 20 minutes later than plasma corticosterone. Interestingly, salivary cortisol also appears to peak later than plasma cortisol in humans, although this pattern is highly variable and more research is needed to characterize these differences (e.g., Study 1 vs. 2 from Schlotz et al., 2008; see also Kudielka, Schommer, Hellhammer, & Kirschbaum, 2004; Petrowski et al., 2013). Regardless, assuming the temporal trajectories of peripheral and central glucocorticoids are comparable between rodents and humans, these findings suggest that studying the effects of peak brain glucocorticoids on cognition would require a further delay after peak peripheral glucocorticoids have been reached.

Despite the delay in timing of peak corticosterone between plasma and brain, it is worth noting that, across several experiments, above-baseline increases in brain corticosterone were detectable much earlier (Table 3). Based on the behavioral findings related to stressor timing discussed earlier (Section 2), waiting until peak stressor-induced increases in brain corticosterone are reached before starting encoding (typically ~60 minutes post-stressor onset) might actually lead to worse memory (for human examples, see Maheu, Collicutt, Kornik, Moszkowski, & Lupien, 2005; Zoladz et al., 2011; Zoladz et al., 2013). In addition, studies in humans using fMRI show that stressor-induced changes in brain function can occur far sooner than peak central or peripheral glucocorticoids would be detected (e.g., during a 6 minute stressor; Sinha, Lacadie, Constable, & Seo, 2016). Such early central changes may be due to the fast-acting adrenergic component of the response. In the context of memory, this suggests that enhancements in memory for information encoded very soon after stress might depend on the interaction between adrenergic responses during encoding and post-encoding glucocorticoid increases (similar to the pattern described in Okuda et al., 2004), although more research is needed to test this mechanism.

Table 3.

Stressor-induced increases in extracellular corticosterone by region and time

Stressor Stressor duration Delay: stressor onset to increase Delay: stressor onset to peak Region Reference
Restraint 20 10* 30* Hippocampus Garrido et al. (2012)
Restraint 20 10* 30* PFC Garrido et al. (2012)
Predator 30 15* 45* Hippocampus Linthorst et al. (2000)
Forced swim 15 15 50* Hippocampus Droste et al. (2008)
Forced swim 15 15 60* Caudate-putamen Droste et al. (2008)
Footshock 1 15* 60* mPFC Dominguez et al. (2014)
Footshock 1 15* 60* Dorsal hippocampus Dominguez et al. (2014)
Footshock 1 15* 60* Dorsal hippocampus Dorey et al. (2012)
Forced swim 15 20 60* BLA Bouchez et al. (2012)
Footshock 1 90* 105* Ventral hippocampus Dorey et al. (2012)
*:

showed statistically significant increases in corticosterone from baseline at the indicated time-point; if not marked, appeared elevated from visual inspection but significance was not reported.

†:

Based on Fig. 4. In Fig. 5, this increase appears evident at 5 min.

mPFC = medial prefrontal cortex, BLA = basolateral amygdala.

3.2.1. How do assays of human stress responses influence the translation of positive stress effects?

Measurements of the physiological stress response in humans are typically peripheral, relying on levels of cortisol on saliva, plasma, or urine. These may differ substantially in magnitude and timecourse from the levels of cortisol in target neural tissue, creating challenges for understanding the role of stressor dosage in modulating human memory. Although effects of acute stress on memory can vary in proportion to the magnitude of the peripheral cortisol response (e.g., Andreano & Cahill, 2006; Goldfarb et al., 2018; McCullough et al., 2015), the neural mechanism underlying these effects is unclear. We cannot assume that dose-dependent relationships between cognition and peripheral glucocorticoids are mirrored by relationships between cognition and glucocorticoids in target tissue. Further research in rodent models is needed to compare post-stressor glucocorticoid elevations in the periphery (ideally using assays similar to those employed in humans) and the brain.

The timecourse of post-stressor elevations in central corticosterone also presents challenges for understanding the mechanisms by which stress enhances memory. The delay from stressor to encoding that leads to enhanced memory is far shorter than the delay from stressor to peak detectable elevations in central corticosterone. Thus, stress may enhance memory before peak corticosterone elevations are measured in the hippocampus. Can these relatively immediate memory enhancements still be driven by glucocorticoid-induced changes in hippocampal LTP? As discussed earlier (Section 2), corticosterone can enhance hippocampal LTP if stimulation is concurrent with corticosterone administration. Relating this to stressor-induced memory benefits is tricky. If corticosterone needs to converge with stimulation to enhance LTP, we might assume that peak corticosterone should converge with encoding in order to enhance memory. Yet hippocampal corticosterone peaks at least 30 minutes after stressor onset—around the same time that stressor-induced impairments in encoding are observed. To understand the role of hippocampal LTP in stressor-induced memory enhancements, we need to know when changes in LTP occur relative to stressor onset, not only relative to corticosterone administration. Studies examining the influence of stressors on LTP typically allow the animals to rest for at least 30 minutes prior to the start of recording (e.g., Yarom, Maroun, & Richter-Levin, 2008) or, if the animal is immediately sacrificed post-stressor, there are around 20 minutes of baseline in vitro recordings prior to stimulation (e.g., Sarabdjitsingh, Kofink, Karst, de Kloet, & Joels, 2012). There is a need for experiments that measure changes in stimulation-evoked LTP closer to stressor onset, when memory has been shown to be enhanced. In one such study, Shors and colleagues measured EPSPs in CA1 during and after restraint/tailshock stressors, finding a transient decrease in CA1 EPSPs (a change that may have been related to motion) but a transient increase in hippocampal theta shortly after the stressor (Shors, Gallegos, & Breindl, 1997). To map stressor-induced changes in memory to this potential biological mechanism, further experiments are needed to address the question of how soon after acute stress there are observable enhancements (and impairments) in synaptic plasticity. For example, would changes in LTP be noticeable only at peak corticosterone, when any extracellular increases in corticosteroids are detected, or even sooner?

Given the rapid behavioral effects of stressors on memory, and the discrepancies between central and peripheral glucocorticoid responses, experiments on stress and memory in humans would benefit from considering wider temporal windows than those indicated by peripheral cortisol elevations. To date, over 70% of studies examining effects of pre-encoding stress on long-term declarative memory wait between 15 and 30 minutes from stressor onset —when significant elevations in salivary cortisol would be expected—before starting encoding (Figure 1). Broadening this window creates opportunities to test whether early elevations in adrenaline/noradrenaline, slightly later initial elevations in brain glucocorticoids, or peak elevations in brain glucocorticoids, best predict that stress will enhance memory formation.

Fig. 1.

Fig. 1.

Time between the onset of acute stressors and the onset of encoding in human experiments. Experiments were included that measured memory at least 24 hours after encoding (so that cortisol levels were only elevated during encoding). Publications including multiple experiments are counted once per experiment. When not specified, saliva sampling and subjective ratings of stress were each assumed to take 1 minute.

Note: Study-average effect sizes of stress effects on memory from many of these references are shown in Figures 4 and 5 of Shields et al. (2017).

References: Cornelisse, Joels, & Smeets, 2011; Cornelisse, van Stegeren, & Joels, 2011; Goldfarb et al., 2018; Henckens et al., 2009; Hoscheidt et al., 2014; Luo et al., 2018; Maheu, Collicutt, et al., 2005; Merz, 2017; Payne et al., 2007; Qin, Hermans, van Marle, & Fernandez, 2012; Quaedflieg et al., 2013; Schwabe, Bohringer, et al., 2008; Schwabe, Bohringer, & Wolf, 2009; Schwabe & Wolf, 2010; Smeets, Giesbrecht, Jelicic, & Merckelbach, 2007; Smeets et al., 2008; van Ast, Cornelisse, Meeter, & Kindt, 2014; Vogel, Kluen, Fernandez, & Schwabe, 2018; Weymar, Schwabe, Low, & Hamm, 2012; Wiemers et al., 2018; Wiemers et al., 2013; Wolf, 2012; Zoladz et al., 2011; Zoladz et al., 2013)

4. Conclusions

Stress can powerfully enhance memory, creating the exciting possibility of using acute stress as an intervention to improve encoding and consolidation. This review has synthesized research on the enhancing effects of stress on memory across species and highlighted key modulatory factors that promote stress-induced memory enhancements. Through examining how declarative memory and stress responses are assessed in human research, this review reveals challenges for generalizing these modulatory factors and mechanisms to understand when stress will facilitate declarative memory.

First, the tasks that are often used to assess stress effects on declarative memory in humans may not critically involve the hippocampus. As many studies in rodents use hippocampal-dependent tasks and posit hippocampal-based neurobiological mechanisms of stress effects, these human memory assays present important challenges for generalizing from rodents to humans. For human researchers, there is a need to employ memory tasks that crucially involve hippocampal processes. For rodent researchers, there is a need to characterize stress effects on the function of neural networks that are homologues of those that support different types of human declarative memory. This will enable us to understand how stress influences processes like declarative memory for individual items.

Second, the (necessarily) peripheral assays of glucocorticoids employed in human studies may yield different results, in both dosage and timecourse, from the central changes in glucocorticoids that are thought to mediate the effects of stress on memory. For human researchers, these findings underscore a need for caution when interpreting the functional roles of peripheral changes in glucocorticoids. There is also a need for human researchers to explore the effects of stressors on encoding at broader timescales, moving beyond the constraints of when significant elevations in salivary cortisol are detectable. For rodent researchers, there is a need to assess how changes in cellular processes unfold relative to the onset of a stressor in order to understand rapid facilitating effects of stressors on memory. There is also a need to further characterize and compare the dosage and timecourse of peripheral and central glucocorticoid responses to stressors.

Addressing these gaps will create novel opportunities to bridge findings from rodent and human research examining the positive effects of stress on memory. Ultimately, this work will enable the prediction of circumstances that enable stress to optimally facilitate declarative memory.

Acknowledgments

David Clewett and Alexa Tompary are gratefully acknowledged for feedback on the manuscript. EVG is supported by the Yale Neuroimaging Sciences Training Program (T32 DA022975).

Footnotes

Competing Interests

The author has no competing interests to declare.

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