Neurobiology of Learning and Memory 173 (2020) 107254

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Neurobiology of Learning and Memory

journal homepage: www.elsevier.com/locate/ynlme

Stress & executive functioning: A review considering moderating factors T

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Thomas Plieger , Martin Reuter
Department of Psychology, Laboratory of Neurogenetics University of Bonn, Kaiser-Karl-Ring 9, D-53111 Bonn, Germany

A R T I C LE I N FO A B S T R A C T

Keywords: A multitude of studies investigating the effects of stress on cognition has produced an inconsistent picture on
Stress whether - and under which conditions - stress has advantageous or disadvantageous effects on executive func-
Cortisol tions (EF).
HPA axis This review provides a short introduction to the concept of stress and its neurobiology, before discussing the
Executive control
need to consider moderating factors in the association between stress and EF. Three core domains are described
Cognitive functioning
Stress reactivity
and discussed in relation to the interplay between stress and cognition: the influence of different paradigms on
physiological stress reactivity, individual differences in demographic and biological factors, and task-related
features of cognitive tasks. Although some moderating variables such as the endocrine stress response have
frequently been considered in single studies, no attempt of a holistic overview has been made so far. Therefore,
we propose a more nuanced and systematic framework to study the effects of stress on executive functioning,
comprising a holistic overview from the induction of stress, via biological mechanisms and interactions with
individual differences, to the influence of stress on cognitive performance.

1. Introduction think of someone who hates doing things at the last minute or who
“chokes” under pressure. Thus, clear individual differences exist in the
Stress is a common experience, which affects almost all aspects of relationship between stress and cognitive performance.
life. References to stress are frequent in everyday conversation and in By definition, stress is a highly subjective experience. For example,
the press, and a plethora of scientific studies have attempted to define it is not the actual workload that induces stress, but the subjective ex-
stress, and to specify its underlying mechanisms and consequences. perience of the lack of control or necessary resources, time pressure, the
While prolonged or chronic stress can cause serious illness when ac- feeling of being evaluated, helplessness, etc. (e.g. Dickerson & Kemeny,
companied by unsuccessful coping, the acute stress reaction is evolu- 2004; Henry, 1992; Mason, 1968; Zhu, Shi, Wang, Wang, & Li, 2014).
tionarily adaptive, providing energy and helping the organism to deal Peters, McEwen, and Friston (2017) argue that it is mainly uncertainty,
with stressors in challenging situations (Dhabhar, 2018). Despite fre- which causes stress in terms of reallocating energy resources in order to
quent negative connotations, there is an implicit acceptance among lay resolve the uncertainty. There may also be developmental aspects such
people of this adaptive stress function, e.g. people who perform their as early life adversity that influence the sensitivity to stress (see Levine,
best when under pressure or working to a deadline. While many studies 2005). Despite its clear importance, this subjective aspect is neglected
have sought to establish the effects of stress on individuals’ perfor- in many studies investigating the effect of stress on both cognitive
mance in different areas, the present review will focus on the concept of functions and other behavioral phenotypes. To address this oversight
stress and its influence on prefrontal cognitive functions (for the effects this review opens with a short section introducing the construct of stress
of stress on long-term memory, see e.g. Schwabe, Wolf et al., 2010; and highlighting its subjectivity. In addition to individual differences,
2012; Schwabe & Wolf, 2013; Wolf, 2009; Wolf, Atsak, De Quervain, other contextual factors, e.g. the experimental design or the partici-
Roozendaal, & Wingenfeld, 2016; Zoladz, Park, & Diamond, 2011). The pant’s emotional state, influence the stress reaction and its con-
extant literature investigating the effects of stress on cognition is both sequences; factors highlighted by the prominent stress model of Lazarus
inconsistent and inconclusive. These inconsistencies point to moder- and Folkman (1984, see chapter 2). Surprisingly, such contextual fac-
ating factors that should be considered when investigating the re- tors are also overlooked by much of the existing literature. To address
lationship between stress and executive functioning (EF). For every these gaps in the literature, the present review aims to shed light on
example of the earlier individual who thrives on a deadline, we can potential moderating variables that may affect the association between

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Corresponding author.
E-mail address: Thomas.plieger@uni-bonn-diff.de (T. Plieger).

https://doi.org/10.1016/j.nlm.2020.107254
Received 17 January 2020; Received in revised form 13 May 2020; Accepted 25 May 2020
Available online 30 May 2020
1074-7427/ © 2020 Elsevier Inc. All rights reserved.
T. Plieger and M. Reuter Neurobiology of Learning and Memory 173 (2020) 107254

Fig. 1. Initial starting point. The aim of the present review is to identify potentially moderating factors in the association between stress and executive functioning
which can explain the diverse and inconclusive results in the field.

stress and executive control. Fig. 1 depicts the starting point for the Goldstein, 1957).
conceptualization of a systematic and differentiated framework. The HPA axis consists of a signal cascade that starts – not surpris-
ingly – in the hypothalamus - or more precisely, the paraventricular
2. What is stress? hypothalamic region - where the corticotropin-releasing hormone
(CRH) is secreted. The increasing levels of CRH prompt the secretion of
Much of our basic understanding of stress originates from research the adrenocortocotropic hormone (ACTH) in the pituitary. When higher
by Hans Selye (Selye & Collip, 1936), whose ideas and empirical find- blood concentrations of ACTH reach the adrenal gland – or more pre-
ings remain influential today. Selye defined stress as the non-specific cisely, the zona fasciculata of the adrenal gland – cortisol is secreted
response of the body to any disturbance of the homeostatic balance (e. (e.g. Tsigos & Crousos 2002). Cortisol is a glucocorticoid and is the most
g. Selye & Fortier, 1950). Therefore, stress applies to every situation important human stress hormone, belonging to the class of steroid
that forces the individual into any kind of adaptive process. Frequently, hormones. It plays various roles in mobilizing the individual to respond
the term “stress” is used to refer to the actual stress reaction. However, to a stressor, of which the modulation of gluconeogenesis is one of the
stress is defined by three consecutive processes (see Lazarus, 1993): most prominent ones. This results in an increase in blood glucose level,
Firstly, the organism is in a steady interaction with its environment, which increases the physical capacity of the individual and fulfills
which is often challenging. This challenging interaction, therefore, several other functions, such as the inhibition of protein synthesis.
qualifies as a potential stressor. Of note, this stressor need not actually Being a steroid hormone, cortisol is also able to cross the blood–brain-
exist, but can also be imaginary (Schneiderman et al., 2004). Secondly, barrier and to modulate processes at the level of the central nervous
the individual actively and passively interprets their interaction with system (Lupien, Maheu, Tu, Fiocco, & Schramek, 2007). In the brain,
the environment. Thus, a stimulus qualifies as a stressor if it is inter- cortisol increases several sensory processes, such as the gustatory,
preted as a stressor by the individual (Lazarus, 1993). This means that tactile, acoustic, and olfactory senses (Klinke et al., 2009). The pro-
the same situation can be perceived as stressful by one person, or po- motion of these processes can be useful in resolving dangerous or
sitively challenging by another. The experience of stress then throws stressful situations, particularly when an organism is faced with an
the individual out of their physical and psychic homeostatic balance in acute stressor. However, one major issue is that the signal cascade of
the third step, which is called the stress reaction. In order to understand the HPA axis is relatively slow because it relies on hormones being
the effects of stress on human behavior, it is important to keep this transported through blood circulation. Furthermore, cortisol does not
subjectivity in mind when conducting stress research. directly affect functions like gluconeogenesis, rather it binds to the
This subjectivity aspect is part of one of the most prominent stress glucocorticoid (GR) and mineralocorticoid (MR) receptors, which in
models: the transactional theory by Richard Lazarus (1966). According turn trigger the expression of many genes related to metabolism, im-
to Lazarus, stress is neither inherent to the person nor to an aspect of mune function and stress reactivity (Joels & de Kloet, 1994). The effects
environment, rather it is always a result of the interaction between the of cortisol can only be detected with a temporal delay, which is why the
individual and the environment (Lazarus & Folkman, 1987; Lazarus, effects of the HPA axis are not apparent until 10 to 15 min after the
1990). Thus, stimuli or potential stressors can become actual stressors onset of the stressor. In addition to cortisol, both CRH and ACTH have
depending on the situational context, the individual’s characteristics some intrinsic modulating functions on the stress reaction beyond
and state, the features of the stimulus itself, and global environmental merely initiating HPA axis reactivity.
factors. CRH secretion begins immediately after the exposure to a stressor,
and plays an important role both in the initiation of HPA axis activity,
as well as in triggering the sympathetic stress reaction (Chrousos,
2.1. The stress reaction
2009). Although Selye mainly focused on the HPA axis in his research,
the sympathetic nervous system (SNS) also plays a crucial role in the
As noted above, Selye and Fortier (1950) describe the stress reaction
biological stress reaction, because its interplay with the para-
as a generalized adaptive process that is non-specific and nearly iden-
sympathetic nervous system is an important prerequisite for the
tical in response to any given stressor. The ultimate aim of the stress
homeostasis of an organism (Jänig, 2008). Moreover, the SNS is re-
reaction is to maximize the chance of survival in a dangerous or chal-
sponsible for the immediate stress response, e.g. it helps us in situations
lenging situation by providing energy and mobilizing or arousing the
where we have to face the threat. Arousal of the sympathetic nervous
individual. This is supported by several processes at the neuronal, im-
system leads to an increase in blood pressure, cardiovascular activity,
munological and endocrine levels (Purves et al., 2008). The most im-
and heart rate. Furthermore, adrenaline and noradrenaline are released
portant of which are the neuroendocrine hypothalamic–pituitarya-
which supports the provision of energy to the organism. This happens
drenal axis (HPA axis) and the sympathetic nervous system (Ramey &

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by dampening functions that are superfluous to the acute stress re- terminal, exhaustion stage, may be characterized by hypocortisolism, a
sponse, such as digestive functions or protein synthesis, so that the proposition supported by Guilliams and Edwards (2010), who suggest
organism can concentrate all its capacities on those functions that are an increasing shift from hypercortisolism (e.g. due to a malfunctioning
necessary for survival or – less dramatically – coping successfully with negative feedback loop) to hypocortisolism in the terminal stage. Given
the stressor. Additionally, the blood vessels of the skeletal muscles the inconclusive evidence and associated uncertainty about the endo-
widen to facilitate transportation of oxygen and sugar, enabling phy- crine processes in chronic stress, we do not want to focus on the effects
sical effort. Furthermore, adrenaline is known to have a lipolytic effect of chronic stress in the present review. Furthermore, the majority of
which facilitates a fast mobilization of stored energy (Konturek, studies investigating the association between stress and cognitive
Konturek, Pawlik, & Brzozowski, 2004; Matthews, Pescola, & Campell, functioning operationalizes stress in acute laboratory designs. Although
1990; Tank & Wong, 2015). In contrast to the function of the HPA axis, chronic stress has been associated with a host of psychopathologies,
activation of the SNS does not depend on endocrine mechanisms (i.e. such as depression and burnout, which may also be accompanied by
hormone transmission via the blood circuitry), but occurs via synaptic cognitive impairments (e.g. Steffens et al., 2006), discussion of the
transmission. Therefore, the sympathetic stress reaction is very fast, mechanisms and effects of chronic stress are beyond the scope of the
enabling it to support the fight-flight reaction in an acute stressful or present review.
dangerous situation (Jansen, Van Nguyen, Karpitskiy, Mettenleiter, &
Loewy, 1995). Besides the fighting and fleeing behavior proposed by 2.3. Indicators of stress reactivity
Cannon (1915), Gray and McNaughton (2000) argue that an additional,
freezing behavior is a potential behavioral outcome of the stress reac- The stress reaction is characterized by several markers, which we
tion. Of course, these very raw and evolutionarily old behaviors are will briefly outline (for a more in-depth review of stress markers, see
expressed in a more controlled or at least less physical way in humans; e.g. Allen, Kennedy, Cryan, Dinan, & Clarke, 2014). The most common
that is anxiety, fear, or aggression, which often accompany a stress stress marker for HPA axis reactivity is the measurement of salivary
reaction (McNaughton & Corr, 2004). Once the stress reaction has been cortisol levels. Salivary cortisol has proven a reliable measure of HPA
resolved, homeostasis is built up again by parasympathetic processes, axis activity, although cortisol sampling must be handled with care, as
which aim to restore resources consumed during the stress response it may be influenced by a range of factors. That is, cortisol levels are
(Ulrich-Lai & Herman, 2009). highly dependent on time of day, food intake, smoking, physical strain
Because of these temporal differences between the sympathetic and and other variables, which must be controlled, before cortisol can be
the neuroendocrine stress reaction, it is important to consider onset considered an adequate measure of biological stress reactivity. Overall,
timing when assessing the behavioral outcome of a stressor. Thus, exact correlations between measures of plasma free-cortisol and salivary
timing is a crucial aspect of the experimental procedure, to enable the cortisol are usually very high, suggesting that cortisol values obtained
comparison of results regarding the effects of a stressor. Fortunately, from saliva are representative of the bioavailability of cortisol
this is the case in most of the studies reported in the field of stress (Hellhammer, Wüst, & Kudielka, 2009) and can, therefore, be con-
research. In contrast, the subjectivity of stress, as stated in Lazarus’ sidered a reliable index of the investigation of psychobiological stress
model, is often neglected in research although it is crucial in evaluating responsivity. Nonetheless, Hellhammer et al. (2009) point out that
the effects of a (potential) stressor on behavioral outcomes such as there are variables that might lead to dissociations between cortisol
cognitive functioning. Consequently, the separation of responders and measurements obtained from saliva compared to blood plasma or urine.
non-responders to a stressor is highly recommended in the analysis of An alternative index of HPA axis activity can be obtained via ACTH
stress effects by subjective ratings and biological markers (Miller, levels, although this method is less commonly employed than the use of
Plessow et al., 2013; see also Section 2.3). In this regard, it is surprising cortisol levels.
that some studies investigating the relationship between stress and There are several common markers that assess the sympathetic
cognition only measure cortisol as manipulation check for successful stress reaction. Cardiovascular markers (i.e. heart rate and heart rate
stress induction rather than predicting executive control performance variability) are widely used proxies for sympathetic activity. The
under stress by cortisol reactivity (e.g. by separating responders and second commonly used, non-invasive measure is electrodermal activity
non-responders or by relating the individual cortisol increase to cog- (or galvanic skin response, GSR) which is also heightened during
nitive performance). Although some studies use this separation by stress sympathetic arousal. Although they are prone to interferences such as
reactivity, there are still many studies which refrain from doing so. movement artefacts or room temperature and humidity, heart rate
(variability) and GSR are advantageous relative to other measures, as
2.2. Acute vs. Chronic stress they can be continuously measured throughout an experimental session
and, therefore, can be related to specific stimuli in a more fine-grained
A further criterion in the analysis of stress reactivity is whether the manner. A third common measure is salivary α-amylase (sAA). A-
focus of interest is on the effects of acute stress in defined temporary amylase is an enzyme released by the parotid gland during sympathetic
situations or the effects of a longer lasting stressful period. The acute activity which is responsible for the catabolism of carbohydrates, and
stress reaction is a highly adaptive process that aims to maximize the has been shown to be significantly increased during stressful conditions
chance of survival or at least increase the chance of a positive situa- (for an in-depth review, see Nater & Rohleder, 2009). However, one
tional outcome. According to Peters et al. (2017), this goes along with considerable issue is that correlations between α-amylase and other
resolving the uncertainty that is caused by the stressor. In contrast, peripheral markers are not high enough (r = 0.0 - 0.54) to justify an
longer lasting stressors - or consistently poor coping in the face of a accurate inference from sAA levels on sympathetic activity. Many stu-
stressor - leads to vastly different effects because the stress that causes dies find robust, but rather moderate associations with adrenaline and
uncertainty remains unresolved (McEwen & Seeman, 1999; Peters et al., noradrenaline levels, whereas others find no significant correlations at
2017). Whereas acute stress mobilizes the organism, chronic stress re- all (Mandel, Des Gachons, Plank, Alarcon, & Breslin, 2010; Nater &
sults in exhaustion, particularly in the absence of opportunities to re- Rohleder, 2009; Thoma, Kirschbaum, Wolf, & Rohleder, 2012). Simi-
store energy (Dallman & Bhatnagar, 2010). This distinction is reflected larly, associations with GSR and cardiac measures are rather small
in Selye (1946) model of the General Adaption Syndrome. Though, the (Bosch, Veerman, de Geus, & Proctor, 2011). Furthermore, Bosch et al.
direction of these differences (i.e. hypo- vs. hyperactivity of the HPA (2011) note that there are several confounding variables that are dif-
axis under chronic stress) remains a topic of debate (Aguilera, 2011; ficult to control and, consequently, seldom considered. It should also be
McEwen, 2004; Epel, 2009; Fries, Hesse, Hellhammer, & Hellhammer, noted that peripheral markers of sympathetic arousal, in general, do not
2005; Silverman & Sternberg, 2012). Selye (1946) proposed that the differentiate between positive and negative arousal; thus these indices

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alone cannot indicate whether the participant is actually stressed, only premise of physiological strain; participants are asked to immerse their
that they are experiencing some form of physiological arousal. There- hand into ice water for several minutes. A major drawback of this test is
fore, experimenters need to ensure (e.g. via subjective stress reports) that it usually produces a stable effect on sympathetic stress parameters
that stress is actually induced by a stimulus before conclusions about as skin conductance, blood pressure, or heart rate variability, but does
negative or stressful sympathetic arousal can be inferred. Consequently, not stimulate the HPA axis reliably (e.g. Duncko et al., 2007, 2009;
the final important stress parameter is the participants’ subjective McRae et al., 2006). Schwabe and colleagues extended the CPT by in-
rating, which can be assessed using standardized questionnaires such as corporating a social evaluative component: first, participants are vi-
the Positive and Negative Affect Scale (PANAS; Watson, Clark, & deotaped during the cold water immersion and have to look into the
Tellegen, 1988) or the Profile of Mood States (POMS; McNair, 1971) to camera during the hand immersion. Second, the (opposite sex) ex-
name but two. Another possibility is to use a visual analogue scale (e.g. perimenter stares at the participant and pretends to document their
Sugaya et al., 2012; Von Dawans, Fischbacher, Kirschbaum, Fehr, & nonverbal behavior, while avoiding any social or socially supportive
Heinrichs, 2012). State anxiety is also occasionally used to assess the conversation or behavior during the whole stress induction. Third, the
subjective effects of a stress induction (e.g. Rimmele et al., 2009). participant is not told that the hand immersion period will last 3 min
(maximum), rather they are told to keep his or her hand in the ice water
3. Induction of stress for as long as possible. If the participant removes their hand before the
3 min are up, they are asked to continue looking into the camera and
Stress can be induced via several experimental procedures. the experimenter continues staring at the participant. By adding these
However, two paradigms in particular seem to be the most reliable in components, Schwabe et al. (2008) were able to show a substantial
eliciting a substantial endocrine stress reaction. In the following sec- increase in HPA axis function following the stressor. Over the last
tion, we will focus on these two procedures, but some alternatives will decade, the SECPT has demonstrated consistent endocrine stress re-
be briefly outlined. sponses and has been used in a vast number of studies. Although cor-
tisol responder rates in the SECPT are a little lower than those obtained
3.1. TSST in the TSST, it has become an accepted alternative to the TSST, due to
the comparably lower demands for resources. In contrast to the TSST,
The Trierer Social Stress Test (TSST; Kirschbaum, Wüst, & the SECPT requires only one room and one experimenter and the stress
Hellhammer, 1992, 1993) was introduced by Kirschbaum and collea- induction lasts a fraction of the time (5 min, compared to 20 min for the
gues, who acknowledged that previous stress studies had produced very TSST). On the downside, the SECPT usually produces lower rates of
inconsistent findings. During the TSST, participants are told that they treatment responders (about 50%) than the TSST (about 75%).
will need to prepare and deliver a five-minute talk in application for a
job, to a panel of three interviewers. Participants are told that their 3.3. Other stress procedures
performance will be video-recorded for use in a later analysis of non-
verbal behavior. They are given 10 min alone in a separate room to Another standardized stress test is the Mannheim Multicomponent
prepare their speech, after which they are taken back to the first room Stress Test (MMST; Kolotylova et al., 2010), which uses a combination of
to deliver their speech. If a participant’s speech lasts less than five cognitive, emotional, motivational, and physical (noise) stressors. The
minutes, they are asked to continue talking until the time ends. Fol- MMST has not received much attention to date, thus, an evidence-based
lowing the speech, participants are given a second, unexpected task, in evaluation of this procedure is not possible. However, the initial evi-
which they are asked to sequentially subtract 13 from 1022 as fast as dence suggests that the MMST is strong enough to trigger sympathetic
possible. Whenever the participant makes a mistake, they are prompted stress markers such as skin conductance level and heart rate variability,
to start anew by one of the committee members (for a detailed de- while the evaluation of its effects on the HPA axis seems premature
scription see Birkett, 2011 or Kirschbaum, Pirke, & Hellhammer, 1993). (Kolotylova et al., 2010; Krause-Utz et al., 2016; Reinhardt et al., 2012,
The TSST has proven to evoke stress responses – including cortisol level 2013; Starcke, Wiesen, Trotzke, & Brand, 2016).
increases - very consistently (Kudielka, Hellhammer, & Kirschbaum, Smeets et al. (2012) developed the Maastricht Acute Stress Test
2007). Key to this evocation of stress, are the task elements of social (MAST) which is a combination of the TSST and the CPT procedure.
evaluation and lack of control of the situation (Gruenewald, Kemeny, Their aim was to provide a stress paradigm that was more cost-effec-
Aziz, & Fahey, 2004). However, the TSST procedure requires con- tive, but equally reliable as the TSST, to improve on the relatively
siderable resources; at least two rooms and three to four experimenters smaller cortisol effects elicited by the SECPT. In the MAST, the parti-
are needed. To address this issue, virtual reality versions of the TSST cipant is required to immerse his/her hand into ice water 5 times for a
have been tested in several more recent studies, and seem to success- random duration between 60 and 90 s. Between the hand immersion
fully evoke endocrine stress reactions (Helminen, Morton, Wang, & trials, participants are confronted with an arithmetic task similar to that
Felver, 2019). The recently developed TSST-VR (Zimmer, Buttlar, of the TSST. Initial evidence supports the efficacy of the MAST; in fact,
Halbeisen, Walther, & Domes, 2019) is modelled on the original pro- Smeets et al. (2012) show greater neuroendocrine stress effects fol-
cedure, but requires only one room and one experimenter. Using the lowing the MAST as compared to the SECPT.
TSST-VR, Zimmer et al. (2019) produced results for HPA axis reactivity Several other stress paradigms have also been introduced, however,
and sAA, which are comparable to those of the original TSST. However, their ability to elicit a response from the HPA axis is questionable. In
the TSST-VR did not produce comparable effects on sympathetic stress these studies, stress was induced by asking participants to perform some
indices, heart rate and skin conductance level. More studies using the cognitive tasks (e.g. an estimation task, a number series task, or an
TSST-VR are necessary to further validate this paradigm. Nonetheless, analogies task) under time pressure. After completing the task, parti-
the TSST-VR may become an interesting and – except for the relatively cipants’ self-reported stress was increased (relative to baseline), how-
high acquisition cost for the VR equipment - more economic option for ever, no biological indices of the stress response are reported in any of
the induction of stress in the future. these studies (Chajut & Algom, 2003; Friedland & Keinan, 1991;
Keinan, Friedland, Kahneman, & Roth, 1999; Steinhauser, Maier, &
3.2. SECPT Hübner, 2007; see Staal, 2004 for an overview). Hence, it may be
concluded that cognitive tasks alone are not capable of evoking a
The Socially Evaluated Cold Pressor Test (SECPT) was introduced by substantial biological stress reaction, despite having an impact on
Schwabe, Haddad, and Schächinger (2008) and is an adaption of the perceived stress. Therefore, it must again be emphasized that experi-
Cold Pressor Test (CPT; Hines & Brown, 1936). The CPT is built on the mental timing is crucial in this context. As endocrine stress effects peak

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T. Plieger and M. Reuter Neurobiology of Learning and Memory 173 (2020) 107254

about 20 to 25 min after stressor-onset and sympathetic and subjective Beyond the relatively sluggish effects of cortisol, experimental
self-reported stress effects show their highest effects in the immediate timing is also crucial to the study of more rapid-onset stress reactions,
aftermath of the stressor, it is important to carefully plan which stress e.g. perceived stress or sympathetic stress markers. Thus, the time at
effects an experimenter is interested in (see also Section 3.6). which cognitive functions are tested will differ, depending on whether
Additional stress paradigms exist, typically designed for specific test one is interested in the effects of the sympathetic or endocrine stress
environments (e.g. Montreal Imaging Stress Task for fMRI experiments) response. For sympathetic reactions, tasks should follow immediately
(for an overview, see Bali & Singh Jaggi, 2015). after the stressor, whereas for the endocrine response, tasks are best
Rather than relying on artificial laboratory paradigms, some work placed 10–20 min after stressor onset. In contrast to these staggered
has sought to harness natural stressors and measure the potential stress experimental designs, some studies administer both the cognitive task
reaction. These stressors can be chronic or acute. Participants under- and the stress induction simultaneously, to assess in-the-moment cog-
going military training (e.g. Friedland, Keinan, & Tytiun, 1999; Taylor nitive effects of the sympathetic stress system (e.g. Marko & Riecansky,
et al., 2014a, 2014b, 2015) and women with a recent experience of 2018). Of note, in that case it has to be considered that comparability
sexual assault (Quidé et al., 2018) constitute two examples of these with other studies using cortisol as the main stress marker for stress
naturalistic designs. Other studies use student samples and ask about reaction is no longer given.
recent life stress (e.g. Shields et al., 2017; Shields, Ramey, Slavich, & Joels et al. (2011) also highlight the importance of experimental
Yonelinas, 2019) or obtain data during the exam period in order to timing, due to the interplay of several transmitter systems involved in
measure stress effects (e.g. Kofman, Meiran, Greenberg, Balas, & Cohen, the stress reaction. For example, the secretion of noradrenaline after a
2006; Vedhara, Hyde, Gilchrist, Tytherleigh, & Plummer, 2000). Of stressor is faster than that of cortisol, leading to a brief overlap of in-
note, whereas subjective stress is consistently higher during an exam creased concentrations of these two stress parameters (see also
period, evidence on sympathetic markers such as heart rate variability Hermans et al., 2014). Hence, different experimental procedures with
(Kofman et al., 2006) and diurnal HPA axis activity (Vedhara et al., different temporal spacing between cognitive tasks and stressor onset
2000) is less conclusive and is often unrelated to the extent of perceived may impede the comparability of different studies. Thus, it would be
stress, impeding comparability with studies which investigate the ef- prudent to consider these timing issues when attempting to compare
fects of acute stress. individual studies.
Taken together, this section shows that there are several methods to Finally, the moderating influence of experimental timing on the
induce stress or the biological mechanisms thereof and that these dif- effects of stress and EF may, in turn, be influenced by the type of task:
ferent paradigms can cause stress reactions at different levels. Hence, Olver, Pinney, Maruff, and Norman (2015) had participants perform
the paradigm chosen may be a factor in influencing the effects of stress different prefrontally mediated cognitive tasks before, immediately
and the stress reaction on other phenotypes. Therefore, it is important after, and 60 min after undergoing the TSST. Participants obtained the
to be aware of which processes (e.g. sympathetic or endocrine) are worst results on an attentional task and on a spatial working memory
affected or triggered by a certain stressor. That is, a sympathetic stress task, taken immediately after the stressor. While participants’ perfor-
reaction could have differential effects on executive control compared mance on the working memory task had fully recovered 60 min after
to an endocrine stress reaction. The specific processes triggered also the stressor, no corresponding improvement was observed for their
have important implications for the experimental timing of the cogni- attentional performance. Although these results should be interpreted
tive or experimental tasks of interest. with caution given the relatively small sample size, they suggest that
task related features may play a moderating role in the association
3.4. Experimental timing between stress and executive functioning. In the following section, we
will, therefore, provide a short overview of different EF and discuss a
A crucial aspect related to both the induction of stress and the stress putative moderating role for task related features on stress effects.
parameters being assessed, is the timing of the experiment. In many
studies, the cognitive tasks take place approx. 20–25 min after the onset 4. Executive functions
of the stressor, i.e. around the expected cortisol peak. Some evidence
supports this timing, suggesting that the most pronounced effects of 4.1. Classification of executive functions
stress on cognition indeed occur around the cortisol peak (e.g. Schoofs,
Preuß, & Wolf, 2008). Plessow, Fischer, Kirschbaum, and Goschke The most basic form of cognitive control is the targeted control of
(2011) demonstrated that the effects of stress on EF increased in par- attention. Here, focusing on relevant information substantially helps in
allel with increases in HPA axis activity. However, no corresponding performing goal-directed behavior. Sänger, Bechtold, Schoofs, and
pattern could be observed for decreases following peak cortisol Blaszkewicz, & Waschner, E. (2014) suggest two competing core pro-
(Plessow, Kiesel et al., 2012). In their meta-analysis on the effects of cesses in attention: the bottom-up sensory process (i.e. salience of the
cortisol administration on executive functioning, Shields, Bonner, and stimulus) and the top-down goal related process, based on task relevant
Moons (2015) also argue that experimental timing likely plays an im- information. When speaking about cognitive control, this latter is cru-
portant role in evaluating the effects of HPA axis reactivity (as mea- cial for selective attention. Therefore, selective attention is an im-
sured by cortisol increases) on executive functioning. portant prerequisite for executive functioning (see the following para-
Building on this point, it should be noted that cortisol effects can graph). However, basic selective attention is a relatively simple process
assume two, temporally distinct forms: non-genomic effects are rapid, that does not require higher level cognition.
occurring within minutes of stressor-onset, whereas genomic effects are The next level of complexity of cognitive functions constitute the so-
slower and only emerge about an hour after the stressor has been ex- called EF, a set of general-purpose control processes that regulate one’s
perienced. These discrete effects emerge when cortisol binds to either thoughts and behaviors (Miyake & Friedman, 2012). The number and
membrane-bound receptors (for non-genomic effects) or nuclear re- quality of putative EF sub-dimensions varies by author, which is why
ceptors (for genomic effects), which permits time-dependent adapta- several researchers, such as Chan, Shum, Toulopoulou, and Chen
tions to a certain stressor (e.g. see Groeneweg, Karst, De Kloet, & Joels, (2008) call them “an umbrella term comprising a wide range of cognitive
2011; Hermans, Henckens, Joëls, & Fernández, 2014; Joels, Fernandez, processes and behavioral competencies” (p. 1). However, the most pro-
& Roozendaal, 2011). As most studies refer to the non-genomic effects minent EF are inhibition (deliberate overriding of dominant or pre-
of cortisol (i.e. the relatively rapid effects of stress, occurring within the potent responses), updating/working memory (constant monitoring
first 60 min following stressor onset), genomic effects will not be dis- and rapid addition/deletion of working memory contents), and cogni-
cussed further. tive flexibility/shifting (switching flexibly between tasks or mental sets)

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(Diamond, 2013; Miyake & Friedman, 2012; St Claire-Thompson & Simerly, Swanson, & Evans, 1988; De Kloet, Fitzsimons, Datson, Meijer,
Gathercole, 2006). The different executive functions (EF) are mainly & Vreugdenhil, 2009; Joels & Krugers, 2007) including hippocampal
based on empirical data and clinical observations and refer to those and prefrontal regions (De Kloet et al., 1998, 2016; Henckens, Van
cognitive processes that demand the transformation of given informa- Wingen, Joels, & Fernández, 2011; Porcelli et al., 2008; Reul & Kloet,
tion (Sue Baron, 2004). In this respect, working memory (WM) capacity 1985; Schwabe, Schächinger et al., 2010). Therefore, cortisol is likely to
is crucial, as the other EF are dependent upon it (Miyake, Friedman, have an effect on many cognitive functions. Hippocampal effects of
Rettinger, Shah, & Hegarty, 2001). stress seem to affect long term memory processes whereas prefrontal
The third level of cognitive complexity encompasses higher order receptor binding mainly seems to influence working memory processes
cognitive functions, i.e. general intelligence (g) factors. Of particular and EF in general (Porcelli et al., 2008; Schwabe, Schächinger et al.,
interest is the strongly heritable part of g, namely fluid intelligence (gf). 2010; Yuan & Raz, 2014). In fact, animal work impressively demon-
Examples of fluid intelligence include reasoning and induction. Of strated that neuronal projections in the rodent PFC undergo significant
course, working memory is substantially associated with gf, as WM remodeling following stress exposure and that these stress-induced
functions are an important prerequisite for more elaborate tasks or changes in PFC neuronal morphology are accompanied by deficits in
higher order abilities, such as reasoning (Engle, Tuholski, Laughlin, & rodent EF such as working memory, attentional set-shifting and cog-
Conway, 1999). Notwithstanding this association, tasks of selective nitive flexibility, as well as emotional dysregulation in the form of
attention, working memory, and inductive reasoning differ sub- impaired fear extinction (Holmes & Wellman, 2009). Several pathways
stantially in terms of their complexity and cognitive demand. These have been proposed to be involved in the stress related modulation of
differences are likely to be important factors in the investigation of the the PFC. First, a bidirectional pathway connecting PFC and amygdala
effects of stress on prefrontal cognitive function, given evidence that (essential for the processing of emotions). Second, a descending pro-
cognitive performance depends on task load (Lavie, Hirst, De Fockert, & jection from the PFC to the hypothalamus and brainstem nuclei that
Viding, 2004). mediates neuroendocrine and autonomic responses to stress, respec-
All three cognitive functions outlined above; working memory, se- tively. Third, a reciprocal connection between the PFC and the mid-
lective attention, and fluid intelligence are believed to be highly heri- brain and brainstem that activates monoamines under stress and which
table (Ando, Ono, & Wright, 2001; Blokland et al., 2011; Cattell, 1963; are known modulators of EF. Fourth, the reciprocal connectivity be-
Gray & Thompson, 2004; Polderman et al., 2006; Vogler et al., 2014) tween the mPFC and the hippocampus that provides the transfer of
and mainly under the control of prefrontal brain regions. Accordingly, complex environmental information. Fifth, the PFC is connected with
repetitive transcranial magnetic stimulation of the prefrontal cortex dorsal and ventral striatal regions related to reward and a propensity to
(PFC) leads to alterations of cognitive performance in several domains the consumption of drugs of abuse (Holmes & Wellman, 2009). Chronic
of executive functioning (Lowe et al., 2018). Although EF are unlikely stress also leads to substantial dendritic atrophy in the PFC (Radley
to be solely localized in specific brain regions, the lateral PFC can be et al., 2006; see also McEwen, Nasca, & Gray, 2016). Lesions in PFC
considered the main region for executive control. Other important re- sub-regions increase stress-induced glucocorticoid release in the para-
gions for executive functioning are the anterior cingulate cortex (ACC), ventricular nucleus of the hypothalamus (PVN) and in the medial
the inferior frontal gyrus (IFG), and further frontoparietal areas (Yuan amygdala (e. g. Spencer, Buller, & Day, 2005). These effects are be-
& Raz, 2014). The PFC controls a variety of higher order EF involved in lieved to be mediated via actions on glucocorticoid and miner-
the selection and processing of information in order to plan, control and alocorticoid receptors abundantly expressed in the rodent mPFC (Fuxe
direct behavior according to environmental demands (Goldman-Rakic, et al., 1985).
1996). Although there is also some evidence to the contrary (e.g. Duarte A reduction in dlPFC activity under acute stress can also be found in
et al., 2006), different study designs yield a positive association be- humans during WM tasks, although the performance does not in-
tween PFC volume and EF that may be moderated by the type of EF evitably worsen under these circumstances so that the deactivation can
(e.g. Gunning-Dixon & Raz, 2003; Colom et al., 2013; Yuan & Raz, also be interpreted as a higher efficiency of the PFC during acute stress
2014). Thus, the importance of the PFC may differ dependent on the (Luettgau, Schlagenhauf, & Sjoerds, 2018; Qin, Hermans, van Marle,
respective executive functioning task. Hedden and Gabrieli (2010) find Luo, & Fernández, 2009). Luettgau et al. (2018) argue that, if the re-
that inhibition and task shifting are represented in vastly overlapping duced activity of the dlPFC under stress is interpreted as a heightened
regions including the dorsolateral PFC (dlPFC), the ACC, and parts of neural processing efficiency, cortisol might serve as a neuromodulator
the basal ganglia, although they also report areas being preferential for for glutamatergic transmission that causes increased excitability of the
one or the other. This allows the conclusion that different EF may not be PFC under stress. Rat models suggest that this effect is mediated by the
differentiated by the extent of dlPFC activation, but rather by the in- GR and that it is specific to the PFC (Song et al., 2017; Yuen et al.,
teraction of the dlPFC with more specific other brain regions, which has 2009). The findings by Yuen et al. (2009) further suggest that there is a
also been proposed by Funahashi (2001). For example, a strong fron- temporally increased expression of NMDA and AMPA membrane bound
toparietal connectivity has been proposed for task switching (Vallesi, receptors during acute stress that causes the potentiation of glutama-
Arbula, Capizzi, Causin, & D'Avella, 2015) and working memory tergic transmission (but see also Houtepen et al., 2017, who find no
(Klingberg, O'Sullivan, & Roland, 1997). Several pathways within the involvement of glutamate in the association between stress and the
PFC that orchestrate inhibition and set shifting have also been reported: PFC). It is typically assumed that the stress-induced effects of cortisol on
Here, the dorsomedial PFC (dmPFC) and dlPFC are believed to be the cognitive functioning are primarily mediated by binding to the lower-
most important areas for task switching, whereas the ventromedial PFC affinity GR, as the high affinity of MR means it binds to cortisol under
(vmPFC) ensures cognitive stability (Domenech & Koechlin, 2015; both tonic and stressful conditions. MR has, therefore, been considered
Wagner, Maril, Bjork, & Schacter, 2001). less sensitive to changes in the concentration of central levels of cor-
tisol. However, in addition to high affinity MR in the nucleus, there are
4.2. Stress and cognitive functioning MR located in the cell membrane, which show a lower affinity and are
sensitive to stress induced alterations of cortisol (De Kloet, 2014; De
Although cortisol is expressed in the periphery, as a steroid hor- Kloet, Karst, & Joels, 2008; Joels, 2018). Thus, both GR and MR play a
mone, it can cross the blood brain barrier and can therefore influence crucial role in mediating the effects of (e.g. stress-induced) cortisol
central nervous processes, including cognitive functioning. In the brain, changes on cognition in humans and rodents (Vogel, Fernández, Joels,
the effects of cortisol are mediated by binding to mineralocorticoid & Schwabe, 2016). Recent evidence suggests that MR functions affect
(MR) and glucocorticoid receptors (GR) (Lupien et al., 2007). Both re- several cognitive functions such as memory, attention, and working
ceptor types are broadly distributed throughout the brain, (Arriza, memory (Hinkelmann, Wingenfeld, Kuehl, Fleischer, & Wiedermann,

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2015; Piber et al., 2016; see also Vogel et al., 2016). of the Stroop task to participants and found better performance in the
Another mechanism discussed is that stress is believed to activate stressful condition, suggesting more effective neglect of irrelevant in-
the amygdala, which in turn activates regions in the midbrain and brain formation, resulting in less inference in the respective tasks. In contrast,
stem including the locus coeruleus, the substantia nigra, and the ventral other researchers claim that faster reaction times in selective attention
tegmental area. These processes lead to a heightened dopaminergic and tasks come at the cost of a reduction in cognitive flexibility (e.g.
nor-adrenergic transmission causing higher prefrontal dopamine (DA) Duncko, Johnson, Merikangas, & Grillon, 2009). Similarly, Plessow
and noradrenaline (NA) concentrations and lower neuronal firing rates. et al. (2011, Plessow, Schade et al., 2012) report increased goal
Here, the dopamine D1 (and D2) and the NA alpha-1 receptors seem to shielding, leading to greater inflexibility on a Simon task and higher
play critical roles in these effects. For both DA and NA, the literature switch costs in a task-switching paradigm. In a follow up study,
assumes an inverted U-shaped relationship between transmitter con- Plessow, Kiesel et al. (2012) had participants perform a dual task
centration and dlPFC function and executive functioning respectively paradigm, in which the subjects had to indicate whether two digits
(Arnsten, 2009; Shinohara et al., 2018). This results in a shift away (presented one above the other) were odd or even. In contrast to their
from slow and very accurate executive control systems to faster, more previous results, the authors found higher error rates in the stressed
SNS controlled processes, which aim to deal with the acute threat in subsample when the digits were incongruent (i.e. one odd, one even),
terms of activating the fight-flight system. As already outlined, there is indicating decreased goal shielding. Thus, stressed participants perform
a phase in the stress response in which increased concentrations of NA poorly on a dual task, despite possible performance gains when com-
and cortisol are overlapping that putatively represents a critical time pleting a single task. In order to explain the conflicting results, Plessow,
window for the effects of stress on prefrontal cognition (see Elzinga & Kiesel et al. (2012) discuss the idea that stressed individuals might
Roelofs, 2005; Schoofs et al., 2008). Thus, the effects of cortisol on adopt a strategy to save resources, this could lead to an inflexible focus
cognitive functioning are likely dependent on the extent of catechola- on a single task, but less task shielding in a dual task in order to fa-
mine-induced arousal in the PFC. cilitate parallel processing. Hence, stress might not lower cognitive
Recent evidence in rat models suggests that the brain derived neu- control per se, but rather lead to a shift in cognitive control processes,
rotrophic factor (BDNF) related to brain plasticity also plays a role in in order to spare limited cognitive resources. Of note, all of the studies
the effects of acute stress on PFC mediated cognitive performance mentioned above used different stress induction protocols: Whereas
(Brivio, Sbrini, Riva, & Calabrese, 2020). Besides, Uribe-Mariño et al. stress was induced by cognitively demanding tasks (under time pressure
(2016) recently showed locally increased mRNA expression of the CRH and with threat to ego) and assessed by participants’ self-reported
receptor 2 that might have an impact on dysfunctions of the PFC via perceived stress in the study by Chajut and Algom (2003), Plessow et al.
proteinkinases A and C. (2011), Plessow, Kiesel et al. (2012), Plessow, Schade et al. (2012) used
Despite the investigation of the neurofunctional mechanisms in the the TSST, Beste, Yildiz, Meissner, and Wolf (2013) used the SECPT, and
PFC during stress, the direction of acute stress effects on human cog- Duncko et al. (2009) stressed their participants using the CPT (and
nitive performance (i.e. on behavioral level) is far from conclusive. In found no effects of the stressor on cortisol levels).
this respect, the type of cognitive function under study is also important In addition to the nature of the task, the difficulty of the task may
(i.e. task performance under stress presumably depends on the com- also influence the effects of stress: Oei, Everaerd, Elzinga, Van Well, and
plexity of the task.) Bermond (2006) report that stress dampens short-term memory per-
formance only on more difficult trials of the Sternberg item recognition
5. Stress and executive functioning: Task related features task, in which participants are presented with a number of stimuli (e.g.
letters) and are asked whether a subsequently displayed stimulus was
Shields et al. (2015, 2016) recently showed that executive control part of the original set of stimuli. Task difficulty is increased by varying
performance depends, at least in part, on the type of task and the re- the number of stimuli that must be held in short-term memory storage,
lated specific EF. According to them, stress has a moderate negative and can be further manipulated by increasing the number of stimuli in
effect (−0.3 ≤ g* < −0.2) on cognitive flexibility and updating. While the second frame, so that the participant must identify a possible target
the overall effect of stress on inhibition did not achieve significance, from several options. Hence, tasks like this also test attentional skills, as
this may be explained by the choice of inhibition paradigm. For ex- selective and goal-directed attention are important prerequisites for
ample, cognitive inhibition decreases under acute stress (g* = −0.21), working memory functions (Sänger et al., 2014). The n-back paradigm,
whereas response inhibition increases following acute stress (g*= a test of similar functions, was used by Schoofs et al. (2008) following
0.29), a finding further supported by more recent evidence on both a an acute stress induction. In contrast to Oei et al. (2006), they found
behavioral and electrophysiological level (Dierolf, Fechtner, Böhnke, impairments in reaction times and error rates for both the high- (i.e. 3-
Wolf, & Naumann, 2017; 2018). Schwabe, Höffken et al. (2013) also back) and low- (i.e. 2-back) taskloads among the stressed subsample.
find enhancing effects of acute stress on response inhibition perfor- This finding also contrasts with a more recent study, in which impair-
mance in a stop-signal task and that this performance is influenced by ments were only evident for the high-load of an n-back task, and were
MR functioning. Furthermore, many of the studies included in the meta- associated with frontal theta activity suggesting poor top-down reg-
analysis by Shields et al. (2016) presented different - sometimes even ulation under acute stress (Gärtner, Rohde-Liebenau, Grimm, &
contradictory - findings, suggesting a role for moderating factors be- Bajbouj, 2014). This is in line with Schwabe, Tegenthoff et al. (2013),
yond the type of EF under study (see section 6): For example, the effects who suggest that stress affects cognitive functioning on a more general
of stress on cognitive flexibility (i.e. set shifting in a variant of the level, rather than influencing specific cognitive functions. They argue
Wisconsin Card Sorting Test; WCST) depend on the perceived un- that stress leads to a shift from hippocampus-controlled declarative
controllability of the stressor (Gabrys, Howell, Cebulski, Anisman, & cognitive strategies to more procedural-learning strategies and that this
Matheson, 2019) and on task demands (Goldfarb et al., 2016). These shift is mediated by MR dependent amygdala activity. In support of this
findings underline the need for a more nuanced view of the effects of argument, Schwabe, Schächinger et al. (2010) experimentally demon-
stress on cognition. strated this shift in mice. This idea complements the conclusions of
With respect to selective attention, Beste, Yildiz, Meissner, and Wolf Plessow, Kiesel et al. (2012) that acute stress evokes the use of the most
(2013) report enhanced performance in a dual task paradigm, following resource-saving strategy in a stressful situation. Similarly, Dierolf et al.
the induction of stress using the SECPT. Participants’ reaction times (2018), Wirz, Wacker et al. (2017), Wirz, Reuter et al. (2017) argue that
were faster on both competing tasks, without any corresponding ne- a reallocation of cognitive resources takes place under acute stress. This
gative effects on accuracy (i.e. error rate). These findings are in line is similar to the assumptions of Arnsten (2009) on the neuronal level
with those of Chajut and Algom (2003), who presented several variants (see Section 4.2) and clearly makes sense from an evolutionary

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perspective: In an acutely dangerous situation, our attention should be mentioned, the MR has been identified to be involved in processes of
improved, allowing us to focus on the most important thing at that cognitive functioning such as selective attention or working memory.
moment, namely dealing with the current stressor or the situational Nevertheless, they also note that evidence from female participants is
challenge; we should thus be less able to perform tasks that require scarce compared to the conclusions drawn from male samples.
more declarative higher cognitive effort, as doing so would detract from Looking at the underlying biological mechanisms, animal models
our ability to effectively respond to the stressor. Thus, one could assume suggest that the effects of stress on PFC activity are more pronounced in
that the relationship between stress and cognition can be explained by males (Sood, Chaudhari, & Vaidya, 2018). Sex differences might in part
an inverted U-function, with the optimal peak being highly dependent be explained by the influence of sex hormones. It has been shown in rats
on the type of cognitive function: The optimal stress level for the best that estrogen and progesterone are capable of decreasing MR expres-
possible performance is higher for attentional tasks as compared to sion rates (Carey, Deterd, de Koning, Helmerhorst, & de Kloet, 1995;
cognitively more demanding tasks. Apart from that, there might also be Quinkler et al., 2002). The inhibition of the MR expression is likely
further task related moderators such as emotionality of the task driven by the activation of the estrogen receptor (Barrett Mueller et al.,
(Smeets, Giesbrecht, Jelicic, & Merckelbach, 2007). 2014). In contrast, androgen treatment led to an increase in MR ex-
Collectively, the evidence suggests that the effects of stress on ex- pression in male rats (Hafidzi, Karimi, Panandam, & Fuzina, 2013) (see
ecutive functioning may be highly dependent on both the cognitive Vinkers, Joels et al., 2015 for a more in-depth discussion). An upre-
function assessed and the level of task difficulty. gulation of the MR expression in the hippocampus and mPFC in male
mice only could also be found in response to early life stress
6. Stress and executive Functioning: Individual differences (Bonapersona et al., 2019). The upregulation of MR supports the as-
sumption of more pronounced stress effects in men on both neuronal
6.1. Age and sex activity and behavioral level (e.g. McEwen et al., 2016; Shields et al.,
2016). In line with this, sex differences have been found in dendritic
Participants' sex is a key moderator of the association between stress atrophy in the mPFC in response to chronic stress: whereas male rats
and executive control. Several studies show that men and women re- and ovariectomized female rats show dendritic atrophy, female rats
spond differently to acute laboratory stressors. Men typically have a with intact ovaries show an expansion of dendrites (Garrett & Wellman,
more pronounced response to a stressor in terms of HPA axis reactivity 2009; for an overview see McEwen et al., 2016). All of these results
(Kirschbaum et al., 1992; see also Kudielka, Hellhammer, & Wüst, indicate that sex differences in stress effects are heavily dependent on
2009). Stroud, Salovey, and Epel (2002) argue that sex differences in estrogen and other sex hormones, which is in line with studies showing
biological reactions to stressors depend on the nature of the stressor. an influence of menstrual cycle on stress effects in women (Kirschbaum
They report greater HPA axis activity in males related to achievement et al., 1999). Some studies also investigated the role of BDNF in sex-
stress, whereas cortisol levels in females were elevated in response to dependent effects of stress and could find that early life stress (e.g.
social stressors (e.g. conflict with a romantic partner). However, these maternal neglect) led to a more pronounced decrease in BDNF ex-
results should be interpreted with caution, as other studies have failed pression in male rodents as compared to females (see Bath, Schilit, &
to replicate these findings (see Kudielka & Kirschbaum, 2005). The sex Lee, 2013 for a review). Clearly, BDNF as a neurotrophic factor might
difference in cortisol reactivity is frequently found in samples where have an influence on PFC volume, which in turn is associated with
women report using oral contraceptives (Cornelisse, Van Stegeren, & executive functioning (as already outlined in Section 4.1).
Joels, 2011; Kirschbaum, Kudielka, Schommer, & Hellhammer, 1999), With respect to age, there are no consistent findings regarding the
which suggests that the use of oral contraception represents a confound HPA axis reactivity (Kudielka, Buske-Kirschbaum et al., 2004; see also
in this respect. Of note, these sex differences are typically not observed Kudielka et al., 2009), although heart rate variability following acute
in the subjective component of stress perception. stress seems to depend on age (Kudielka, Schommer et al., 2004).
There is also evidence that sex may moderate the relationship be- Dierolf et al. (2018) did not find any effects of age on response in-
tween stress and executive control. For example, Schoofs, Pabst, Brand, hibition performance in men under acute stress. A very recent review by
and Wolf (2013) had participants perform a 2-back task. They report Hidalgo, Pulopulos, and Salvador (2019) also shows inconsistent effects
quicker reaction times among men following TSST-induced stress, of age on the effects of stress on EF. Therefore, any effects of age on the
whereas reaction times for females were slower in the stress condition relationship between stress and cognitive functioning may be negli-
compared to the non-stress control condition. Response accuracy was gible.
not affected by the stress induction. Cornelisse et al. (2011) report si-
milar effects of stress for their male sample (i.e. working memory en- 6.2. Genetic factors
hancement on a 2-back task). In contrast, no effects of stress could be
observed in women, which - at least partly - supports the results in the Individual differences in genetic factors also seem to influence both
study by Schoofs et al. (2013). Further complicating this pattern of stress reactivity (Kreek, Nielsen, Butelman, & LaForge, 2005) and the
results, earlier studies by Shoofs et al. (2008, 2009) revealed impaired association between stress and cognitive functioning (Keller et al.,
working memory in males (on both 2-back and 3-back versions of the n- 2017; Plieger et al., 2017a). With respect to stress reactivity, herit-
back task and an O-span task) following TSST-induced stress. In their ability has been shown for perceived stress (Federenko et al., 2006),
meta-analysis, Shields, Sazma, and Yonelinas (2016) conclude that the cardiovascular markers (Wu, Snieder, & de Geus, 2010), and HPA axis
negative effects of stress on EF are somewhat stronger in men than in activity (Franz et al., 2010) and reactivity (Federenko, Nagamine,
women. In a more recent experimental study, stress led to a decrease in Hellhammer, Wadhwa, & Wüst, 2004; Steptoe, Van Jaarsveld, Semmler,
cognitive flexibility on a WCST, but this effect was only observed for Plomin, & Wardle, 2009).
males (Kalia et al., 2018). However, the authors argue that the more From a molecular genetic perspective, polymorphisms on several
pronounced effects in males may be due to the fact that stress effects genes have been shown to influence the HPA axis reactivity following
can be measured with higher reliability in male samples because of the an acute stress induction. For example, the NR3C1 gene coding for the
less moderating influence of sex hormones. Therefore, they conclude GR and the NR3C2 gene coding for the MR seem to be associated with
that effects could, in fact, be stronger in women, but that there is a lack the increase in cortisol after a stressor (e.g. De Rijk, 2009; De Rijk et al.,
of sufficiently precise studies to test this until now. In a similar vein, 2006; Li-Tempel et al., 2016; Van Leeuwen et al., 2011). A very pro-
Vogel et al. (2016) argue that MR functionality might be dependent on minent single nucleotide polymorphism (SNP) that has been associated
sex, as gonadal hormones are - just like glucocorticoids - steroid hor- with HPA axis reactivity is the BCL1 [G/C] (rs42423247). Male
mones and can therefore alter central nervous processes. As already homozygous carriers of the G-allele showed less increase in response to

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an acute stressor than carriers of at least one C-allele (Kumsta et al., participants’ performance in attention tasks, working memory, and
2007; Wüst et al., 2004). However, Kumsta et al. (2007) report op- executive functioning, whereas NR3C2 genetic variation was associated
posing results for their female subsample, suggesting that there might with memory performance (Keller et al., 2017). The only study to date
be an interaction with sex. Besides the BCL1 polymorphism, there are to investigate the interaction between cortisol reactivity under acute
other prominent polymorphisms on the NR3C1 gene that have been stress and genetic variation reported an influence of NR3C2 poly-
associated with stress reactivity (see DeRijk, 2009; DeRijk & De Kloet, morphisms (in combination with cortisol reactivity) on attentional
2005). Newer approaches have also identified haplotypes (i.e. com- performance (Plieger et al., 2017a, 2018). In this study, no effects of
bined influences of several polymorphisms) on the NR3C1 gene that cortisol or genetic variation on reasoning performance (i.e. high cog-
seem to influence cortisol reactivity after undergoing an acute stress nitive load tasks as compared to low load attentional tasks) were ob-
induction (Li-Tempel et al., 2016; Plieger et al., 2017a). Evidence for an served, which supports the idea that task complexity may also be a
influence of polymorphisms on the MR coding NR3C2 gene is rather moderating factor in the association between stress and executive
scarce, because the MR has mainly been associated with tonic processes control. With respect to learning, Wirz, Wacker et al. (2017) recently
or the maintenance of homeostasis due to its comparably lower acti- showed that a shift in learning strategies (i.e. from cognitive hippo-
vation threshold. Nonetheless, several studies also suggest an associa- campal to habitual striatal) under acute stress was dependent on a
tion between polymorphisms on the NR3C2 gene and stress reactivity variant of the gene coding for the alpha-2b-adrenoreceptor (ADRA2B)
(de Kloet et al., 2006; Van Leeuwen et al., 2011). MR I180V [G/A] in two different samples. The study also gives a clue for the underlying
(rs5522) and MR-2 [G/C] (rs2070951), in particular, have been found neuronal mechanism of this effect: connectivity between amygdala,
to have an impact on cortisol levels under acute stress. Both have been hippocampus, and dorsal striatum during the task significantly differed
shown to be functional in in vitro analyses (DeRijk et al., 2006; Van between ADRA2B genotypes, which – according to the authors – was
Leeuwen et al., 2010). likely driven by non-genomic cortisol actions. This assumption is sup-
Another prominent polymorphism that has been investigated in the ported by other findings in the same samples, which also suggest a
context of stress reactivity is the 5-HTTLPR, which is an insertion/de- modulating role of a NR3C2 haplotype (including the prominent SNPs
letion polymorphism located in the promoter region of the SLC6A4 MR-2G/C and MR-I180V) in the strategy shift (Wirz, Reuter et al.,
gene and which modulates the expression rate of the serotonin trans- 2017). The latter results further underline the importance of MR in
porter (5-HTT). It has been shown that the long variant (L allele) has an cognitive functioning. Of note, Xie, Cappiello, Meng, Rosenthal, and
up to threefold higher expression rate than the short variant (S allele) Zhang (2018) suspect that the influence of the ADRA2B gene on the
(Canli & Lesch, 2007; Lesch et al., 1996). The serotonergic system is an association between stress and cognitive performance may be of par-
interesting candidate for the stress reaction because 5-HT influences the ticular importance for emotionally laden task stimuli.
initiation of the hypothalamic CRH secretion (Calogero et al., 1990; Clearly, more research is needed on the possible interaction effects
Heisler et al., 2007). Several studies show an influence of the 5-HTTLPR of stress (reactivity) and genetic variation in the candidate genes re-
on stress reactivity in both laboratory designs (Mueller et al., 2011; viewed above, on prefrontal cognitive tasks of any kind. We re-
Way & Taylor, 2010) and in the field (Taylor et al., 2014a, 2014b), commend considering individual genetic differences because the effects
although these studies do not permit conclusive results. However, of cortisol on brain and body depend on several other processes: For
Miller, Wankerl et al. (2013) suggest higher HPA axis reactivity among example, cortisol effects are mediated by the MR and GR. The activity
carriers of the S allele in their meta-analysis. In addition to cortisol and density of these receptors are, in turn, affected by our genetic
reactivity, the 5-HTTLPR also seems to influence the sympathetic stress make-up. Therefore, it is highly plausible to assume interaction effects
reaction (Plieger et al., 2017b), which is likely, as CRH is the starting of HPA axis reactivity and genetic factors. This supposition also holds
point of both the HPA axis signaling cascade and the sympathetic stress for genes coding for other receptors or enzymes, such as COMT or MAO-
reaction (Tsigos & Crousos, 2002). A. Obviously, an influence of these genes is conceivable. COMT is an
Beyond these genes, occasional evidence points to the influence of important modulator of dopaminergic transmission that very likely
other genes on HPA axis reactivity, including the COMT gene, MAO-A plays a role in the effects of stress on executive functioning by mod-
gene, GABA-A receptor gene, BDNF gene and the CRHR1 gene, al- ulating dlPFC activity. Similarly, MAO-A is an important modulator of
though the latter has only been tested for its influence on dex- the concentration of several neurotransmitters including NA and – to a
amethasone reactivity (a synthetic glucocorticoid) and has not been lesser extent - DA by catabolizing active transmitter molecules (Berry,
examined in the context of a psychological stress paradigm (Alexander Juorio, & Paterson, 1994; Kalgutkar, Dalvie, Castagnoli, & Taylor,
et al., 2010; DeRijk, 2009; Dougherty, Klein, Congdon, Canli, & 2001; Lakshmana et al., 1998; La Regina et al., 2007). Therefore, it is
Hayden, 2010). likely that individual differences in the genetic constitution of these
In addition to HPA axis reactivity, it is also of interest whether ge- systems modulate the DA and NA mediated effects of stress on pre-
netic variation influences the association between stress and cognitive frontal functioning. Given the plausibility of such interactions, we re-
functioning. Unfortunately, few studies have tested this moderation commend considering individual differences in genetic make-up
effect, although some studies hypothesize a modulatory role for the MR alongside sex, as prospective moderators of the relationship between
in the effects of stress on cognitive processes (Schwabe, Schächinger stress and cognitive control functioning.
et al., 2010, Schwabe, Tegenthoff et al., 2013; Vogel et al., 2016), and Besides molecular genetic variation that deals with individual dif-
other studies show that genetic variation on the NR3C2 (MR coding) ferences in the hardware of the genome (e.g. alterations in nucleotide
gene is associated with phenotypes related to cognitive dysfunction sequences that exist before birth and that are invariant across life),
such as depression (De Kloet et al., 2016; Hamstra, De Kloet, Van some attempts have been made to link differences in the methylation of
Hemert, DeRijk, & Van der Does, 2015; Vinkers, Joels et al., 2015). An several genes to stress associated mechanisms. This consideration of
association with depression has also been shown for other genes such as epigenetic processes is a rather recent and very promising approach in
the NR3C1 gene (e.g. Szczepankiewicz et al., 2011; Galecka et al., the field of molecular genetics, because epigenetic changes related to
2013) or the SLC6A4 gene (Caspi et al., 2003; Clarke, Flint, Attwood, & the transcription of genes can be influenced by environmental factors.
Munafo, 2010; Karg, Burmeister, Shedden, & Sen, 2011; for a review see Several studies report an impact of life stress in childhood (Perroud
Canli & Lesch, 2007). However, direct effects of these genes on ex- et al., 2011) and adolescence (Van Der Knaap et al., 2014) on increased
ecutive functioning have rarely been shown. In a genome wide asso- methylation in several CpG sites in exon 1F of the NR3C1 gene (see also
ciation study (GWAS), Pan, Wang, and Aragam (2011) found evidence Palma-Gudiel, Córdova-Palomera, Leza, & Fananás, 2015). Further re-
that NR3C2 polymorphisms are associated with IQ. Another study search shows that maternal stress correlates with NR3C1 methylation in
shows an influence of NR3C1 polymorphisms, including the BCL1, on newborns (Mulligan, D'Errico, Stees, & Hughes, 2012). In their review,

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T. Plieger and M. Reuter Neurobiology of Learning and Memory 173 (2020) 107254

Vinkers, Kalafateli et al. (2015) also show associations between stress at basolateral amygdala, nor-adrenergic projections from the locus coer-
several life stages and methylation of sequences on various genes in- uleus, and the mPFC (Daviu, Bruchas, Moghaddam, Sandi, & Beyeler,
cluding NR3C1, NR3C2, SLC6A4, BDNF, and others. However, they 2019). Thus, interplay between stress and anxiety in prefrontal activity
stress the importance of longitudinal studies and argue that many of the during cognitive tasks seems inevitable. In fact, Goette, Bendahan,
studies published in this area are difficult to compare due to metho- Thoresen, Hollis, and Sandi (2015) showed that highly anxious people
dological issues, such as measuring methylation patterns in different became less confident in a competitive decision making game after
tissues (e.g. blood vs. brain tissue). To the best of our knowledge, to undergoing the TSST, whereas, in contrast, low-anxiety participants
date no studies have investigated the effects of methylated gene se- became over-confident under acute stress.
quences on acute stress reactivity or cognitive functioning. Nonetheless, While trait anxiety has been considered as a moderating factor in
the inclusion of epigenetic patterns in the association between stress the association between stress and cognitive functioning, state anxiety
and executive functioning is a promising research avenue for future has been suggested instead as a mediating factor such that stress leads
studies. to a state of anxiety that in turn results in altered working memory
performance (Hood, Pulvers, Spady, Kliebenstein, & Bachand, 2015). Of
6.3. Personality traits note, this effect was moderated by HPA axis reactivity: the mediation
was only observable in participants who responded with a significant
In contrast, trait-like characteristics of an individual may play an cortisol increase following exposure to the stressor. These results sug-
important role. For example, coping and emotion regulation abilities gest that trait-like characteristics, particularly coping and emotion
have been discussed as potential influencers, as some studies suggest regulation, are involved in the interplay between stress and prefrontal
that coping and EF are interdependent constructs (Andreotti et al., cognition.
2013; Nieto et al., 2019). Furthermore, individual differences in EF Additionally, results by Jentsch et al. (2019) and Reising et al.
have been found to have predictive power for successful emotion reg- (2018) show that individual differences in neuronal activation may be
ulation and coping (Schmeichel & Tang, 2015). Recent work by Jentsch, of interest in evaluating the effects of stress on cognitive control. Be-
Merz, and Wolf (2019) suggests that stress-induced cortisol elevations sides functional neural differences, a moderating effect of structural
influence coping abilities at both behavioral and neuronal levels in a differences is also possible. For example, Pruessner, Pruessner,
stressful situation. Vice versa, conscious and unconscious coping can Hellhammer, Pike, and Lupien (2007) report that cortisol reactivity
enable people to actively control their stress reaction following a following a stressor is positively related to hippocampal volume which
stressor (e.g. Plieger et al., 2017b)). There is also evidence from a is, in turn, related to declarative memory performance.
longitudinal study that combines all the three variables and shows that
coping mediates the association between EF and depression in adoles- 7. Conclusion
cents (Evans et al., 2016). Other studies show an interplay of cognitive
functioning, coping, and chronic stress in female breast cancer patients Substantial efforts have been made to investigate and characterize
(Ayala-Feliciano, Pons-Valerio, Pons-Madera, & Acevedo, 2011; Reid- the effects of stress on prefrontal cognitive functions. However, given
Arndt & Cox, 2012) and in adolescents with depressed (vs. non-de- the heterogeneity of findings in the literature, a firm conclusion about
pressed) mothers (Reising et al., 2018). Reising et al. (2018) further the direction of these effects remains elusive. This is likely due to the
found that the activation of areas typically associated with executive fact that many studies in the field are difficult to compare with one
control (i.e. the dorsolateral prefrontal cortex and the dorsal anterior another without consideration of important moderating factors. The
cingulate) predicted the use of specific coping strategies. aim of the present review was to present an overview of different
Furthermore, anxiety has been identified as an important moder- variables which have been proposed as moderators, such as individual
ating personality trait in the association between cognitive functioning differences, differences in stress paradigms, and differences in experi-
and stress. As Attentional Control Theory (Derakshan & Eysenck, 2009; mental procedures. Therefore, we tried to delineate how the relation-
Eysenck, Derakshan, Santos, & Calvo, 2007) suggests, anxiety leads to a ship between stress and cognitive function is influenced by these vari-
shift from goal-directed, top-down attention to bottom-up, stimulus ables (see Fig. 2). Table 1 provides an overview of important studies
driven attention. This results in an allocation of attentional resources to addressing this topic, as well as a variable classification pattern to help
threat-related stimuli and, therefore, has a detrimental effect on ex- categorize future studies on this topic. This classification helps high-
ecutive control performance. According to Attentional Control Theory, light inconsistencies across studies based on heterogeneous research
cognitive efficiency (i.e. the effort to achieve an outcome) is decreased designs.
by high levels of anxiety rather than effectiveness (i.e. the actual out- With respect to stress induction, several factors should be con-
come independent of the invested effort). The detrimental effects of sidered as potential moderators. First, not all stress paradigms reported
anxiety are particularly found in tasks requiring task switching and in the literature reliably evoke HPA axis responses, which is why stu-
inhibition (Moran, 2016; Park & Moghaddam, 2017; Visu-Petra, Miclea, dies should only be compared if paradigms used have a similar impact
& Visu-Petra, 2013). Of note, these effects are believed to be greater in on the respective marker of stress reactivity. To date, only the SECPT
situations of heightened state anxiety such as under acute stress. and the TSST seem to reliably evoke the HPA axis and lead to stress
Edwards, Edwards et al. (2015) report a combined effect of stress (only induced cortisol elevations, although the MAST may be a promising
induced by an ego-threat) and trait anxiety on efficiency in a shifting candidate for the targeted stimulation of the HPA axis. However, due to
task (i.e. WCST). However, these effects are only observable in parti- its newness there is insufficient data to permit a conclusive evaluation
cipants who perceived the WCST to be quite simple and not in parti- of its utility. Other paradigms prompt sympathetic stress responses or
cipants who reported that they invested great mental effort in the task. only result in a subjective perception of stress. Field studies reporting
Virtually the same interaction effects were found in another study by effects of naturalistic stressors outside the laboratory and studies re-
the same work group using a different stressor (the TSST counting task) porting effects of chronic rather than acute stress, must also be analyzed
and other shifting tasks (Sternberg paradigm and oddball tone-dis- separately because of less standardization (in the case of field studies)
crimination) (Edwards, Moore et al., 2015). Hence, the moderating and differing time perspectives (in case of studies dealing with chronic
effects of anxiety in the association between stress and executive stress). Second, the experimental time schedule should be adjusted,
functioning may further be moderated by cognitive load, which clearly based on the points raised above: Measurement of sympathetic or
demonstrates that the possible moderators discussed in the present re- subjective stress on cognitive functioning should occur immediately
view obviously interact with each other. Interestingly, we can also find after the stressor, whereas the measurement of endocrine stress (i.e.
overlaps of stress and anxiety on the neuronal level, including the cortisol) effects on cognitive functioning should take place around the

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T. Plieger and M. Reuter Neurobiology of Learning and Memory 173 (2020) 107254

Fig. 2. Moderated interplay between stress and cognitive functioning. The cognitive performance of individuals under stress is influenced by aspects of the stress
induction and its measurement, on the one hand, and by task-related aspects on the other. Additionally, the individual and its characteristics is an important regulator
for all three parts: a) stress reaction (e.g. sex and inherited stress reactivity), b) cognitive functioning (e.g. general intelligence or specific cognitive abilities), and c)
the association between both stress and cognition (e.g. coping mechanisms, traits, genetic constitution). Thus, personal characteristics such as the genetic make-up or
sex not only influence the stress reaction and cognitive abilities, but are also believed to be differentially influential on the association between them. For example,
there may be no difference between carriers of different genotypes in the perception of and psychophysiological reaction to stress and in their general cognitive
capability. Nevertheless, they may perform differently on specific cognitive tasks while in a state of acute stress, depending on their genotype.

expected stress-induced cortisol peak - about 20–25 min after the onset Initial evidence suggests a prominent moderating role for several genes,
of the stressor. such as the MR coding NR3C2 gene. Similarly, the consideration of
With respect to the measurement of EF, task quality and task load epigenetic processes, though under-researched, is a promising factor in
seem to moderate the association between stress and cognition. the understanding of individual moderators in the stress-cognition as-
Evidence suggests that inhibition and selective attention performance sociation. Third, personality characteristics such as coping behavior or
profit from stress to a certain extent, whereas stress seems to decrease anxiety may also interact with stress effects on cognitive control per-
performance in cognitive flexibility and higher order cognitive func- formance.
tions. This inflexible focus makes sense from an evolutionary perspec- We think that a more fine-grained and differentiated view is ne-
tive and can be explained by the Yerkes-Dodson-Law, with the optimal cessary to facilitate a more accurate insight into the effects of stress on
arousal level for the best performance being dependent on task load executive functioning. Of course, we are aware that some of the aspects
(compare Diamond et al., 2007). That is, easier tasks requiring only discussed in this review are controlled for in many studies. This is
selective attention should be solved most efficiently with a comparably especially true of the effects of sex on stress reactivity or individual
high arousal because the organism switches to resource-saving strate- differences in cortisol reactivity following an acute stressor. However,
gies and ignores irrelevant information more efficiently. Additionally, in order to achieve a deeper understanding of the interplay between
the performance should decrease only marginally with increasing levels stress and cognition, we need to look at those factors more system-
in arousal because of the simplicity of the task. In contrast, tasks de- atically and comprehensively, rather than publishing single studies that
manding more elaborate cognitive processing (e.g. reasoning) should be only control for one or two factors. Moving forward, studies assessing
solved most efficiently with comparably lower arousal, because of the the influence of stress on executive functioning should systematically
shift from declarative, top-down regulated cognitive processes to more control for the moderating influences of the variables discussed in the
resource-saving, non-declarative strategies in presence of high arousal. present review. Failure to do so, will perpetuate existing problems in
However, as attention is also required for higher cognitive processing the literature, making studies difficult to compare or replicate. Some
(i.e. high cognitive load) there should at least be a medium arousal in initial promising and valuable attempt to systematically order the lit-
order to perform well in more difficult or elaborate tasks (Fig. 3). erature take the form of the recent meta-analyses by Shields and col-
Finally, individual differences very likely influence the association leagues, who discuss the effects of stress (2016) and cortisol (2015) on
between stress and cognition. In the current review, we discuss the different EF. In the future, these analyses should be widened to include
well-studied sex differences in HPA axis reactivity. Nonetheless, it is other cognitive functions (that differ in nature and complexity) and
still unclear, whether there is a moderating effect of sex on the asso- individual factors, as well as separating evidence from different stress
ciation between stress and cognitive functioning. The second aspect paradigms, which evoke different stress reactions. Nevertheless, in our
discussed here is the individual genetic factors that have been shown to opinion future studies on stress and cognitive control functioning
influence HPA axis reactivity and cognitive functioning. However, to should be classified using the systematic pattern outlined in Table 1, in
date, moderating effects of genetic variability have rarely been studied. aid the comparability of different studies.

11
 Table 1
Overview on studies measuring the effects of acute stress on executive functioning: Predictors, markers, cognitive tasks, and the direction of the stress effect. Note: the classification of cognitive load (+ = low load task; ++
+ = high load task) is an arbitrary classification made by the authors. Abbreviations: SECPT = Socially Evaluated Cold Pressor Test; TSST = Trier social stress test; CPT = Cold Pressor Test; ANS = autonomic nervous system;
BP = blood pressure; HR = heart rate; sAA = salivary alpha amylase; SCL = skin conductance level; EEG = electroencephalography; fNIRS = functional near-infrared spectroscopy, fMRI = functional magnetic resonance imaging.
study stress paradigm cortisol ANS subjective stress other participants‘ sex cognitive load type of EF (task) effects on performance (notes)
markers perception biomarkers (+, ++, +++)
T. Plieger and M. Reuter

Beste et al. (2013) SECPT x x (BP, HR) x – male ++ Shifting Improved

(dual task paradigm; tone &
letter)
Chajut and Algom Stress induced by demanding – – x – male and female ++ Inhibition Improved
(2003) tasks (Stroop task)
[delayed picture recall]
Cornelisse et al. TSST x x (sAA, HR, x – male and female ++ Working Memory [& long term Improved
(2011) SCL) +++ memory] (only 2-back in males)
(n-back task; 2, 3)
Dierolf et al. (2017) SECPT x – – EEG male ++ Inhibition No effect
(go/ no-go task) (effects on response inhibition related
components N2 and P3; frontal &
frontocentral)
Dierolf et al. (2018) TSST x – x EEG male ++ Inhibition Improved
(go/ no-go task) (fewer errors in No-Go trials; effects on
response inhibition related components N2
and P3; frontal & frontocentral)
Duncko et al. (2009) CPT x x (HR) – – male and female ++ Working Memory Improved RTs; Impaired accuracy (note: no
(Sternberg item recognition task) effects of stress on cortisol)
Edwards, Edwards Evaluative stress (Ego-threat – – x – male and female ++ Shifting Altered efficiency in low load tasks
et al. (2015) by negative task feedback) (Wisconsin card sorting test) (imparied in stressed individuals with high
trait anxiety; improved in individuals with low

12
anxiety)
Edwards, Moore et al. Counting task (second half of – – x – male and female ++, Working Memory & Shifting Altered efficiency in low load tasks
(2015) TSST) +++ (Operation span/ dual task (impaired in stressed individuals with high
paradigm; Sternberg item trait anxiety; improved in individuals with low
recognition task & auditive anxiety)
oddball-task)
Elzinga and Roelofs TSST x X (HR, BP) x – male and female ++, Working Memory Impaired
(2005) +++ (Digit span; forward &
backwards; 3–8 digits)
Gabrys et al. (2019) TSST x – x – male and female ++ Shifting Improved
(Wisconsin card sorting test)
Gärtner et al. (2014) Negative video clips x – x EEG male ++, Working Memory Impaired
+++ (n-back task; 0–3) (only in high-load condition)
Goldfarb et al. (2016) CPT x – x – male and female ++ Working Memory & Shifting No effects on RTs;
(listening span task/ DMS task) Impaired accuracy
(only in task switching in cortisol responders)
Hood et al. (2015) CPT (at the forehead) x – – – male and female ++, Working Memory Impaired
+++ (Letter-number-sequencing test & (only in cortisol responders with high state
digit span; backwards) anxiety)
Kalia et al. (2018) CPT – – x fNIRS male and female ++ Shifting Impaired
(Wisconsin card sorting test) (only in male participants)
Luettgau et al. (2018) TSST x – x fMRI male ++ Working Memory No effect
(n-back task; 2) (effect on WM-related activation of the dlPFC)
Marko and Riecansky TSST variant (simultaneous – x (SCL, HR) x – male and female ++ Shifting & Working Memory [& Impaired WM; Impaired Shifting
(2018) assessment of cognitive Verbal fluency) (mediated by sympathetic arousal)
performance) (remote associates test/
operation span task)
[semantic fluency task]
(continued on next page)
Neurobiology of Learning and Memory 173 (2020) 107254
 Table 1 (continued)

study stress paradigm cortisol ANS subjective stress other participants‘ sex cognitive load type of EF (task) effects on performance (notes)
markers perception biomarkers (+, ++, +++)

Oei et al. (2006) TSST x x (BP, HR) – – male ++ Working Memory [& memory Impaired
retrieval] (only in high-load condition)
T. Plieger and M. Reuter

(Sternberg item recognition task)

[Wechsler Memory Scale-
Logical Memory]
Olver et al. (2015) TSST x x (BP, HR) x – male and female + Working Memory & Selective Impaired Selective Attention;
++ Attention [& verbal memory] Impaired WM
(simple reaction time task/
spatial working memory task)
[Hopkins verbal learning task]

Plessow et al. (2011) TSST x x (sAA) x – male and female + Selective Attention (Simon No effects
task) (hints toward impaired flexibility)
Plessow, Kiesel et al. TSST x x (sAA) x – male and female ++ Shifting Impaired
(2012) (dual task paradigm)
Plessow, Schade et al. TSST x x (sAA) x – male and female ++ Shifting Impaired
(2012) (task-switching paradigm)
Plieger et al. (2017b) SECPT x – x genetics male + Selective Attention & Improved Selective Attention;
+++ Reasoning No effects on Reasoning
(FAIR-2;
IST-2000R matrices/ figures
tasks)
Porcelli et al. (2008) CPT x – – – male and female ++ Working memory No effects
(Sternberg item recognition task)
Qin et al. (2009) Negative video clips x X (HR) x fMRI, (eye- female ++ Working memory No effect

13
tracking) (n-back task; 2) (effect on WM-related activation of the dlPFC;
note: no effects of stress on cortisol)
Sänger et al. (2014) SECPT x x (sAA) x EEG male ++ Selective Attention (change Impaired
detection task)
Schoofs et al. (2008) TSST x x (sAA) x – male ++ Working Memory Impaired
+++ (n-back task; 2, 3) (low-load and high-load condition)
Schoofs, Wolf, and CPT x – x male ++ Working Memory Impaired
Smeets (2009) (operation span & digit span; (no effects in forward digit span)
forward/backwards)
Schoofs et al. (2013) TSST x x (sAA) x – male and female ++ Working Memory Improved in men;
(n-back task; 2) Imapired in women
Schwabe, Höffken SECPT x X (BP) x – male and female ++ Inhibition Improved
et al. (2013) (stop-signal task)
Steinhauser et al. IQ test with ego threat and – – x – male and female ++ Shifting No effect
(2007) time pressure (task-switching paradigm) (trend toward impairment)
Neurobiology of Learning and Memory 173 (2020) 107254
T. Plieger and M. Reuter Neurobiology of Learning and Memory 173 (2020) 107254

Fig. 3. This figure shows a schematic asso-

ciation between stress level and cognitive
performance dependent on cognitive load
(red: low load task; blue: high load task) and
the influence of additional moderating ef-
fects (dotted lines; e.g. individual char-
acteristics). The optimal arousal level
should be higher for low-demand cognitive
tasks, such as selective attention. In con-
trast, the best performance for high-load
tasks should be achieved in states of lower
arousal. Furthermore, there are effects of
personal characteristics such as stress re-
activity, personality, and genetic make-up
which lead to a shift towards more- or less-
stress sensitivity in terms of cognitive ca-
pacity.

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