The HPA and SAM axis mediate the impairment of creativity under
stress
Abstract: With the ever-changing social environment, individual
creativity is facing a severe challenge induced by stress. However,
little is known about the
physiological mechanisms by which acute stress affects creative
cognitive processing. The current study explored the effects of
neuroendocrine response on creativity under stress and its underlying
cognitive flexibility mechanisms. The Enzyme-Linked Immuno Sorbent Assay
was used to assess salivary cortisol, which acted as a marker of
stress-induced activation of the hypothalamic-pituitary-adrenal (HPA)
axis. Eye blink rate (EBR) and pupil diameter were measured as
respective indicators of dopamine and noradrenaline released by
activation of the sympathetic-adrenal medullary (SAM) axis. The
Wisconsin Card Task (WCST) measured cognitive flexibility, while the
Alternative Uses Task (AUT) and the Remote Association Task (RAT)
measured separately divergent and convergent thinking in creativity.
Results showed higher cortisol increments following acute stress
induction in the stress group compared to the control group. Ocular
results showed that the stress manipulation significantly increased
EBR and pupil diameter compared to
controls, reflecting increased SAM activity. Further analysis revealed
that stress-released cortisol impaired the originality component of the
AUT by increasing perspective errors of the WCST. Serial mediation
analyses showed that both EBR and pupil diameter were also associated
with increased perspective errors leading to poor originality on the
AUT. These findings confirm that physiological arousal under stress can
impair divergent thinking through the regulation of different
neuroendocrine pathways, in which the deterioration of flexible
switching plays an important mediating role.
Keywords: acute stress, hormones, neuroendocrine, cognitive
flexibility, creativity1. Introduction
Creativity, as a unique gift of human
beings, has become the core competence and key talent in the 21st
century (Ananiadou & Claro, 2009; Heilman, 2016). Creativity is defined
as the ability to generate novel output in an appropriately useful
manner (Sternberg & Lubart, 1996). Nowadays, with the advent of the
VUCA (Volatile, Uncertain, Complex, and Ambiguous) era, stress has
become a regular part of life and work that people have to face.
Creative problem-solving under stress seems to be the norm for
organizations and individuals. In recent years, researchers have made
some explorations into the relationship between stress and creativity
(Alexander et al., 2007; Chrousos,
2009; Ulrich-Lai & Herman, 2009; Villarejo et al., 2012).
However, the physiological mechanisms
by which stress affects creativity processes remain incompletely
revealed.
Upregulated activity of the
hypothalamic-pituitary-adrenal (HPA) axis and
sympathetic-adrenal-medullary (SAM) axis under acute stress is a central
effect of such stress (Chrousos, 2009; Ulrich-Lai & Herman, 2009).
Under stressful situations, the SAM pathway immediately stimulates the
amygdala in the central nervous system and rapidly activates the adrenal
medulla via the hypothalamus. This causes catecholamines (i.e., dopamine
and norepinephrine) to be released, which induces sympathetic excitement
in the peripheral nervous system
(Arnsten, 2009). It is manifested by an increase in heart rate, blood
pressure, skin electrical levels, and salivary alpha-amylase (sAA)
concentration, which speeds metabolic breakdown and saves energy for the
body’s response to stressful stimuli (Villarejo et al., 2012). At the
same time, activation of the HPA axis results in the release of
corticotrophin-releasing hormone (CRH) and vasopressin from the
hypothalamus. These neuropeptides stimulate the release of the
adrenocorticotropic hormone (ACTH) in the anterior pituitary (Pariante
& Lightman, 2008). ACTH activates the adrenal cortex to release
glucocorticoid hormones, which help the body restore homeostasis by
mobilizing the body’s readily available resources (Allen et al., 2014).
Therefore, catecholamines and glucocorticoids are valid biochemical
indicators to assess the stress response (Fogelman & Canli, 2018;
Walker et al, 2017). They can influence creative activities that require
divergent thinking, attention and memory by directly or indirectly
regulating the central nervous system (Sanchez-Ruiz et al, 2015; Shansky
& Lipps, 2013).
Evidence has demonstrated that the cortisol generated by HPA axis
activation is critical to behavioral and neuroendocrinological
adaptations to acute stress (Yeh et al., 2015). However, to our
knowledge, no research has examined the influence of stress-induced
cortisol levels on creative processing. Cortisol has the ability to
cross the blood-brain barrier and enter the brain, where it binds to
glucocorticoid receptors in the hippocampus, prefrontal cortex (PFC) and
amygdala (Lovallo & Buchanan, 2016). These brain regions play important
roles in executive function and are associated with fundamental
executive processes such as working memory, flexibility, cognitive
function, and the processing of novelty (Blackford et al., 2010;
D’Esposito & Postle, 2015; Plessow et al., 2011). Accordingly, the
relationship between stress-induced cortisol and creativity may be
established through some cerebral mechanisms and mediated by executive
functions.
Cognitive flexibility, as a stress-sensitive cognitive function, has a
close relationship with creativity (Chakravarty, 2010; Heilman, 2016).
Plessow (2011) investigated the effects of acute psychosocial stress on
dynamic control adjustments, using the Trier Social Stress Test (TSST)
to induce stress responses and a selective attention task to measure
individual cognitive flexibility. The results revealed that stressed
participants showed tonically increased goal shielding at the expense of
decreased cognitive flexibility. Moreover, the stress effects on
cognitive functions were not presented immediately after the stress
experience but developed gradually over time, paralleling the time
course of the HPA stress response. In the present research, we predicted
that the altered cognitive flexibility resulting from HPA axis
activation is an essential mediation mechanism for how stress affects
creativity. In the reported study, salivary cortisol was used as an
indicator of HPA under stress.
Dopamine (DA) and norepinephrine (NE) are SAM axis indicators closely
associated with creativity.
Increased central dopaminergic
activity under stress leads to a high release of DA (Abercrombie et al.,
1989; Neri et al., 1995; Thierry et al., 1976). Multiple dopaminergic
pathways could affect excitatory signaling within the
frontal-hippocampal network, involving a range of cognitive functions
involving creative processing (Dave et al., 2021). We predicted that DA
release may play an important role in the effect of stress on
creativity. Neuropharmacological research has shown that DA may improve
creative performance. For example, striatal DA seems to be associated
with specific dimensions of divergent thinking performance, especially
with the categorical diversity (flexibility) of ideas (Dodds et al.,
2008). Moreover, novel stimuli have been shown directly to influence DA
release in the brain, which promotes cognitive flexibility and
facilitates the onset of the epiphany phase of creative tasks (Wingo et
al., 2016; Zhang et al., 2020). However, some studies have indicated
that DA secretion can impair creativity. High-intensity stress leads to
excessive DA release in the prefrontal lobe, showing attentional
rigidity and inflexibility (Cools & D’Esposito, 2011), which may be
detrimental to creative performance (Boot et al., 2017).
We assumed that stress can not only affect individual creativity
directly by altering brain activity and regulating the DA levels, but
that it can also affect individual creative performance by altering
cognitive flexibility. Direct measurements of DA are mostly performed in
animal experiments via blood measurements, which are used less for
humans in the laboratory. Spontaneous eye blink rate (EBR) has been
verified by numerous findings to be a reliable biomarker of DA in the
central nervous system. According to Kaminer et al. (2011), DA inhibits
the trigeminal complex via effects on the nucleus raphe magnus,
increasing spontaneous blinking. Moreover, clinical observations in
patients with DA-related dysfunctions, such as schizophrenics. Indicate
that they have both elevated EBRs (Freed, 1980) and elevated striatal DA
uptake. Furthermore, pharmacological research in nonhuman primates has
demonstrated that the dopaminergic agonists and antagonists,
respectively, increase and reduce EBRs (Kleven & Koek, 1996). Decades
of research have shown that spontaneous EBR is a well-established
clinical marker (Shukla, 1985; Jongkees & Colzato, 2016) thought to
index striatal DA production, with higher EBR predicting higher DA
function. In the present research, spontaneous EBR was employed as a
reliable method of assessing DA function.
Norepinephrine (NE) is one of the brain’s most important
neurotransmitters and has a critical role in modulating the brain’s
arousal (Heilman, 2016). The locus coeruleus-norepinephrine (LC-NE)
system releases large amounts of NE under stressful conditions. Like DA,
NE plays an important role in how acute stress affects creative
processing. NE increases the brain’s signal-to-noise-ratio, which
enhances attention and reduces intrinsic associative activity (Hasselmo
et al, 1997). In such a state, cognitive flexibility is reduced and
creative performance is impaired (Beversdorf et al., 2002). Thus, acute
stress states could lead to elevated NE levels so as ultimately to
affect creativity by altering cognitive flexibility. However, the
laboratory measurement of NE is still a methodological challenge. In
this regard, pupil diameter as an ocular measure could provide insight
into neuromodulatory activity, which is strongly connected with the
enhanced activity of noradrenergic neurons in the locus coeruleus (de
Rooij et al., 2011; Murphy et al., 2011). A strong correlation between
baseline pupil diameter and tonic locus coeruleus firing rate has been
observed in monkeys during task performance involving 90 min target
detection (Rajkowski et al., 1993). Human experimentation has also
demonstrated that the pupil diameter at rest is relatively large when
individuals are hyperaroused (Unsworth et al., 2019). Moreover, pupil
dilation indicates higher noradrenergic activity and is associated with
enhanced arousal and alertness (Knapen et al., 2016; Pajkossy et al.,
2018). In the current study, pupil diameter was used as an indirect
indicator of noradrenergic activity.
To sum up, the present study aimed to elucidate the cognitive
flexibility mechanism by which acute stress affects creativity from a
neuroendocrine perspective by using enzyme-linked immunosorbent assay
(ELISA) and eye-tracking techniques. The arousal of the HPA axis was
indicated by salivary cortisol concentrations. Eye blink rate and pupil
diameter were used as indicators of DA and NE activity, reflecting the
activation of the SAM axis under acute stress conditions. The stress
condition was manipulated with the Montreal Imaging Stress Task (MIST),
and the corresponding psychological and physiological indexes were
collected to confirm that the acute stress induction was successful.
Measures reflecting the activation of these biological stress systems
alongside the behavioral measures were included in serial mediation
models in order to illuminate the neuroendocrine pathways contributing
to creative degradation under stress. We expected that impaired
creativity under stress results from degraded cognitive flexibility
mediated by HPA and SAM activation.