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.