University of Groningen
Motivation, reward and stress: individual difference and neural basis
Xin, Yuanyuan
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10.33612/diss.143843592
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Publication date: 2020
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Xin, Y. (2020). Motivation, reward and stress: individual difference and neural basis. University of Groningen. https://doi.org/10.33612/diss.143843592
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CHAPTER 1
Stress is ubiquitous in our daily life and varies across intensity and duration. Some stressors are easily controlled for most people, whereas others, such as a presentation, an exam, or an interview can cause high stress levels. Some stressful events can be so overwhelming that they are perceived as traumatic, putting body and mind in a state of shock. Such severe cases of stressful experiences can cause major stress disorders like posttraumatic stress disorder (PTSD). Yet other stressors seem not very obvious and influence people unconsciously, like the global economic recession, hegemonism, and in the current pandemic, some of us may be seeking information updates about the coronavirus and the death rates associated with COVID-19 on and on at irregular intervals during the day, causing further stress.
Human beings usually have an appropriate capability to deal with stress and can even become more resilient after having successfully handled a highly stressful situation which may be the evolutional meaning of stress. However, our adaptive capability lies within a certain range, limited by our physiological basis and cognitive resources. If the intensity of an encountered stressor exceeds one’s maximum regulatory ability, for example when being exposed to early life trauma, a traffic accident or a natural catastrophe, people can collapse or develop stress-related illnesses. Compared to traumatic experiences, it happens more often in life that repeated exposure to mild and moderate stressors without sufficient recovery accumulates over a certain period of time, increasing one’s physiological and psychological load. Evidence has amounted showing that chronic stress is associated with conditions such as generalized anxiety disorder, depression, addiction and eating disorders. While stress does not cause disease directly, repeated exposure to stress without appropriate recovery can weaken the immune system and increase the risk to develop diseases. This is also the case for psychiatric disorders such as anxiety disorders and depression. Therefore, it is important to understand effects of stress, the underlying neurobiology and psychological mechanisms, and possible implications for management and recovery.
1 What does stress mean for the body?
When researchers say they are working on ‘stress’, it is not easy for others to know what they are specifically investigating: feelings like anxiety, fear, being depressed, or the reality of too much work, too many exams? Although the term
‘stress’ has been used widely in both academic and real word, it is not a well-defined term. In fact, studies in the field of stress are amounting rapidly, but the definition of stress is still under debate and a theoretical foundation is lacking. Here, a clarification of stress-related terminology and its development over time may assist in understanding stress.
The very first study related to stress may go back to Claude Bernard (An introduction to the study of experimental medicine, 1865). He first defined the term ‘milieu interieur’ (French), which refers to the internal environment of the body. He had proposed that the maintenance of life critically depends on keeping one’s internal milieu constant in the face of a changing environment. Based on Bernard’s work, Cannon coined the concept ‘homeostasis’ (Cannon, 1932). Cannon described ‘homeostasis’ as the condition of perfectly balanced body chemistry and indicated that the body works constantly to maintain homeostasis. Notably, Cannon also came up with the fight-or-flight response model as the first acute stress response theory. This early stage in stress studies emphasized on the importance of internal balance.
Subsequently, Selye (1936) formulated the ‘general adaptation syndrome’ representing a generalized effort of the organism to adapt itself to new conditions. Then he provided the first definition of stress as “the nonspecific neuroendocrine response of the body” (Selye, 1950) and used the term “stress” to represent the effects of anything that seriously threatens homeostasis (Selye, 1956). Selye’s definition of stress thus emphasized how the individual reacts to stressors. Of note, he also discovered the hypothalamus-pituitary-immune axis, the most important structure for physiological stress responses. A further term, allostasis, is sometimes used in the context of stress in some studies. Allostasis was first referred to as ‘achieving stability though changes’ (Sterling, P., & Eyer 1988), and recently re-defined as ‘a brain-centered, predictive mode of physiological regulation’ which requires homeostasis as its complement (Schulkin and Sterling 2019). Compared to homeostasis, allostasis was designed as a more broad and complex concept, emphasizing that the internal milieu varies to meet perceived and anticipated demands; and additionally pointing to the role of brain in achieving variation (Sterling, P., & Eyer 1988). Based on the concept of allostasis, McEwen formulated the item ‘allostatic load’ to address the long-term effect of the physiologic response to stress (McEwen and Stellar 1993), such as wear and tear from chronic overactivity or underactivity of the allostatic system (McEwen 1998).
Some other important perspectives about the nature of stress are noteworthy in recent years. Koolhaas et al., (2011) demonstrated that situations like exercise, appetitive or sexual stimuli exert the same physiological and neuroendocrine activity as responses induced by stressors. To distinguish stressors from situations/stimuli with similar biological responses, they emphasized the importance of considering the cognitive and perceptual aspects of stress in addition to the behavioral and physiological responses. Specifically, they argued that stress terminology should emphasize uncontrollability (represented by a delayed recovery of the response and the presence of an adrenaline response) and/or unpredictability of stimuli (characterized by the absence of an anticipatory response) (Koolhaas et al., 2011). Furthermore, Peters and colleagues took the concept of stress into a novel perspective from an information-theory approach based on the ‘free energy principle’, defining stress as “the individual state of uncertainty about what needs to be done to safeguard physical, mental or social well-being” (Peters et al. 2017). In this viewpoint, stress basically originates from uncertainty, and the stress response seems like a self-organizing process of the brain by minimizing the entropy and diminishing the uncertainty. Similarly, Trapp et al. (2018) proposed that stress can be conceptualized as a cumulative state of prediction errors as the encoding of an ongoing acute stress is characterized by continuous unpredictability. In addition, Schulkin and Sterling (2019) also re-explained the term allostasis with ‘brain-centered, predictive model’, in which the brain predicts what is likely to be needed and encourages the organism to learn effective regulatory behaviors (Schulkin and Sterling 2019). These three points provide new interesting perspectives from information theory and computation science and may stimulate novel methodological approaches for research on stress.
In summary, it is essential to know the origin and development of stress research, which can tell us why and how we should study it in practice. The current terminology in the field of stress research mainly includes stress, stressor, homeostasis, allostasis and allostatic load. Briefly, it may be concluded that mismatch, uncertainty, prediction error or entropy increase is part of the nature of stress, and the stress response is a dynamic balance-seeking state in body and mind. Figure 1 shows the etiology and theory related to stress. In this thesis, our studies are based on laboratory stress induction, which is mild to moderate in intensity and short in time, we used the term of ‘acute stress’ to refer to the state of the organism and use ‘stressor’ as the external cause.
Figure 1. A list of stress-related etiology and theory by time.
2 Multi-dimensional mechanism of the acute stress response
Being a dynamic process, the stress response comprises a multilevel neurobiological mechanism, including a peripheral cardiovascular response by the autonomic nervous system (ANS) and the hormone response by the hypothalamus-pituitary-adrenal (HPA) axis. Moreover, neuroimaging research has begun to shed light on the neural activity during an acute stress response. 2.1 Cognitive response to acute stress
When something unpredictable and/or uncontrollable happens or will happen soon, it will first trigger an immediate alarm, resulting in increased arousal, vigilance and attention (Qi and Gao 2020). Then, individuals appraise the stressors/anticipated stressors by searching similar experiences in memory and appraise the match between demands and their capability, all of which is
aimed at finding out what the situation is and resolve it as soon as they can. The alerted state in attention keeps on until the stressor has disappeared or been dealt with, and covaries with stress intensity. During the response, feelings of excitement (arousal) and emotions like anxiety, worry and fear may occur (Balderston et al. 2017).
2.2 Cardiovascular response to acute stress
Acute stress will trigger a cardiovascular response, resulting in heart rate (HR) increase by a hyperactivity of the sympathetic nervous system (SNS); and a decreased heart rate variability (HRV) for a autonomic balance between the SNS and the parasympathetic nervous system (PNS) activation (for a review, Castaldo et al. 2015). Cardiovascular responses can be measured throughout stress, but diminish rapidly when the challenge is eliminated. Notably, these cardiovascular reactions are not specific to stress as other activities like exercise or sexual stimulation trigger similar cardiovascular responses.
2.3 Hormone and neurotransmitter response to acute stress
Cortisol, the ‘stress hormone’ (or ‘preparation hormone’), is the final hormone of the HPA axis response to acute stress. In response to stress, the paraventricular nucleus (PVN) of the hypothalamus first releases corticotropin-releasing factor/hormone (CRF/CRH) and arginine vasopressin (AVP) to the pituitary gland, which in turn stimulates the secretion of adrenocorticotropic hormone (ACTH), which then induces glucocorticoid synthesis and release from the adrenal glands. The main glucocorticoid is cortisol in humans and corticosterone in animals. When the cortisol concentration is high, a negative feedback is sent to the HPA axis to decrease the secretion of ACTH and cortisol (see Figure 2). The functions of cortisol vary widely, from mobilizing the body’s energy to resolve the current stressor (Munck et al. 1984), enhancing the immune function to protect the self (Dhabhar 2014) to regulating the HPA axis back to normal functioning. Compared to the cardiovascular response to stress, increased cortisol is a slower but more specific biomarker of the body’s stress response.
Most studies have focused on cortisol as an indicator of acute stress reactivity. Although this is a valid approach, acute stress-related hormone and neurotransmitter activity is much more complex. In addition to cortisol, other hormones or neurotransmitters (e.g., norepinephrine (NE), dopamine - please see chapter 1.4.2 below, and CRF beyond HPA responses to acute stress in the
brain), and growth factors like brain‐derived neurotrophic factor (BDNF) were also observed from studies in rodents, though such studies are still sparse in humans. Furthermore, interactions between different neurotransmitters also influence acute stress responses, for example, other neurons releasing serotonin (5-HT), NE, g-aminobutyric acid (GABA), or endogenous opioids can also regulate HPA function, as shown in Figure 2. Therefore, a broad perspective of how acute stress affects neurotransmitters in the brain and the connection to behavior should be kept in mind.
2.4 Individual brain regions involved in acute stress
As the acute stress response is a dynamic process, which may trigger sensorimotor activity, emotion, reward and valuation within a short period of time, its underlying neural mechanism is also complex. A wide range of brain regions involving the limbic forebrain, hypothalamus and brainstem have been found to coordinate the stress response dynamically (Ulrich-Lai and Herman 2009). Activity in insula and amygdala is enhanced during stress, which may be related to their role in threat detection and vigilance regulation (Gianaros et al. 2008; Henckens et al. 2010; van Marle et al. 2009). The amygdala is of relevance too: individual threat-related amygdala reactivity predicts psychological vulnerability to future life stress (Swartz et al. 2015).Ventral and medial regions of the prefrontal cortex (PFC) are active during stress (van Oort et al. 2017), which may be related to stress appraisal and HPA axis regulation. The hippocampus generally exhibits less activity during acute stress (Pruessner et al. 2007; Dedovic et al. 2009). Results regarding dorsal PFC response during acute stress are inconsistent (Rosenbaum et al. 2017; van Oort et al. 2017), although interactions between stress and working memory showed that stress weakens PFC functioning (Arnsten 2009, 2016). Some studies also showed dopamine fluctuation in reward regions of nucleus accumbens (NAcc) during acute stress (Pascucci et al. 2007; Cabib and Puglisi-Allegra 2012), showing that NAcc dopamine increases first, followed by a decrease. The brain’s response to acute stress may vary across stress types, e.g., physical and psychological, reactive and anticipatory stress, time, and intensity.
2.5 Large scale brain network activity underlying acute stress
The involvement of large-scale brain networks under acute stress has been of increasing interest over the past decade. A systematic review on functional magnetic resonance imaging (fMRI) studies concluded that the acute stress response is consistently associated with both increased activity and connectivity in the salience network (SN) (e.g., thalamus, insula, dorsal anterior cingulate) and surprisingly also with increased activity in the default mode network (DMN) (e.g., medial prefrontal cortex (mPFC), hippocampus), whereas no consistent changes in the central executive network (ECN) were noted (van Oort et al. 2017), see Figure 3. The result was partly supported by a resting-state functional connectivity study with a big sample size (335 subjects), which showed that stress-induced cortisol increase was associated with increased connectivity with SN, decreased coupling within DMN, and decreased coupling between DMN to
other regions (Zhang 2019). Token together, the brain shifts into a more vigilant state during acute stress, increasing activity and connectivity in SN, but ECN and DMN activity during acute stress need further investigation.
Figure 3. Triple network model of acute stress (van Oort et al. 2017)
3 Individual differences: from adaptive to excessive acute
stress responses
A normal response to stress is the manifest that an individual is able to meet both external and internal demands flexibly, whereas exaggerated or blunted responses to stress may be a signal of allostatic overload or vulnerability to psychosomatic diseases (Lovallo 2012). However, even response of one person to the same stressor can vary from time to time. Something that is perceived as a major trouble by some people might be regarded as a minor bother by others. Therefore, a better understanding of individual differences regarding vulnerability and resilience to stress is very useful and practical in real life such as in selection of military personnel. Below, factors related to different stress responses are introduced separately. Furthermore, Chapter 2and Chapter 3 explored individual factors in altered stress responses from the aspects of personality and environment separately.
3.1 Sex and age
Sex differences in acute stress response have been found consistently over the past decades. For example, in a meta-analysis with a large sample (1350 subjects), men were observed to have higher cortisol values following acute stress compared to women (Liu et al. 2017). Age is another possible factor in the stress response as it is related to the development of brain function and structure. There is evidence that younger adults may have greater heart rate increases in response to acute stress than older adults, but results of HPA axis response are mixed (Kudielka et al. 2004; Steptoe et al. 2005; Almela et al. 2011). Although there are differences in stress responsivity regarding sex and age in healthy people, the response in each group is still within a normal range of the whole stress distribution. However, altered stress responses in disease-prone or ill people may be maladaptive.
3.2 Personality
Personality reflects a stable disposition involving specific biological and psychological mechanisms. A number of personality traits were found associated with altered HPA axis responses to stress, including depressive symptoms, trait anxiety (Fiksdal et al. 2019), the big five personality traits (Bibbey et al. 2013), mindset (Crum et al. 2013), mindfulness trait (Manigault et al. 2018), and perfectionism (Wirtz et al. 2007). Although results are not consistent, traits of suboptimal emotion regulation generally contributed to a more unreactive cortisol response and more negative affect experienced under acute stress. The reason behind the deviation from an adaptive acute response may be altered biological mechanisms underlying deviant levels of personality traits, for example, negative affect −a common trait in depression, anxiety, and anger − was related with impairments in cardiac autonomic function in a large sample using structural equation modeling (Bleil et al. 2008).
3.3 Stressful life events
A negative association between total number of life events and cardiovascular responses was shown by a cohort study (Phillips et al. 2005), and the same relationship was found for cortisol responses to acute stress and lifetime stress exposure (Lam et al. 2019). Similarly, subjectively perceived levels of chronic stress/self-reported distress in the last two weeks was negatively associated with cortisol responses (Brooks and Robles 2009; Pruessner et al. 2013). Moreover, individuals with a history of early-life adverse events still exert
blunted cortisol responses to social stress in adulthood (for a review, Bunea et al. 2017). As individuals who frequently experienced negative life events are at greatest risk for disease, blunted stress reactivity may present a marker of physical allostasis load.
3.4 Brain disorders
Mental disorders including major depression disorder (Zorn et al. 2017; Kamradt et al. 2018; Buske-Kirschbaum et al. 2019), attention deficit/hyperactive disorder (ADHD) (for a review, Druzhkova et al. 2019), substance dependence (Stephens and Wand 2012), and posttraumatic stress disorder (Sack et al. 2004) were found to be associated with altered acute stress responses, but results are not unidirectional. For example, results from major depression disorders differ in direction between onset depression and recurrent depression; in ADHD, an overall 0 effect was observed between symptoms and HPA stress responses, but with significant heterogeneity in the meta-analyses (for a review, Druzhkova et al. 2019).
3.5 Cognitive and perceptive sensitivity
In addition, further traits regarding perception and cognition sensitivity were also reported to affect individuals’ acute stress responses. For instance, attention bias toward salient information predicted HPA axis activity to acute psychosocial stress (Ellenbogen et al. 2010, Pilgrim et al. 2010); and the amplitude of the error positivity (Pe) significantly predicted both cardiovascular and HPA axis response in the TSST (Wu et al. 2017). Thus, differences in sensory and cognitive sensitivity may constitute a further factor involved in individual responses to acute. However, further studies are needed to gain a better understanding of the influence of these additional factors on stress perception. 3.6 Other social factors
Some social factors have buffering /modulating roles in the acute stress response, including education (Fiocco et al. 2007), social support (Roy et al. 1998; Ditzen et al. 2008), adult attachment (Ditzen et al. 2008), and positive couple interaction (Ditzen et al. 2007).
In summary, individual differences in acute stress reactivity have been found to be associated with a diversity of factors, such as personality aspects, mental disorders and negative life experiences, but little is currently known as to how each of these factors affect one’s individual stress reactivity.
4 Stress and reward-motivation
As comorbid symptoms of anhedonia and acute stress dysregulation are found in some stress triggered disorders like PTSD, depression, eating disorder, etc., more and more attention is being payed to the stress-reward link. For example, one study investigated how mesoaccumbens dopamine, the most important neurotransmitter in reward and motivation, was involved in the stress response (Cabib and Puglisi-Allegra 2012). The relationship between stress and reward processing is introduced below.
4.1 Hypoactivation of reward-motivation system in stress-related disorders Chronic life stress exposure, depression, ADHD, PTSD and substance dependence, factors as described above associated with abnormal acute stress responsivity, are also related to reward and motivation deficiency. Studies in animals and humans have elucidated that the translation from prolonged stress to anhedonia (diminished interest or pleasure in all, or almost all, activities) involves a complex alteration of neural and endocrine mechanisms. At the neural level, chronic stress has a negative impact on regions implicated in reward valuation, including impaired hippocampal structure (Gianaros et al. 2007), causing architectural changes in PFC dendrites (Arnsten 2009) and giving rise to alterations in mPFC function (Stanton et al. 2019). At the molecular signaling level, chronic stress-induced altered glucocorticoid and inflammation responses may disrupt reward processing by interfering with dopamine synthesis (Cabib and Puglisi-Allegra 2012; Stanton et al. 2019; Douma and de Kloet 2020). 4.2 Acute stress and reward-motivation system
Compared to the stress - anhedonia link in neurobiology implicated in some neuropsychiatric disorders, the relationship between acute stress and the brain’s reward system is less clear. Moreover, the association of acute stress to the reward system is likely to be different from the relationship between chronic stress and reward.
4.2.1 Dopamine release in mesolimbic system to acute stress
Dopamine is the most critical neuromodulator playing a role in reward, learning and motivation, especially in the reward prediction error (Schultz et al. 1997; Schultz and Dickinson 2000). Studies found that dopamine activity in the brain, especially in the mesolimbic system, is altered in acute stress situations.
For example, a study in rats showed that increasing CRF/CRH release by the HPA response to an acute stressor enabled increased dopamine release in the NAcc (Pascucci et al. 2007; Lemos et al. 2012). Evidence from human studies is similar, with one study showing that the tonic level of dopamine in the NAcc was initially increased by novel uncontrollable stressful conditions (Cabib and Puglisi-Allegra 2012), and another study reporting that coping with stress increased ventral tegmental area (VTA) dopamine excitability (Douma and de Kloet 2020).
The short, immediate increase of dopamine in the NAcc may indicate an active coping with stressful situations, which is coordinated with energy mobilization by stress-induced glucocorticoid activity to enable increased short-term control of behavior (Cabib and Puglisi-Allegra 2012; Fiore et al. 2015). After a rapid increase NACC dopamine levels, they return back to baseline within about one hour and then continue to decrease (Pascucci et al. 2007). Considering this dynamic release of dopamine, time is likely an important factor for individual differences in one’s response to acute stressors.
4.2.2 Reward-motivation system under acute stress
Acute stress may affect reward and motivation in different ways. At the behavioral level, some studies showed that stress-reactive individuals (responders) have diminished reward sensitivity (lower accuracy in choosing differently rewarded items as well as longer reaction times) in condition of electric shock threats than in neutral control conditions (Bogdan and Pizzagalli 2006; Berghorst et al. 2013). However, some other studies found no significant difference in reaction times to reward between acute stress and neutral conditions (Ossewaarde et al. 2011; Porcelli et al. 2012; Kumar et al. 2014). At the level of neural activity, one study observed that during reward anticipation, acute stress enhanced ventral striatal (VS) activity to incentives (Gorka et al. 2018), but another study found that stress induction resulted in a significant decrease in the mPFC activity without affecting VS response (Ossewaarde et al. 2011). Regarding reward consumption, most studies reported that acute stress decreased reward consumption processing in the brain (Born et al. 2010; Porcelli et al. 2012; Kumar et al. 2014; Oei et al. 2014), but also non-effects were found in two studies (Gorka et al. 2018; Gaillard et al. 2019).
In brief, it is conceivable that chronic stress and stress-induced disorders have a negative impact on the reward-motivation system, whereas the interaction between acute stress and the reward-motivation system may vary
across the different stage of one’s acute stress response as well as across the different components of reward processing.
5 Acute stress and cognition
Integrating studies regarding the effect of acute stress on cognition, we may conclude that acute stress has a negative influence on higher-order cognitive tasks including working memory (Al’Absi et al. 2002; Shields et al. 2016), goal-directed decision making (Maier et al. 2015) and cognitive flexibility such as reversal learning (Lind et al. 2016) and prospective planning (Margittai et al. 2016; Brown et al. 2020). On the other hand, acute stress may enhance sensory information processing (van Marle et al. 2009; Schwabe and Wolf 2010) and automatic, habitual and intuitive behaviors (Schwabe et al. 2010; Otto et al. 2013; Margittai et al. 2016) due to an increased alertness and a decreased higher-order cognitive capacity. These results are consistent with the observation of increased activity within the salience network in response to acute stress.
6 Overview of the present thesis
Stress is linked to vulnerability for developing psychiatric disorders, highlighting the importance of research into a better understanding of individual differences in stress responses. Recently, there has been an increasing interest in the neural mechanisms underlying the role of stress in mental illness risk, in which abnormal reward and motivation processing might play an important part (Carroll et al. 2017). The present thesis focuses on these two aspects: vulnerability and protective factors related to acute stress responses; and the possible neural mechanisms underlying altered reward processing and motivation during stress.
In Chapter 2, we examined the association between the Big Five personality traits and a comprehensive measure of stress responses to TSST.
In Chapter 3, we investigated how the frequency of recent life stress was associated with stress responses and the role of executive control within this context.
of brain activation, which are measured using cognitive tasks, to elucidate how acute stress influences reward processing in brain, including both reward anticipation and reward consumption.
In Chapter 5, we explored the relationship between trait motivation and reward-time decision making and investigated the underlying neural mechanisms using resting state functional connectivity.
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