Risk and Reward Are Processed Differently in Decisions Made Under Stress Author(s): Mara Mather and Nichole R. Lighthall Source: Current Directions in Psychological Science, Vol. 21, No. 1 (FEBRUARY 2012), pp. 36-41 Published by: Sage Publications, Inc. on behalf of Association for Psychological Science Stable URL: https://www.jstor.org/stable/23213118 Accessed: 18-10-2019 22:19 UTC REFERENCES Linked references are available on JSTOR for this article: https://www.jstor.org/stable/23213118?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references. JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org. Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at https://about.jstor.org/terms Sage Publications, Inc., Association for Psychological Science are collaborating with JSTOR to digitize, preserve and extend access to Current Directions in Psychological Science This content downloaded from 205.208.116.24 on Fri, 18 Oct 2019 22:19:23 UTC All use subject to https://about.jstor.org/terms aps WfWiMgSI I A'l'iOQATiON "OS PSYCHOLOGICAL SCIENCE Current Directions in Psychological Science 21(1)36-41 Risk and Reward Are Processed Differently in Decisions Made Under Stress ©The Author(s) 2012 Reprints and permission: sagepub.com/journalsPermissions.nav DOI: 10.1177/0963721411429452 http://cdps.sagepub.com i)SAGE Mara Mather and Nichole R. Lighthall University of Southern California Abstract Years of research have shown that stress influences cognition. Most of this research has focused on how stress affe and the hippocampus. However, stress also affects other regions involved in cognitive and emotional processing, the prefrontal cortex, striatum, and insula. New research examining the impact of stress on decision processes r consistent findings. First, acute stress enhances selection of previously rewarding outcomes but impairs avoidance of negative outcomes, possibly due to stress-induced changes in dopamine in reward-processing brain regions. Secon amplifies gender differences in strategies used during risky decisions, as males take more risk and females take les stress.These gender differences in behavior are associated with differences in activity in the insula and dorsal stria regions involved in computing risk and preparing to take action. Keywords choice, decision making, impulsivity, reward learning, risk taking, stress, valuation, ventral and dorsal striatum The word stress describes experiences that are emotionally or core brain-body feedback loops involved in the stress response physiologically challenging (McEwen, 2007). Stressful expe also are involved in assessing risk and reward (Bechara & riences elicit sympathetic-nervous-system responses and stim Damasio, 2005). As part of this brain-body feedback system, the insula helps represent somatic states and signals the prob ulate the release of stress hormones (e.g., Cortisol in humans; Sapolsky, 2004) that mobilize the body's resources to respond to a challenge. The physiological effects of a stressful experi ence such as making a speech are evident not only during the event, but also in the next hour or so (Dickerson & Kemeny, 2004). When stressors are constantly present or anxiety about potential stressors is high, stress levels may become chroni cally elevated. Beyond the physiological effects of stress, a substantial literature indicates that both acute and chronic ability of aversive outcomes during risky decisions (Clark et al., 2008). Both physical and psychological stress activate the insula, but differently for males and females (Naliboff et al., 2003; Wang et al., 2007). In the following sections, we review recent evidence for two distinct effects of stress. First, stress enhances learning about positive choice outcomes and impairs learning about negative choice outcomes. This effect appears to be similar stress affect cognitive function. across gender and age groups. Second, stress affects decision Until recently, most studies examining stress and cognitionstrategies differently for males and females, with behavior have focused on stress effects on memory; effects on other diverging under stress when decision making involves imme aspects of cognition, including decision making, have receiveddiate risk taking. less attention. However, it is crucial to understand whether and how stress may alter decision making, as important decisions are often made under stress. For example, decisions aboutSeeing STARS: Stress Can Make Rewards finances, health care, and social relationships are frequently Gleam More Brightly accompanied by stress or cause stress. Early work on stress What makes decisions difficult? Often, it is the challenge of and decision making determined that stressors like time pres weighing and integrating positive and negative aspects of sure and noise impaired decision making, resulting in decisiondecision options. Is a higher salary worth a longer commute? making that is hurried, unsystematic, and lacking full consid Is the pleasure of watching your favorite television show eration of options (Janis & Mann, 1977). worth the sacrifice of staying up later to meet an assignment More recent work focuses on how stress influences how people respond to the risks and rewards of decisions. Acute Corresponding Author: stress potentiates dopaminergic reward pathways in the brainMara Mather, University of Southern California, 3715 McClintockAve., (Ungless, Argilli, & Bonci, 2010), which may intensify the Los Angeles, CA 90089 allure of potential gains associated with decision options. TheE-mail: mara.mather@usc.edu This content downloaded from 205.208.116.24 on Fri, 18 Oct 2019 22:19:23 UTC All use subject to https://about.jstor.org/terms Risk and Reward Processing Under Stress 37 deadline? In addition to their about negative immediate outcomes (Fig. 1; impact Lighthall, Gorlick, onSchoeke, cho Frank, & Mather, 2011; Plessow, Goschke, & rewarding and aversive outcomes ofPetzold, a decision can infl future choices through Kirsehbaum, learning. For 2010). In these studies,instance, participants completedreceiv a poor grade on the assignment probabilistic reinforcement-learning might influence task after either future experi allocation decisions. But the encing an pleasure acute stressor or performing of laughing a no-stress control and task. rel during the show might instead make it learning even harder to r The reinforcement task involved probabilistic asso watching future episodes.ciations between visual cues and different types of feedback. We propose that stress alters Using trial anddecision error, participants value learned whichassignmen cues were because stress triggers additional most likely to result in correct reward or incorrect feedback salience and were (ST The STARS model is based asked on to select research the cues that gave positive examining feedback most often. how s affects dopaminergic reward-processing In both studies, stress led to relatively brain better learning regions. from minergic regions and their positive target feedback andstructures—such worse learning from negative feedback.1 as the tum (especially the nucleus The similaraccumbens) pattern in the two studies occurred and despite orbitofr differ types of stress inductions. Lighthall, Gorlick, et al., 2011 cortex—play key roles inentrepresenting reward value (R induced stress before the startacute of the reinforcement-learning Camerer, & Montague, 2008). In rats, stress incre task by having participants their hands in ice water (cold extracellular levels of dopamine inhold the nucleus accum (Abercrombie, Keefe, Difrischia, pressor stress), whereas & Petzold Zigmond, et al. (2010) induced psycho 1989; K & Duffy, 1995), an effectsocial that stress by is making mediated participants anticipate, by then Cortisol give, a (R Pont, Deroche, Le Moal, & Piazza, 1998). Stress also speech and also do difficult mental arithmetic in front of an incr audience. Of additional interest, both studies found that the firing rates in rat midbrain dopamine neurons (Anstro effects of stress on reinforcement learning were similarin for dop Woodward, 2005) and long-term potentiation males and & females. Lighthall et al. also 2003). found similar effects neurons (Saal, Dong, Bonci, Malenka, among older adults. In positron emission tomography (PET) studies, people increased learning fromresearchers positive outcomes under stress injected with a radiotracer The that allows to trac seen in these studies is consistentsuch with the STARS model pro activity of specific neurotransmitters, as dopamine posalincreases that increased dopaminePET from stress should facilitate learnof st riencing painful stressors measures ing reward-associated behaviors (Scott, but not punishment-associated dopamine among healthy young adults Heitzeg, Ko Stohler, & Zubieta, 2006; behaviors. Wood et levels al., In addition Cortisol also 2007). appear to be associated with much Cortisol levels increase impaired avoidance when learning, exposed as Lighthall and to colleagues a psychol found that Cortisol was related to higher rates of erroneously selecting stressor (mental arithmetic) correlates with PET measu striatal dopamine (Pruessner, Champagne, Meaney, & Dag Q Control observed B Stress 2004). It appears that, similar to findings in rats, enhances striatal dopamine in humans. Consistent with idea, stress appears to increase drug craving and often in relapse in drug addicts (Sinha, 2009). Importantly, dopa plays a role in desire for drugs, suggesting that stress increase dopamine levels in drug addicts and thereby am the reward value attached to their drug of choice—an ex of how the STARS effect can have negative consequences We propose that stress enhances reward salience via mo lation of the dopamine system, resulting in reward-bia learning and decision making under stress, a pattern tha benefit or impair decisions, depending on the context. T lowing studies support a STARS account of stress effec option valuation in humans. Choose Avoid Positive Positive Influence of Stress on Learning About Decision Values Fig. I. Proportion of correct choices (choosing positive outcomes versus We often use past experiences in decision making, as previous avoiding negative outcomes) made under stress. Participants were asked choices may carry positive or negative associations. to For makethis repeated choices among options that probabilistically delivered positive or negative feedback (Lighthall, Gorlick, Schoeke, Frank, & Mather, reason, it is important to consider the impact of stress on learn 201 I). If they did this learning task after experiencing an acute stressor, they ing associations between decisions and their outcomes. Recent were better able to later select the option that delivered the most positive behavioral studies with humans suggest that stressfeedback enhances but were less effective at avoiding the option that delivered the most negative feedback. learning about positive outcomes while diminishing learning This content downloaded from 205.208.116.24 on Fri, 18 Oct 2019 22:19:23 UTC All use subject to https://about.jstor.org/terms 38 Mather, negative toward Lighthall feedback risk taking (more pumps per balloon) cues. in pursuit of greater So potentially reward, whereas stress effects were reward opposite for females ance of negative (Fig. 3). As risk taking in stressed options. males did not reach a level previously rewarding of diminishing returns, they were able to earn morebut reward example, food the in nonstressed bling Task (Preston, Buchanan, participant Stansfield, & Bechara, 2007; obtain that occurred also as one than their female counterparts. study, Similarly, gender differences part in stress effects were observed by others using the Iowa Gam rewards; after becomin food van den Bos, Harteveld,(Schwabe & Stoop, 2009), such that men after satiation exposed to a psychological stressor prior to the task selected(Sc suggests card decks that that offered greater stress reward at the cost of higher aff risk participants of losses. Selecting who cards from thesewere risky decks resulted in an worse than lower control earnings overall. In a study with only partici males, administer back was given but not wh ing Cortisol increased choices of risky gambles, especially for Wolf, Markowitsch, Bra gambles with a large probability of losing and a& large possible used did not gain (Putman, distinguish Antypa, Crysovergi, & van der Does, 2010). b learning about losses. Similarly, formerly heroin-addicted male patients made more disadvantageous risky choices after stress than they did before stress, an effect that was blocked by the ^-adrenoceptor antag Gender-Divergence onist propranolol (Zhang et al., 2011). Across the various labo Amplify ratory Gender decision studies, stress enhanced males' performanceDi stress when increased risk taking affects was beneficial but impaired males'lea outcomes similarly for performance when increased risk taking was detrimental, and m vice versa for females. In addition, unlike the STARS effects gender divergence under when people choose outlinedmust earlier, these gender-divergence effects on decision Although lower potential gains but a strategies seem unrelated to learning processes. For instance, (higher potential for studies conducted in our lab, gains gender-by-stress interactions bu participants received poin were similar in initial and final blocks of the games. shown on the computer In a follow-up to Lighthall et al.'s (2009) balloon game sc 2009). The larger athe cold balloon study, participants completed either pressor stress task with each additional pum or a warm-water control task before entering a functional mag and loss earnin netic resonance imaging (fMRI) of scanner and playing an fMRI participants had to choose adapted version of the balloon game (Lighthall, Sakaki, et al., explosion Half of the 2011 participants ). In this adapted version, participants each played for the co about 20 minutes before p ing cold pressor stress bef 11 Control ■ Stress Gender-Divergenc Males Females Stress/Cortisol Fig. 3. Risk taking by males and females after a stressor versus a control Fig. 2. Gender-divergence effect for risk taking under stress.When stress task. or Experiencing an acute stressor before playing a balloon-pumping game Cortisol is low, risk taking is similar for males and females, but when stress or(reward increased as simulated balloons were inflated, but so did risk of a Cortisol increases, risk taking diverges by gender—increasing for males and balloon bursting) increased males' risk-seeking behavior but decreased decreasing for females. females' risk-seeking behavior (Lighthall, Mather, & Gorlick, 2009). This content downloaded from 205.208.116.24 on Fri, 18 Oct 2019 22:19:23 UTC All use subject to https://about.jstor.org/terms Risk and Reward Processing Under Stress 39 ■ Control (/) c ■ Stress § -* same total time, resulting in a variable number of balloons played. This change meant that playing more balloons more quickly was an alternate strategy to earn more money. In this co o 25 co s version of the game, stress did not affect the number of pumps m 15 uti IJ per balloon that participants made (risk taking) but instead affected their decision speed and number of balloons "cashed o i 20 out." The frequency of reward collections (cash outs) during £ -2 in 3 <u ,u the risky-decision task was altered by stress in a gender Z a. c <D E 5 dependent manner (Fig. 4). Gender-by-stress interactions were O) O A 20 0 a) < Males Females also seen in brain activation in the insula, a brain region impli cated in signaling the probability of aversive outcomes and learning about risky outcomes (Clark et al., 2008), and in the putamen (in the dorsal striatum), a brain region thought to Fig. 4. Number of balloons "cashed out" under stress versusintegrate a control sensorimotor, cognitive, motivational, and emotional condition. In this risk task, pumping up simulated balloons yielded rewardsto help select and initiate actions and to help control signals but also increased risk of the balloon bursting, and participants could work habit-based behaviors (Balleine, Delgado, & Hikosaka, 2007; through more balloons by pumping them faster. In the control condition, Balleine & O'Doherty, 2010). Stress increased activity in both males and females completed a similar number of balloons, whereas under stress their strategies diverged. the insula and putamen during the task (compared with a -MNI = -2 Whole-Brain Z = 4.0 o Structural Masked Mask r> Activation □ No Stress □ Stress Male Female L Putamen Activation Male Female L Insula Activation Fig. 5. Interaction between stress, gender, and brain activation. Under stress, the putamen and insula (a) showed significant gender-by-stress interactions (as indicated by regions colored orange) while participants played a decision game to earn money (Lighthall, Sakaki, et al„ 201 I ). Outlines ("masks") of the structurally defined putamen and insula (regions in blue; b) were overlaid on the activation maps to distinguish the activity in these two regions (c). Average brain activation from these two clusters revealed that, under stress, males showed greater activity in the putamen (d) and insula (e) while playing the decision game while females showed the opposite pattern. This content downloaded from 205.208.116.24 on Fri, 18 Oct 2019 22:19:23 UTC All use subject to https://about.jstor.org/terms 40 Mather, Lighthall no-decision females control) Ungless, M. A., Argilli, E., & Bonci, for A. (2010). Effects male of stres (Fig. and 5). aversion on Also, dopamine neurons: Implications activa for addiction associated with increased reward-collection rate under stress Neuroscience & Biobehavioral Reviews, 35, 151-156. A compre in males but not females. hensive review of how stress affects dopamine neurons. Wang, J., Korczykowski, M., Rao, H. Y., Fan, Y., Pluta, J., Gur R. C.,... Detre, J. A. (2007). (See References). A study revealing Conclusions gender differences in cerebral blood flow during acute stress— Making decisions involves interacting brain mechanisms that showing more activity in ventral striatum, putamen, females compute the potential value of options and adjust that value insula,toand cingulate cortex and men showing more activity in account for uncertainty and risk. Such calculations need to be orbital and other regions in prefrontal cortex. translated into action, often under time pressure. The effects of Declaration of Conflicting Interests stress on these processes are beginning to be examined, and initial research reveals some consistent patterns. The authors declared no potential conflicts of interest with respect t First, stress enhances learning about positive outcomes the research, but authorship, and/or publication of this article. impairs learning about negative outcomes of choices (Light Note hall, Gorlick, et al., 2011; Petzold et al., 2010), effects that may help explain how stress increases the likelihood1.of Inacquir one study the enhancement but not the impairment was signifi ing and maintaining drug addiction (Saal et al., 2003; Sinha, cant, and in the other study the impairment but not the enhancement 2009). In the laboratory, these STARS effects are wassimilar significant. Due to the way the learning phase of the task was set across gender and age groups, but when it comes up,to attention drug to cues yielding positive outcomes could detract from addiction, gender differences in how stress influences learning learning about cues yielding negative outcomes; future work is about rewards and losses may be more likely, as drugs needed affect to independently examine learning about positive versus the stress system differently for men and women negative (Foxoutcomes. & Sinha, 2009). Second, when decisions must be made under References risk and uncertainty, stress alters decision strategies—but in opposite ways for men versus women (Lighthall et Abercrombie, al., 2009; E. D., Keefe, K. A., Difrischia, D. S., & Zigmond, Lighthall, Sakaki, et al., 2011; Preston et al., 2007; van M. J.den (1989). Differential effect of stress on in vivo dopamine Bos et al., 2009). 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