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
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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
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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
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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).
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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.
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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
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