Stress shifts brain activation towards ventral 'affective' areas during emotional distraction.

Abstract

Acute stress has been shown to impair working memory (WM), and to decrease prefrontal activation during WM in healthy humans. Stress also enhances amygdala responses towards emotional stimuli. Stress might thus be specifically detrimental to WM when one is distracted by emotional stimuli. Usually, emotional stimuli presented as distracters in a WM task slow down performance, while evoking more activation in ventral 'affective' brain areas, and a relative deactivation in dorsal 'executive' areas. We hypothesized that after acute social stress, this reciprocal dorsal-ventral pattern would be shifted towards greater increase of ventral 'affective' activation during emotional distraction, while impairing WM performance. To investigate this, 34 healthy men, randomly assigned to a social stress or control condition, performed a Sternberg WM task with emotional and neutral distracters inside an MRI scanner. Results showed that WM performance after stress tended to be slower during emotional distraction. Brain activations during emotional distraction was enhanced in ventral affective areas, while dorsal executive areas tended to show less deactivation after stress. These results suggest that acute stress shifts priority towards processing of emotionally significant stimuli, at the cost of WM performance.

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Stress shifts brain activation towards ventral
?affective? areas during emotional distraction
Nicole Y. L. Oei,1,2Ilya M. Veer,1,2,3Oliver T. Wolf,4Philip Spinhoven,1,2,5Serge A. R. B. Rombouts,1,2,3and
Bernet M. Elzinga1,2
1Department of Clinical, Health and Neuropsychology, Institute of Psychology, Leiden University, Leiden,2Leiden Institute for Brain
and Cognition, Leiden,3Department of Radiology, Leiden University Medical Center, Leiden, The Netherlands,4Department of
Cognitive Psychology, Ruhr-University Bochum, Germany, and5Department of Psychiatry, Leiden University Medical Center, Leiden,
The Netherlands
Acute stress has been shown to impair working memory (WM), and to decrease prefrontal activation during WM in healthy
humans. Stress also enhances amygdala responses towards emotional stimuli. Stress might thus be specifically detrimental to
WM when one is distracted by emotional stimuli. Usually, emotional stimuli presented as distracters in a WM task slow down
performance, while evoking more activation in ventral ?affective? brain areas, and a relative deactivation in dorsal ?executive?
areas. We hypothesized that after acute social stress, this reciprocal dorsal–ventral pattern would be shifted towards greater
increase of ventral ?affective? activation during emotional distraction, while impairing WM performance. To investigate this,
34 healthy men, randomly assigned to a social stress or control condition, performed a Sternberg WM task with emotional
and neutral distracters inside an MRI scanner. Results showed that WM performance after stress tended to be slower during
emotional distraction. Brain activations during emotional distraction was enhanced in ventral affective areas, while dorsal
executive areas tended to show less deactivation after stress. These results suggest that acute stress shifts priority towards
processing of emotionally significant stimuli, at the cost of WM performance.
Keywords: stress; emotional distraction; cortisol; working memory; imaging
INTRODUCTION
Several studies in healthy humans showed that acute stress
and stress hormones, catecholamines and glucocorticoids
(GC), impair working memory (WM) (Lupien et al., 1999;
Oei et al., 2006; Ramos and Arnsten, 2007; Luethi et al.,
2008; Schoofs et al., 2008; Arnsten, 2009). WM is the ability
to maintain relevant information in mind and to keep irrele-
vant information out of mind. Stress might be especially
detrimental to WM by decreasing one’s ability to keep ir-
relevant emotional information out of mind, because stress
heightens the sensitivity towards potentially threatening sti-
muli (van Marle et al., 2009), while also compromising the
efficiency of conscious effortful information processing by
decreasing prefrontal activation during WM performance
(Qin et al., 2009). The present study was, therefore, aimed
at examining whether acute social stress enhances emotional
distraction during WM, and at investigating the stress-
induced changes in the underlying neural patterns, using
functional magnetic resonance imaging (fMRI).
The preferential processing of emotional cues is con-
sidered adaptive, as these are likely to be important for our
survival. Accordingly, healthy humans under stress-free cir-
cumstances attend to emotional stimuli, even when these are
irrelevant to the WM task at hand, and consequently per-
form poorer at WM (e.g. Kensinger and Corkin, 2003). At
the neural level, several studies found an antagonistic rela-
tionship between neural activations associated with emo-
tional vs executive processing, revealing that ‘affective
processing’ is favoured over ‘executive processing’ (Drevets
and Raichle, 1998). When comparing neutral vs emotional
distracters in a WM task, ventral ‘affective’ brain areas, such
as the inferior frontal gyrus (IFG) and amygdala show
increased activation, along with a deactivation of more
dorsal ‘executive’ brain areas, such as parietal regions and
the right dorsolateral prefrontal cortex (DLPFC) (Perlstein
et al., 2002; Dolcos and McCarthy, 2006; Mitchell et al.,
2008; Morey et al., 2009; Anticevic et al., 2010).
Attending to emotional stimuli becomes maladaptive
when one is biased towards negative cues, and/or unable
to disengage from negative information that is unrelated to
the task, which is frequently observed in stress-related psy-
chiatric disorders such as post-traumatic stress disorder
(PTSD). PTSD, which presumably is precipitated by acute
traumatic stress, is associated with an over responsive amyg-
dala and impaired prefrontal function (Elzinga and Bremner,
2002; Shin et al., 2006). Recently, in a task combining
emotional and executive processing (Morey et al., 2009) evi-
dence for an imbalance in the interaction between ventral
Received 3 February 2010; Accepted 15 March 2011
The authors are very grateful to Judith Dekker and Mascha Nuijten for their help with the data collection.
The authors also thank Eveline Crone for her helpful advice with regard to the data analysis. The contribution
of OTWolf was supported by a grant from the German Research Foundation (DFG WO 733/6-2).
Correspondence should be addressed to Nicole Oei, Leiden Institute for Brain and Cognition, Postzone C2-S,
PO Box 9600, 2300 RC Leiden. Email: noei@xs4all.nl
doi:10.1093/scan/nsr024SCAN (2011) 1of10
? TheAuthor (201 1).Publishedby OxfordUniversity Press.For Permissions,pleaseemail:journals.permissions@oup.com

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affective and dorsal executive brain areas was found in PTSD
patients. PTSD patients showed higher activations in ventral
affective brain regions, which was positively related to PTSD
symptom severity, and conversely, higher activity in fronto-
parietal brain regions with lower PTSD symptom severity.
Although the acute stress response in healthy individuals
is considered adaptive (De Kloet et al., 1999), its (temporary)
effect on the brain shows similarities with PTSD, as even
acute mild psychological stress impairs prefrontal cortex
(PFC) function (Elzinga and Roelofs, 2005; Oei et al.,
2006; Ramos and Arnsten, 2007; Schoofs et al., 2008;
Arnsten, 2009; Qin et al., 2009), and heightens the sensitivity
of the amygdala towards threatening stimuli (van Marle
et al., 2009). We therefore expected that acute social stress
would impair WM performance compared with a control
condition, especially when distracters are emotional. We fur-
ther hypothesized that the social stress would lead to an
alteration in the reciprocal dorsal–ventral pattern during
emotional distraction, with increased activations in ventral
‘affective’ brain areas compared with a non-stressful control
condition. To examine our hypothesis, we analysed behav-
ioral performance and dorsal and ventral a priori selected
regions of interest (ROIs) implicated in emotional distrac-
tion during WM (dorsal system: right DLPFC and bilateral
parietal regions, ventral system: bilateral IFG and right
amygdala) in previous studies (i.e. Dolcos et al., 2006;
Mitchell et al., 2008) We also explored the role of GCs (sal-
ivary cortisol) in relation to behavioral performance and
neural responses during distraction.
METHODS
Participants
Male volunteers from the general population were recruited
by means of advertisements. Eligibility criteria were: no his-
tory of disease or chronic disease requiring medical atten-
tion, no dyslexia, no colour blindness, no current use of
prescribed medication or the use of remedies containing
corticosteroids, no use of psychotropic drugs, no current
orpast psychiatricproblems,
Amsterdam Biographical interview (ABV; de Wilde, 1963).
The Dutch version of the Symptom checklist (SCL-90)
(Arrindell and Ettema, 1986) was used to assess psychoneur-
oticism (the cut-off score for exclusion was 145, following
norm scores for a healthy population), the Dutch version of
the Beck Depression Inventory, using a cut-off score for ex-
clusion of >10 (BDI; Bouman et al., 1985). Furthermore, a
body mass index (BMI; kg/m2) between 19 and 26, an age
between 18 and 35 years, and right-handedness was required.
Lastly, participants were required to have a total IQ score of
>90, determined by the relevant subtests of the Wechsler
Adult intelligence Scale-III (WAIS-III, Wechsler, 1997).
Altogether, 40 healthy, male participants were included in
the present study and randomly assigned to an experimental
and a control group in a randomized two-group design.
From this sample two participants with IQs lower than 90
determinedbythe
were excluded from analyses in the present study. Four other
participants were excluded from the analyses: two partici-
pants were outliers because of extreme cortisol levels at base-
line, probably reflecting saliva sample contamination or an
acute infectious disease (one from stress group, 120nmol/l;
one from the control group, 36nmol/l). Data from one par-
ticipant from the stress group could not be collected because
of a computer failure. One other participant from the con-
trol group was a multivariate outlier with regard to task
performance. Each participant gave signed informed consent
in which confidentiality, anonymity and the opportunity to
withdraw without penalty were assured. The study was
approved by the Medical Ethics Committee of the Leiden
University Medical Center and carried out according to the
standards of the Declaration of Helsinki (2000).
Materials
To ascertain that no pre-stress differences between groups
existed on intelligence and WM performance, the subscales
Picture Completion, Arithmetic, Information, Block Design,
of the WAIS-III (Wechsler 1997) were used to estimate total
IQ (TIQ), while Arithmetic, Digit span and Numbers and
Letters were used to assess WM Index (WMI). Also state
and trait anxiety (State-Trait anxiety inventory, STAI,
Spielberger, 1983) was assessed.
Emotional Sternberg task
WM was measured using an adapted version of the
Sternberg item-recognition task (Sternberg, 1966), de-
veloped and described by Oei et al. (2009). In the present
version, the task consisted of a total of 180 trials, which
lasted no >25min. Half of the trials were of low load (i.e.
comparison load 4) and the other half of high load (com-
parison load 16). Comparison load was defined by the
number of targets (1 or 4) to hold in WM, multiplied by
the number of stimuli (4) in the item-recognition display.
Comparison load 16 (4:4; target:recognition display) means
that four targets (e.g. RZAS) have to be held in WM while
there are four stimuli on the item-recognition display (e.g.
CDMA), leading to 16 possible comparisons to perform
before answering (i.e. RC-RD-RM-RA-ZC-ZD-ZM-ZA-SC-
SD-SA-SM-AC-AD-AM-AA etc.). Each trial started with a
blue fixation cross (500ms), followed by the target presen-
tation (1000ms), a distracter (1500ms) and a recognition
display (<2000ms). Random jitter in between trials ranged
from 1500 to 4500ms. Participants were instructed to ignore
the distracter pictures, and to fixate their eyes on a red cross
centred in each distracter. The target letter then had to be
recognized from four letters in a recognition display.
Participants pressed a ‘yes’ button indicating they had recog-
nized a target, or a ‘no’ button, when no target letter was
present. A target was present (present-target trials) in half of
the trials, in the other half the target was absent
(absent-target trials). Distracters consisted of validated pic-
tures selected from the International Affective Pictures
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System (IAPS; Langet al., 2001), of which 60 neutral pictures
[rated on 9-points Likert scales (1 very negative, 9 very
positive) M?s.d., valence: 5.09?0.54; arousal (1 not arous-
ing at all, 9 highly arousing): 3.21?0.77] and 60 negatively
arousing pictures (M?s.d., valence: 2.86?0.93; arousal:
6.22?0.52), that matched in background colour, and com-
plexity, e.g. amount of people or animals in the scene. A
third category consisted of scrambled versions of both the
neutral and emotional pictures (Dolcos and McCarthy
2006). Trial order was pseudorandomized using MATLAB,
to optimize independence between regressors (the random
generated order was confined by the rule that none of the
categories would be presented more than three consecutive
times). Task stimuli were back-projected on a screen located
at the end of the scanner bore via an LCD projector located
outside the scanner room. Subjects viewed stimuli on a
screen through a mirror located on the head coil. Stimulus
software (e-prime) was used for stimulus presentation and
recording of responses.
Subjective ratings
After the experiment participants rated all distracters on a
5-point Likert scale for distractibility (1 not distracting at all,
5 highly distracting), whereas arousal (1 not arousing at all, 5
highly arousing) and valence (1 very positive, 5 very negative)
wereassessed on5-points
Self-Assessment Manikin (Bradley and Lang, 1994).
Likertscales usingthe
Stress induction
To induce stress, the Trier Social Stress Task (TSST) was
employed (Kirschbaumet al., 1993). The TSST protocol has
consistently proven to raise cortisol levels (Kirschbaum and
Hellhammer, 1994). This laboratory stressor consists of a
10-min period in anticipation of a 5-min free speech, and a
5-min arithmetic task (counting backwards from 1033 to
zero, in steps of 13) in front of a selection committee of
three psychologists. One committee member responded to
incorrect answers by saying out loud ‘incorrect, please start
over’, while keeping up participant’s performance by means
of a clearly visible scoreboard. In the control condition, par-
ticipants used the same anticipation period of 10min to think
of a movie to their liking, of which they were informed to
having to answer open questions on paper for 5min, in the
same laboratory room,but without audience. Thereafter, they
had 5min to count backwards from 50 to 0 at a slow pace.
Physiological assessments
Salivary cortisol was assessed using Salivettes (Sarstedt,
Germany). Saliva sampling is a stress-free method to assess
unbound cortisol (Kirschbaum and Hellhammer, 1994).
Saliva samples were stored at ?208C until assayed at
Proffessor Kirschbaum’s laboratory (http://biopsychologie
.tu-dresden.de). Cortisol concentrations in saliva were mea-
sured using a commercially available chemiluminescence-
immuno-assay kit with high sensitivity (IBL, Hamburg,
Germany). Inter- and intra-assay coefficients of variation
were below 10%. Systolic blood pressure (SBP, mmHg), dia-
stolic blood pressure (DBP, mmHg), and heart rate (HR,
bpm) were recorded using an automatic wrist blood pressure
monitor (OMRON, R5-I).
Scan protocol
Imaging was carried out on a 3 T Philips Achieva MRI scan-
ner (Philips, Best, The Netherlands), using an 8-channel
SENSE head coil. For fMRI, T?
echo planar images (EPI) sensitive to BOLD contrast
were obtained with the following acquisition param-
eters: repetition time (TR)¼2.2 s, echo time (TE)¼30ms,
flipangle¼808,
FOV¼220?220mm, 2.75mm isotropic voxels, 0.25mm
slice gap. A high-resolution anatomical image (T1-weighted
ultra-fastgradient-echo
TE¼4.59ms, flip angle¼88, 140 axial slices, FOV¼
224?224mm, in-plane resolution 0.875?0.875mm, slice
thickness¼1.2mm), and a high-resolution T?
gradient echo EPI scan (TR¼2.2 s, TE¼30ms, flip
angle¼808, 84 axial slices, FOV¼220?220mm, in-plane
resolution 1.96?1.96mm, slice thickness¼2mm) were
acquired for registration purposes. The scan procedure con-
sisted of EPI during the emotional WM task (<25min), the
T1-weightedanatomical
high-resolution EPI(1min).
resting-state fMRI scans were acquired at the end of the
procedure (to be reported elsewhere).
2-weighted gradient echo,
SENSE factor¼3,38axial slices,
acquisition;TR¼9.75ms,
2-weighted
scan(6min) and
DTI
the
andFurthermore,
Procedure
Participants were invited on two occasions. The first time for
further screening purposes (BDI, SCL-90, STAI, WAIS subt-
ests) and the second time for the scan session. Participants
were asked to refrain from caffeine or sugar containing
drinks, and not to eat 2h before arrival time. All participants
arrived at either 8.30 a.m. or 10.30 a.m. Arrival time was
balanced between and within groups, to keep morning cor-
tisol levels as even as possible. After arrival, participants were
given instructions regarding the protocol and the emotional
WM task. Thirty minutes after arrival, the TSST protocol
started. After the TSST, participant got into the scanner,
where the emotional Sternberg task, the structural scan,
high resolution EPI, DTI and resting states scans were mea-
sured. Saliva was sampled at five times: before (‘baseline’)
and after the anticipation phase of the TSST (‘pre-speech’),
at the end of the TSST (‘post-TSST’), after finishing the
emotionalWMtaskwhile
(‘post-WM’) and after the scan procedure (‘post-scan’).
Blood pressure and heart rate were sampled at all the same
time points, except for those inside the scanner room. After
scanning, participants were seated in front of a PC, to pro-
vide subjective ratings of the distracters on arousal, valence
and distractibility. Hereafter, an exit-interview and a debrief-
ing regarding the TSST followed. Participants were thanked
and paid for their participation.
still insidethescanner
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Data processing and analysis
Physiological data
Cortisol/BP/HR was analysed using repeated measures (RM)
ANOVA, and unpaired t-tests.
Task data
Reaction times (RTs) were checked for errors, misses and
outliers. Errors and misses were scored and removed.
Univariate outliers were replaced by the mean per load by
distracter type þ 2 s.d. Mahanolobis distance was calculated
to check for multivariate outliers [P(D2)<0.05]. RTs of cor-
rect trials were analysed using RM ANOVAs, with as
between-subjects factor Group (Stress vs Control), and as
within-subjects factors Target (present vs absent), Load
(high vs low) and Distracter (emotional vs neutral). Errors
were analysed similarly. Follow-up analysis of RM ANOVA
effects, if relevant, was done with t-tests. Greenhouse–Geisser
corrections were applied when the sphericity assumption was
not met. SPSS (version 16) was used for the analyses.
FMRI data
FMRI data processing was carried out using FMRI Expert
Analysis Tool (FEAT) Version 4.1, part of [FMRIBs Software
Library (FSL), www.fmrib.ox.ac.uk/fsl; Smith et al., 2004].
The following pre-statistics processing was applied: motion
correction (Jenkinson et al., 2002); non-brain removal
(Smith, 2002); spatial smoothing using a Gaussian kernel
of FWHM 8mm; grand-mean intensity normalization of
the entire 4D data set by a single multiplicative factor;
high-pass temporalfiltering
squares straight line fitting, with ? ¼50.0s). Time-series
statistical analysis was carried out with local autocorrelation
correction (Woolrich et al., 2001). FMRI EPI data were
registered to the high resolution EPI scan of each participant,
which was registered to the individual T1-weighted structural
scan, which was registered to the 2mm MNI-152 standard
space template (Jenkinson and Smith, 2001; Jenkinson et al.,
2002). For each participant, eight explanatory variables
(EVs) were included in the general linear model: six EVs
describing the period between target onset and distracter
offset (total length 2.5s) separate for load (low/high) ? dis-
tracter type (Neu/Emo/Scr) on correct trials. Target-
recognition periods on correct trials were modelled in one
EV, independent of load or preceding distracter type, with
variable durations depending on the response times of the
participants. A last EV was included describing error trials,
modelling the entire trial from target onset to target-
recognition response.
Each EV was convolved with a double gamma haemo-
dynamic response function to account for the haemodynam-
ic response. The images of contrasts of parameter estimates
and corresponding variances were then fed into a higher
level mixed effects analysis, carried out with FMRIBs Local
Analysis of Mixed Effects (FLAME) (Beckmann et al., 2003;
Woolrich et al., 2004). The significance level of the Z-
(Gaussian-weightedleast-
statistic image of the contrast of interest (Emo>Neu) was
set to P<0.001 (Z>3.1, uncorrected). Before further ana-
lysis, the whole-brain activation map, consisting of all par-
ticipants, was used to select ROIs, defined as clusters of
significantly activated contiguous voxels in the four a
priori chosen ROIs, involved in coping with emotional dis-
traction, i.e. the right amygdala, the bilateral IFG, right
dorsolateral PFC and bilateral parietal lobe (Dolcos and
McCarthy, 2006; Dolcos et al., 2006; Mitchell et al., 2008).
These activated clusters were further confined within bound-
aries of preselected atlas-based ROIs (from the anatomical
Harvard–Oxford cortical probability atlas, with the excep-
tion of the right amygdala, which was confined by bound-
aries from the Harvard–Oxford subcortical probability
atlas). Then, from these ROIs, parameter estimates (PE)
were extracted (Emo and Neu at both Low and High
Load) with zero determined by each individual’s implicit
baseline (Poldrack, 2007). Then, to examine whether stress
modulated the specific pattern of more activity in ventral
areas, and less activity in dorsal areas during emotional dis-
traction, and the differential (interaction) effects of Load and
Distracter, a RM ANOVA was performed on the percentage
change of the MR signal (PE/implicit baseline *100) in the
regions of interest, with as within-subjects factors neural
system (dorsal, ventral), Load (Low vs High), Distracter
type (neutral vs emotional), and Group as between-subjects
factor.
RESULTS
There were no significant differences in the remaining
groups with regard to Age, BMI, BDI, SCL-90, Total IQ,
WMI and state anxiety, although trait anxiety showed a
trend towards higher anxiety in the stress group (see
Table 1 for means and standard deviations).
Stress induction
As expected, the stress induction raised the cortisol levels in
the stress group, as evidenced by a Group by Time
Table 1. Means (M) and standard deviations (s.d.) of subject variables in
stress and control group
Control (M?s.d.) Stress (M?s.d.)F(1,33)P-value
Age
BMI
BDI
SCL-90
STAI-trait
STAI-state
TIQ
WMI
24.00?2.62
22.70?1.55
2.71?3.53
103.24?16.78
29.82?6.78
29.76?6.24
113.35?14.66
114.47?13.39
24.47?4.13
22.29?2.56
3.53?3.61
104.82?11.51
34.06?7.45
32.47?7.32
114.00?15.30
109.41?10.13
0.16
0.32
0.45
0.10
3.01
1.34
0.02
1.54
0.69
0.57
0.51
0.75
0.09
0.26
0.90
0.22
BMI¼body mass index; BDI¼Beck Depression Inventory; SCL-90¼Symptom
Checklist-90; STAI-trait¼Trait version of the State-Trait anxiety index: TIQ¼Total
Intelligence Quotient: WMI¼Working memory index.
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interaction [F(1.81, 57.83)¼6.95, P¼0.003] (Figure 1).
Follow-up t-tests showed that the groups did not differ
at baseline [t(32)¼0.59, P¼0.55], while right after the
stress induction, cortisol levels were significantly higher
in the stress group compared with the control group
[t(32)¼?2.32, P¼0.027]. After the task, cortisol levels
were still higher in the stress group [t(32)¼?3.42,
P¼0.002). The between-subjects factor Group was not sig-
nificant, F(1,32)¼2.19, P¼0.15.
Heart rate. There were no significant differences between
groups in heart rate (all P’s>0.05).
Blood pressure. There were significant within-subjects ef-
fects of Time [SBP, F(3,96)¼9.11, P<0.0005, DBP,
F(3,96)¼8.64, P<0.0005] and Condition by Time [SBP,
F(3,96)¼12.52,P<0.0005;DBP,F(3,96)¼8.00,
P<0.0005]. After the stress induction, SBP and DBP was
significantly higher in the stress group than the control
group [respectively,t(32)¼?3.09,
?4.70,
between-groups effect of DBP [F(1,32)¼6.56, P<0.02],
with a higher mean in the stress group (M?s.e.¼
79.25?1.79) than in the control group (M?s.e.¼
72.75?1.79).
P¼0.004,
also
t(32)¼
significantP<0.0005].There wasa
Emotional WM performance
See means and standard deviations of RTs in Table 2. Within
subjects, RTs were faster at low load compared with high
load, at present vs absent target trials and when the distracter
was neutral vs emotional (all P’s<0.001). Overall, the stress
group tended to be slower than the control group
Fig. 1 Mean levels of cortisol in saliva and standard errors in stress and control group. Note. Significant difference between groups, *P<0.05, **P<0.005.
Table 2 Means (M) and standard deviations (s.d.) of RTs and errors on the emotional Sternberg task in the stress and control group.
Control (M?s.d.) Stress (M?s.d.)
Target PresentAbsentPresentAbsent
LoadDistracter
Emo
Neu
Emo
Neu
RTs
Low 784.10?180.74
736.53?141.68
1168.38?302.61
1138.61?253.51
794.50?220.72
798.66?222.85
1431.22?415.09
1357.21?397.44
949.40?202.67
849.29?165.43
1301.25?194.71
1240.20?208.66
943.00?183.97
973.02?206.98
1590.8?281.41
1537.74?275.57
High
Errors
Low Emo
Neu
Emo
Neu
1.12?1.11
0.06?0.68
3.41?2.48
2.82?1.63
0.18?0.39
0.35?0.61
0.65?0.79
0.35?0.99
0.64?0.86
0.35?0.61
2.94?1.98
3.11?2.29
0.65?0.86
0.47?0.72
1.18?1.19
1.06?1.30
High
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[F(1,32)¼3.66, P¼0.06]. Group, Target and Distracter
interactedattrend levels
Post hoc t-tests showed that during present-target trials, the
stress group was slower than controls when distracters were
emotional [t(32)¼?2.03, P¼0.05], but not when they were
neutral [t(32)¼?1.65, P¼0.11] (Figure 2). In the control
group, there was no significant difference in RTs between
neutral and emotional trials. There were also no differences
during absent-target trials.
[F(1,32)¼3.61,P¼0.07].
WM errors
See Table 2 for means and standard deviations of Errors.
Within subjects analyses showed that more errors were
made at high compared with low load, more during
present-target trials vs absent target trials, and also more
errors were made when distracters were emotional compared
with neutral [F(1,32)>5.99, P’s<0.002]. There were no
interactions with group, target or load, and there was no
main effect of group [F(1,32)¼0.70, P¼0.41].
Subjective ratings of neutral and emotional distracters
Participants were subjectively more distracted by emotional
pictures (M?s.d.¼1.78?0.57) than by neutral pictures
(M?s.d.¼1.21?0.22)
ratedemotionaldistracters
more arousingthan neutral
1.18?0.20) [t(33)¼9.99, P<0.0005)]. The valence of emo-
tional pictures was rated as more negative (M?s.d.¼
3.83?0.46)
2.72?0.35) [t(33)¼?15.99, P<0.0005]. There was no dif-
ference between stress- and control-group in these ratings
(all F’s<2.34, and P’s>0.14).
[t(33)¼6.75,
(M?s.d.¼2.07?0.63)
distracters
P<0.0005], and
as
(M?s.d.¼
than theneutral pictures(M?s.d.¼
FMRI analyses
The results from the Emo vs Neu contrast in the whole-brain
analysis of the combined groups are presented in Table 3.
Consistent with previous reports (e.g. Dolcos et al., 2006),
the typical pattern of dorsal ‘executive’ deactivations and
ventral ‘affective’ activations was found (Figure 3A). The
four a priori ROIs (right DLPFC, bilateral LPC, right amyg-
dala, bilateralIFG) were selected from these activations, dis-
carding extended activation in voxels outside these regions
(specifically in bilateral orbitofrontal regions) as determined
by the probabilistic Harvard–Oxford atlases. Within the
right DLPFC, the ROI was selected from the same region
as reported by Dolcos et al. (2006).
The RM ANOVA performed on the percentage change of
the MR signal in the ROIs showed that there was a Group by
Distracter type interaction [F(1,32)¼5.06, P¼0.03], which
indicated more activation during emotional distraction in
the stress group than in the control group, but not during
neutral distraction. To specifically address our hypothesis
that ventral activation would be enhanced, and dorsal acti-
vation decreased during emotional distraction, we further
inspected this interaction in the dorsal and ventral ROIs.
Separate ANOVAs revealed that the stress group compared
to control group had a smaller deactivation in the dorsal
systemduring emotional
[F(1,33)¼3.09, P¼0.08], and significantly greater activa-
tion of the ventral system [F(1,33)¼4.74, P¼0.04] (see
Figure 3b for mean signal change and standard error of
the individual ROIs, as a function of group and distracter
type).
Finally, Neural system interacted with Load [F(1,32)¼
15.05, P<0.0001], with at low load, more activation in the
ventral system than in the dorsal system [t(33)¼?3.29,
P¼0.002), and a tendency for less deactivation of the
dorsal systemathigh compared
[t(33)¼?1.74, P¼0.09].
distraction attrend levels
with lowload
Correlational analyses
Higher increases in cortisol levels at the time of task per-
formance (mean pre- and post-WM minus baseline) were
associated with less interference by emotional distraction
(RTs emotional trials minus RTs neutral trials) at trend
levels in the stress group (r¼?0.37, P¼0.06), but not in
the control group (P’s>0.13). In the stress group, the cor-
tisol response was negatively correlated with neural response
in the ventral system during emotional distraction (r¼?50,
P¼0.04; amygdala, r¼?0.45, P¼0.07; IFG, r¼?0.30,
P¼0.24). There was no significant relation between cortisol
response and dorsal activation in stress or control group.
DISCUSSION
In the present study, healthy men were exposed to acute
social stress before entering the MRI scanner. Inside the
scanner, when cortisol levels were high, participants per-
formed a Sternberg WM task with emotionally negative
and neutral distracting pictures, shown during the delay
phase of each trial. Emotional distracters evoked more ven-
tral activation after acute social stress, and a tendency to-
wards less deactivation (i.e. a smaller magnitude of
Fig. 2 Present-target trials: Mean RTs (and s.e.’s) in emotional and neutral trials of
the stress- and control group. *P¼0.05
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below-implicit baseline BOLD signal) in dorsal areas com-
pared to the control group. Furthermore, compared to the
control group, WM performance tended to be impaired in
the stress group during emotional distraction.
The present study is the first to use a validated stress
procedure, the TSST, to test the stress effects on emotional
distraction in WM. Our findings lend support to the recent
accumulation of ideas on acute stress effects, that?although
tackling different memory systems or processes?stress
modulates the interaction between ‘higher executive’ and
‘lower emotional’ processes (Luethi et al., 2008; Schwabe
and Wolf, 2009; van Marle et al., 2009). Intuitively, the
idea that acute effects of stress on memory and cognition
have survival value, is attractive as it seems adaptive to pri-
oritize attending to dangerous?instead of neutral stimuli, for
later superior recall?and to be more ready to flee than
ponder (Joels et al., 2006). For instance, Luethi et al.
(2008) showed that stress enhanced implicit memory of
negativeemotional stimuli,
memory and WM. Stress also induced a shift from
goal-directed behaviour towards habits in instrumental
stimulus–response processes (Schwabe and Wolf, 2009).
Other recent imaging studies reported either enhanced
whileimpairingexplicit
ventral
stress-induced heightened amygdala and inferior temporal
activity towards threat-related stimuli (van Marle et al.,
2009), or that stress-reduced dorsal prefrontal activations
during WM (Qin et al., 2009). We found comparable effects
within one task design, which enhances the convergent val-
idity of the idea that stress facilitates emotional processing at
the cost of executive processing. Moreover, consistent with
the idea that stress shifts brain activation towards ventral
areas during emotional distraction, a recent study (Chuah
et al., 2010) reported increased amygdala activation asso-
ciated with increased emotional distraction during WM
after 24 h sleep deprivation, which can be considered as an
acute stressor (McEwen, 2006).
The present findings are also consistent with results from
other studies showing that stress induces WM impairment
(Oei et al., 2006; Schoofs et al., 2008). However, it remains
unclear what the specific contribution of GCs is to these
stress effects. On the one hand, GCs released during
(Elzinga and Roelofs, 2005) and after stress (Oei et al.,
2006; Schoofs et al., 2008) have been related to reduced
WM performance. On the other hand, GC actions appear
to be beneficial in dealing with emotional distraction
activationafter stress,for instance,that
Table 3 Peak voxels of significantly activated clusters in brain areas during distraction (Emotional vs Neutral distracters and vice versa), in the whole sample
(n¼34).
Contrast Area BA VoxelsL/R MNI-coordinatesZ-value
xyz
Emo>neu
Occipital fusiform gyrus
Inferior lateral occipital cortex
Inferior orbitofrontal cortex
IFG, triangularis
Amygdala
Anterior temporal fusiform cortex
Temporal pole
Insular cortex
37
19
4544
3924
1766
1182
R
L
L
R
R
L
R
R
42
?62
?70
?12
12
?2
7.24***
6.97***
5.20***
4.58***
3.98
4.11
3.65
3.48
?52
?36 30
3052
22
4
72
60
24
14
?4
?10
?18
?36
?32
?16
?30
54
38
218
0
Neu>Emo
Superior temporal gyrus
Superior temporal gyrus
Precentral gyrus
Pre-/post-central gyrus
Frontal pole
Precuneus
Occipital pole
Middle frontal gyrus
Superior frontal gyrus
Middle frontal gyrus
Lateral occipital cortex, superior division
Frontal pole (DLPFC)
Supramarginal gyrus
Post-central gyrus
Pre-/post-central gyrus
Middle frontal gyrus
Supramarginal gyrus
22
22
3656
3391
1466
777
399
224
180
125
115
84
79
62
49
29
25
16
13
R
L
R
L
R
62
?4
?28
?26
?30
?4 5.12***
5.14***
4.76***
4.55***
4.23***
3.95
4.41
4.12
4.34
4.05
3.54
3.79
3.55
3.52
3.33
3.39
3.39
?668
3 2470
66
?24
42 52
?10
22
?10
54
46
32
38
16
52
56
48
34
38
0
?70
?94
22
38
28
?60
R
L
R
R
L
R
R
R
R
L
R
30
6
?30
24
509
39
46
?36
46
54
52
36
44
?38
?22
?24
?2434
4046
?42
Note. ***cluster corrected (Z>3.1), P<0.05. All other areas significant at Z¼3.1, P<0.001 (uncorrected). No small volume corrections were applied. BA¼Brodmann area;
L/R¼Left/right in the brain; Voxel size is 2mm isotropic.
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(Putman et al., 2007; Oei et al., 2009). Here, individuals that
responded to stress with high cortisol levels, showed less
interference by emotional distraction and a smaller neural
response to emotional distracters in the ventral ROIs, espe-
cially the amygdala. Although these effects were significant at
trend levels, they are consistent with a previous study from
our lab, showing that administration of 35mg hydrocorti-
sone significantly reduced emotional distraction using the
same task (Oei et al., 2009). Hydrocortisone administration
has also found to reduce selective attention for threat
(Putman et al., 2007). Cortisol might act to suppress the
first wave stress activity [e.g. noradrenergic (NA) activity]
towards emotional stimuli. High NA activity has been shown
to increase amygdala responses towards emotional stimuli
(Onur et al., 2009), and is also associated with impaired
WM performance and PFC function (Arnsten et al., 1999;
Birnbaum et al., 1999; Mao et al., 1999; Ramos et al., 2005;
Ramos and Arnsten, 2007). Moreover, blocking NA activity
has shown to reduce interference by emotional distraction in
the present task, which was partially mediated by individual
cortisol levels (Oei et al., 2010). Thus, future studies (e.g.
using pharmacological manipulations) aimed at further
disentangling the specific contributions and interactions of
cortisol and NA activity during stress on processing of emo-
tional stimuli should monitor both cortisol and NA.
Given that WM is especially impaired after stress or GCs
at high loads (Lupien et al., 1999; Oei et al., 2006), it could
be expected that our stressed participants would be particu-
larly distracted by emotional pictures at high load. This was,
however, not confirmed. At high load, overall performance
speed was quite low and only differentiated between emo-
tional or neutral trials at the descriptive level. This might
have been a drawback from having to perform the task inside
the scanner, resulting in slightly altered behavioural response
patterns compared with similar task data (Oei et al., 2009).
At the neural level, more ventral activity was evoked when
load was low than when load was high, which is consistent
with other reports. Interference by similar emotionally nega-
tive distracting pictures was only observed under low- but
not high load (Erthal et al., 2005), while amygdala responses
to negative distracters under high load were shown to be
reduced compared with low load, presumably because high
load claims so much attention, that not enough attentional
resources were left to be captured by emotional distracters
Fig. 3 Brain activation during emotional compared with neutral distraction, and percent signal change in the ROI. (A) Combined group activation showing the typical pattern of
dorsal deactivation and ventral activation in the presence of emotional distraction. LPC¼lateral parietal cortex; DLPFC¼dorsolateral prefrontal cortex; IFG¼inferior frontal
gyrus. (B) Graphs depict mean percent signal change and standard error in the four regions of interest in control (left) and stress group (right) as a function of distracter.
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(Pessoa et al., 2005). Furthermore, similar to Dolcos and
McCarthy (2006) amygdala activity was higher when con-
trasting emotional vs neutral distraction. In the control
group, however, amygdala activity was not increased when
comparing emotional distraction with baseline. As several
studies have shown a higher sensitivity to threatening stimuli
in women than in men (Canli et al., 2002; Hamann, 2005)
the fact that we only tested males, whereas Dolcos and
McCarthy tested females, might explain why they found
increased amygdala activation during emotional distraction
compared to baseline.
Furthermore, only present-target trials appeared sensitive
enough to detect effects of distraction in this paradigm,
whereas absent-target trials did not differentiate between
neutral and emotional distraction (Oei et al., 2009).
Present- and absent-target trials usually produce different
performances, probably because they elicit/evoke different
search strategies (i.e. for present-target trials a self-
terminating and for absent-target trials an exhaustive
search strategy) (Corbin and Marquer, 2008). Nonetheless,
because neural activation during the delay of each trial pre-
ceded the participants/knowledge of target presence or ab-
sence, wedidnot analyse
present-targets only. Discarding half of the imaging data
would also have greatly reduced the power to detect
differences.
Together, the present results show greater activation in
ventral ‘affective’ areas after stress, and smaller deactivation
in dorsal ‘executive’ areas, during emotional distraction.
This was related to slower WM performance during emo-
tional distraction. These results might suggest that acute
stress shifts priority towards processing of emotionally sig-
nificant stimuli, at the cost of WM performance. Further
research into the effects of stress on cognitive functioning
and attention to (distracting) emotional stimuli in the en-
vironment should be aimed at elucidating the specific effects
of cortisol and other stress hormones on neural and behav-
ioural performance.
theimaging datafor
Conflict of Interest
None declared.
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