Frontal Lobe Activation Mediates the Relation

Between Sensation Seeking and Cortisol Increases
Hani D. Freeman and Jennifer S. Beer
University of Texas at Austin
ABSTRACT Low sensation seekers are theorized to avoid risk more
often because risk is emotionally more costly for them (in comparison to
high sensation seekers). Therefore, individual differences in sensation seeking
should predict differences in risk task–induced cortisol changes. Further-
more, the neural mediation that accounts for the relation between sensation
seeking and cortisol changes has not been studied. The current study tested
whether individual differences in sensation seeking predicted cortisol changes
in relation to a risk task and whether this relation was mediated by frontal
lobe activation. Participants (N517) who varied in sensation seeking com-
pleted an fMRI study in which they rated the likelihood they would take
various risks. Cortisol was measured from saliva samples collected prior to
and after the fMRI procedure. The findings show that low sensation seekers
showed the greatest rise in cortisol after the risk procedure, and this relation
was partially mediated by increased orbitofrontal cortex activity.
Why are people who are high in sensation seeking more willing to
engage in risk (Horvath & Zuckerman, 1993)? The relation between
individual differences in sensation seeking and risk taking has been
theorized to reflect differences in physiological costs associated with
risk taking (Horvath & Zuckerman, 1993; Jonah, 1997; Solomon,
1995; Solomon, Ginzburg, Neria, & Ohry, 1995; Zuckerman, 2005).
Research shows that high sensation seekers are less likely to expe-
rience increased baseline and stress task–related cortisol (Couture
et al., 2008; Croissant, Demmel, Rist, & Olbrich, 2008; Netter, Hen-
nig, & Roed, 1996; Rosenblitt, Soler, Johnson, & Quadagno, 2001;
Correspondence concerning this article should be addressed to Jennifer S. Beer,
PhD, 1 University Station A8000, Department of Psychology, University of Texas at
Austin, Austin, TX 78712. Email: beer@mail.utexas.edu.
Journal of Personality 78:5, October 2010
r 2010 The Authors
Journal of Personality r 2010, Wiley Periodicals, Inc.
DOI: 10.1111/j.1467-6494.2010.00659.x
Wang et al., 1997). Even though risky situations reflect stressful
circumstances in which an outcome is unknown, the uncertainty may
not elicit as strong of a stress response in high sensation seekers. As
such, high sensation seekers may not engage self-regulatory pro-
cesses often associated with frontal lobe activation to regulate stress
responses when taking a risk. However, the relation between sensa-
tion seeking and cortisol changes has not been studied in relation to
risk-taking tasks. Furthermore, the neural mediation that accounts
for the relation between sensation seeking and cortisol changes has
not been studied. The current study addresses these unresolved ques-
tions by testing whether individual differences in sensation seeking
predict cortisol changes in relation to a risk task and whether this
relation is mediated by frontal lobe activation.
Sensation seeking is defined as ‘‘the seeking of varied, novel, com-
plex, and intense sensations and experiences, and the willingness to
take physical, social, legal, and financial risks for the sake of such
experience’’ (Zuckerman, 1994, p. 27).
Individual differences in sensation seeking are also associated with
reduced perceptions of risk (Horvath & Zuckerman, 1993; Jonah,
1997; Rosenbloom, 2003; Solomon et al., 1995). For example, people
who are higher in sensation seeking report that they expect to
experience less anxiety when deliberating about risks they might take
in the future, even if they have not taken the risk before (when com-
pared to low sensation seekers; Horvath & Zuckerman, 1993). To-
gether this research suggests that decisions about risk taking should be
emotionally less costly for high sensation seekers when compared to
low sensation seekers. Furthermore, the difference in emotional cost
may not arise in relation to a final decision to take a risk but might
arise as early as deliberation about whether or not to take a risk.
The differences in emotional cost associated with individual differ-
ences in sensation seeking are mirrored by the differences in circulat-
ing cortisol levels. People who have higher levels of sensation seeking
tend to have lower baseline or average cortisol levels (Rosenblitt et al.,
2001; Wang et al., 1997; see Zuckerman, 1994, for a review). These
studies typically take a baseline measure of salivary cortisol levels
when participants come to the lab; this baseline cortisol measure is
then correlated with scores on a questionnaire measuring individual
differences in sensation seeking. Although there has been relatively
less research on how individual differences in sensation seeking relate
to task-related changes in cortisol, the few studies of stress task–
1498 Freeman & Beer
related changes are consistent with the baseline cortisol studies. High
sensation seekers exhibit less of a rise in cortisol in relation to a
stressful task (i.e., mental arithmetic tasks) when compared to low
sensation seekers (Couture et al., 2008; Croissant et al., 2008).
An integration of the research on (a) sensation seeking and risk
and (b) sensation seeking and cortisol suggests that high sensation
seekers are more likely to take risks and that their risk taking should
be accompanied by a reduced rise in cortisol when compared to low
sensation seekers. A further step in understanding the biological un-
derpinnings of the relation between sensation seeking and risk is to
examine how neural activity is related to sensation seeking, risk, and
cortisol. Hormonal changes are mediated through neural activity,
and therefore, it is important to understand neural regions that may
mediate the relation between individual differences in sensation
seeking and cortisol changes.
Although the bulk of neural research on cortisol has focused on
the hypothalamic-pituitary-axis (HPA) in relation to production and
release of cortisol in the body (Cullinan, Herman, Helmreich, &
Watson, 1995; Herman, Ostrander, Mueller, & Figueiredo, 2005),
some recent studies have found a positive association between fron-
tal lobe activation and cortisol change (Kern et al., 2008; Liberzon
et al., 2007; Wang et al., 2005, Wang et al., 2007; but see Ahs et al.,
2006; Pruessner, et al., 2008). Specifically, the orbitofrontal cortex,
medial prefrontal cortex, and ventral lateral prefrontal cortex have
been associated with increased cortisol in healthy individuals and
individuals with PTSD (Kern et al., 2008; Liberzon et al., 2007;
Wang et al., 2005, Wang et al., 2007). These same neural regions are
associated with emotion regulation (e.g., Bishop, Duncan, Brett, &
Lawrence, 2004; Ochsner, Bunge, Gross, & Gabrieli, 2002; see also
Beer, 2009, for a review), leading researchers to posit that these
frontal lobe regions are engaged in relation to increases in cortisol
because they support processes used to regulate elicited stress.
In addition to the studies on frontal lobes, cortisol, and stress,
other studies show that the orbitofrontal cortex is a likely candidate
for mediating the relation between sensation seeking and cortisol
change in a risk task. The orbitofrontal cortex is characterized by
large numbers of glucocorticoid receptors and has been implicated in
enhanced HPA responses (in contrast to regions such as the anterior
cingulate, which is implicated in inhibiting HPA responses; Amat
et al., 2005; Herman et al., 2005). The orbitofrontal cortex is
Sensation Seeking, Cortisol, and Brain 1499
also associated with magnitude of risk but does not predict whether
participants choose to take the risk. It was activated in studies where
participants decided not to take the risk (Brown & Braver, 2007;
Cohen, Heller, & Ranganath, 2005; Critchley, Elliot, Mathias, &
Dolan, 2000; Eshel, Nelson, Blair, Pine, & Ernst, 2007; Rogers et al.,
2004; Van Leijenhorst, Crone, & Bunge, 2006). Therefore, the or-
bitofrontal cortex may be important for considering risk but is not
specific to situations in which risk is taken or rejected.
Overview of the Current Study
The current study tests several hypotheses to better understand the
interrelations between individual differences in sensation seeking, risk
taking, cortisol changes, and frontal lobe activation. Consistent with
previous research, low sensation seeking is expected to be associated
with reduced risk taking (Horvath & Zuckerman, 1993). In the con-
text of a risk task, low sensation seeking is expected to be associated
with increases in cortisol just as it is in non-risk-related stress tasks
(Couture et al., 2008; Netter et al., 1996). Finally, the orbitofrontal
cortex is likely to mediate the relation between sensation seeking and
cortisol change because of its role in emotion regulation (e.g., Bishop
et al., 2004; Ochsner et al., 2002; see also Beer, 2009, for a review),
risky decisions (Brown & Braver, 2007; Cohen et al., 2005; Critchley
et al., 2000; Eshel et al., 2007; Rogers et al., 2004; Van Leijenhorst
et al., 2006), and cortisol modulation (Herman et al., 2005; Kern et al.,
2008; Liberzon et al., 2007; Wang et al., 2005; Wang et al., 2007).
However, a single neural region is unlikely to fully account for the
psychologically complex relation between sensation seeking and cor-
tisol changes. Therefore, it is expected that while the orbitofrontal
cortex is a potential mediator, it should only partially mediate this
relation rather than fully account for it. Finally, under what condi-
tions does orbitofrontal cortex activation mediate the relation be-
tween sensation seeking and rise in cortisol? Models of decision
making suggest that deliberating about options can be just as emo-
tion inducing as making a final decision about which option to choose
(Achtziger, Gollwitzer, & Sheeran, 2008). This raises the question of
whether orbitofrontal cortex activation mediates the relation between
sensation seeking and rise in cortisol in conditions of deliberation
about potential risk irrespective of final decision or whether it is spe-
cific to conditions in which low sensation seekers decide to take a risk.
1500 Freeman & Beer
In order to examine our hypotheses about individual differences in
sensation seeking, risk decision, cortisol changes, and neural mediation,
we conducted an fMRI study in which participants who varied in sen-
sation seeking made decisions about the likelihood they would engage
in risky scenarios. Task-related changes in cortisol were assessed
through saliva samples collected before and after the fMRI procedure.
Participants evaluated risk scenarios across three different conditions:
risk scenarios likely to appeal to both low and high sensation seekers
(Highly Acceptable Risk), risk scenarios likely to appeal only to high
sensation seekers (Less Acceptable Risk), and an experimental control
condition designed to isolate neural activity associated with evaluating
contextual information about a risk. This design permitted the exam-
ination of the theorized frontal lobe mediation of the relation between
sensation seeking and cortisol in conditions where low sensation seekers
were likely to accept or reject the risk.
METHOD
Participants
Seventeen right-handed men who were native English speakers participated
in the study. fMRI studies tend to involve smaller populations because of
monetary restrictions and the hypothesized analyses already focused on
one individual difference. Therefore, only men were included in this par-
ticular study to reduce possible effects from other individual differences
and preserve statistical power in the small sample. The participants ranged
in age from 18 to 33 years (M520.7 years, SD54.7 years) and had normal
or corrected-to-normal vision. All subjects were screened for contraindi-
cations for MRI. Informed consent was obtained from subjects in accor-
dance with procedures approved by the Internal Review Board at the
University of Texas at Austin. Participants received either class credit or
$10 per hour for their participation in the study.
Individual Differences in Sensation Seeking
Participants completed the 11-item sensation-seeking subscale of the Im-
pulsive Sensation-Seeking Scale (Zuckerman, 1994) using a 2-point scale
(1 5false; 2 5true; M56.7, SD53.3; Cronbach’s alpha 5.80). This
questionnaire measures individual differences in deliberation about risk
taking. Example items include ‘‘I like doing things just for the thrill of it,’’
‘‘I often get so carried away by new and exciting things and ideas that I
never think of possible complications,’’ and ‘‘I tend to change interests
Sensation Seeking, Cortisol, and Brain 1501
frequently.’’ Although efforts were made to include participants who
showed normal distribution in the sensation seeking variable, the small
sample made it difficult to achieve. Therefore, log-transformed sensation
seeking scores were used in all analyses. Additionally, Spearman rank
correlations are provided as complementary information to the Pearson’s
r reported in the planned analyses.
Cortisol Data Collection
The experiment was conducted between 12:30 p.m. and 3:30 p.m. to min-
imize the effects of circadian fluctuations in cortisol levels (Touitou &
Haus, 2000). Participants were also instructed to not ingest anything for
30 min before the study nor to engage in substantial physical exercise on
the day of the study. Cortisol levels were measured by collecting two sa-
liva samples from each participant following procedures and precautions
noted in Schultheiss and Stanton (2009). The first saliva sample was col-
lected approximately 15 min before the fMRI scan and more than 15 min
after participants had begun preparation for the scanning procedure. In
order to collect the first saliva sample, participants rinsed out their
mouths to remove any food particles. Next, participants chewed on a
piece of Trident sugar-free gum for 3 min to stimulate salivation. Then
participants drooled 2.5 mL of saliva into a sterile polypropylene micro-
tubule and spit out their gum. Saliva samples were immediately stored in
a freezer in an adjacent lab room in order to avoid hormone degradation
and to precipitate mucins. The same procedure was used to collect a sec-
ond sample approximately 15 min after the fMRI scan was completed.
The samples were analyzed at the Yerkes National Primate Research
Center using a commercially prepared kit by Diagnostic Laboratories.
There were six replicates performed on the data. The interassay coeffi-
cients of variance (CVs) were between 2.9% and 4.4%. The intra-assay
CV was 8.7%. There was a positive skew in the distribution of the cortisol
data, as is common for cortisol. To correct for this skew, the data were
log-transformed. Cortisol change was operationalized by using a regres-
sor variable method (Allison, 1990). Specifically, cortisol change was cal-
culated as the unstandardized residuals of a regression analysis with Time
1 cortisol as the predictor and Time 2 cortisol as the dependent variable.
This approach is favorable over a simple change score when there is an
expectation that variation in the individual difference predictor might
range from decreases to increases.
Alcohol Consumption and Sleep
Sensation seeking and cortisol can be affected by variables such as drug
use and sleep. To test for potential confounds, participants reported their
1502 Freeman & Beer
weekly alcohol consumption (e.g., ‘‘How many drinks did you have on
Monday?’’) and their sleep the night before the study took place (i.e.,
‘‘How many hours did you sleep last night?’’). These variables were ex-
amined in relation to our individual differences measures, hormone mea-
sure, and blood oxygen level dependent (BOLD) responses.
Behavioral Task
While in the scanner, participants were presented with risk scenarios and
had to rate the likelihood that they would take each risk using a four-
button response box (i.e., (1) Never take, (2) Probably not take, (3)
Probably take, or (4) Always take the risk). Risk scenarios included a
picture and a short description of the risk (see Figure 1). Three different
risk scenario conditions were created by using different descriptions for
each risk picture (50 pictures, 150 total trials). In the Highly Acceptable
Risk condition, pictures were paired with scenario descriptions that
framed the risk as having potential benefits other than pleasure seeking
(e.g., You are offered an experimental drug for an illness by a doctor). In
the Less Acceptable Risk condition, the same pictures were paired with
scenarios that framed the risk as having only thrill-seeking benefits (e.g.,
You are offered a pill of ecstasy from a friend). In the Experimental
Figure1
Example of three conditions and timing presented to participants
in the scanner.
Sensation Seeking, Cortisol, and Brain 1503
Control condition, the pictures were paired with the basic risk scenario
without additional contextual information (e.g., You are offered a pill).
The purpose of this condition was to make it possible to isolate neural
activation that specifically related to considering contextual factors that
might bias decisions to take a risk in an Acceptable or Less Acceptable
direction. By including the Experimental Control condition, we could
specifically control for neural activity associated with evaluating the basic
scenario in the Highly Acceptable and Less Acceptable conditions rather
than a risk decision in general.
The 150 trials (50 trials per condition) were presented in a pseudoran-
domized order. Pseudorandomization was generated by using a random
number generator to assign the order of trials and examining the orthog-
onality of experimental conditions in SPM2. Pictures were presented for
6 s and were separated by intertrial intervals of 6-, 8-, or 10-s displays of
a fixation point (50%: 6 s; 25%: 8 s; 25%: 10 s; Donaldson, Petersen,
Ollinger, & Buckner, 2001). Participants were instructed to clear their
minds when presented with the fixation point screens. The experiment
included five runs that each included 30 trials and lasted for 6 min and
46 s. The task was presented using DMDX software. Behavioral data
were log-transformed to ensure normal distribution.
Image Acquisition and Analysis
All images were acquired with a GE Sigma Excite 3-T magnetic resonance
image scanner using a GRAPPA parallel imaging echo-planar image
(EPI) sequence (e.g., Hoge, Gallego, Xiao, & Brooks, 2008; Skare et al.,
2007). Functional EPI images were collected utilizing whole-head cover-
age with slice orientation to reduce artifact (approximately 20 degrees off
the anterior-commisure–posterior-commisure (AC–PC) plane, repetition
time (TR) 52,000 ms, parallel imaging (PI) acceleration factor 53, echo
delay time (TE) 530 ms, flip angle of 90^o, field of view (FOV) 5240, 35
slices, voxel size 53 Â 3 Â 3 mm with a .3 mm interslice gap; for an ex-
ample of orbitofrontal coverage and signal using this approach, see Ap-
pendix A and Mehta & Beer, in press). The first four volumes were
discarded to allow scans to reach equilibrium. Stimuli were viewed uti-
lizing a back projection screen and a mirror mounted on the top of the
head coil. Responses were collected with MR-compatible buttons that
were held in the right hand. A whole-brain structural scan was acquired
using a T1-weighted SPGR sequence, which facilitated localization and
coregistration of functional data. Structural and functional volumes were
normalized to T1 and EPI templates, respectively. The normalization
algorithm used a 12-parameter affine transformation together with a
nonlinear transformation involving cosine basis functions, and resampled
1504 Freeman & Beer
the volumes to 2 mm cubic voxels. Templates were based on the Montreal
Neurological Institute (MNI) stereotaxic space.
Image analysis was performed using SPM 2.0 software (Wellcome De-
partment of Cognitive Neurology, Institute of Neurology, London, UK).
The functional images were corrected for sequential slice timing using
temporal sinc-interpolation. In addition, the images were realigned to the
first image to adjust for residual head movement and corrected for move-
ment using rigid-body transformation parameters. Images were then
smoothed with a 5 mm full-width/half maximum Gaussian kernel. A
high-pass filter with a cut-off period of 128 s was applied to remove drifts
within sessions.
A fixed-effects analysis was used to model event-related responses for
each participant. Responses related to judgment in the Highly Accept-
able, Less Acceptable, and Experimental Control conditions were mod-
eled with a canonical hemodynamic response function with a temporal
derivative. Contrasts from each participant were used in a second-level
analysis treating participants as a random effect. Group analyses were
focused on identifying orbitofrontal cortex activation that might poten-
tially mediate the relation between sensation seeking and change in cor-
tisol within the Highly Acceptable and Less Acceptable conditions. High
sensation seekers are expected to show weak or nonexistent activation of
the orbitofrontal cortex, which may result in nonsignificant activation
when averaged with low sensation seekers, making the restrictions of
region of interest (ROI) to regions significantly activated in maps of direct
contrasts between experimental conditions inappropriate. Regression an-
alyses are more appropriate because they detect neural regions that vary
in relation to individual differences variables. Therefore, group average
SPM{t} maps were created for regression analyses of interest: regressions
of sensation seeking and cortisol change on the Highly Acceptable4Ex-
perimental Control and Less Acceptable4Experimental Control con-
trasts. These regression analyses were used to identify potential neural
mediators of the relation between sensation seeking and change in cortisol
in the Highly Acceptable Risk and the Less Acceptable Risk conditions.
Several constraints were used to identify potential neural mediators: (a)
significant correlation with individual differences in sensation seeking and
significant conjunction with individual differences in change in cortisol,
(b) minimum extent threshold of 10 contiguous voxels, (c) voxels within
the orbitofrontal cortex as defined by Brodman’s Broca’s area (BA) 11
and the inferior and lateral portion of BA 47 as defined by the Automated
Anatomical Labeling map (AAL map; Tzourio-Mazoyer, et al., 2002),
and (d) activation clusters corrected by an 8 mm radius sphere at .05
false discovery rate control (FDR) (derived from the half width of the
smoothing kernel and rounded up to the next resampled voxel). These
Sensation Seeking, Cortisol, and Brain 1505
constraints were executed by conducting conjunction analyses of two re-
gression maps for each of the risky decision conditions. The conjunction
analyses were performed using the Minimum Statistic compared to the
Conjunction Null method (MS/CN; Nichols, Brett, Andersson, Wager, &
Poline, 2005). First, we computed the intersection between the regression
of sensation seeking on the Highly Acceptable Risk4Experimental Con-
trol and the regression of change in cortisol on the Highly Acceptable
Risk4Experimental Control map. Similarly, we computed the intersec-
tion of the regression maps for the regression of change in cortisol on the
Less Acceptable Risk4Experimental Control condition and the regres-
sion of change in cortisol on the Less Acceptable Risk4Experimental
Control map. Small volume correction was used for the predicted or-
bitofrontal cortex region. Parameter estimates were extracted from hy-
pothesized activation clusters in the group maps using Marsbar (Brett,
Anton, Valabregue, & Poline, 2002).
Importantly, this analysis does not selectively focus on activation
clusters determined by a single individual difference variable. Nor does
it permit the possibility that activation in different subregions of the
orbitofrontal cortex account for the statistical mediation of sensation
seeking and cortisol change (as would be the case with parameter esti-
mates extracted from a neuroanatomically, rather than functionally,
defined region of interest). Instead, the conjunction analyses appropri-
ately limit potential neural mediators within our hypothesized neural
region to those that are consistent with standardized criteria for extent
and threshold as well as statistical mediation (see below, Baron &
Kenny, 1986; Preacher & Hayes, 2004). Finally, examining BOLD re-
sponses in relation to individual differences variables, such as sensation
seeking, that reflect dispositional tendencies that transpire across con-
texts raises questions about whether BOLD responses show reasonable
test-retest reliability. Research examining the test-retest reliability of
BOLD responses has found reliability for BOLD responses for scanning
sessions taking place anywhere from 3 weeks to 1 year apart (Aron,
Gluck, & Poldrack, 2006; Wei et al., 2004). For example, one study had
participants perform the same task in sessions occurring 1 year apart
and found that intraclass correlations for BOLD responses ranged from
.5 to .9 (Aron et al., 2006).
Statistical Mediation Analysis
A mediation analysis was conducted to test whether neural activity ex-
plained the negative correlation between sensation seeking and change in
cortisol (Baron & Kenny, 1986). Parameter estimates for each of the
neural regions identified in the conjunction analysis (see ‘‘Image Acqui-
1506 Freeman & Beer
sition and Analysis’’ above) were extracted using Marsbar (Brett et al.,
2002) and entered into a series of regression analyses that test for medi-
ation (Baron & Kenny, 1986). The relation between variable X (i.e., sen-
sation seeking) and variable Y (i.e., change in cortisol) is considered to be
mediated by variable Z (i.e., neural activity) when all of the variables are
correlated and the correlation between X and Y is significantly reduced
when controlling for Z. Partial mediation is operationalized as a marginal
reduction (po.15) in the correlation X and Y when controlling for Z (see
Figure 2). Sensation seeking was regressed on neural maps, cortisol
change was regressed on neural maps controlling for sensation seeking,
and sensation seeking was regressed on cortisol change controlling for
neural activity.
Mediation analyses in small samples can be challenging because of
limited power and non-normal distribution (e.g., MacKinnon, Lock-
wood, & Williams, 2004; Preacher & Hayes, 2004). In light of these issues,
some researchers have suggested that a bootstrapping approach is more
appropriate for small samples (Preacher & Hayes, 2004) than the ap-
proach using the Sobel test (Baron & Kenny, 1986). Therefore, we also
analyzed our data using a bootstrapping approach (bootstrap sam-
ple 51,000). This approach yielded nearly identical results.
RESULTS
Task Performance
As hypothesized, participants’ likelihood to take the risk was sig-
nificantly different across all three conditions (see Figure 3). Partic-
Sensation
Seeking
Change in
Cortisol
Brain Region
Parameter
a b
c (c’)
Figure2
Diagram of mediation analysis.
Sensation Seeking, Cortisol, and Brain 1507
ipants decided to take the risk significantly more in the Highly Ac-
ceptable Risk condition (M53.05, SE5.43; t(16) 55.05, po.05)
and significantly less in the Less Acceptable Risk condition
(M52.08, SE5.41; t(16) 5 À14.18, po.05) when compared to
the Experimental Control condition (M52.8, SE5.40). Partici-
pants’ decision to accept the risk was significantly higher in the
Highly Acceptable Risk condition compared to the Less Acceptable
Risk condition (t(16) 515.2, po.05).
Participants took longer to make ratings in the Highly Acceptable
(M54.41 s, SD5.68 s; t(16) 59.2, po.05) and Less Acceptable
Risk conditions (M53.94 s, SD5.59 s; t(16) 510.15, po.05) in
Figure3
Average ratings and reaction times for Highly Acceptable, Less
Acceptable, and Control conditions. Within each graph, different
letters indicate statistically significant differences.
1508 Freeman & Beer
comparison to the Experimental Control condition (M53.2 s,
SD5.78 s). Participants also took longer to make ratings in the
Highly Acceptable condition compared to the Less Acceptable con-
dition (t(16) 53.3, po.05; see Figure 3).
Individual Differences in Sensation Seeking
Although the conditions were associated with different ratings on
average, participants high in sensation seeking were more likely to
take the risk in all three conditions. Specifically, sensation seeking
positively correlated with ratings in the Highly Acceptable risk con-
dition (r 5.65, po.05), the Less Acceptable Risk condition (r 5.54,
po.05), and Experimental Control condition (r 5.75, po.05). Sen-
sation seeking significantly predicted Time 2 cortisol (r 5 À.52,
po.05) but did not significantly predict Time 1 cortisol (r 5 À.12,
p4.05). Sensation seeking did not significantly relate to reaction
time (see Table 1 for correlations among all variables).
Change in Cortisol
The mean level for the first cortisol measurement was .59 mg/dl, with
a standard deviation of .25 mg/dl. The mean level for the postscan
cortisol measurement was .51 mg/dl with a SD of .24 mg/dl. The av-
erage for the residuals from the regression of cortisol at Time 2 con-
trolling for Time 1 was .00 with a range of À.31 to .54, suggesting
that there was a tendency for some individuals to show a decrease
whereas others experienced an increase in cortisol as a result of the
task. Change in cortisol negatively correlated with sensation seeking
(r 5 À.51, po.05). High sensation seekers tended to exhibit less of a
rise in cortisol than low sensation seekers. In terms of task relation to
change in cortisol, ratings in the Experimental Control condition
were significantly related to Time 2 cortisol (r 5 À.48, po.05) but
were not significantly related to change in cortisol (r 5 À.39,
p 5.12). Greater likelihood of taking risks in the Experimental Con-
trol condition was associated with lower cortisol levels after per-
forming the task. Change in cortisol did not significantly correlate
with reaction times or with ratings in the Highly Acceptable and
Less Acceptable conditions (see Table 1 for correlations between all
variables).
Sensation Seeking, Cortisol, and Brain 1509
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Effects of Alcohol and Sleep
Weekly alcohol consumption did not correlate with sensation seeking
(r 5.05, p4.05), change in cortisol (r 5 À.24, p4.05), or any of the
BOLD response parameter estimates (rs range from À.21 to .13).
Sleep did not correlate with sensation seeking (r 5 À.04, p4.05),
change in cortisol (r 5.02, p4.05), or any of the BOLD response pa-
rameter estimates (rs range from À.16 to .12). Additionally, the re-
lation between sensation seeking and cortisol remained significant
after controlling for weekly alcohol consumption and hours of sleep
(r 5 À.52), as did the relation between sensation seeking and the
BOLD response from regions identified in the mediation analyses de-
scribed below (rs ranged from À.60 to À.70).
Mediation Analyses
Consistent with our hypothesis, low sensation seekers exhibited higher
increases in cortisol after performing the risk tasks, and this relation
was partially mediated by increased activity in the subregions of the
medial and lateral orbitofrontal cortex in both the Highly Acceptable
and Less Acceptable conditions (see Table 2 and Figures 4–7). In the
Highly Acceptable condition, the negative correlation between sensa-
tion seeking and change in cortisol (b5 À.51, po.05) was partially
reduced when controlling for activity in regions of the medial orbito-
frontal cortex ( À4 52 À16, b5 À.13, Sobel test: Z5 À1.80, po.08).
In order to better understand this mediation, sensation seeking was
examined in relation to the Highly Acceptable condition compared to
baseline and the Experimental Control condition compared to baseline
(see Received 0000-00-00, Panel A). Sensation seeking shows a nega-
tive associative trend with medial orbitofrontal cortex activation in the
Highly Acceptable condition (compared to baseline, r 5 À.39, p 5.12)
and a positive associative trend in the Experimental Control condition
(compared to baseline, r 5.48, p 5.05). Low sensation seekers showed
greater increases in cortisol, and this relation was partially mediated by
medial orbitofrontal activity. The analyses of the parameter estimates
in relation to baseline suggest that the mediation occurred from both
greater engagement of medial orbitofrontal cortex by low sensation
seekers for the Highly Acceptable condition as well as greater engage-
ment of medial orbitofrontal cortex by high sensation seekers for the
Experimental Control condition.
Sensation Seeking, Cortisol, and Brain 1511
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was also partially explained by activity in regions of the medial ( À2,
Figure4
Medial orbitofrontal cortex (z 5 À16) partially mediates the relation
between sensation seeking and change in cortisol in the Highly
Acceptable Condition.
Figure5
Scatterplots of the regression of (a) sensation seeking and cortisol
change, (b) sensation seeking and neural parameter estimates, and
(c) cortisol change and neural parameter estimates in the Highly
Acceptable condition.
Sensation Seeking, Cortisol, and Brain 1513
Figure6
Neural regions mediating sensation seeking and change in cortisol
in the Less Acceptable condition. (A) Medial Orbitofrontal Cortex
(z 5 À18); (B) Lateral Orbitofrontal Cortex (z 5 À24); (C) Lateral
Orbitofrontal Cortex (z 5 À12).
1514 Freeman & Beer
32, À18, b 5 À.09, Sobel test: Z5 À2.00, po.04; À10, 28, À24,
b 5 À.19, Sobel test: Z5 À1.70, po.08; but note that the relation
between sensation seeking and the parameter estimate for this latter
region is not significant when analyzed using Spearman’s rank cor-
relation) and lateral orbitofrontal cortex (49, 26, À12, b 5 À.22,
Sobel test: Z5 À1.58, po.11). As above, sensation seeking was ex-
amined in relation to the Less Acceptable condition compared to
baseline and the Experimental Control condition compared to base-
line (see Appendix B, Panels B–D). As in the Highly Acceptable
condition, one medial orbitofrontal region ( À2, 32, À18) showed a
negative associative trend with the Less Acceptable condition and a
positive associative trend with the Experimental Control condition.
Therefore, mediation in this region may have occurred from both
greater engagement of the medial orbitofrontal cortex by low sen-
sation seekers for the Less Acceptable condition as well as greater
Figure7
Scatterplots of the regression of (a) sensation seeking and neural
parameter estimates and (b) cortisol change and neural parameter
estimates in the Less Acceptable condition.
Sensation Seeking, Cortisol, and Brain 1515
engagement of the medial orbitofrontal cortex by high sensation seek-
ers for the Experimental Control condition. However, the other medial
orbitofrontal cortex region ( À10, 28, À24) and the lateral orbito-
frontal cortex region (49, 26, À12) showed negative associative trends
with the Less Acceptable condition but did not show an associative
trend with the Experimental Control condition (see Appendix B). In
this case, these regions may have mediated the relation between sen-
sation seeking and cortisol change because of increased engagement by
low sensation seekers in the Less Acceptable condition.
The bootstrapping approach advocated by Preacher and Hayes
(2004) yielded very similar results (see Table 3). In the Highly Ac-
ceptable condition, the negative correlation between sensation seek-
ing and change in cortisol (t 5 À2.29, po.05) was partially reduced
when controlling for activity in the regions of the medial orbito-
frontal cortex ( À4, 52, À16, t 5 À.67, p4.10). In the Less Ac-
ceptable condition, the negative correlation between sensation
seeking and change in cortisol (t 5 À2.29, po.05) was also partially
explained by activity in regions of the medial ( À2, 32, À18,
t 5 À.28, p4.10; À10, 28, À24, t 5 À.58, p4.10) and lateral or-
bitofrontal cortex (49, 26, À12, t 5 À.40, p4.10).
Although different subregions within the orbitofrontal cortex me-
diated the relation between low sensation seeking and change in
cortisol across the Highly Acceptable and Less Acceptable condi-
tions, both conditions were associated with significant orbitofrontal
cortex mediation.
Orbitofrontal Cortex Activation Across Conditions
The focus of the article was to identify regions of the orbitofrontal
cortex that ranged from increased activation for low sensation seek-
ers to lack of activation or deactivation for high sensation seekers (in
relation to baseline). Regions fitting this pattern would not be re-
vealed in direct contrasts between conditions. Direct contrasts be-
tween conditions confirmed that orbitofrontal regions that mediated
the relation between sensation seeking and cortisol change were not
differentially engaged across conditions (see Table 4). This analysis
showed that regions of the orbitofrontal cortex were significantly
activated in the Highly Acceptable condition (in comparison to the
Experimental Control condition and the Less Acceptable condition),
especially the lateral region.
1516 Freeman & Beer
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DISCUSSION
Although the relation between individual differences in sensation
seeking and risk taking has been theorized to reflect neurophysio-
logical differences, no single study has examined the hormonal and
neural systems involved in this relation. The current study replicated
Table4
Orbitofrontal Cortex Activations in Conjunction Analyses and Direct
Contrasts
ROI MNI Coordinates t-stat Cluster Size
Sensation Seeking and Highly Acceptable4Control
Left Medial OFC (BA 11) À10, 60, À16 4.10 48
Cortisol Change and Highly Acceptable4Control
Left Medial OFC (BA 11) À4, 50, À16 4.12 92
Conjunction Analysis: Highly Acceptable4Control
Left Medial OFC (BA 11) À4, 52, À16 3.69 55
Sensation Seeking and Less Acceptable4Control
Left Medial OFC (BA 11) À12, 30, À22 3.82 70
Right Lateral OFC (BA 47) 54, 26, À24 2.82 17
Cortisol Change and Less Acceptable4Control
Left Medial OFC (BA 11) À10, 28, À24 4.27 59
Right Lateral OFC (BA 47) 52, 30, À16 4.02 76
Conjunction Analysis: Less Acceptable4Control
Left Medial OFC (BA 11) À2, 32, À18 3.88 49
Left Medial OFC (BA 11) À10, 28, À24 4.02 57
Right Lateral OFC (BA 47) 49, 26, À12 4.27 25
Highly Acceptable4Control
Right Lateral OFC (BA 47) 58, 30, À6 3.57 31
Less Acceptable4Control
No OFC Regions
Highly Acceptable4Less Acceptable
Left Lateral OFC (BA 47) À50, 22, À8 3.33 13
Right Lateral OFC (BA 47) 48, 54, À10 3.43 48
Left Lateral OFC (BA 47) À48, 50, À8 4.35 30
Left Medial OFC (BA 11) À30, 44, À18 4.52 18
Right Lateral OFC (BA 47) 54, 28, À8 4.54 201
Less Acceptable4Highly Acceptable
No OFC Regions
Note. ROI 5regions of interests; OFC5orbitofrontal cortex; MNI 5Montreal
Neurological Institute.
1518 Freeman & Beer
previous research that has found a negative correlation between
sensation seeking and risk taking. The current study extended pre-
vious research by showing that (a) sensation seeking is negatively
correlated with rise in cortisol in relation to a risk task, (b) this neg-
ative correlation was partially explained by activation in the orbito-
frontal cortex, and (c) regions of the medial orbitofrontal cortex
partially mediated this negative correlation regardless of whether
activation was derived from conditions in which risk tended to be
accepted or rejected. The findings have a number of implications for
research that has examined pairwise relations between individual
differences in sensation seeking, risk, cortisol changes, and frontal
lobe activation.
One contribution of the present study is testing pairwise relations
between key variables that have previously been posited but had not
been empirically tested. Previous research on sensation seeking and
the brain has rarely examined the modulation of specific neural re-
gions in relation to a task. Studies have shown a relation between
sensation seeking and baseline frontal EEG asymmetry (e.g., San-
tesso et al., 2008) and overall increases in cortical activation
(Buchsbaum, 1971; Coursey, Buchsbaum, & Frankel, 1975; Haier,
Robinson, Braden, & Williams, 1984; Hegerl, Prochno, Ulrich, &
Muller-Oerlinghausen, 1989; Lukas, 1987; Lukas & Mullins, 1985;
Mullins & Lukas, 1984, 1987; Orlebeke, Kok, & Zeillemaker,
1989; Roger & Raine, 1984; Stenberg, Risberg, Warkentin, &
Rosen, 1990; Stenberg, Rosen, & Risberg, 1988; von Knorring,
1980; Zuckerman, Murtaugh, & Siegel, 1974; Zuckerman, Simons, &
Como, 1988). Studies that have examined task-related modulation of
specific brain regions have mostly focused on dopaminergic systems
in relation to reward. For example, sensation seeking predicted the
degree to which nucleus accumbens tracked reward probability in a
delayed incentive task (Abler, Walter, Erk, Kammerer, & Spitzer,
2006). Delayed incentive tasks are distinct from the risk task used in
the current study. Unlike a risk task, participants are informed of the
precise probability of a potential outcome. The present research
builds on previous research by showing that low sensation seeking is
associated with increased frontal lobe activation in response to a risk
task. Furthermore, sensation seeking was negatively associated with
medial orbitofrontal cortex activation regardless of whether this re-
gion’s activation was derived from a condition in which risk was
likely to be accepted or rejected. This suggests that low sensation
Sensation Seeking, Cortisol, and Brain 1519
seekers’ recruitment of their medial orbitofrontal cortex may sup-
port consideration of risk rather than thought specific to a final de-
cision about whether to take risk.
Additionally, previous research has found mixed results for the re-
lation between cortisol increases and frontal lobe activation. Some
studies have found a positive relation between cortisol increases and
frontal lobe activation (Kern et al., 2008; Liberzon et al., 2007; Wang
et al., 2007; Wang et al., 2005); others have found a negative relation
(Ahs et al., 2006; Pruessner et al., 2008). The results from the current
study additionally provide support for the positive association of
frontal lobe activation and cortisol increases. Future research is
needed to more fully understand why this relation varies from study
to study. One possibility is that these findings reflect differences in the
magnitude of emotional regulation demand. Stress responses may
vary in magnitude across studies, resulting in samples that are faced
with more or less challenging emotion regulation demands. Individ-
uals may not even engage regulatory processes or may attempt and
fail in especially stressful studies. In this case, frontal lobe deactivation
may reflect failure or excessive demand on an individual’s ability to
regulate emotion. Therefore, it may be that a rise in cortisol is pos-
itively associated with frontal lobe activation when emotion regula-
tion can be achieved and negatively associated with frontal lobe
activation when emotion regulation is not engaged or exceeds an in-
dividual’s regulatory resources. However, some of the studies that
found opposite patterns used the same general stress-eliciting proce-
dure, so reconciliation of these findings remains an open question.
Finally, most sensation seeking and cortisol studies have exam-
ined baseline or average cortisol levels (Croissant et al., 2008;
Rosenblitt et al., 2001; Wang et al., 1997). Studies that have exam-
ined the relation between sensation seeking and task-related changes
in cortisol have been exclusively in relation to stress tests that are not
specifically about risk taking (Couture et al., 2008; Netter et al.,
1996). The present study extends this research by showing that low
sensation seekers experience greater increases in cortisol in relation
to a risk task. One concern about the design of the current study is
that changes in cortisol reflect low sensation seekers’ stress elicited by
undergoing an experiment in a scanner environment. All participants
were aware that they would be going in a scanner, and the Time 1
cortisol sample was measured 15 min after participants had begun
preparation for the scanner. Stress associated with the scanner
1520 Freeman & Beer
procedure could have already been elicited at that time, yet sensation
seeking did not predict differences in Time 1 cortisol. Furthermore,
cortisol change was associated with general risk ratings but not rat-
ings in the conditions designed to elicit rejection or acceptance. This
suggests that cortisol change did not arise from general stress that
was constant across the scanner session. Future research that mea-
sures cortisol changes after separate sessions for different experi-
mental conditions will provide more robust evidence for the relation
between sensation seeking and cortisol changes associated with risk.
At a more mechanistic level, the findings of the present research
suggest some insight into the biological and psychological processes
associated with individual differences in sensation seeking. As men-
tioned above, low sensation seekers experienced greater rises in
cortisol after performing the risk task. It is unlikely that the orbito-
frontal cortex activation actually explains simple differences in re-
action time. Cortisol changes were not significantly correlated with
reaction time. The mediation analyses identified neural activity that
was (a) present regardless of whether low sensation seekers were
likely to either accept or reject the risk (i.e., medial orbitofrontal
cortex) and (b) specific to a condition in which low sensation seekers
were likely to reject the risk (i.e., lateral orbitofrontal cortex). Ad-
ditionally, two patterns characterized the relation between sensation
seeking and orbitofrontal cortex modulation across the experimental
conditions. Some of the medial orbitofrontal regions (Highly Ac-
ceptable: À4, 52, À16, BA 11; Less Acceptable: À2, 32, À18, BA
11) showed a trend toward greater engagement by low sensation
seekers for situations in which context for the risk was provided,
which contrasted with high sensation seekers’ trend toward greater
engagement for situations in which context for the risk was not pro-
vided. This pattern of findings may explain why previous research
has found both positive and negative associations between medial
orbitofrontal cortex function and ambiguity. Patients with orbito-
frontal damage do not show sensitivity to varying levels of ambigu-
ity, leading some researchers to conclude that this region is
fundamentally involved in tracking ambiguity (e.g., Hsu, Bhatt,
Adolphs, Tranel, & Camerer, 2005). In terms of the precise nature
of the relation between orbitofrontal cortex activation and ambigu-
ity, some studies have found that orbitofrontal cortex activation in-
creases as tasks become more ambiguous, particularly when the
task is ambiguous and affective (e.g., Elliot, Dolan, & Frith, 2000;
Sensation Seeking, Cortisol, and Brain 1521
Simmons, Murray, Matthews, Feinstein, & Paulus, 2006), whereas
other studies have found that orbitofrontal cortex activation de-
creases as ambiguity is reduced (e.g., Bhanji, Beer, & Bunge, 2010).
The findings in the current study suggest that the relation between
orbitofrontal cortex activation and ambiguity may be shaped by an
individual’s preference or tolerance for engaging in ambiguous tasks.
In other words, these regions do not predict what choice someone
might make in an ambiguous situation but instead are related to how
much ambiguous tasks are preferred or tolerated. High sensation
seekers are likely to have a high tolerance for ambiguity or even prefer
ambiguous situations to well-defined situations (Horvath & Zucker-
man, 1993). In this way, thinking over the more ambiguous scenarios
in the Experimental Condition may have been more enjoyable or tol-
erated than thinking over the scenarios that provided more context for
the high sensation seekers. In contrast, low sensation seekers should
want to avoid thinking about risk altogether, but if they must, they
may prefer or tolerate thinking about risk when more contextual in-
formation is provided. In this way, thinking over the scenarios in the
Highly Acceptable and Less Acceptable conditions may have been
more tolerable than the ambiguity of the Experimental Control con-
dition for low sensation seekers. Therefore, high sensation seekers
show a positive association between medial orbitofrontal activation
and the more ambiguous Experimental Control condition, whereas
low sensation seekers show a positive association between medial or-
bitofrontal activation and the less ambiguous Highly Acceptable and
Less Acceptable conditions.
Other orbitofrontal regions (Less Acceptable: À10, 28, À24, BA
11; 49, 26, À12, BA 47) showed a trend toward modulation by sen-
sation seeking in the Less Acceptable condition (but not the Exper-
imental Control condition). Both the medial and orbitofrontal
cortex have previously been associated with emotion regulation
(Beer, 2009; Ochsner et al., 2002). This pattern is consistent with
the view that risk taking requires more emotion regulation for low
sensation seekers. It is possible that the additional recruitment of the
lateral orbitofrontal cortex in the Less Acceptable condition reflects
greater magnitude of stress. In this case, it might be expected that
low sensation seekers engage additional neural structures to cope
with the greater emotion regulation demand.
Other models of orbitofrontal function suggest that there are psy-
chological distinctions between the medial and lateral portions of the
1522 Freeman & Beer
orbitofrontal cortex as well as distinctions between anterior and
posterior activation within the medial orbitofrontal cortex (Kringel-
bach & Rolls, 2004). For example, the medial orbitofrontal cortex is
important for encoding reward aspects of decisions, and the lateral
orbitofrontal cortex is important for encoding punishment aspects of
decisions. From this perspective, the contextual information across
the risk conditions may have elicited computations of potential re-
wards in both conditions, but the Less Acceptable condition addi-
tionally elicited computations of punishment. Furthermore,
individual differences predicted activation within the anterior por-
tion of the medial orbitofrontal cortex in the Highly Acceptable
condition, whereas they predicted activation within a relatively more
posterior portion in the Less Acceptable condition. It has been sug-
gested that more abstract rewards activate the anterior medial or-
bitofrontal cortex, whereas simpler reinforcers engage the posterior
medial orbitofrontal cortex. This distinction is consistent with the
differences manipulated across these conditions. The Highly Accept-
able condition focused on risks that may have long-term payoffs
(i.e., improved health), whereas the Less Acceptable condition was
focused on risks that had the potential for more concrete payoffs
(i.e., physical thrills). These findings raise the possibility that focus-
ing on direct contrasts between final decisions to take risks and de-
cisions to reject risks obscures processes that are differentiated by
sensation seeking much earlier in the decision process.
The present study illustrates an initial step toward building models
that incorporate variables at multiple levels, including individual
differences, task behavior, hormones, and neural activity. Much
more research is needed to flesh out the relations between sensation
seeking, risk taking, cortisol, and frontal lobe activation. Caution is
needed when interpreting mediation analyses in small samples. More
robust evidence for the current findings will require replications in
future studies involving larger samples that also include women. An-
other potential limitation of the current study is that confounding
factors such as drug abuse were self-reported and restricted to alcohol.
Future research needs to address potential confounds associated with
nicotine and other drug abuse as well as use more objective measure-
ment of alcohol abuse. Additionally, as mentioned above, separate
scanner sessions for each experimental condition will be critical for
fully understanding the modulation of cortisol in relation to these
decision processes. Finally, these findings should be investigated using
Sensation Seeking, Cortisol, and Brain 1523
experimental designs that more precisely isolate the psychological
meaning of the neural activation that explains the relation between
sensation seeking and risk-induced cortisol increases.
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SUPPORTING INFORMATION
Additional supporting information may be found in the online ver-
sion of this article:
Appendix SA1: Example coverage and signal for the orbitofrontal
regions. Individual subject’s co-registered, mean GRAPPA coverage
before smoothing (example subject from the beginning and end of
data collection). Crosshaires indicate the peak of the group activation;
individual subject’s time series for this cluster for the Experimental
and Control conditions are shown (y-axis 5percent signal chage).
Appendix SB1: Correlations between Sensation Seeking scores and
activation due to Experimental Control compared to Baseline (Null)
Condition in the left column and activation due to Risk Condition
compared to Baseline (Null) Condition in the right column for (A)
Medial Orbitofrontal Cortex (z 5 À18); (B) Lateral Orbitofrontal
Cortex (z 5 À24); (C) Lateral Orbitofrontal Cortex (z 5 À12).
Please note: Wiley-Blackwell is not responsible for the content or
functionality of any supporting materials supplied by the authors.
Any queries (other than missing material) should be directed to the
corresponding author for the article.
1528 Freeman & Beer
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