Frontal Lobe Sensation Seeking

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 moreoften because risk is emotionally more costly for them (in comparison tohigh sensation seekers). Therefore, individual differences in sensation seekingshould predict differences in risk task–induced cortisol changes. Further-more, the neural mediation that accounts for the relation between sensationseeking and cortisol changes has not been studied. The current study testedwhether individual differences in sensation seeking predicted cortisol changesin relation to a risk task and whether this relation was mediated by frontallobe activation. Participants (N5 17) who varied in sensation seeking com-pleted an fMRI study in which they rated the likelihood they would takevarious risks. Cortisol was measured from saliva samples collected prior toand after the fMRI procedure. The findings show that low sensation seekersshowed the greatest rise in cortisol after the risk procedure, and this relationwas 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 betweenindividual differences in sensation seeking and risk taking has been

theorized to reflect differences in physiological costs associated withrisk 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 (Coutureet 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: [email protected].

Journal of Personality 78:5, October 2010r 2010 The AuthorsJournal of Personality r 2010, Wiley Periodicals, Inc.DOI: 10.1111/j.1467-6494.2010.00659.x

mailto:[email protected]

Wang et al., 1997). Even though risky situations reflect stressful

circumstances in which an outcome is unknown, the uncertainty maynot 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 accountsfor 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 seekingpredict 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 totake 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, peoplewho are higher in sensation seeking report that they expect to

experience less anxiety when deliberating about risks they might takein 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 tolow sensation seekers. Furthermore, the difference in emotional cost

may not arise in relation to a final decision to take a risk but mightarise 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 levelswhen participants come to the lab; this baseline cortisol measure is

then correlated with scores on a questionnaire measuring individualdifferences in sensation seeking. Although there has been relatively

less research on how individual differences in sensation seeking relateto 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 astressful 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 sensationseekers are more likely to take risks and that their risk taking should

be accompanied by a reduced rise in cortisol when compared to lowsensation seekers. A further step in understanding the biological un-

derpinnings of the relation between sensation seeking and risk is toexamine how neural activity is related to sensation seeking, risk, andcortisol. Hormonal changes are mediated through neural activity,

and therefore, it is important to understand neural regions that maymediate 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 andrelease 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 havebeen 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 thesefrontal lobe regions are engaged in relation to increases in cortisolbecause 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 cortisolchange in a risk task. The orbitofrontal cortex is characterized by

large numbers of glucocorticoid receptors and has been implicated inenhanced HPA responses (in contrast to regions such as the anterior

cingulate, which is implicated in inhibiting HPA responses; Amatet 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 whereparticipants 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 theinterrelations between individual differences in sensation seeking, risktaking, cortisol changes, and frontal lobe activation. Consistent with

previous research, low sensation seeking is expected to be associatedwith reduced risk taking (Horvath & Zuckerman, 1993). In the con-

text of a risk task, low sensation seeking is expected to be associatedwith increases in cortisol just as it is in non-risk-related stress tasks

(Couture et al., 2008; Netter et al., 1996). Finally, the orbitofrontalcortex is likely to mediate the relation between sensation seeking and

cortisol change because of its role in emotion regulation (e.g., Bishopet 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 Leijenhorstet 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 thisrelation 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 decisionmaking 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 betweensensation 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 engagein 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 controlcondition designed to isolate neural activity associated with evaluatingcontextual information about a risk. This design permitted the exam-

ination of the theorized frontal lobe mediation of the relation betweensensation 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 participatedin the study. fMRI studies tend to involve smaller populations because ofmonetary restrictions and the hypothesized analyses already focused onone individual difference. Therefore, only men were included in this par-ticular study to reduce possible effects from other individual differencesand preserve statistical power in the small sample. The participants rangedin age from 18 to 33 years (M5 20.7 years, SD5 4.7 years) and had normalor 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 theUniversity 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(15 false; 25 true; M5 6.7, SD5 3.3; Cronbach’s alpha5 .80). Thisquestionnaire measures individual differences in deliberation about risktaking. 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 Inever think of possible complications,’’ and ‘‘I tend to change interests


frequently.’’ Although efforts were made to include participants whoshowed normal distribution in the sensation seeking variable, the smallsample made it difficult to achieve. Therefore, log-transformed sensationseeking scores were used in all analyses. Additionally, Spearman rankcorrelations are provided as complementary information to the Pearson’sr 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 for30 min before the study nor to engage in substantial physical exercise onthe day of the study. Cortisol levels were measured by collecting two sa-liva samples from each participant following procedures and precautionsnoted in Schultheiss and Stanton (2009). The first saliva sample was col-lected approximately 15 min before the fMRI scan and more than 15 minafter participants had begun preparation for the scanning procedure. Inorder to collect the first saliva sample, participants rinsed out theirmouths to remove any food particles. Next, participants chewed on apiece of Trident sugar-free gum for 3 min to stimulate salivation. Thenparticipants drooled 2.5 mL of saliva into a sterile polypropylene micro-tubule and spit out their gum. Saliva samples were immediately stored ina freezer in an adjacent lab room in order to avoid hormone degradationand 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 ResearchCenter 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-assayCV was 8.7%. There was a positive skew in the distribution of the cortisoldata, as is common for cortisol. To correct for this skew, the data werelog-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 Time1 cortisol as the predictor and Time 2 cortisol as the dependent variable.This approach is favorable over a simple change score when there is anexpectation that variation in the individual difference predictor mightrange from decreases to increases.

Alcohol Consumption and Sleep

Sensation seeking and cortisol can be affected by variables such as druguse and sleep. To test for potential confounds, participants reported their

1502 Freeman & Beer

weekly alcohol consumption (e.g., ‘‘How many drinks did you have onMonday?’’) 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 andhad 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 apicture and a short description of the risk (see Figure 1). Three differentrisk scenario conditions were created by using different descriptions foreach risk picture (50 pictures, 150 total trials). In the Highly AcceptableRisk condition, pictures were paired with scenario descriptions thatframed the risk as having potential benefits other than pleasure seeking(e.g., You are offered an experimental drug for an illness by a doctor). Inthe Less Acceptable Risk condition, the same pictures were paired withscenarios 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

Figure 1Example of three conditions and timing presented to participants

in the scanner.


Control condition, the pictures were paired with the basic risk scenariowithout additional contextual information (e.g., You are offered a pill).The purpose of this condition was to make it possible to isolate neuralactivation that specifically related to considering contextual factors thatmight bias decisions to take a risk in an Acceptable or Less Acceptabledirection. By including the Experimental Control condition, we couldspecifically control for neural activity associated with evaluating the basicscenario in the Highly Acceptable and Less Acceptable conditions ratherthan 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 randomnumber generator to assign the order of trials and examining the orthog-onality of experimental conditions in SPM2. Pictures were presented for6 s and were separated by intertrial intervals of 6-, 8-, or 10-s displays ofa fixation point (50%: 6 s; 25%: 8 s; 25%: 10 s; Donaldson, Petersen,Ollinger, & Buckner, 2001). Participants were instructed to clear theirminds when presented with the fixation point screens. The experimentincluded five runs that each included 30 trials and lasted for 6 min and46 s. The task was presented using DMDX software. Behavioral datawere log-transformed to ensure normal distribution.

Image Acquisition and Analysis

All images were acquired with a GE Sigma Excite 3-T magnetic resonanceimage 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 offthe anterior-commisure–posterior-commisure (AC–PC) plane, repetitiontime (TR)5 2,000 ms, parallel imaging (PI) acceleration factor5 3, echodelay time (TE)5 30 ms, flip angle of 90^o, field of view (FOV)5 240, 35slices, voxel size5 3 � 3 � 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 werediscarded to allow scans to reach equilibrium. Stimuli were viewed uti-lizing a back projection screen and a mirror mounted on the top of thehead coil. Responses were collected with MR-compatible buttons thatwere held in the right hand. A whole-brain structural scan was acquiredusing a T1-weighted SPGR sequence, which facilitated localization andcoregistration of functional data. Structural and functional volumes werenormalized to T1 and EPI templates, respectively. The normalizationalgorithm used a 12-parameter affine transformation together with anonlinear transformation involving cosine basis functions, and resampled

1504 Freeman & Beer

the volumes to 2 mm cubic voxels. Templates were based on the MontrealNeurological 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 usingtemporal sinc-interpolation. In addition, the images were realigned to thefirst image to adjust for residual head movement and corrected for move-ment using rigid-body transformation parameters. Images were thensmoothed with a 5 mm full-width/half maximum Gaussian kernel. Ahigh-pass filter with a cut-off period of 128 s was applied to remove driftswithin sessions.

A fixed-effects analysis was used to model event-related responses foreach 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 temporalderivative. Contrasts from each participant were used in a second-levelanalysis treating participants as a random effect. Group analyses werefocused 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. Highsensation seekers are expected to show weak or nonexistent activation ofthe orbitofrontal cortex, which may result in nonsignificant activationwhen averaged with low sensation seekers, making the restrictions ofregion of interest (ROI) to regions significantly activated in maps of directcontrasts between experimental conditions inappropriate. Regression an-alyses are more appropriate because they detect neural regions that varyin relation to individual differences variables. Therefore, group averageSPM{t} maps were created for regression analyses of interest: regressionsof 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 neuralmediators of the relation between sensation seeking and change in cortisolin 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 andsignificant conjunction with individual differences in change in cortisol,(b) minimum extent threshold of 10 contiguous voxels, (c) voxels withinthe orbitofrontal cortex as defined by Brodman’s Broca’s area (BA) 11and the inferior and lateral portion of BA 47 as defined by the AutomatedAnatomical Labeling map (AAL map; Tzourio-Mazoyer, et al., 2002),and (d) activation clusters corrected by an 8 mm radius sphere at � .05false discovery rate control (FDR) (derived from the half width of thesmoothing kernel and rounded up to the next resampled voxel). These


constraints were executed by conducting conjunction analyses of two re-gression maps for each of the risky decision conditions. The conjunctionanalyses were performed using the Minimum Statistic compared to theConjunction Null method (MS/CN; Nichols, Brett, Andersson, Wager, &Poline, 2005). First, we computed the intersection between the regressionof sensation seeking on the Highly Acceptable Risk4Experimental Con-trol and the regression of change in cortisol on the Highly AcceptableRisk4Experimental Control map. Similarly, we computed the intersec-tion of the regression maps for the regression of change in cortisol on theLess Acceptable Risk4Experimental Control condition and the regres-sion of change in cortisol on the Less Acceptable Risk4ExperimentalControl 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 activationclusters determined by a single individual difference variable. Nor doesit permit the possibility that activation in different subregions of theorbitofrontal cortex account for the statistical mediation of sensationseeking 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 neuralregion to those that are consistent with standardized criteria for extentand 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 sensationseeking, that reflect dispositional tendencies that transpire across con-texts raises questions about whether BOLD responses show reasonabletest-retest reliability. Research examining the test-retest reliability ofBOLD responses has found reliability for BOLD responses for scanningsessions taking place anywhere from 3 weeks to 1 year apart (Aron,Gluck, & Poldrack, 2006; Wei et al., 2004). For example, one study hadparticipants perform the same task in sessions occurring 1 year apartand 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 incortisol (Baron & Kenny, 1986). Parameter estimates for each of theneural 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 bemediated by variable Z (i.e., neural activity) when all of the variables arecorrelated and the correlation between X and Y is significantly reducedwhen controlling for Z. Partial mediation is operationalized as a marginalreduction (po.15) in the correlation X and Y when controlling for Z (seeFigure 2). Sensation seeking was regressed on neural maps, cortisolchange was regressed on neural maps controlling for sensation seeking,and sensation seeking was regressed on cortisol change controlling forneural activity.

Mediation analyses in small samples can be challenging because oflimited 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 moreappropriate for small samples (Preacher & Hayes, 2004) than the ap-proach using the Sobel test (Baron & Kenny, 1986). Therefore, we alsoanalyzed our data using a bootstrapping approach (bootstrap sam-ple5 1,000). 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-

SensationSeeking

Change inCortisol

Brain RegionParameter

a b

c (c’)

Figure 2Diagram of mediation analysis.


ipants decided to take the risk significantly more in the Highly Ac-ceptable Risk condition (M5 3.05, SE5 .43; t(16)5 5.05, po.05)

and significantly less in the Less Acceptable Risk condition(M5 2.08, SE5 .41; t(16)5 � 14.18, po.05) when compared to

the Experimental Control condition (M5 2.8, SE5 .40). Partici-pants’ decision to accept the risk was significantly higher in theHighly Acceptable Risk condition compared to the Less Acceptable

Risk condition (t(16)5 15.2, po.05).Participants took longer to make ratings in the Highly Acceptable

(M5 4.41 s, SD5 .68 s; t(16)5 9.2, po.05) and Less AcceptableRisk conditions (M5 3.94 s, SD5 .59 s; t(16)5 10.15, po.05) in

Figure 3Average ratings and reaction times for Highly Acceptable, Less

Acceptable, and Control conditions. Within each graph, differentletters indicate statistically significant differences.

1508 Freeman & Beer

comparison to the Experimental Control condition (M5 3.2 s,

SD5 .78 s). Participants also took longer to make ratings in theHighly Acceptable condition compared to the Less Acceptable con-

dition (t(16)5 3.3, po.05; see Figure 3).

Individual Differences in Sensation Seeking

Although the conditions were associated with different ratings onaverage, participants high in sensation seeking were more likely to

take the risk in all three conditions. Specifically, sensation seekingpositively correlated with ratings in the Highly Acceptable risk con-

dition (r5 .65, po.05), the Less Acceptable Risk condition (r5 .54,po.05), and Experimental Control condition (r5 .75, po.05). Sen-

sation seeking significantly predicted Time 2 cortisol (r5 � .52,po.05) but did not significantly predict Time 1 cortisol (r5 � .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, witha 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 � .31 to .54, suggestingthat there was a tendency for some individuals to show a decrease

whereas others experienced an increase in cortisol as a result of thetask. Change in cortisol negatively correlated with sensation seeking

(r5 � .51, po.05). High sensation seekers tended to exhibit less of arise in cortisol than low sensation seekers. In terms of task relation to

change in cortisol, ratings in the Experimental Control conditionwere significantly related to Time 2 cortisol (r5 � .48, po.05) butwere not significantly related to change in cortisol (r5 � .39,

p5 .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 correlatewith reaction times or with ratings in the Highly Acceptable and

Less Acceptable conditions (see Table 1 for correlations between allvariables).


Ta

ble

1In

terc

orr

ela

tio

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Am

on

gV

ari

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les

Variables

01

23

45

67

8

1.SensationSeeking

—

2.Changein

Cortisol

(�.48n)

�.51n

—

3.RatingHighly

Acceptable

(.68n)

.65n

�.22

—

4.RatingLessAcceptable

(.70n)

.54n

�.12

.80n

—

5.RatingsExperim

entalControl

(.77n)

.75n

�.39^

.88n

.85n

—

6.ReactionTim

eHighly

Acceptable

(.53n)

.25

�.02

.07

.28

.23

—

7.ReactionTim

eLessAcceptable

(.58n)

.23

.14

.19

.34

.30

.85n

—

8.ReactionTim

eExptl.Control

(�.02)

.10

�.41

.15

�.08

�.02

�.65n

�.79

—

Note.0indicatesSpearm

anrankcorrelationsforthesensationseekingvariable.

np�

.05.^p=

.12.

Effects of Alcohol and Sleep

Weekly alcohol consumption did not correlate with sensation seeking(r5 .05, p4.05), change in cortisol (r5 � .24, p4.05), or any of the

BOLD response parameter estimates (rs range from � .21 to .13).Sleep did not correlate with sensation seeking (r5 � .04, p4.05),

change in cortisol (r5 .02, p4.05), or any of the BOLD response pa-rameter estimates (rs range from � .16 to .12). Additionally, the re-lation between sensation seeking and cortisol remained significant

after controlling for weekly alcohol consumption and hours of sleep(r5 � .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 � .60 to � .70).

Mediation Analyses

Consistent with our hypothesis, low sensation seekers exhibited higherincreases in cortisol after performing the risk tasks, and this relation

was partially mediated by increased activity in the subregions of themedial and lateral orbitofrontal cortex in both the Highly Acceptable

and Less Acceptable conditions (see Table 2 and Figures 4–7). In theHighly Acceptable condition, the negative correlation between sensa-tion seeking and change in cortisol (b5 � .51, po.05) was partially

reduced when controlling for activity in regions of the medial orbito-frontal cortex (� 4 52 � 16, b5 � .13, Sobel test:Z5 � 1.80, po.08).

In order to better understand this mediation, sensation seeking wasexamined 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 theHighly Acceptable condition (compared to baseline, r5 � .39, p5 .12)

and a positive associative trend in the Experimental Control condition(compared to baseline, r5 .48, p5 .05). Low sensation seekers showedgreater increases in cortisol, and this relation was partially mediated by

medial orbitofrontal activity. The analyses of the parameter estimatesin relation to baseline suggest that the mediation occurred from both

greater engagement of medial orbitofrontal cortex by low sensationseekers for the Highly Acceptable condition as well as greater engage-

ment of medial orbitofrontal cortex by high sensation seekers for theExperimental Control condition.


Ta

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2R

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ion

An

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sis

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lyA

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tab

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tab

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s

ROI

(a)Sensation

seekingand

parameter

estimate

(b)Parameter

estimate

and

cortisol

change

controllingfor

sensation

seeking

(c)Sensation

seekingand

cortisol

change

(c’)Sensation

seekingand

cortisol

change

controllingfor

parameter

estimate

Sobel

Test

Statistic

pMediator?

Highly

Acceptable4Control

MedialOFC

(�4,52,�16)

(�.49n)�.70n

.55n

�.51n

�.13

�1.80

.08

Partial

LessAcceptable4

Control

MedialOFC

(�2,32,�18)

(�.57n)�.66n

.63n

�.51n

�.09

�2.00

.04

Yes

MedialOFC

(�10,28,�24)

(�.46)�.60n

.53n

�.51n

�.19

�1.70

.08

Partial

LateralOFC

(49,26,�12)

(�.56n)�.60n

.48n

�.51n

�.22

�1.58

.11

Partial

Note.Column(a):()indicatesSpearm

anrankcorrelationsforthesensationseekingvariable.ROI

5regionsofinterest;OFC

5orbito-

frontalcortex.

np�

.05.

In the Less Acceptable condition, the negative correlation be-tween sensation seeking and change in cortisol (b5 � .51, po.05)was also partially explained by activity in regions of the medial (� 2,

Figure 4Medial orbitofrontal cortex (z 5 � 16) partially mediates the relation

between sensation seeking and change in cortisol in the HighlyAcceptable Condition.

Figure 5Scatterplots 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.


Figure 6Neural regions mediating sensation seeking and change in cortisol

in the Less Acceptable condition. (A) Medial Orbitofrontal Cortex(z 5 � 18); (B) Lateral Orbitofrontal Cortex (z 5 �24); (C) Lateral

Orbitofrontal Cortex (z 5 � 12).

1514 Freeman & Beer

32, � 18, b5 � .09, Sobel test: Z5 � 2.00, po.04; � 10, 28, � 24,b5 � .19, Sobel test: Z5 � 1.70, po.08; but note that the relation

between sensation seeking and the parameter estimate for this latterregion is not significant when analyzed using Spearman’s rank cor-

relation) and lateral orbitofrontal cortex (49, 26, � 12, b5 � .22,Sobel test: Z5 � 1.58, 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 (� 2, 32, � 18) showed anegative 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

Figure 7Scatterplots of the regression of (a) sensation seeking and neural

parameter estimates and (b) cortisol change and neural parameterestimates in the Less Acceptable condition.


engagement of the medial orbitofrontal cortex by high sensation seek-

ers for the Experimental Control condition. However, the other medialorbitofrontal cortex region (� 10, 28, � 24) and the lateral orbito-

frontal cortex region (49, 26, � 12) showed negative associative trendswith the Less Acceptable condition but did not show an associative

trend with the Experimental Control condition (see Appendix B). Inthis case, these regions may have mediated the relation between sen-

sation seeking and cortisol change because of increased engagement bylow 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 (t5 � 2.29, po.05) was partially reducedwhen controlling for activity in the regions of the medial orbito-

frontal cortex (� 4, 52, � 16, t5 � .67, p4.10). In the Less Ac-ceptable condition, the negative correlation between sensation

seeking and change in cortisol (t5 � 2.29, po.05) was also partiallyexplained by activity in regions of the medial (� 2, 32, � 18,

t5 � .28, p4.10; � 10, 28, � 24, t5 � .58, p4.10) and lateral or-bitofrontal cortex (49, 26, � 12, t5 � .40, p4.10).

Although different subregions within the orbitofrontal cortex me-

diated the relation between low sensation seeking and change incortisol across the Highly Acceptable and Less Acceptable condi-

tions, both conditions were associated with significant orbitofrontalcortex 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 notdifferentially engaged across conditions (see Table 4). This analysis

showed that regions of the orbitofrontal cortex were significantlyactivated in the Highly Acceptable condition (in comparison to the

Experimental Control condition and the Less Acceptable condition),especially the lateral region.

1516 Freeman & Beer

Ta

ble

3M

ed

iati

on

An

aly

sis

Usi

ng

Bo

ots

tra

pM

eth

od

for

Hig

hly

Ac

ce

pta

ble

an

dL

ess

Ac

ce

pta

ble

Co

nd

itio

ns

ROIregions

b(M

X)Sensationseeking

andparameter

estimate

b(Y

M.X

)Parameter

estimate

andcortisol

change

b(X

Y)Sensation

seekingandcortisol

change

b(Y

X.M

)Sensation

seekingandcortisol

changecontrolling

forparameter

estimate

Coefficient

SE

tCoefficientSE

tCoefficientSE

tCoefficientSE

t

Acceptable4

Control

MedialOFC

(�4,52,�16)

�6.52

.08�2.88n

.14

.07

1.90w�1.56

.68�2.29n

�.67

.78

.86

LessAcceptable4

Control

MedialOFC

(�2,32,�18)

�9.10

2.68�3.39n

.14

.05

2.48n�1.56

.68�2.29n

�.28

.78�.36

MedialOFC

(�10,28,�24)�4.19

1.44�2.91n

.23

.11

2.12n�1.56

.68�2.29n

�.58

.77

.46

LateralOFC

(49,26,�12)

�9.53

2.59�3.68n

.12

.06

1.94w�1.56

.68�2.29n

�.40

.86

.65

Note.SE

5standard

error;ROI

5regionsofinterest;OFC

5orbitofrontalcortex;MNI=

MontrealNeurologicalInstitute.

npo

.05.w p

o.10.

DISCUSSION

Although the relation between individual differences in sensationseeking and risk taking has been theorized to reflect neurophysio-

logical differences, no single study has examined the hormonal andneural systems involved in this relation. The current study replicated

Table 4Orbitofrontal 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) � 10, 60, � 16 4.10 48

Cortisol Change and Highly Acceptable4Control


Conjunction Analysis: Highly Acceptable4Control


Sensation Seeking and Less Acceptable4Control


Right Lateral OFC (BA 47) 54, 26, � 24 2.82 17

Cortisol Change and Less Acceptable4Control



Conjunction Analysis: Less Acceptable4Control




Highly Acceptable4Control


Less Acceptable4Control

No OFC Regions

Highly Acceptable4Less Acceptable

Left Lateral OFC (BA 47) � 50, 22, � 8 3.33 13


Left Lateral OFC (BA 47) � 48, 50, � 8 4.35 30



Less Acceptable4Highly Acceptable

No OFC Regions

Note. ROI5 regions of interests; OFC5 orbitofrontal cortex; MNI5Montreal

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 cortexpartially mediated this negative correlation regardless of whether

activation was derived from conditions in which risk tended to beaccepted or rejected. The findings have a number of implications for

research that has examined pairwise relations between individualdifferences in sensation seeking, risk, cortisol changes, and frontallobe activation.

One contribution of the present study is testing pairwise relationsbetween key variables that have previously been posited but had not

been empirically tested. Previous research on sensation seeking andthe brain has rarely examined the modulation of specific neural re-

gions in relation to a task. Studies have shown a relation betweensensation 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 systemsin relation to reward. For example, sensation seeking predicted the

degree to which nucleus accumbens tracked reward probability in adelayed 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 theprecise probability of a potential outcome. The present research

builds on previous research by showing that low sensation seeking isassociated with increased frontal lobe activation in response to a risk

task. Furthermore, sensation seeking was negatively associated withmedial orbitofrontal cortex activation regardless of whether this re-

gion’s activation was derived from a condition in which risk waslikely to be accepted or rejected. This suggests that low sensation


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 andfrontal 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 offrontal lobe activation and cortisol increases. Future research isneeded to more fully understand why this relation varies from study

to study. One possibility is that these findings reflect differences in themagnitude of emotional regulation demand. Stress responses may

vary in magnitude across studies, resulting in samples that are facedwith more or less challenging emotion regulation demands. Individ-

uals may not even engage regulatory processes or may attempt andfail in especially stressful studies. In this case, frontal lobe deactivation

may reflect failure or excessive demand on an individual’s ability toregulate 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 lobeactivation when emotion regulation is not engaged or exceeds an in-

dividual’s regulatory resources. However, some of the studies thatfound 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 changesin cortisol have been exclusively in relation to stress tests that are notspecifically about risk taking (Couture et al., 2008; Netter et al.,

1996). The present study extends this research by showing that lowsensation seekers experience greater increases in cortisol in relation

to a risk task. One concern about the design of the current study isthat changes in cortisol reflect low sensation seekers’ stress elicited by

undergoing an experiment in a scanner environment. All participantswere aware that they would be going in a scanner, and the Time 1

cortisol sample was measured 15 min after participants had begunpreparation 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. Thissuggests 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 relationbetween sensation seeking and cortisol changes associated with risk.

At a more mechanistic level, the findings of the present researchsuggest some insight into the biological and psychological processesassociated with individual differences in sensation seeking. As men-

tioned above, low sensation seekers experienced greater rises incortisol 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 thatwas (a) present regardless of whether low sensation seekers were

likely to either accept or reject the risk (i.e., medial orbitofrontalcortex) and (b) specific to a condition in which low sensation seekerswere likely to reject the risk (i.e., lateral orbitofrontal cortex). Ad-

ditionally, two patterns characterized the relation between sensationseeking and orbitofrontal cortex modulation across the experimental

conditions. Some of the medial orbitofrontal regions (Highly Ac-ceptable: � 4, 52, � 16, BA 11; Less Acceptable: � 2, 32, � 18, BA

11) showed a trend toward greater engagement by low sensationseekers for situations in which context for the risk was provided,

which contrasted with high sensation seekers’ trend toward greaterengagement for situations in which context for the risk was not pro-

vided. This pattern of findings may explain why previous researchhas found both positive and negative associations between medialorbitofrontal 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 thetask is ambiguous and affective (e.g., Elliot, Dolan, & Frith, 2000;


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 betweenorbitofrontal 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 howmuch ambiguous tasks are preferred or tolerated. High sensation

seekers are likely to have a high tolerance for ambiguity or even preferambiguous 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 shouldwant 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 beenmore 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 activationand 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: � 10, 28, � 24, BA

11; 49, 26, � 12, 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 orbitofrontalcortex 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 lowsensation seekers. It is possible that the additional recruitment of the

lateral orbitofrontal cortex in the Less Acceptable condition reflectsgreater magnitude of stress. In this case, it might be expected that

low sensation seekers engage additional neural structures to copewith 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 lateralorbitofrontal cortex is important for encoding punishment aspects of

decisions. From this perspective, the contextual information acrossthe 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 Acceptablecondition, 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 posteriormedial 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 wasfocused 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 individualdifferences, task behavior, hormones, and neural activity. Much

more research is needed to flesh out the relations between sensationseeking, risk taking, cortisol, and frontal lobe activation. Caution is

needed when interpreting mediation analyses in small samples. Morerobust evidence for the current findings will require replications infuture studies involving larger samples that also include women. An-

other potential limitation of the current study is that confoundingfactors such as drug abuse were self-reported and restricted to alcohol.

Future research needs to address potential confounds associated withnicotine and other drug abuse as well as use more objective measure-

ment of alcohol abuse. Additionally, as mentioned above, separatescanner sessions for each experimental condition will be critical for

fully understanding the modulation of cortisol in relation to thesedecision processes. Finally, these findings should be investigated using


experimental designs that more precisely isolate the psychological

meaning of the neural activation that explains the relation betweensensation 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 orbitofrontalregions. Individual subject’s co-registered, mean GRAPPA coveragebefore 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-axis5percent signal chage).

Appendix SB1: Correlations between Sensation Seeking scores andactivation due to Experimental Control compared to Baseline (Null)

Condition in the left column and activation due to Risk Conditioncompared to Baseline (Null) Condition in the right column for (A)Medial Orbitofrontal Cortex (z5 � 18); (B) Lateral Orbitofrontal

Cortex (z5 � 24); (C) Lateral Orbitofrontal Cortex (z5 � 12).

Please note: Wiley-Blackwell is not responsible for the content orfunctionality of any supporting materials supplied by the authors.

Any queries (other than missing material) should be directed to thecorresponding author for the article.

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This document is a scanned copy of a printed document. No warranty is given about the accuracy of the copy.

Users should refer to the original published version of the material.

Frontal Lobe Sensation Seeking

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