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Neuropsychologia 45 (2007) 755–766

The neural processing of moral sensitivity to issues of justice and care

Diana Robertson a, John Snarey b, Opal Ousley c, Keith Harenski c,F. DuBois Bowman d, Rick Gilkey a, Clinton Kilts c,∗

a Goizueta Business School, Emory University, Atlanta, GA 30322, United Statesb Candler School of Theology, Emory University, Atlanta, GA 30322, United States

c Department of Psychiatry and Behavioral Sciences, Emory University School of Medicine, Atlanta, GA 30322, United Statesd Department of Biostatistics, Emory University School of Public Health, Atlanta, GA 30322, United States

Received 20 January 2006; received in revised form 4 August 2006; accepted 13 August 2006

bstract

The empirical and theoretical consideration of ethical decision making has focused on the process of moral judgment; however, a preconditiono judgment is moral sensitivity, the ability to detect and evaluate moral issues [Rest, J. R. (1984). The major components of morality. In W.urtines & J. Gewirtz (Eds.), Morality, moral behaviour, and moral development (pp. 24–38). New York, NY: Wiley]. Using functional magnetic

esonance imaging (fMRI) and contextually standardized, real life moral issues, we demonstrate that sensitivity to moral issues is associated withctivation of the polar medial prefrontal cortex, dorsal posterior cingulate cortex, and posterior superior temporal sulcus (STS). These activationsuggest that moral sensitivity is related to access to knowledge unique to one’s self, supported by autobiographical memory retrieval and socialerspective taking. We also assessed whether sensitivity to rule-based or “justice” moral issues versus social situational or “care” moral issues isssociated with dissociable neural processing events. Sensitivity to justice issues was associated with greater activation of the left intraparietal sulcus,hereas sensitivity to care issues was associated with greater activation of the ventral posterior cingulate cortex, ventromedial and dorsolateral

refrontal cortex, and thalamus. These results suggest a role for access to self histories and identities and social perspectives in sensitivity to moralssues, provide neural representations of the subcomponent process of moral sensitivity originally proposed by Rest, and support differing neuralnformation processing for the interpretive recognition of justice and care moral issues.

2006 Elsevier Ltd. All rights reserved.

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eywords: Functional magnetic resonance imaging (fMRI); Moral sensitivity;

. Introduction

Ethics refers to the body of moral values and principleseld by an individual or group. The ability to engage in eth-cal decision making is central to human social behavior andncompasses the detection and interpretation of moral issues, asell as the ability to reason and act based on moral principles.he determinants and underlying processes of moral thought andction have long been the subject of theorizing and debate. Early

mphasis was placed on a cognitive-developmental model basedn stages of moral reasoning ability that emphasized moral rea-oning as a conscious, deliberative process (Kohlberg, 1958,

∗ Corresponding author at: 4001 Woodruff Memorial Research Building, 101oodruff Circle, Emory University School of Medicine, Atlanta, GA 30322,nited States. Tel.: +1 404 727 8262.

E-mail address: sdpcdk@emory.edu (C. Kilts).

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028-3932/$ – see front matter © 2006 Elsevier Ltd. All rights reserved.oi:10.1016/j.neuropsychologia.2006.08.014

e; Care; Self-reference

984; Piaget, 1932, 1965). Later, neo-Kohlbergian theoristsdvanced theories emphasizing a context-dependent processnvolving components of moral decision making in addition toeasoning (Greene & Haidt, 2002; Haidt, 2001; Rest, 1994).hese theorists proposed that moral conflicts engage the auto-atic, implicit recruitment of cognitive structures, such as the

ctivation of social schemas or tacit knowledge (Narvaez &ock, 2002), that allow the detection and interpretation of aoral issue or situation (Rest, 1994). These processes may occur

elow the level of conscious awareness (Narvaez & Bock, 2002;est, Narvaez, Bebeau, & Thoma, 1999), and are generally anal-gous to the processes of moral sensitivity and moral intuition,hich have been described by Rest (1994) and Haidt (2001),

espectively. In particular, moral sensitivity refers to the detec-ion and interpretation of a moral issue or situation, includingwareness of how different individuals may be affected by anction taken in response to the issue (Rest, 1994). This inter-

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56 D. Robertson et al. / Neuro

retative awareness is the first component of ethical decisionaking in that it gives rise to the need to make a moral judg-ent, select a moral action, and other component processes oforal behavior. Understanding the process of moral sensitivity

s important, given its theoretical distinction from deliberativeoral reasoning (Brabeck & Rogers, 2000), its potential for

mprovement by training and education (Bebeau, 2002), sincendividuals vary dramatically in their ability to detect moralssues (Rest, 1984), and because moral failure can result from aack of moral sensitivity (Narvaez & Rest, 1995).

Additional advances in moral theory emphasized the distinc-ion between moralities of justice and care. Justice issues andthics apply to moral conflicts that are solved by universal ethi-al principles in the form of rules, rights, obligations and codesn the pursuit of fairness and impartiality. Justice issues rest onn ideal of reciprocity and equal respect and an injunction noto treat others unfairly. In the workplace, examples of justiceilemma issues are common (e.g., turning down a request to fal-ify information for a report; admitting responsibility for an erroreing blamed on someone else; declining a friend’s offer to pro-ide classified, insider information). Care issues and ethics applyo moral conflicts solved by a focus on the situational variableeeds and relationships of the people involved and guided byocial emotions such as empathy and altruism (Gilligan, 1982).are issues rest on an ideal of attention and response to individ-als’ needs and an injunction not to turn away from someone ineed (Gilligan & Attanucci, 1988). In the workplace, examplesf care dilemmas also are common (e.g., setting limits on workours in order to spend time with one’s children; visiting theym instead of working late; mentoring a difficult employee).evertheless, different professions are differentially associatedith justice (e.g., police) and care (e.g., nursing) modes of moral

hinking. Sex differences in justice and care thinking have beenroposed by Gilligan (1982), who contended that justice and careoral orientations, due to their consideration of different facts,

erspectives, and experiences, drive decision making behaviorsy relying on distinct cognitive processes. The research has,owever, been only partially supportive of such sex differences.n the one hand, women tend to have an elective affinity for theoice of care and men for the voice of justice. On the other hand,oth men and women are able to and do use both ethical voicesith equal levels of dexterity and complexity—that is, they areot significantly different.

Defining the neural information processing related to moralhought may inform these theories and their debate and pro-ide useful inferences as to the bases of immoral actions. Theelationship between brain states and states of moral thoughtnd behavior has been informed by neurological case studies.uch studies, perhaps most famously represented by that ofhineas Gage in the 19th century (Damasio, Grabowski, Frank,alaburda, & Damasio, 1994), indicate that moral thought andehavior are mediated, in large part, by the prefrontal cortex inhat damage to this area results in impaired social and moral

udgment (Anderson, Bechara, Damasio, Tranel, & Damasio,999). Recent in vivo functional neuroimaging studies have pro-ided an elaborated model of the neural representations of moralognitions, implicating a distributed cortical network involving

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ologia 45 (2007) 755–766

iverse frontal and posterior cortical areas including the ante-ior medial prefrontal and orbital frontal (OFC) cortex, posterioringulate cortex, anterior temporal lobes, posterior superior tem-oral sulcus (STS), and limbic regions (e.g., amygdala) (Greene,ommerville, Nystrom, Darley, & Cohen, 2001; Moll et al.,002; see Moll, Zahn, de Oliveira-Souza, Krueger, & Grafman,005 for an excellent review).

In the present functional magnetic resonance imaging (fMRI)tudy, we sought to isolate the neural correlates of one spe-ific component of moral thought, the ability to recognize andnterpret moral issues (i.e., moral sensitivity), and to comparehe neural processing related to moral sensitivity to two differ-nt types of moral content represented by issues of justice andare. We hypothesized that the social and personal implicationselated to the interpretive detection of moral issues are associatedith distinct neural information processing events when com-ared to the same task for nonmoral problems encountered inveryday decisions. To test this possibility, we developed narra-ives that depicted issues (both moral and nonmoral) encounteredy a hypothetical individual in a typical work setting. These nar-atives were designed to adhere to the principles of modern moralheory and its instruments and to enhance ecological validity byresenting contexts and issues highly familiar to our sample ofesearch volunteers. We also hypothesized that their relatednesso differing facts, suppositions and perspectives would resultn dissociable neural correlates of moral sensitivity to justiceersus care issues. Thus, we tested a topology of moral cog-ition that included the isolation of moral sensitivity and theistinction between the ethics of justice and care. At the neuralrocessing level, we hypothesized that moral sensitivity woulde associated with orbitofrontal cortex and perhaps amygdalactivations related to social cognitions, and that care and justicessues would differ in this regard.

. Materials and methods

.1. Subjects

The participants were 16 right-handed men (35 ± 5.1 years of age, range7–42) (means ± 1 S.D.) enrolled in the Executive Masters in Business Admin-stration (EMBA) degree program at the Goizueta Business School of Emoryniversity. Subjects had an average duration of occupation in business settingsf 13.5 ± 4.8 years prior to matriculation into the program.

Subjects had no personal history of psychiatric or neurologic disorders byelf-report and were financially compensated for their participation. Subjectsere pre-tested for reading speed using the Sight Word Efficiency subtest of theest of Word Reading Efficiency (Torgesen et al., 1999). The mean estimatedtandard score for the subject pool was 94.3 ± 7.1, indicating average sight wordfficiency for the group. The study was conducted in the Biomedical Imagingechnology Center at Emory Hospital. Following thorough discussion of the

ntent and risks associated with the study, subjects gave written informed consento participate in a study protocol approved by the Institutional Review Board ofmory University.

.2. Stimuli and tasks

We sought to adhere to a test of major elements of modern moral theory andherefore incorporated into the task stimuli features common to instruments usedn this field. Our choice of stimuli was driven by five key considerations, eachf which we discuss further below. The stimuli needed to meet the followingriteria: (i) be constructed by experts in the field of ethics and moral reasoning,

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ii) be ecologically valid for our sample, (iii) provide contrast between moralnd nonmoral issues, (iv) provide contrast between the moral issues of justicend care, and (v) satisfy criteria for content validity.

The base context of the stimuli was a revised version of the business casecenario developed by marketing ethicists Sparks and Hunt (1998) in their studyf ethical sensitivity. The characteristics of the Sparks and Hunt case scenariof greatest import to the design of the present study are that (i) the scenarioevelops both ethical and nonethical issues, and (ii) the issues are realistic andommonly faced in business settings. This case scenario consists of a descriptionf a workday in the life of “Bob,” a fictional marketing research analyst. As Boboes through his day, he reflects on the issues and decisions he faces. Using thisase context, the scenario content was modified to mirror situations in whichBA students are typically taught to problem solve, i.e., they are presentedith a business case scenario, which usually contains a wealth of information,uch of it irrelevant. The student’s task is to determine which issues and facts

n the case are important and which are unimportant. The revised scenario wasritten in the passive voice. Although Bob’s thoughts and actions, and prefer-

nces and concerns about particular situations were described, he did not exhibitntense displays of primary emotions (happiness, sadness, fear, surprise, anger,isgust).

We specifically adapted this revised case scenario by modifying and expand-ng it to reflect five types of discrete issues or events: strategic, tactical, justice,are, and neutral. The justice issues inherent in the Sparks and Hunt scenarioere modified and the care, strategic and tactical issues, and neutral events,ere created within the business situational context. The sequence of issues and

vents was developed as evolving “story segments” that comprised the overallase scenario or story. We developed a total of 41 story segments, 12 containedoral issues (describing six justice and six care issues), 12 contained nonmoral

ssues (describing six strategic and six tactical issues), and 17 contained neutralvents (see Appendix A for examples). A greater number of neutral events waseveloped to allow their interspersion with the other story segment types, and toenerate sufficient numbers of responses to neutral events to support their usen an event-related image analysis. Each story segment was 2–3 sentences (and3–35 words) in length and was written at approximately the ninth grade levelf reading comprehension, according to the Flesch–Kincaid scale that assesseseadability based on the average number of syllables per word and the averageumber of words per sentence. The 41 story segments were presented visuallyne at a time for 15 s each without interruptions between them. Story segmentsere presented in a block design in which two segments of a given type were

eparated by a neutral story segment, e.g., two care issues, followed by a neutraltory segment, followed by two strategic issues, etc. (Fig. 1).

Story segment content conformed to the following definitions:

Justice concerns fairness and impartiality. A just or fair person aims to treatanother person as an end rather than simply as a means to an end. Justicemeans liberating others from injustice.Care concerns benevolence and compassion. A caring person treats another

person with sensitive discernment of, and response to, his or her contextuallyembedded need. Care means liberating others from their state of need andactively promoting their welfare.Strategic decisions in organizations are typically concerned with the overallwell-being of the organization and involve long-range planning. Strategic

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ig. 1. A schematic illustration of the fMRI study design for the moral sensitivityegments processed for the identification of “important” issues or events is shown. Telated to the subject’s response.

ologia 45 (2007) 755–766 757

decisions may require the use of substantial resources, be characterized byuncertainty, and involve multiple participants in the decision process.Tactical decisions tend to be concerned with one part of the organization andwith immediate and routine day-to-day operations. Tactical decisions requirefew resources, are well structured, and are not expected to have long-termeffects.Neutral story segments described an event related to Bob or more generalinformation (e.g., the location of a vendor’s office) that did not pose a justiceor care moral issue or a strategic or tactical problem.

The story segments were examined for descriptions of social interactionsor the protagonist, Bob. Social interaction refers to Bob directly interacting orommunicating with others, e.g., “Bob telephoned a friend.” The incidence ofocial interaction was similar in the justice (5 of 6), care (4 of 6), and strategic3 of 6) story segments; the tactical story segments, by design, did not includeocial interaction.

The developed story segments were subjected to content validation by expertaters. A prototype set of 12 story segments (3 of each of the 4 types of moralnd nonmoral issues) was initially developed collaboratively by the authors,rawing upon their collective expertise related to ethical reasoning and businessecision making. The moral and nonmoral issues were then evaluated throughhe use of 10 graduate students who had completed advanced course work in thesychology of moral reasoning and who received brief supplemental training ontrategic and tactical reasoning. The student experts independently rated eachf the 12 dilemmas as primarily representing justice, care, strategic or tacticalssues. The experts showed a moderate level of agreement at this stage of storyegment development. When their rating differed from the intended category,ach rater was unblinded as to the construct the story segment was intended toddress and they were asked to write a brief explanation of why they had ratedhe story segment as they did and how the story segment might be improvedo better reflect the intended issue type. This feedback was used to revise thetory segments. The final set of prototype issues used in this study was againated independently by 10 additional graduate student expert raters. The expertshowed a high level of agreement in their ratings. All raters completely agreedn 112 of the 120 ratings and the eight errors (6.6%) were evenly distributedcross the four story segment types. Overall, average agreement among the 10aters was 93.3%, which supported the content validity of the story segmentssed in this study.

During fMRI acquisitions, story segments were presented through rearrojection to a screen placed at the end of the magnet bore and viewed by theubject via mirrors mounted on the head coil. Subjects were told that they wouldead a story about a workday in the life of Bob. They were instructed to readhe content of the story segments and respond using an MRI compatible buttonox to indicate with a right hand button press when they were able to “identifyn important point or issue” in the story. These instructions were intentionallyeneral, so as not to bias the subjects toward identifying one particular type ofssue included in the story. Subjects were instructed to respond as often as they

ished for each story segment, or not at all if no issue seemed important. Later

n the task protocol, three story segments within each category were sequentiallyepresented, and subjects were asked to rate their level of importance on aour-point scale; a rating of one indicated an issue that was “not important,” andscore of four indicated an issue that was “very important.” Before imaging,

task. An example of a sequential presentation of the different types of storyhe fMRI response and its statistical analysis focused on a “floating window”

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ubjects were familiarized with the stimuli and task and response requirementsf the study by identifying “important” items in a practice story segmentnvolving the purchase of an automobile by a separate fictional character, Joel.

.3. Behavioral data analysis

The total number and mean number of important issues detected for eachtory segment were calculated for the group, and pairwise comparisons acrosstory segment categories were made using the Wilcoxon Signed ranks test. Meanmportance ratings were also averaged for the story segment categories. Behav-oral measures were compared between the neutral story segment and the moralnd nonmoral story segment categories, and between the moral and nonmoralssue categories, with significant differences defined at a p < 0.05 level.

.4. fMRI acquisition and processing

All studies were conducted on a Siemens 3T whole body MRI scanner sitedn Emory Hospital. Brain imaging involved the acquisition of 25 axial slicesf 4 mm thickness, acquired parallel to the AC-PC line with a matrix size of4 × 64 over a field of view of 22 cm × 22 cm. Blood oxygenation level depen-ent (BOLD) contrast images were acquired (TE of 30 ms) using T2*-weightedradient echo, echo-planar pulse sequences with a TR of 4 s for a total of 154cans. In addition, a 3-D MP-RAGE sequence was collected at an isotropic res-lution of 1 mm × 1 mm × 1 mm for 3-D anatomic analysis and visualization ofask-related activations. Head movement was limited by padding and restraint.fter discarding the first five scans to allow longitudinal relaxation to equalize,

mages were resliced and corrected for motion by registration to the first func-ional image acquired for each subject using a six parameter transformation.mages were then spatially normalized to the Montreal Neurological InstituteMNI) template by applying a 12 parameter affine transformation followed byonlinear warping using basic functions. Images were smoothed using a Gaus-ian kernel of 8 mm full width at half maximum to enhance signal to noiseatios and facilitate the within group analysis. Differences in global BOLD sig-al were controlled by proportional scaling. Low frequency noise was removedsing a high-pass filter, and an autoregressive model was used to account forerial correlations in the data.

.5. fMRI data analysis

The data were analyzed in a two-stage, random effects procedure. In therst stage, the BOLD response for each story segment category for each sub-

ect was modeled with the standard canonical hemodynamic response functioncHRF). Parameter estimates of the cHRF were created via within subject con-rasts collapsed across conditions. The resulting summary statistic images werehen entered into a second stage analysis that treated each subject as a randomariable. In this way, both within and between subject variance is accounted

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able 1ehavioral ratings for the number of identified “important” issues and the level of the

ask Story segment category

Care Justice

otal numbera 54 ± 3.3b 86 ± 5.1ean number per story segmentd 0.59 ± 0.27 0.89 ± 0.19angee 0.17–1.00 0.67–1.33ean level of importancee,f 2.7 ± 0.6 3.0 ± 0.7

a Data represent the mean ± 1 S.D. number of identified issues of importance acrategories.b p < 0.005 compared to justice story segments.c p < 0.005 for pairwise comparisons for identified issues in neutral story segmentsd Data represent the mean number of issues identified as important per story segmee As indicated by the range data, subjects sometimes identified multiple issues with

egment. Data represent the mean ratings on a four point scale, with 1 = not importanf Data based on ratings for 15 of the 16 subjects.g p < 0.005 compared to strategic story segments.

ologia 45 (2007) 755–766

or in the model. Image analysis was conducted using MATLAB and Statisti-al Parametric Mapping software (SPM2; Wellcome Department of Cognitiveeurology, http://www.fil.ion.ucl.ac.uk/spm). A “window” of time bracketingsubject’s recognition of an important issue that included 2 s prior to and 1R after the subject’s button response (a total of 6 s) was used for the sta-

istical analysis (Fig. 1). In this way, the analysis is not a conventional eventelated design, but rather models the neural response related to moral sensi-ivity as a temporally extended “event” involving both issue awareness andnterpretive evaluation (Rest, 1984). Thus, the process of moral sensitivity ismplicitly captured by the explicit task of identifying “important” issues by but-on presses; as few as 27 and as many as 86 button responses were made for theeutral and justice issue categories, respectively. Isolating the neural responseo moral issues involved contrasting the response to moral issues to that of mul-iple control conditions. In planned comparisons to the moral (care and justice)ssues, neutral story segments were used to correct for neural activations relatedo attention, reading and comprehension, context processing and sensorimotorspects of task performance. Nonmoral (strategic and tactical) issues were useds additional control conditions to correct for activations related to temporallyxtended decisions involving multiple response options and that impact others.esponses to neutral story segments were included in the data analysis as 14f 16 individuals identified an important issue within at least one neutral storyegment. For the remaining two individuals, an event window within one neutraltory segment was selected at random in order to retain all subjects in the datanalysis. Unless otherwise indicated, all activations were assessed at a signifi-ance level of p < 0.001 (uncorrected) and an extent threshold of k > 5 voxels.n addition, functional volumes-of-interest (VOI) were defined based on activa-ions from the moral-nonmoral issue contrast and included all significant voxelsp < 0.001, uncorrected) within an eight mm radius of the peak voxel at an acti-ation location. Time courses for these VOI were plotted using finite impulseesponse functions (Burock & Dale, 2000; Ollinger, Shulman, & Corbetta, 2001)s implemented in SPM within the ROI toolbox created by Poldrack (SPM ROIoolbox, http://spm-toolbox.sourceforge.net).

. Results

.1. Behavior

Table 1 displays the total number and the average number ofssues per story segment perceived as “important” for each storyegment category. A significantly greater number of issues was

etected as important for all issue categories (i.e., justice, care,trategic, tactical) compared to neutral events. More justice thatare issues were identified, a finding consistent with the notionhat men, and perhaps business professionals, have a greater

ir perceived importance for the study story segment

Strategic Tactical Neutral

85 ± 4.9 66 ± 3.9 27 ± 1.6c

0.85 ± 0.2 0.67 ± 0.18 0.12 ± .08c

0.50–1.33 0.33–1.00 0–0.233.4 ± 0.7 2.8 ± 0.6g 1.4 ± 0.7c

oss subjects for the 13 neutral story segments and for six in each of the other

vs. the other story segment categories.nt, within each category.in one story segment as important or failed to recognize such an issue in a storyt and 4 = very important for three selected story segments in each category.

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ffinity for an ethic of justice. The mean level of importanceatings are also displayed in Table 1. Statistically significant dif-erences in mean level of importance ratings were obtained forll issue categories compared to neutral events, and for strate-ic versus tactical issues. Overall, these behavioral data supporthe intended greater salience of the care, justice, strategic andactical story segments relative to the neutral story segments.

.2. fMRI

To identify the neural correlates of moral sensitivity, anmplicit processing task involving the BOLD fMRI responsemmediately preceding and following the recognition of animportant” issue was considered in the data analyses. In thenitial analysis of moral sensitivity, we compared the neuralesponse to the combined story segments involving justice andare moral issues to the response to combined story segmentsnvolving strategic and tactical problems. This contrast indicatedhe differential activation of the medial prefrontal cortex, bilat-ral posterior superior temporal sulcus (STS), dorsal posterior

ingulate cortex, and medial orbitofrontal cortex for sensitivityo moral issues (Table 2). The medial frontal cortical activa-ion for this contrast spanned polar (BA 9) and ventral (BA0) prefrontal sites, and the orbitofrontal cortex. The combined

able 2natomical and stereotaxic locations of neural activations related to the implicit

ecognition of moral and nonmoral issues

rain region (Brodmann area) Voxel T Coordinates

x y z

ncreasesCare/justice (moral) > neutral (nonmoral)a

Posterior cingulate gyrus (31) 7.43 6 −49 30Insula 6.26 −30 −20 19Medial frontal cortex (9) 5.75 2 48 29Posterior STS (L22) 4.75 −59 −50 14Posterior STS (R22) 4.21 65 −52 14

Care/justice (moral) > strategic/tactical (nonmoral)a

Medial frontal cortexPolar (9) 7.69 4 62 32Ventral (10) 6.27 2 59 6

Posterior STS (R22) 7.2 65 −52 17Posterior STS (L22) 7.05 −59 −50 17Precuneus (7) 6.71 8 −50 45Orbital frontal cortex (11) 4.14 2 58 −11

ecreasesNeutral (nonmoral) > care/justice (moral)a

STS (R22) 7.28 65 −30 16Inferior frontal gyrus (R45) 5.68 48 35 2Middle frontal gyrus (R9) 5.55 48 17 27Middle frontal gyrus (L10) 5.18 −46 53 3Middle frontal gyrus (R10) 4.67 44 54 −6Ventrolateral prefrontal cortex (11) 4.36 24 48 −16

a p < 0.001, uncorrected. Stereotaxic locations are defined in Talairach coor-inate space (Talairach and Tournoux, 1988) in millimeters relative to theidsagittal plane (x), anterior/posterior to the anterior commissure (y), and

uperior/inferior to the anterior commissure–posterior commissure (AC–PC)lane (z).

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ologia 45 (2007) 755–766 759

esponse to the justice and care story segments was also com-ared to the response to the neutral story segments. This contrastas associated with relative activation of the dorsal posterior cin-ulate cortex, insula, polar medial (BA 9) prefrontal cortex, andilateral posterior STS for the combined moral issues (Table 2,ig. 2). Relative to the neutral story segments, the implicit recog-ition of moral issues was associated with decreased activationn distributed lateral frontal cortical sites, and the right STSTable 2).

The time course of the peristimulus hemodynamic responseunction for each story segment category for a VOI centered onhe voxel maxima for the polar medial prefrontal cortex, dor-al posterior cingulate cortex, and left posterior STS (Table 2)s illustrated in Fig. 2. These plotted relationships indicate thatolar medial prefrontal cortex activation associated with sensi-ivity to moral issues was related to both increases in activityor the recognition of moral issues and decreases in activity forhe recognition of non-moral (strategic and tactical) problems oreutral events (Fig. 2). Activations in the dorsal posterior cin-ulate cortex (Table 2) were apparently similarly attributable tooth recognition-related increases for moral issues and decreasesor non-moral problems or neutral events. Observed left poste-ior STS activations were the result of greater recognition-relatedncreases for moral issues.

Justice and care moral issues were also considered separately.direct comparison of justice and care moral issues indicated

hat sensitivity to care moral issues was associated with greaterctivation (p < 0.001, uncorrected) in the ventral posterior cingu-ate cortex, medial orbitofrontal cortex, right middle and inferiorrontal gyri, left posterior STS, and thalamus (Table 3; Fig. 3).elative to care issues, sensitivity to justice moral issues wasssociated with greater activation of the left intraparietal sulcusIPS) extending into the dorsal bank of the posterior STS, albeitt a less stringent statistical threshold. Compared to issue recog-ition in neutral story segments, sensitivity to care moral issuesas associated with activation of the dorsal posterior cingulate

ortex, polar and ventral medial prefrontal cortex, bilateral pos-erior STS, and insula (Table 3). Sensitivity to justice moralssues, relative to neutral events, similarly activated the dorsalosterior cingulate cortex, insula, polar medial prefrontal cortex,nd left posterior STS (Table 3; Fig. 3).

. Discussion

Theoretical accounts of moral decision making distinguishetween the component processes of moral sensitivity or intu-tion, judgment, motivation, and character related to moralehavior (Rest, 1984; Haidt, 2001). The primary goal of theresent in vivo functional neuroimaging study was to localizehose neural activations that are related to moral sensitivity,

component process proposed to involve both the detectionnd interpretation of a moral issue or situation. Moral behaviornd its cognitive and neural processing correlates are strongly

ependent on stimulus variables such as situational context andamiliarity, and subject variables such as beliefs, cultural affilia-ions, sex and occupation (Casebeer, 2003; Gilligan, 1982; Moll,ahn et al., 2005). In addressing these demands of ecological

760 D. Robertson et al. / Neuropsychologia 45 (2007) 755–766

Fig. 2. Location of significant (p < 0.001, uncorrected) neural activations related to sensitivity to moral (i.e., care and justice) vs. nonmoral (strategic and tactical)issues in the study story segments. The left side of the figure depicts the results of the random-effects group analysis and illustrates those brain regions that weredifferentially activated by the moral vs. nonmoral story segments superimposed on the standard MNI brain. The activation map and standard brain were importedf d subst f intero Supe

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rom SPM2 into the Analysis of Functional Neuroimaging (AFNI) software anype, the time course of the hemodynamic response for three brain activations on the peak voxel. PCC = Posterior Cingulate Cortex, Posterior STS = Posterior

alidity, this study design focused on the implicit recognition ofeal life ethical challenges encountered by male business pro-

essionals in a typical business setting. The value of this studyies, however, not in its ability to inform the neural representa-ions of moral sensitivity in business professionals, but rather tonform this process using ecologically relevant tasks to render

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ig. 3. Location of significant (p < 0.001, uncorrected) neural activations related to serom the SPM2 analyses are shown superimposed on axial images of the MNI brain s

equently rendered. The right side of the figure depicts, for each story segmentest computed as the impulse response function (IRF) for a 3D volume centeredrior Temporal Sulcus.

he results meaningful to everyday behavior for other subjectamples in familiar contexts. We speculate that similar results

ould be obtained related to the neural processing of moral

ssues in nurses confronting such issues in a hospital care settingr police functioning in a law enforcement setting. Such com-arisons would perhaps represent an informative assessment of

nsitivity to care vs. justice moral issues in the study story segments. The resultstandard.

D. Robertson et al. / Neuropsych

Table 3Anatomical and stereotaxic locations of differential neural activations related tothe implicit recognition of care and justice moral dilemmas

Brain region (Brodmann area) Voxel T Coordinates

x y z

Care > neutrala

Posterior cingulate gyrus (31) 6.55 8 -51 30Medial frontal cortex

Polar (9) 6.77 4 56 32Ventral (10) 4.84 4 58 3

Posterior STS (L 22) 5.44 −61 −52 15Insula 4.92 −30 −22 20Posterior STS (R22) 4.84 65 −52 14

Care > justicea

Retrosplenial cortex (31) 7.62 −6 −61 16Orbital frontal cortex (11) 5.27 2 46 −16Middle frontal gyrus (R8) 4.88 36 33 48Posterior STS (L22) 4.74 −67 −33 9Inferior frontal gyrus (R46) 4.26 50 32 11Thalamus 4.03 8 −11 13

Justice > neutrala

Posterior cingulate gyrus (31) 6.91 6 −49 30Insula (L) 5.47 −30 −22 21Medial frontal gyrus (9) 5.09 2 48 29Posterior STS (L 22) 4.05 −57 −42 9

Justice > careb

Posterior STS (left 22) 6.43 −59 −40 22

Stereotaxic locations are defined in Talairach coordinate space (Talairach andTournoux, 1988) in millimeters relative to the midsagittal plane (x), ante-rior/posterior to the anterior commissure (y), and superior/inferior to the anteriorc

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he influence of different affinities for care versus justice morali-ies on the neural representation of the sensitivity or interpretivewareness of care and justice moral issues. This contention,owever, needs to be evaluated.

.1. Moral sensitivity as a special case of self-referentialhinking?

The results of this study implicated three brain areas as criticalo moral sensitivity: the medial prefrontal cortex, the poste-ior cingulate cortex, and the posterior STS. Despite remarkableariability in stimuli and tasks between studies, these findingsre strikingly consistent with the results of prior fMRI studiesf implicit and explicit moral judgments (Greene et al., 2001;eekeren, Wartenburger, Schmidt, Schwintowski, & Villringer,003; Moll et al., 2002; Moll, Oliveira-Souza, Bramati, &rafman, 2002; Moll, Zahn et al., 2005) that revealed primaryeural activations in mesial cortical regions and the posteriorTS.

.1.1. Medial prefrontal cortex

In the current study, greater activation of the polar medial

refrontal cortex was associated with sensitivity to moral issuesersus either neutral events or nonmoral issues. The medial pre-rontal cortex has been implicated in diverse brain functions

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ncluding imitation (Chaminade, Meltzoff, & Decety, 2002),rocessing rewarded behavioral outcomes (Knutson, Fong,ennett, Adams, & Hommer, 2003), emotion response monitor-

ng (Lane, Reiman, Ahern, Schwartz, & Davidson, 1997), erroretection (Garavan, Ross, Murphy, Roche, & Stein, 2002), eval-ative judgments (Zysset, Huber, Ferstl, & Yves von Cramon,002), pain perception, and the temporal sequencing of behaviorDreher, Koechlin, Ali, & Grafman, 2002). All of these func-ions are arguably linked to self-monitoring behavior. RecentMRI studies of neural activations related to the concept of “self”ave demonstrated activation of the anterior medial prefrontalortex during self-referential processing (Fossati et al., 2003;ohnson et al., 2002; Kelley et al., 2002; Phan et al., 2004). Sim-lar to self referential processing (Kelley et al., 2002) and theroposed role of the medial prefrontal cortex in spontaneous selfeferential mental activity as a default mode of brain functionGusnard, Akbudak, Shulman, & Raichle, 2001), the implicitecognition of moral issues was associated with medial pre-rontal cortex “activations” that were, in significant part, theesult of deactivations of this area by the contrasted control con-itions (i.e., strategic and tactical or neutral story segments).lso, polar medial prefrontal cortex activation associated withoral judgments was observed for the comparison of personal

ersus impersonal moral issues—essentially a self-referenceask (Greene et al., 2001). Thus, a plausible functional inferences that access to knowledge of self is critical to moral sensitivity.his interpretation is consistent with a proposed role of tempo-

ally extended representations of event sequence knowledge inoral cognitions (Moll, Zahn et al., 2005), but emphasizes the

pecific involvement of self semantic knowledge perhaps akin tohe temporally extended, relatively context-independent “narra-ive” self (Gallagher et al., 2000). Such an overarching role forhe polar medial prefrontal cortex in moral cognition explainsts common activation across diverse moral cognition tasks.

The medial prefrontal cortex has, however, also been asso-iated with performance on “theory of mind” tasks, whichequire an ability to imagine or predict another’s perspective,ntentions, or actions (Castelli, Happe, Frith, & Frith, 2000;ogeley et al., 2004; but see Bird, Castelli, Malik, Frith, &usain, 2004). Although participants in the current study wereot instructed to consider the mental states of others in the storyegments, the observed medial prefrontal cortex activation mayeflect an implicit theory of mind process. Thus, a seeminglyompeting interpretation is that medial prefrontal cortex activa-ions related to moral sensitivity represent the involvement ofhird-person, rather than first-person, perspective taking. Whileecent fMRI studies have sought to dissociate the neural corre-ates of first- and third-person perspectives, their attribution ofbserved medial prefrontal cortex activations to either the first-r third-person perspective are remarkably discordant (Ruby

Decety, 2003; Vogeley et al., 2004). This discrepancy mayeflect differences between studies in the object of perspectivee.g., inanimate objects, their mothers), or the belief that self

erspective is an integral process in assessing the perspectivef others (e.g., Gilovich, Medvec, & Savitsky, 2000). Consis-ent with this belief, recent reviews (Frith, 2001; Wicker, Ruby,oyet, & Fonlupt, 2003) concluded that medial prefrontal cortex

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62 D. Robertson et al. / Neuro

ctivations observed when mental states are attributed to othersverlap those associated with the monitoring of one’s own men-al state. We therefore propose that the medial prefrontal cortexctivation observed in this study is consistent with moral sen-itivity as a perspective-taking process involving access to bothelf and social semantic knowledge. This interpretation is con-istent with theoretical models of moral thinking that proposehat moral decisions and actions are related to self-identity andelf-interests (Bersoff, 1999; Haviv & Leman, 2002) and thatoral thinking is dependent on understanding others’ perspec-

ives (Rest, 1984).

.1.2. Dorsal posterior cingulate cortexSensitivity to moral issues was associated with activation of

osterior cingulate cortex located on the dorsal bank of theingulate gyrus. This activation was observed in prior stud-es of moral reasoning and was specifically associated withvaluating the appropriateness of solutions to personal moralilemmas (Greene et al., 2001). The posterior cingulate cortexas been implicated in seemingly diverse functions includinghe experience of emotion (Mayberg et al., 1999), recall of emo-ional memories (Maratos, Dolan, Morris, Henson, & Rugg,001; Maddock, Garrett, & Buonocore, 2003), reward process-ng (Knutson et al., 2003), forgivability (Farrow et al., 2001),nd self-reference (Fossati et al., 2003; Johnson et al., 2002;elley et al., 2002; Ruby and Decety, 2003). The posterior

ingulate cortex is also activated by the successful recall of auto-iographical memories (Maddock, Garrett, & Buonocore, 2001;iefke, Weiss, Zilles, Markowitsch, & Fink, 2003). Andersont al. (1999) have argued that moral judgments are related toccess to memories of outcomes of past moral decisions. Thus,he observed posterior cingulate cortex activation may reflecthe dependence of moral sensitivity on access to one’s emo-ional, cognitive and somatic experiences related to previous

oral conflicts. In particular, the posterior cingulate cortex mayediate the process by which knowledge of past experiences is

sed to guide an interpretive awareness of moral situations. Fur-hermore, the posterior cingulate cortex may contribute to moralvaluations made by taking a first-person perspective (Ruby &ecety, 2003) and predicting one’s own responses, emotional ortherwise, to a specific moral action. This interpretation is con-istent with the posterior cingulate cortex as an interface betweenmotion and cognition (Bush, Luu, & Posner, 2000; Vogt, Finch,

Olson, 1992) and with the social intuitionist model proposedy Haidt (2001) and Greene and Haidt (2002).

.1.3. Posterior STSBrain regions bordering the STS, particularly its posterior

xtent, have been implicated in perceptions related to social cog-ition (Adolphs, 2003). Cortex within and adjacent to the STSs activated by social signals involving expressive movements ofhe face, hands, mouth and eyes, and referred to as “biological

otion” (Allison, Puce, & McCarthy, 2000; Grezes et al., 2001;

axby, Hoffman, & Gobbini, 2000; Kilts, Egan, Gideon, Ely, &offman, 2003). The posterior STS is also activated during effort

elated to assessing the intentions of other individuals or viola-ions of expectation, often modeled in theory of mind paradigms

fiao

ologia 45 (2007) 755–766

Castelli et al., 2000; Gallagher et al., 2000; Grezes, Frith, &assingham, 2004). Its demonstrated roles in social perceptionnd maintaining social behavioral representations are consistentith a role of the posterior STS in social perspective taking in

he service of moral sensitivity. This interpretation is consistentith the view of moral decision making as a social process atten-

ive to the actions of external audiences (Carpendale & Krebs,995). Even in Kohlberg’s (1984) theory of moral judgment,he ability to perceive the perspectives of others and social roleaking were deemed essential to moral decision making, partic-larly for individuals at higher stages of moral reasoning ability.osterior STS activation is consistent across tasks that requireerceptual, cognitive, and emotional perspective taking (Frith,001; Ruby & Decety, 2001). The role of the posterior STS inultimodal sensory integration (Karnath, 2001; Taylor, Moss,tamatakis, & Tyler, 2006) suggests that its further role maye to integrate perspectives taken from these different vantageoints.

Two brain areas implicated in prior functional neuroimagingtudies of moral cognitions – the amygdala (Moll et al., 2002;reene et al., 2001) and anterior temporal cortex (Moll, Zahn

t al., 2005) – were not activated by this moral sensitivity task.imilar to the results of an fMRI study of moral judgments foron-emotional stimuli (Moll, Oliveira-Souza et al. 2002), amyg-ala activation was not observed in the present study of moralnd non-moral story segments that were devoid of overt emotionontent. Absent amygdala and anterior temporal cortex activa-ions may reflect the omission of overt emotional responses inhe story segments and the resulting lack of processing demandsor evaluating emotional salience and motivation, or for accesso the representations of social emotions (Moll et al., 2005).

.2. Common and distinct neural representations ofensitivity to moral issues of justice and care

Moral sensitivity to either care or justice issues was associatedith activation of the dorsomedial prefrontal cortex, posteriorTS and posterior cingulate cortex. However, the results of thistudy also support a distinction between neural information pro-essing related to sensitivity to justice and care moral issues. Thethics of justice relies on processing issues based on rules, andocial codes and mores. In contrast, the ethics of care emphasizeseeling rather than thinking in processing moral issues, presum-bly drawing on social and primary emotions in evaluating moralonflicts. The direct comparison of responses to care and justiceoral issues revealed activation of the medial orbitofrontal cor-

ex, a paralimbic sensory association area implicated in socialnd emotional behavior (Adolphs, 2003; Anderson et al., 1999;rothers, 1990) and in the processing of social emotions (DecetyChaminade, 2003; Moll et al., 2002; Moll, Oliveira-Souza

t al., 2002; Moll et al., 2005) for sensitivity to care moralssues. The role of social emotions in sensitivity to care issues isupported by the additional engagement of the ventromedial pre-

rontal cortex, relative to the neutral condition, an area involvedn social and emotional semantic representations (Moll, Zahn etl., 2005) and in emotional empathy (Saxe, 2006). The medialrbitofrontal cortex has also been implicated in third-person

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erspective taking (Ruby & Decety, 2004). With the thalamus,he medial orbitofrontal and ventromedial prefrontal cortex mayomprise a neural pathway by which affective, somatosensory,nd autonomic representations are used to detect and evaluateare issues. Sensitivity to moral issues of care was also associ-ted with differential activation of the ventral posterior cingulateortex, suggesting that its role in the integration of emotion andemory-related processes (Maddock et al., 2003) is distinctly

nvolved in the interpretive awareness of care versus justiceoral issues. Sensitivity to moral issues of care may thus involve

motion processing at both the first-person and third-person per-pective, and the recall of social-emotional representations ofast moral conflicts. This interpretation is consistent with theonceptualization of the “ethics of care” proposed by Gilligan1977) and reinforced by Noddings (1984), that emphasizesonsiderations of emotional response and a balance of self-erspective versus other perspectives.

The direct comparison of sensitivity to justice relative toare moral issues revealed a preferential activation for justicessues in only the left IPS, and only at a less stringent statisticalhreshold. Left IPS activations have been associated with the pro-essing of categorical representations (Saneyoshi, Kaminaga,

Michimata, 2006), of behavioral actions and their intentionsFogassi et al., 2005), and the processes of imitation (Iacoboni,005) and heteromodal association for crossmodal binding ofeatures to form coherent object or situational representationsTaylor et al., 2006). Thus, greater left IPS activation observedn the current study for justice versus care issues may reflect inte-rating situational features and simulating their representationor reference to categorical properties of laws, mores and rules.hese implied functional attributes of a differential left IPS acti-ation associated with an interpretive awareness of justice moralssues are consistent with the application of a standard set of ruleso the evaluation of justice moral issues (Colby & Kohlberg,987), though this inference is highly speculative based on theimited available evidence.

.3. Limitations of the study

Several limitations of this study of moral sensitivity exist androvide direction for future studies of moral behavior. First, thistudy included only male subjects. The selection of a single sexas motivated by a prominent, though controversial, contention

hat sex differences exist in moral orientation (Gilligan, 1982). Alear need exists to replicate this study with female subjects, par-icularly a study of possible sex effects on the neural correlatesf care and justice moral judgments. Second, this study focusedn the implicit recognition of moral versus non-moral issues asmeasure of moral sensitivity. The dissociation of neural infor-ation processing related to implicit versus explicit tasks has

een the subject of recent functional neuroimaging studies (e.g.,ritchley et al., 2000) and would be of interest here in assess-

ng whether the putative topology of moral behavior (Narvaez

Rest, 1995; Rest, 1994) includes dissociable neural correlates

or moral sensitivity versus post-hoc reasoning. Third, the defi-ition of a functional neuroanatomy of moral sensitivity wouldenefit from the consideration of individual variation in abil-

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ologia 45 (2007) 755–766 763

ty. Structured instruments and interviews (i.e., Moral Judgmentnterview and the Ethics of Care Interview) were used to assesshis variance, but yielded an insufficient dynamic range of scoreso permit their use in regression models analyzing the fMRIata. Although the functional inferences from this study provideestable hypotheses for such future research, much remains to beone in elaborating a more definitive model of the neural basisf moral cognition. Fourth, the study focused on business pro-essionals enrolled in an executive MBA degree program andhus the results could be considered to be informative of thisample only. However, research has shown that the moral rea-oning of business graduate students and business professionalss comparable to that of college students and adults in generalRest, 1994) and more representative of the general populationhan that of other professional groups (e.g., law, medicine).

In summary, the results of this study are consistent withhe involvement of a network of brain regions in moral sen-itivity which perhaps subserve complementary roles related torst-person perspective taking, access to autobiographical mem-ries and knowledge related to self and social cognition andhird-person attributions of mental states. We found a distinc-ion between the neural representation of care and justice moralensitivity that emphasizes differences in the roles of socialnd emotional information in their interpretive awareness. Ouresults provide support at the level of neural processing modelsor the contentions of the theorists Rest and Kohlberg that self-nd other-perspective taking is an important component of moralhought, as well as support for Gilligan’s distinction betweenustice and care issues and her emphasis on the importance ofmotion in the “ethics of care.” Future research may focus onorollaries of these findings—that immoral actions may reflectn exaggerated or dysfunctional self-representation, inaccessi-ility of internal models of behavior formed by past experiences,faulty perspective of the outcome of actions on others, or theirombination. Our findings also have implications for the devel-pment of moral sensitivity, suggesting that efforts to sensitizendividuals to moral issues focus on methods that tap into intro-pection based on personal experiences, as well as the use oferspective taking techniques such as role playing.

cknowledgments

We gratefully acknowledge the research assistance of Ajayambiar, Andrew Bates, Brittany Bragg, J. Aaron George, and F.lark Power. We also acknowledge the invaluable contributionsf Dr. Xiaoping Hu and the staff of the Emory University-eorgia Tech Biomedical Imaging Technology Center.

ppendix A

.1. Instructions

You will read the story one paragraph at a time. You will

ave fifteen seconds to read each paragraph. Please take yourime and read each paragraph carefully. If you believe that anmportant issue is raised in the paragraph, push button number1) on the keypad with your index finger.

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64 D. Robertson et al. / Neuro

It was a late morning in mid-December. Bob Smith, a researchnalyst, was in his office at the L & H Marketing Researchompany, a firm located in a metropolitan center on the Eastoast. N1

Bob was working furiously to complete the marketing strat-gy report for his client, Standard Grooming Products. The clientas in the process of introducing a new men’s hair spray product.

Standard Grooming needed data on the buying practices andedia habits of men who use hair spray. Print, TV and radioedia outlets were of particular interest. NBob began to review his current situation and his on-going

istory with the project. NTwo years ago, Bob had joined L & H, a marketing research

ompany specializing in consumer products. Before that he hadorked for another marketing research firm. NA long series of problems had slowed the marketing research

eport that was due on Monday. Bob regretted having to leaveis wife and children to come into the office today, a Saturday,o complete the report. C

He really did not like spending weekends away from his fam-ly. Most of all, he did not like disappointing his 12 year-oldaughter by missing her Saturday morning basketball game. C

Bob’s thoughts returned to the marketing strategy report andhe client’s files sitting on his mahogany desk. N

Bob’s boss, Barry Michaels, had originally recommendedhat they focus on TV advertising. Barry had made it clear thate only wanted to see data that supported his thinking. Bob nownew that the survey results painted a different picture. J

Bob felt pressured by Barry, his boss, to “bend” thenterpretation of the data. Bob, however, was reluctant to

ake the survey results appear more consistent with Barry’siases. J

A telephone call from the weekend guard served as a remindero Bob that he had ordered a take-out lunch from the local deli.ob told the guard to allow the delivery person access to L & Harketing’s suite of offices. NBob continued to review the history of the project. He recalled

hat back in September he had followed L & H Marketing’semplate for standard sampling procedures for projects of thisype. T

On this basis, he had considered surveying 250 users of men’sair spray from each of 15 different cities. This would haveesulted in a total sample of 3750 men. T

The building was almost empty. Bob found that a quiet envi-onment facilitated his ability to think through the history of theroject. N

Bob recalled disagreeing with Charles Chastain, from Stan-ard Grooming’s marketing department. Charles had arguedor samples proportional to city sizes. This, however, wouldean committing more money and resources over the life of

he project. SIn the end, they disagreed. Charles stressed the importance

f collecting more representative data that would increase the

1 N: Neutral; C: Care; J: Justice; T: Tactical; S: Strategic.

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ologia 45 (2007) 755–766

tudy’s validity. Bob, however, was concerned about the increasen cost that would interfere with doing other studies of equalmportance. S

While Bob was going over these issues in his mind, his lunchrrived: a beverage and sandwich in a plain cardboard container.fter finishing his lunch, Bob returned to thinking about hisarketing report. N

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