Abstract

Converging evidence suggests that emotion processing mediated by ventromedial prefrontal cortex (vmPFC) is necessary to prevent personal moral violations. In moral dilemmas, for example, patients with lesions in vmPFC are more willing than normal controls to approve harmful actions that maximize good consequences (e.g., utilitarian moral judgments). Yet, none of the existing studies has measured subjects' emotional responses while they considered moral dilemmas. Therefore, a direct link between emotion processing and moral judgment is still lacking. Here, vmPFC patients and control participants considered moral dilemmas while skin conductance response (SCR) was measured as a somatic index of affective state. Replicating previous evidence, vmPFC patients approved more personal moral violations than did controls. Critically, we found that, unlike control participants, vmPFC patients failed to generate SCRs before endorsing personal moral violations. In addition, such anticipatory SCRs correlated negatively with the frequency of utilitarian judgments in normal participants. These findings provide direct support to the hypothesis that the vmPFC promotes moral behavior by mediating the anticipation of the emotional consequences of personal moral violations.

INTRODUCTION

For decades, moral psychology has been concerned with identifying a rational basis of human morality (Kohlberg, 1969; Piaget, 1965). A different and more recent approach, however, places strong emphasis on the causal power of affective and intuitive processes to drive our moral judgment and convictions (Haidt, 2001). Integrating these opposite views, recent work in psychology and neuroscience has suggested that moral judgments are mediated by two classes of computational processes (Greene, Nystrom, Engell, Darley, & Cohen, 2004; Greene, 2003; Greene & Haidt, 2002; Greene, Sommerville, Nystrom, Darley, & Cohen, 2001). One class, referred to as moral intuition, consists of emotion-laden processes that automatically evaluate socially relevant stimuli along a right–wrong or like–dislike dimension. A second class, moral reasoning, consists of controlled, deliberative processes that arrive at moral judgment or decision through laborious steps of deductive reasoning and cost–benefit analyses.

For the most part, these processes work cooperatively to promote moral behavior. Certain ethical dilemmas, however, involve decisions in which the tension or conflict between intuitive and deliberative processes becomes apparent (Greene et al., 2001). One such dilemma is illustrated by the classic trolley problem (Thomson, 1986; Foot, 1978), in which two moral scenarios, impersonal versus personal, are contrasted. On the impersonal version (trolley dilemma), a bystander can use a switch to redirect a runaway trolley away from five victims and onto a single victim; on the personal version (footbridge dilemma), a bystander can push a single victim off of a bridge in front of a runaway trolley in order to stop its progress toward five victims. From a simple “economic” point of view, the two dilemmas are identical (i.e., killing one person to save five lives). Yet, numerous empirical studies have demonstrated that a large majority of individuals consider it morally acceptable to sacrifice one person to save five in the impersonal dilemma, whereas they believe that it is wrong to push the large man to save the five victims (Ciaramelli, Muccioli, Ladavas, & di Pellegrino, 2007; Koenigs et al., 2007; Mikhail, 2007; Cushman, Young, & Hauser, 2006; Valdesolo & DeSteno, 2006; Greene et al., 2001, 2004; Petrinovich, O'Neill, & Jorgensen, 1993).

According to Greene et al. (2001), the reason for these seemingly contradictory responses lies in the stronger tendency of personal scenarios (i.e., the push case), compared to impersonal scenarios (i.e., the switch case), to engage emotional processes which would affect moral decisions. Supporting this proposal, neuroimaging has revealed that impersonal and personal moral dilemma yield dissociable patterns of neural activation (Greene et al., 2001). Specifically, impersonal moral scenarios characteristically yield greater activation in brain areas associated with problem solving and deliberate reasoning [including dorsolateral prefrontal cortex (dlPFC) and inferior parietal lobule], whereas personal moral scenarios yield greater activation in brain areas that have been implicated in emotion and social cognition (such as medial prefrontal cortex and posterior cingulate gyrus).

In this view, the thought of pushing someone in front a trolley (i.e., a personal moral violation) elicits prepotent, seemingly negative, emotional responses that oppose or prohibit such repugnant act. In this case, making “more rational,” “utilitarian” choices (i.e., deciding that is acceptable to make a harmful act in order to maximize overall utility) would require overriding a strongly aversive emotional response. Accordingly, in a later study, Greene et al. (2004) found that the (infrequent) selection of utilitarian responses in the context of personal moral dilemmas elicits heightened activity in both “cognitive” (such as dlPFC) and emotional brain areas (including medial prefrontal cortex, posterior cingulate area, and anterior insula). Interestingly, utilitarian decisions were also associated with increased activity in anterior cingulate cortex, which is thought to reflect the conflict between competing processes (Botvinick, Cohen, & Carter, 2004), namely, cognitive processes favoring a utilitarian judgment and the emotional response to the prospect of doing harm to others.

Perhaps the most direct evidence supporting a necessary role of emotion in shaping moral decisions has emerged from the neuropsychological investigation of individuals with selective deficits in affective processing. More specifically, patients with adult-onset lesions in ventromedial prefrontal cortex (vmPFC) develop a marked, albeit isolated, impairment in social behavior that has been consistently attributed to a defective engagement of social emotions, such as guilt, embarrassment, and shame. Recent research has demonstrated that vmPFC patients respond normally to impersonal moral scenarios. However, they are more likely than control groups to endorse moral violations (i.e., inflicting serious harm to people) in personal moral scenarios (Ciaramelli et al., 2007), specifically, “high-conflict” personal scenarios, situations in which there are no clear social norms to decide whether a behavior is morally right or wrong (Koenigs et al., 2007; Hauser, 2006).

One interpretation of this result is that vmPFC patients lack automatic affective responses, or aversion signals, impeding any personal moral violation. When affective reactions dissolve (due to brain damage), principled reasoning aimed at maximizing benefits and minimizing costs may prevail, thereby increasing the rate of “rationally appropriate” utilitarian choices (Greene, 2007; but see also Moll & de Oliveira-Souza, 2007, for a different view).

Patient lesion studies, thus, strongly suggest that emotions, particularly those subserved by vmPFC, are integral constituents of our moral views. These conclusions, however, rest entirely on the assumption of general emotional blunting or flattened affect following vmPFC damage, a notion based on previous work concerning vmPFC and nonmoral (and nonsocial) decision-making (i.e., gambling task; Bechara & Damasio, 2005; Bechara, Tranel, Damasio, & Damasio, 1996; Damasio, 1994), or the evaluation of emotional responses to standardized social stimuli (see Koenigs et al., 2007). None of the existing studies has systematically measured subjects' emotional responses emerging during (and, presumably, having an impact on) evaluation of moral dilemmas. This is particularly relevant considering that in specific social circumstances, vmPFC patients have been found to exhibit increased, rather than reduced, emotional reactivity (Koenigs & Tranel, 2007; Barrash, Tranel, & Anderson, 2000; Grafman et al., 1996). Therefore, critical evidence linking vmPFC, emotion, and moral judgments is still lacking.

The aim of the present study is the gathering of direct psychophysiological evidence, both in healthy and neurologically impaired individuals, that emotions are crucially involved in shaping moral judgment, by preventing personal moral violations. Toward this end, 8 patients with focal lesion involving the ventromedial sectors of prefrontal cortex (vmPFC patients), 7 control patients with lesions outside the frontal lobe (non-FC patients), and 18 healthy controls responded to personal as well as impersonal moral dilemmas while skin conductance response (SCR) was recorded as a physiological index of affective state.

The SCR is related to the sympathetic division of the autonomic nervous system (Boucsein, 1992), and is widely used as a sensitive and objective measure of emotional processing (Dawson, Schell, & Filion, 2007; Naqvi & Bechara, 2006; Büchel, Morris, Dolan, & Friston, 1998). Moreover, among cortical regions, vmPFC is presumed to be critically implicated in the generation and feedback representation of bodily states of arousal (i.e., somatic markers), indexed by SCR, in the context of social, emotional, and motivational behavior (Nagai, Critchley, Featherstone, Trimble, & Dolan, 2004; Bechara, Damasio, Damasio, & Lee, 1999; Bechara et al., 1996; Damasio, 1994; Tranel & Damasio, 1994). Consequently, SCR is a measure ideally suited to study the relationship among vmPFC, emotion, and moral decision-making.

First, we expected to replicate previous evidence that, compared to normal controls, patients with vmPFC damage are more willing to judge moral violations as acceptable behaviors in personal moral dilemmas, whereas their performance in impersonal and nonmoral dilemmas is comparable to the controls. If emotional state activation mediated by vmPFC plays a critical and selective role in shaping personal moral judgments, then we should observe differences in SCRs between patients with vmPFC damage and comparison groups during contemplation of personal moral scenarios (such as the footbridge dilemma), but not during contemplation of impersonal moral scenarios (such as the trolley dilemma).

An additional prediction, derived from the hypothesis that emotional reactions drive disapproval of harmful actions (even when aimed at promoting the greater good), was that skin conductance activity during contemplation of personal moral dilemmas would be negatively correlated with the tendency toward utilitarianism (i.e., percentage of utilitarian judgment made) in normal controls. In other words, we predicted that SCR would be higher in participants exhibiting fewer utilitarian choices than in those with a higher rate of utilitarian responses.

METHODS

Participants

Three groups of subjects participated in the study: (a) a group of patients with focal lesions involving vmPFC bilaterally (the vmPFC group, n = 8); (b) a control group of patients with damage sparing frontal cortex (the non-FC group, n = 7); and (c) a control group of healthy subjects (the HC group, n = 18), who were matched on age, education, and sex with the vmPFC group.

Brain-damaged patients were recruited from the Centre for Studies and Researches in Cognitive Neuroscience in Cesena, and from the Azienda Ospedaliera Spedali Civili in Brescia. They were selected on the basis of the location of their lesion evident on CT or MRI scans. Table 1 shows demographic and clinical data, as well as the Mini-Mental Status Examination score (MMSE; Folstein, Robins, & Helzer, 1983). There were no significant differences between vmPFC patients and comparison groups with regard to age, education, clinical and personality variables (p > .05 in all cases).

Table 1. 

Summary Data for Participants [Mean (Standard Deviation)]

Group
Sex (M/F)
Age at Test (Year)
Education (Year)
Time since Lesion (Year)
Lesion Volume (cc)
MMSE
vmPFC (n = 8) 7/1 53.1 (10.8) 13.3 (4.9) 5.1 (3.2) 35.3 (16.7) 27.1 (1.8) 
non-FC (n = 7) 6/1 52.7 (16.6) 11.8 (4.5) 3.4 (2.6) 25.5 (10.4) 27.5 (1.3) 
HC (n = 18) 16/2 53.5 (12.6) 13.5 (5.7) – – 28.7 (0.5) 
Group
Sex (M/F)
Age at Test (Year)
Education (Year)
Time since Lesion (Year)
Lesion Volume (cc)
MMSE
vmPFC (n = 8) 7/1 53.1 (10.8) 13.3 (4.9) 5.1 (3.2) 35.3 (16.7) 27.1 (1.8) 
non-FC (n = 7) 6/1 52.7 (16.6) 11.8 (4.5) 3.4 (2.6) 25.5 (10.4) 27.5 (1.3) 
HC (n = 18) 16/2 53.5 (12.6) 13.5 (5.7) – – 28.7 (0.5) 

MMSE = Mini-Mental State Examination.

In the vmPFC group, lesions were caused by rupture and repair of anterior communicating artery (ACoA) aneurysm. Lesions involved vmPFC—defined as the medial one-third of the orbital surface and the ventral one-third of the medial surface of the frontal lobe, following the boundaries laid out by Stuss and Levine (2002)—and adjacent basal forebrain area.1 The vmPFC damage was bilateral in all cases, although often asymmetrically so. All vmPFC patients presented with clinical evidence of a decline in social interpersonal conduct, impaired decision-making, and emotional functioning, but had generally intact intellectual abilities (see Table 2).

Table 2. 

Results of Selected Neuropsychological Tests [Mean (SD)]

Group
SRM
Digit Span Forward
Phonemic Fluency
Semantic Fluency
WMS
Stroop Task Errorsa
vmPFC 43.8 (4.7) 5 (0.8) 24.5 (7.8) 39.6 (7) 84.6 (5.4) 6 (3.4)a 
non-FC 43.1 (4.4) 5.1 (0.9) 23.2 (6.3) 39.8 (2.8) 89.8 (4.1) 3.7 (0.8) 
HC 46.3 (3.4) 5.1 (0.9) 26.9 (5) 43.1 (4.7) 96.9 (5.4) 1.9 (1.3) 
Group
SRM
Digit Span Forward
Phonemic Fluency
Semantic Fluency
WMS
Stroop Task Errorsa
vmPFC 43.8 (4.7) 5 (0.8) 24.5 (7.8) 39.6 (7) 84.6 (5.4) 6 (3.4)a 
non-FC 43.1 (4.4) 5.1 (0.9) 23.2 (6.3) 39.8 (2.8) 89.8 (4.1) 3.7 (0.8) 
HC 46.3 (3.4) 5.1 (0.9) 26.9 (5) 43.1 (4.7) 96.9 (5.4) 1.9 (1.3) 

SRM = Standard Raven Matrices (scores in percentile values); WMS = Wechsler Memory Scale.

aValues that differ significantly between groups.

The non-FC patients were selected on the basis of having damage that did not involve the frontal lobe, and also spared the amygdala and the insula in both hemispheres. In this group, lesions were unilateral in six patients (in the left hemisphere in 2 cases, and in the right hemisphere in 4 cases) and bilateral in one patient. Brain lesions were caused by arterial–venous malformation in one case, and by ischemic or hemorrhagic stroke in the remaining six cases. Lesion sites included the occipital lobe in two patients, the lateral occipito-temporal junction in three patients, and the lateral occipito-parietal junction in the remaining two patients.

All subject groups were administered a short neuropsychological battery including tests with potential sensitivity to frontal damage, as well as intelligence and memory tests (results are provided in Table 2). The groups differed significantly only in their performance on the Stroop task, with vmPFC subjects making more errors than both non-FC patients and healthy controls (Mann–Whitney U test, p < .05). Patients were not receiving psychoactive drugs at the time of testing, and had no other diagnosis likely to affect cognition or interfere with participation in the study (e.g., significant psychiatric disease, alcohol misuse, history of cerebrovascular disease, focal neurological examination). Neuropsychological and experimental studies were all conducted in the chronic phase of recovery, more than a year post-onset. All lesions were acquired in adulthood. Patients gave informed consent to participate in the study according to the Declaration of Helsinki (International Committee of Medical Journal Editors, 1991) and the Ethical Committee of the Department of Psychology, University of Bologna.

Normal participants were healthy volunteers who were not taking psychoactive medication, and were free of current or past psychiatric or neurological illness as determined by history. Normal controls scored at least 28 out of 30 on the MMSE.

Lesion Analysis

Lesion analysis was based on the most recent clinical CT or MRI. The location and extent of each lesion were mapped by using MRIcro software (Rorden & Brett, 2000). The lesions were manually drawn by a neurologist with experience in image analysis onto standard brain template from the Montreal Neurological Institute, which is based on T1-weighted MRI scans, normalized to Talairach space. This scan is distributed with SPM99 and has become a popular template for normalization in functional brain imaging. For superimposing of the individual brain lesions, the same MRIcro software was used. Figure 1 shows the extent and overlap of the brain lesions in the brain-damaged patients. Brodmann's areas (BA) affected in vmPFC group were areas 10, 11, 32 (subgenual portion), and 24, with region of maximal overlap occurring in BA 10 and 11.

Figure 1. 

Location and overlap of brain lesions. The panel shows the lesions of the eight patients with vmPFC damage projected on the same seven axial slices and on the mesial view of the standard Montreal Neurological Institute brain. The level of the axial slices has been marked by white horizontal lines on the mesial view of the brain. z-Coordinates of each axial slice are given. The color bar indicates the number of overlapping lesions. In each axial slice, left hemisphere is on the left side. Maximal overlap occurs in the ventral and anterior portions of medial prefrontal cortex (Brodmann's areas 10, 11, and 32).

Figure 1. 

Location and overlap of brain lesions. The panel shows the lesions of the eight patients with vmPFC damage projected on the same seven axial slices and on the mesial view of the standard Montreal Neurological Institute brain. The level of the axial slices has been marked by white horizontal lines on the mesial view of the brain. z-Coordinates of each axial slice are given. The color bar indicates the number of overlapping lesions. In each axial slice, left hemisphere is on the left side. Maximal overlap occurs in the ventral and anterior portions of medial prefrontal cortex (Brodmann's areas 10, 11, and 32).

Materials

Stimuli in the present study were 15 personal moral dilemmas, 15 impersonal moral dilemmas, and 15 nonmoral dilemmas, randomly selected from a battery of 60 dilemmas developed by Greene et al. (2001), and used in our previous study (Ciaramelli et al., 2007). Ten out of 15 personal moral scenarios were “high-conflict” dilemmas, whereas the remaining 5 were “low-conflict” dilemmas, as identified by Koenigs et al. (2007) on the basis of the reaction times and level of agreement among normal controls.

Moral dilemmas are supposed to elicit moral emotions (i.e., emotions that respond to moral violations, or that motivate moral behavior, such as shame, guilt, pride, and compassion; Haidt, 2007; Tangney, Stuewig, & Mashek, 2007), whereas nonmoral dilemmas are not (Greene et al., 2001). Typical examples of nonmoral dilemmas posed questions about whether to buy a new television or to have your old television repaired for the same price, or whether to travel by bus or train given certain time constraints.

Task Procedure

An IBM-compatible Pentium IV computer running E-Prime software (Psychology Software Tools, 2002, Pittsburgh, PA) controlled the presentation of dilemmas, timing operation, and behavioral data collection. Subjects sat in front of a computer screen (21-in. VGA monitor) in a quiet and dimly lit room. Each dilemma was presented as text through a series of two screens. The first screen described the scenario and was presented for 45 sec. The second screen posed a question about the appropriateness of an action one might perform in that scenario, that is, the “dilemmatic question” (e.g., “Is it appropriate to save the five persons by pushing the stranger to death?”). Participants indicated their judgments by pressing one of two different keys on the computer keyboard. There was no time limit. Participants were told to respond as soon as they had reached a decision. The intertrial interval, during which a blank screen was displayed, lasted for 20 sec in each trial, allowing the psychophysiological response (see below) to return to baseline after each trial.

For all dilemmas being tested, (“appropriate”) affirmative responses implied the maximization of overall consequences (Greene, 2003), for instance, killing one instead of five persons (in a moral dilemma), or buying a new television instead of repairing the old one for the same price (in a nonmoral dilemma). However, only for moral dilemmas did “appropriate” responses result in moral violations. Note that “appropriate” and “inappropriate” is a value-neutral description of what the participant said about the action in the dilemma and not an evaluation of the participant's decision. Both the number of “appropriate, affirmative responses and response times (RTs; i.e., the time from the onset of the dilemmatic question to the moment a response was given)” were collected. Dilemmas were presented in random order in a single session that lasted approximately 70 min.

Psychophysiological Data Acquisition and Reduction

We used the skin conductance activity as a dependent measure of emotional arousal and somatic state activation. For each participant, prewired Ag/AgCl electrodes (TSD203 Model; Biopac Systems, Goleta, CA), filled with isotonic hyposaturated conductant, were attached to the volar surface of the middle and index fingertip of the nondominant hand and held firmly in place with Velcro straps. Importantly, doing so left the dominant hand free for behavioral responses. The electrode pairs forming part of the input circuit were excited by a constant voltage of 0.5 V (Fowles et al., 1981; Lykken & Venables, 1971) and the current change representing conductance was recorded using a DC amplifier (Biopac GSR100) with a gain factor of 5 μS/V and low-pass filter set at 10 Hz. The analog signal was digitized using the MP-150 digital converter (Biopac Systems) at a rate of 200 Hz and fed into AcqKnowledge 3.9 recording software (Biopac Systems). As subjects performed the moral judgment task seated in front of the computer, SCR was collected continuously and stored for off-line analysis on a second PC. Each testing session began with a 10-min rest period during which the participants' SCR acclimated to the environment, and the experimenter ensured a correct attachment and conductance of the electrodes. Presentation of each dilemma was synchronized with the sampling computer to the nearest millisecond. Furthermore, each time the subject pressed a response key, this action coincided with a mark on the SCR polygram. During acquisition of the psychophysiological data, the participants were asked to remain quiet and as still as possible to avoid confounding these measurements.

After acquisition, skin conductance values were transformed to microsiemens values using the AcqKnowledge software. Also, this software provides an extensive array of measurements that can be applied to the collected data. Raw skin conductance data were low-pass filtered to remove high-frequency noise. The slow downward drift in baseline skin conductance level was removed using a moving difference function with a difference interval of 0.05 sec. Before the start of recording, we ensured that subjects were able to generate SCRs to external stimuli, such as loud sounds (i.e., hands clapping).

RESULTS

Behavioral Data

The proportion of affirmative responses (e.g., utilitarian choices in the context of personal moral dilemmas) for each type of dilemma and each participant group were computed (see Figure 2). The data were subjected to a mixed-design ANOVA, with group (vmPFC, non-FC, HC) as a between-subject factor, and dilemma (personal, impersonal, nonmoral) as a within-subject factor. The ANOVA yielded a significant main effect of group [F(2, 30) = 4.4, p < .05], as well as of dilemma [F(2, 30) = 6.3, p < .005]. Critically, the two-way interaction between group and dilemma was significant [F(4, 60) = 2.6, p = .05]. Pairwise comparisons showed that both control groups gave fewer affirmative responses to personal (HC = 0.32, non-FC = 0.30) as compared to impersonal (HC = 0.51, non-FC = 0.57) and nonmoral dilemmas (HC = 0.52, non-FC = 0.51; all ps < .05). By contrast, vmPFC patients made a similar proportion of “appropriate,” affirmative responses across all types of dilemma (0.59, 053, and 0.57, for personal, impersonal, and nommoral dilemma, respectively; all ps > .05).

Figure 2. 

Proportion of affirmative responses to personal, impersonal, and nonmoral dilemmas in ventromedial prefrontal patients (vmPFC), nonfrontal patients (non-FC), and healthy controls (HC). Bars refer to 1 standard error of the mean.

Figure 2. 

Proportion of affirmative responses to personal, impersonal, and nonmoral dilemmas in ventromedial prefrontal patients (vmPFC), nonfrontal patients (non-FC), and healthy controls (HC). Bars refer to 1 standard error of the mean.

A more focused analysis on response patterns within the personal moral dilemmas revealed that vmPFC patients were more likely to endorse the “appropriate” (e.g., utilitarian) response than either comparison groups when high-conflict scenarios were presented (Kruskal–Wallis test, H = 11.9, df = 2, p < .01). In contrast, for low-conflict personal scenarios, the frequency of selecting the affirmative response was negligible and with no significant difference between vmPFC patients and control groups (H = 1.3, df = 2, p = .5).

The RT data (Figure 3) were also subjected to a mixed-design ANOVA with group (vmPFC, non-FC, HC) as a between-subject factor, and dilemma (personal, impersonal, nonmoral) and response (affirmative, negative) as within-subject factors. As a violation of the ANOVA, assumption of sphericity was detected using the Mauchly sphericity test and the Greenhouse–Geisser correction for repeated measures was applied.

Figure 3. 

Mean response time for affirmative and negative responses to personal, impersonal, and nonmoral dilemmas in ventromedial prefrontal patients (vmPFC), nonfrontal patients (non-FC), and healthy controls (HC). Bars refer to 1 standard error of the mean.

Figure 3. 

Mean response time for affirmative and negative responses to personal, impersonal, and nonmoral dilemmas in ventromedial prefrontal patients (vmPFC), nonfrontal patients (non-FC), and healthy controls (HC). Bars refer to 1 standard error of the mean.

The analysis revealed a significant main effect of group [F(2, 30) = 5.4, p < .01], as well as a significant two-way interaction between choice and dilemma [F(2, 60) = 5.9, p < .01]. Moreover, the ANOVA yielded a marginally significant three-way interaction [F(4, 60) = 2.6, p = .07]. Pairwise comparisons showed that healthy controls and nonfrontal, control patients took longer to make affirmative relative to negative responses in personal moral dilemmas (HC: 4996 vs. 3625 msec; non-FC: 8805 vs. 5709 msec; both ps < .01), but not in impersonal moral dilemmas (HC: 3548 vs. 3654 msec; non-FC: 6352 vs. 6597; both ps > .5), and in nonmoral dilemma (HC: 3837 vs. 3759 msec; non-FC: 6140 vs. 6496 msec; both ps > .5). In stark contrast, vmPFC patients showed similar RTs for affirmative and negative responses in either personal (5315 vs. 6341 msec), impersonal (6937 vs. 7365 msec), and nonmoral dilemmas (7725 vs. 7854 msec; all ps > .1).

Psychophysiological Data

For analysis, each trial was divided off-line into four separate time periods: (a) baseline, the 15-sec time period immediately preceding each dilemma; (b) contemplation, the 45-sec time window during which participants viewed the dilemma; (c) decision, the time period comprised between the presentation of the dilemmatic question and the emission of a response; (d) postresponse, the 5-sec time period following participants' response. To examine psychophysiological changes in more detail, the contemplation period was further divided into three consecutive epochs, lasting 15 sec each. SCRs were computed for each epoch of a trial as “area under the curve” (Naqvi & Bechara, 2006; Vianna & Tranel, 2006; Damasio et al., 2000). The “area under the curve” measurement is similar to the function of an “integral” except that, instead of using zero as a baseline for integration, a straight line is drawn between the endpoints of the selected area to function as the baseline. The area is expressed in terms of amplitude units (microsiemens, μS) per time interval (sec). All SCRs were square-root-transformed to attain statistical normality.

Baseline SCRs

Skin conductance levels during the baseline period were submitted to a mixed design ANOVA with group (vmPFC, non-FC, HC) as a between-subject factor, and dilemma (personal, impersonal, nonmoral) as a within-subject factor. Although baseline skin conductance level of vmPFC patients was somewhat lower than control groups, the analysis did not reveal a significant main effect of group, or a significant interaction between group and dilemma (F < 1 in both cases). Likewise, the main effect of dilemma was not significant (F < 1).

Contemplation SCRs

Figure 4 shows mean SCRs elicited during each of three consecutive epochs of the contemplation period of personal, impersonal, and nonmoral dilemmas, separately for each participant group and type of response (affirmative vs. negative response). Psychophysiological responses were subjected to a mixed-design ANOVA with group (vmPFC, non-FC, HC) as a between-subject factor, and dilemma (personal, impersonal, nonmoral), epoch (I, II, III), and response (affirmative, negative) as within-subject factors. The analysis revealed a significant main effect of dilemma [F(2, 60) = 5.3, p < .01], indicating higher SCRs during contemplation of personal relative to impersonal and nonmoral scenarios, as well as a highly significant effect of response [F(1, 30) = 22.4, p < .0001], due to increased levels of skin conductance for affirmative versus negative responses. Also, there was a significant interaction between dilemma and response [F(2, 60) = 9.9, p < .001], and between group and response [F(1, 30) = 5.7, p < .01]. More important for the present purposes, however, the analysis showed a marginally significant three-way interaction between group, dilemma, and response [F(4, 60) = 2.4, p = .058], whereas the four-way interaction was not significant [F(8, 120) = 0.9, p = .5].

Figure 4. 

Mean SCRs elicited during each of three consecutive epochs of the contemplation period of personal, impersonal, and nonmoral dilemmas, separately for each participant group and type of response (affirmative vs. negative). SCR was measured as “area under the curve” in μS/sec. vmPFC = ventromedial prefrontal patients; non-FC = nonfrontal patients; HC = healthy controls. Bars refer to 1 standard error of the mean.

Figure 4. 

Mean SCRs elicited during each of three consecutive epochs of the contemplation period of personal, impersonal, and nonmoral dilemmas, separately for each participant group and type of response (affirmative vs. negative). SCR was measured as “area under the curve” in μS/sec. vmPFC = ventromedial prefrontal patients; non-FC = nonfrontal patients; HC = healthy controls. Bars refer to 1 standard error of the mean.

To uncover the source of the marginally significant three-way interaction, separate ANOVAs were conducted on contemplation SCRs (collapsing across epochs) for the different types of dilemma. For the personal dilemmas, both the main effect of response [F(1, 30) = 19.4, p ≤ .001] and the two-way interaction between group and response [F(2, 30) = 4.9, p < .01] were significant. Pairwise comparisons using the Fisher LSD test, which is considered the most powerful technique for post hoc tests involving three groups (Cardinal & Aitken, 2006), revealed that both non-FC patients and healthy controls generated larger SCRs during contemplation of personal moral dilemmas that were associated with affirmative responses (e.g., utilitarian judgments) (all ps < .01); in contrast, vmPFC patients showed no differential skin conductance activity preceding affirmative and negative responses in personal moral dilemmas (p = .91).

For both impersonal and nonmoral dilemmas, ANOVAs showed that the factor group did not result in a main effect; neither did it alter any of the interactions, suggesting that contemplation of impersonal and nonmoral scenarios resulted in similar skin conductance activity across all groups of participants.

To ensure that our findings were not driven by group differences in tonic level of electrodermal activity, we repeated the main ANOVA with baseline skin conductance activity as a covariate. The previously (marginally) significant Group by Dilemma by Response interaction remained significant [F(4, 58) = 2.9, p = .026], as did the Group by Response interaction [F(2, 29) = 5.5, p < .01]. The response deficit in the vmPFC patients is, therefore, not a function of lower baseline electrodermal activity.

Decision SCRs

Mean SCRs elicited during the 5-sec period following the dilemmatic question were subjected to a mixed-design ANOVA, with group (vmPFC, non-FC, HC) as a between-subject factor, and dilemma (personal, impersonal, nonmoral) and choice (utilitarian, nonutilitarian) as within-subject factors. Both the main factor of choice [F(1, 30) = 19.4, p < .001] and the interaction between choice and dilemma [F(2, 60) = 4.5, p < .01] were significant. In contrast, the three-way interaction was not significant [F(2, 60) = 1.4, p = .2]. Nevertheless, for completeness, we also conducted planned comparisons. Particularly, we found that normal controls and non-FC patients generated larger SCRs prior to utilitarian as compared to nonutilitarian judgments in personal moral dilemma (p < .05), whereas vmPFC patients showed similar skin conductance activity regardless of choice type (p = .31). Again, no group difference emerged when both impersonal and nonmoral dilemmas were considered. Finally, adding baseline skin conductance activity as a covariate in the ANOVA did not alter the pattern of results.

Postresponse SCRs

Mean SCRs elicited during the 5-sec period following participants' response were subjected to a mixed-design ANOVA, with group (vmPFC, non-FC, HC) as a between-subject factor, and dilemma (personal, impersonal, nonmoral) and choice (utilitarian, nonutilitarian) as within-subject factors. The main effect of choice was significant [F(1, 30) = 7.1, p < .05], indicating overall larger SCRs following utilitarian versus nonutilitarian choices. However, the factor group was not significant (F < 1), nor did it enter in any significant interactions (all Fs < 1).

To sum up, the results from the ANOVAs revealed that, for healthy subjects and nonfrontal patients, SCRs were stronger during evaluation of personal moral dilemmas that subsequently attracted an affirmative (e.g., utilitarian) response than during evaluation of personal moral dilemmas that subsequently attracted a negative (e.g., nonutilitarian) response. These individuals, on average, selected nonutilitarian over utilitarian choices in personal moral dilemmas. In contrast, for vmPFC patients, who were more inclined toward utilitarian judgment, SCRs did not change for personal moral dilemmas, subsequently attracting utilitarian versus nonutilitarian choices. This finding relates increases in SCR during the anticipation of a utilitarian choice (and therefore, a personal moral violation) with low tendency toward utilitarian judgment. One possibility is that anticipatory SCRs, by marking a particular option–outcome pair with a negative tag, bias individuals to avoid similar scenarios in the future (Bechara et al., 1996; Damasio, 1996).

To investigate whether anticipatory skin conductance activity was predictive of the type of choice on personal moral dilemmas, a further analysis was performed. We computed an autonomic utilitarian index [(SCRs prior to utilitarian choices − SCRs prior to nonutilitarian choices)/(SCRs prior to utilitarian choice + SCRs prior to nonutilitarian choices)] for each healthy control participant, and then entered into a regression analysis with the percent of utilitarian choices made by each subject in response to personal moral dilemmas. Results showed that the autonomic utilitarian index correlated negatively with the proportion of utilitarian judgments (r = −.64, p < .005). Indeed, the autonomic utilitarian index decreased linearly as the percent of utilitarian choices increased, indicating that low-utilitarian participants exhibited higher skin conductance activity prior to utilitarian judgments of personal moral dilemmas, whereas high-utilitarian participants showed the opposite pattern. By contrast, this was not the case for impersonal moral dilemmas (r = .10, p = .7), thereby revealing that utilitarian judgments were not related to skin conductance activity for this type of moral dilemmas.

DISCUSSION

Recent findings from human lesion (Ciaramelli et al., 2007; Koenigs et al., 2007) and brain imaging studies (Greene et al., 2001, 2004) converge to suggest that medial prefrontal cortex constitutes a critical neural underpinning of judgments about personal moral dilemmas, where one option involves directly inflicting serious harm to other persons. In particular, it has been found that vmPFC-lesioned patients, relative to healthy individuals and neurological patients with brain damage in other cerebral regions, are more likely to endorse personal moral violations in order to maximize good consequences (i.e., the utilitarian response). According to one account, this abnormally increased utilitarian pattern of moral judgment would result from impaired affective and intuitive processes, mediated by vmPFC, which normally oppose deviations from moral values and rules shared by a social group (Greene, 2007). Although these results strongly suggest a causally necessary role of emotions in morally relevant decision-making, a mechanistic account of how, and at which point, emotional states subserved by vmPFC influence moral judgment is still lacking (see Huebner, Dwyer, & Hauser, 2008 for a discussion).

The present study was designed to examine the pattern of skin conductance changes, used as an autonomic index of individuals' affective responses, associated with personal versus impersonal moral judgments, both in vmPFC patients and control participants.

In complete agreement with previous data (Ciaramelli et al., 2007; Koenigs et al., 2007), our present findings reveal that patients with vmPFC damage made significantly more utilitarian choices in response to high-conflict personal moral scenarios, compared to patients with brain damage that spared vmPFC and to healthy controls. Moreover, patients with vmPFC lesions were also faster than control groups to approve personal moral violations. On the other hand, their behavior in low-conflict personal, impersonal, and nonmoral dilemmas was comparable to that of controls, both in terms of the quality of the choices they made and in the time they needed to make their decisions, further demonstrating the rather selective role played by vmPFC-mediated emotions on personal moral judgments (Young & Koenigs, 2007; Hauser, 2006).

The psychophysiological data mirrored the behavioral results: Whereas autonomic bodily signals during consideration of impersonal and nonmoral dilemmas did not differ across participant groups, skin conductance recordings during contemplation of personal moral scenarios differed considerably between patients with vmPFC damage and control groups. Both healthy subjects and brain-damaged control patients exhibited increased skin conductance activity several seconds before choosing the utilitarian option in personal moral dilemmas, for instance, deciding that it would be appropriate to kill one person in order to save others. In striking contrast, vmPFC patients did not generate SCRs in anticipation of utilitarian choices in personal moral dilemmas. These findings indicate profound differences in the making of moral judgment between vmPFC patients and controls: In control groups, emotional/somatic signals were critically recruited during moral judgment, and characterized the anticipation of personal moral violations. In contrast, no apparent emotional/somatic response accompanied personal moral violations in vmPFC patients. Importantly, somatic responses shaped personal moral judgment. A preliminary analysis showed a negative correlation between anticipatory skin conductance activity and frequency of utilitarian responses in normal controls, such that individuals with higher SCRs before utilitarian choices were more reluctant to judge moral infractions as acceptable behaviors than those with lower SCRs. One possibility, therefore, is that emotional responses mark utilitarian choices in personal moral dilemmas with a negative tag, discouraging the selection of those options in future decisions.

Studies of patients with discrete brain lesions and, more recently, functional imaging techniques have strongly implicated vmPFC in both generation and feedback representation of states of bodily arousal, indexed by SCRs, which may influence cognition and bias motivational behavior (Nagai et al., 2004; Critchley, Mathias, & Dolan, 2001; Damasio, Tranel, & Damasio, 1990). In several studies, vmPFC patients often exhibit impaired autonomic arousal and subjective feeling in response to emotionally charged events (Roberts et al., 2004; Blair & Cipolotti, 2000; Tranel & Damasio, 1994; Damasio et al., 1990).

Importantly, in a now seminal series of studies, Bechara et al. (1996, 1999), Bechara, Damasio, Tranel, and Damasio (1997) and Damasio et al. (1990) have shown that vmPFC-lesioned patients perform poorly on a gambling task, and unlike normal controls, fail to show anticipatory SCRs immediately before selecting a high-risk option (i.e., one offering immediate gain but a high probability of long-term monetary loss). These findings have led to a proposal that central representations of bodily states of arousal guide social behavior and bias decision-making, formulated as the “somatic marker hypothesis” (Bechara & Damasio, 2005; Bechara et al., 1996; Damasio, 1994, 1996; Damasio et al., 1990). According to this hypothesis, the SCR would operate as an alarm signal that, by marking a specific option–outcome combination with a negative tag, promotes the avoidance of similar options in the future. This interpretation of the SCR is also broadly consistent with the observation of anticipatory SCRs in aversive conditioning paradigms (Tabbert, Stark, Kirsch, & Vaitl, 2005; Büchel et al., 1998), and with the proposal that the SCR might represent a “somatic marker of erring” (Hajcak, McDonald, & Simons, 2003, 2004).

Our current finding of increased somatic arousal in control participants immediately before endorsing morally reprehensible actions (in the context of personal dilemmas) is highly consistent with the anticipatory SCR obtained with Bechara gambling task. In keeping with the somatic marker hypothesis, anticipatory somatic states of arousal, supported in part by circuits in vmPFC, may help forecast the negative emotional consequences (e.g., shame, guilt or remorse) of approving personal moral transgressions (e.g., utilitarian judgments), thereby motivating individuals to avoid actions that generate such negative somatic states in subsequent choices. Thus, the SCR signal could not only serve as an affective signal that alerts us to the moral relevance of a rule transgression (particularly if that transgression may cause serious harm to others), but also as a teaching signal aimed at decreasing the likelihood of morally impermissible behaviors. Accordingly, the absence of anticipatory SCRs in vmPFC patients may indicate that they fail to represent the affective expectations of highly aversive personal moral transgressions, thereby lacking a powerful biasing signal (e.g., a moral reinforcer) that is critical for driving changes of behavior and compliance with moral values (Tangney et al., 2007; Amodio & Frith, 2006; Frijda, 2005). This conclusion appears in accordance with current theories maintaining that vmPFC is a critical neural substrate for representing potential positive and negative action outcomes in order to promote approach/avoidance learning and behavior flexibility (Murray, O'Doherty, & Schoenbaum, 2007; Montague, King-Casas, & Cohen, 2006; Oya et al., 2005).

The interpretation that we offer is compatible with recent evidence from fMRI, showing that imagined socio-moral transgressions associated with sentiments of guilt elicited activation within medial sectors of prefrontal cortex (Zahn et al., 2009; Kédia, Berthoz, Wessa, Hilton, & Martinot, 2008). Moreover, data from economic games indicate that patients with vmPFC damage are abnormally insensitive to guilt in social and economic interactions (Krajbich, Adolphs, Tranel, Denburg, & Camerer, 2009). Finally, our view is also in agreement with the finding that early damage to vmPFC can lead to severe deficits in moral sentiments, including guilt, remorse, and empathy, as well as profound impairments of moral reasoning (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999), thereby suggesting that emotional processing mediated by this area is developmentally necessary for the learning and acquisition of moral concepts.

A different, but not necessarily mutually exclusive, account of the present findings would instead invoke the concepts of attention regulation rather than emotion and affective valuation of consequences (Botvinick, 2007; Dawson et al., 2007). Indeed, SCR variability has been often used as an index of attention-related arousal (Boucsein, 1992). Notably, a recent study has shown elevation in skin conductance immediately before actions associated with a high demand of controlled cognitive processing (Botvinick & Rosen, 2009). On this view, the increase in arousal preceding the endorsement of personal moral violations could be related to the recruitment of cognitive control needed to solve the conflict between incompatible outcomes (e.g., utilitarian and nonutilitarian outcomes) in response to difficult (e.g., personal) moral dilemmas (Greene et al., 2004).

One way of reconciling these two seemingly disparate accounts is to consider that the anticipatory SCRs obtained in our experiments may reflect both affective valuation of the degree of cognitive effort and conflict associated with utilitarian judgments, and the socially negative consequences of endorsing moral violations in personal moral dilemmas (Botvinick & Rosen, 2009; Botvinick, 2007). Such a conclusion would be consistent with model proposing that vmPFC represents the composite values of different predictions for subsequent decisions and judgments (Montague & Berns, 2002).

To conclude, the present results suggest that emotion processing mediated by vmPFC plays a necessary role in guiding moral decisions about whether or not sacrificing an individual in order to save a greater number of persons (e.g., high-conflict personal moral dilemmas). In particular, we found that activation of somatic states (monitored through SCRs) prior of utilitarian moral judgments is impaired following vmPFC lesion. That is, contemplating morally impermissible actions was not emotionally taxing in patients with vmPFC damage. We argue that this deficit may prevent vmPFC patients to anticipate the negative emotional consequences of moral violations, and, as a consequence, to conform their behavior to moral norms and values shared by their social group.

Acknowledgments

This work was supported by a PRIN grant (2005111741) from MIUR to G. di Pellegrino. We thank Elisa Ciaramelli and two anonymous reviewers for their valuable comments on an earlier draft of the manuscript.

Reprint requests should be sent to Giuseppe di Pellegrino, Dipartimento di Psicologia, Università di Bologna, Viale Berti Pichat, 5 - 40127 Bologna, Italy, or via e-mail: g.dipellegrino@unibo.it.

Note

1. 

Neurobehavioral consequences commonly observed following ACoA aneurysm rupture may include memory loss, confabulation, decision-making deficits, and altered personality (see DeLuca & Diamond, 1995, for a review). Many researchers in the field currently agree that damage to the basal forebrain primarily mediate the memory loss, whereas damage to vmPFC is thought to underlie the personality changes and poor decision-making of ACoA patients (DeLuca & Chiaravalloti, 2002; Mavaddat, Kirkpatrick, Rogers, & Sahakian, 2000; Eslinger & Damasio, 1984). Future studies of patients with functional imaging and increased autopsy data may help clarifying which structures are involved in producing various aspects of the ACoA aneurysm syndrome.

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