A Psychophysiological Investigation of Moral Judgment

after Ventromedial Prefrontal Damage

Giovanna Moretto1,2, Elisabetta Làdavas1, Flavia Mattioli3,

and Giuseppe di Pellegrino1

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

INTRODUCTION
Foot, 1978), in which two moral scenarios, impersonal ver-
For decades, moral psychology has been concerned with sus personal, are contrasted. On the impersonal version
identifying a rational basis of human morality (Kohlberg, (trolley dilemma), a bystander can use a switch to redirect
1969; Piaget, 1965). A different and more recent approach, a runaway trolley away from five victims and onto a single
however, places strong emphasis on the causal power of victim; on the personal version (footbridge dilemma), a
affective and intuitive processes to drive our moral judg- bystander can push a single victim off of a bridge in front
ment and convictions (Haidt, 2001). Integrating these op- of a runaway trolley in order to stop its progress toward five
posite views, recent work in psychology and neuroscience victims. From a simple “economic” point of view, the two
has suggested that moral judgments are mediated by two dilemmas are identical (i.e., killing one person to save five
classes of computational processes (Greene, Nystrom, lives). Yet, numerous empirical studies have demonstrated
Engell, Darley, & Cohen, 2004; Greene, 2003; Greene & that a large majority of individuals consider it morally ac-
Haidt, 2002; Greene, Sommerville, Nystrom, Darley, & ceptable to sacrifice one person to save five in the im-
Cohen, 2001). One class, referred to as moral intuition, personal dilemma, whereas they believe that it is wrong
consists of emotion-laden processes that automatically to push the large man to save the five victims (Ciaramelli,
evaluate socially relevant stimuli along a right–wrong or Muccioli, Ladavas, & di Pellegrino, 2007; Koenigs et al.,
like–dislike dimension. A second class, moral reasoning, 2007; Mikhail, 2007; Cushman, Young, & Hauser, 2006;
consists of controlled, deliberative processes that arrive Valdesolo & DeSteno, 2006; Greene et al., 2001, 2004;
at moral judgment or decision through laborious steps of Petrinovich, OʼNeill, & Jorgensen, 1993).
deductive reasoning and cost–benefit analyses. According to Greene et al. (2001), the reason for these
For the most part, these processes work cooperatively to seemingly contradictory responses lies in the stronger ten-
promote moral behavior. Certain ethical dilemmas, how- dency of personal scenarios (i.e., the push case), compared
ever, involve decisions in which the tension or conflict to impersonal scenarios (i.e., the switch case), to engage
between intuitive and deliberative processes becomes ap- emotional processes which would affect moral decisions.
parent (Greene et al., 2001). One such dilemma is illus- Supporting this proposal, neuroimaging has revealed that
trated by the classic trolley problem (Thomson, 1986; impersonal and personal moral dilemma yield dissociable
patterns of neural activation (Greene et al., 2001). Specifi-
cally, impersonal moral scenarios characteristically yield
1
Università di Bologna, Italy, 2Centro studi e ricerche in Neuro- greater activation in brain areas associated with problem
scienze Cognitive, Polo Scientifico-Didattico di Cesena, Italy, solving and deliberate reasoning [including dorsolateral
3
Spedali Civili, Brescia, Italy prefrontal cortex (dlPFC) and inferior parietal lobule],

© 2009 Massachusetts Institute of Technology Journal of Cognitive Neuroscience 22:8, pp. 1888–1899
whereas personal moral scenarios yield greater activation emotional responses to standardized social stimuli (see
in brain areas that have been implicated in emotion and Koenigs et al., 2007). None of the existing studies has
social cognition (such as medial prefrontal cortex and pos- systematically measured subjectsʼ emotional responses
terior cingulate gyrus). emerging during (and, presumably, having an impact on)
In this view, the thought of pushing someone in front a evaluation of moral dilemmas. This is particularly relevant
trolley (i.e., a personal moral violation) elicits prepotent, considering that in specific social circumstances, vmPFC
seemingly negative, emotional responses that oppose or patients have been found to exhibit increased, rather than
prohibit such repugnant act. In this case, making “more reduced, emotional reactivity (Koenigs & Tranel, 2007;
rational,” “utilitarian” choices (i.e., deciding that is accept- Barrash, Tranel, & Anderson, 2000; Grafman et al., 1996).
able to make a harmful act in order to maximize overall Therefore, critical evidence linking vmPFC, emotion, and
utility) would require overriding a strongly aversive emo- moral judgments is still lacking.
tional response. Accordingly, in a later study, Greene et al. The aim of the present study is the gathering of direct
(2004) found that the (infrequent) selection of utilitarian psychophysiological evidence, both in healthy and neuro-
responses in the context of personal moral dilemmas elicits logically impaired individuals, that emotions are crucially
heightened activity in both “cognitive” (such as dlPFC) and involved in shaping moral judgment, by preventing perso-
emotional brain areas (including medial prefrontal cortex, nal moral violations. Toward this end, 8 patients with focal
posterior cingulate area, and anterior insula). Interestingly, lesion involving the ventromedial sectors of prefrontal cor-
utilitarian decisions were also associated with increased tex (vmPFC patients), 7 control patients with lesions out-
activity in anterior cingulate cortex, which is thought to re- side the frontal lobe (non-FC patients), and 18 healthy
flect the conflict between competing processes (Botvinick, controls responded to personal as well as impersonal moral
Cohen, & Carter, 2004), namely, cognitive processes favor- dilemmas while skin conductance response (SCR) was re-
ing a utilitarian judgment and the emotional response to corded as a physiological index of affective state.
the prospect of doing harm to others. The SCR is related to the sympathetic division of the
Perhaps the most direct evidence supporting a necessary autonomic nervous system (Boucsein, 1992), and is widely
role of emotion in shaping moral decisions has emerged used as a sensitive and objective measure of emotional pro-
from the neuropsychological investigation of individuals cessing (Dawson, Schell, & Filion, 2007; Naqvi & Bechara,
with selective deficits in affective processing. More specifi- 2006; Büchel, Morris, Dolan, & Friston, 1998). Moreover,
cally, patients with adult-onset lesions in ventromedial pre- among cortical regions, vmPFC is presumed to be critically
frontal cortex (vmPFC) develop a marked, albeit isolated, implicated in the generation and feedback representation
impairment in social behavior that has been consistently of bodily states of arousal (i.e., somatic markers), indexed
attributed to a defective engagement of social emotions, by SCR, in the context of social, emotional, and motiva-
such as guilt, embarrassment, and shame. Recent research tional behavior (Nagai, Critchley, Featherstone, Trimble,
has demonstrated that vmPFC patients respond normally & Dolan, 2004; Bechara, Damasio, Damasio, & Lee, 1999;
to impersonal moral scenarios. However, they are more Bechara et al., 1996; Damasio, 1994; Tranel & Damasio,
likely than control groups to endorse moral violations (i.e., 1994). Consequently, SCR is a measure ideally suited to
inflicting serious harm to people) in personal moral sce- study the relationship among vmPFC, emotion, and moral
narios (Ciaramelli et al., 2007), specifically, “high-conflict” decision-making.
personal scenarios, situations in which there are no clear First, we expected to replicate previous evidence that,
social norms to decide whether a behavior is morally right compared to normal controls, patients with vmPFC dam-
or wrong (Koenigs et al., 2007; Hauser, 2006). age are more willing to judge moral violations as accept-
One interpretation of this result is that vmPFC patients able behaviors in personal moral dilemmas, whereas their
lack automatic affective responses, or aversion signals, im- performance in impersonal and nonmoral dilemmas is
peding any personal moral violation. When affective reac- comparable to the controls. If emotional state activation
tions dissolve (due to brain damage), principled reasoning mediated by vmPFC plays a critical and selective role in
aimed at maximizing benefits and minimizing costs may pre- shaping personal moral judgments, then we should ob-
vail, thereby increasing the rate of “rationally appropriate” serve differences in SCRs between patients with vmPFC
utilitarian choices (Greene, 2007; but see also Moll & de damage and comparison groups during contemplation of
Oliveira-Souza, 2007, for a different view). personal moral scenarios (such as the footbridge dilemma),
Patient lesion studies, thus, strongly suggest that emo- but not during contemplation of impersonal moral sce-
tions, particularly those subserved by vmPFC, are integral narios (such as the trolley dilemma).
constituents of our moral views. These conclusions, how- An additional prediction, derived from the hypothesis
ever, rest entirely on the assumption of general emotional that emotional reactions drive disapproval of harmful ac-
blunting or flattened affect following vmPFC damage, a tions (even when aimed at promoting the greater good),
notion based on previous work concerning vmPFC and was that skin conductance activity during contemplation
nonmoral (and nonsocial) decision-making (i.e., gambling of personal moral dilemmas would be negatively corre-
task; Bechara & Damasio, 2005; Bechara, Tranel, Damasio, lated with the tendency toward utilitarianism (i.e., percen-
& Damasio, 1996; Damasio, 1994), or the evaluation of tage of utilitarian judgment made) in normal controls. In

Moretto et al. 1889

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)

MMSE = Mini-Mental State Examination.

other words, we predicted that SCR would be higher in presented with clinical evidence of a decline in social inter-
participants exhibiting fewer utilitarian choices than in personal conduct, impaired decision-making, and emo-
those with a higher rate of utilitarian responses. tional functioning, but had generally intact intellectual
abilities (see Table 2).
The non-FC patients were selected on the basis of
METHODS having damage that did not involve the frontal lobe, and
also spared the amygdala and the insula in both hemi-
Participants spheres. In this group, lesions were unilateral in six pa-
Three groups of subjects participated in the study: (a) a tients (in the left hemisphere in 2 cases, and in the right
group of patients with focal lesions involving vmPFC bi- hemisphere in 4 cases) and bilateral in one patient. Brain
laterally (the vmPFC group, n = 8); (b) a control group lesions were caused by arterial–venous malformation in
of patients with damage sparing frontal cortex (the non- one case, and by ischemic or hemorrhagic stroke in the
FC group, n = 7); and (c) a control group of healthy sub- remaining six cases. Lesion sites included the occipital lobe
jects (the HC group, n = 18), who were matched on age, in two patients, the lateral occipito-temporal junction in
education, and sex with the vmPFC group. three patients, and the lateral occipito-parietal junction in
Brain-damaged patients were recruited from the Centre the remaining two patients.
for Studies and Researches in Cognitive Neuroscience in All subject groups were administered a short neuro-
Cesena, and from the Azienda Ospedaliera Spedali Civili in psychological battery including tests with potential sensitiv-
Brescia. They were selected on the basis of the location of ity to frontal damage, as well as intelligence and memory
their lesion evident on CT or MRI scans. Table 1 shows de- tests (results are provided in Table 2). The groups differed
mographic and clinical data, as well as the Mini-Mental Sta- significantly only in their performance on the Stroop task,
tus Examination score (MMSE; Folstein, Robins, & Helzer, with vmPFC subjects making more errors than both non-
1983). There were no significant differences between FC patients and healthy controls (Mann–Whitney U test,
vmPFC patients and comparison groups with regard to p < .05). Patients were not receiving psychoactive drugs
age, education, clinical and personality variables ( p > .05 at the time of testing, and had no other diagnosis likely
in all cases). to affect cognition or interfere with participation in the
In the vmPFC group, lesions were caused by rupture and study (e.g., significant psychiatric disease, alcohol misuse,
repair of anterior communicating artery (ACoA) aneurysm. history of cerebrovascular disease, focal neurological ex-
Lesions involved vmPFC—defined as the medial one-third amination). Neuropsychological and experimental studies
of the orbital surface and the ventral one-third of the me- were all conducted in the chronic phase of recovery, more
dial surface of the frontal lobe, following the boundaries than a year post-onset. All lesions were acquired in adult-
laid out by Stuss and Levine (2002)—and adjacent basal hood. Patients gave informed consent to participate in the
forebrain area.1 The vmPFC damage was bilateral in all study according to the Declaration of Helsinki (Interna-
cases, although often asymmetrically so. All vmPFC patients tional Committee of Medical Journal Editors, 1991) and

Table 2. Results of Selected Neuropsychological Tests [Mean (SD)]

Group SRM Digit Span Forward Phonemic Fluency Semantic Fluency WMS Stroop Task Errors a

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.
a
Values that differ significantly between groups.

1890 Journal of Cognitive Neuroscience Volume 22, Number 8

the Ethical Committee of the Department of Psychology, vious study (Ciaramelli et al., 2007). Ten out of 15 personal
University of Bologna. moral scenarios were “high-conflict” dilemmas, whereas
Normal participants were healthy volunteers who were the remaining 5 were “low-conflict” dilemmas, as identi-
not taking psychoactive medication, and were free of cur- fied by Koenigs et al. (2007) on the basis of the reaction
rent or past psychiatric or neurological illness as determined times and level of agreement among normal controls.
by history. Normal controls scored at least 28 out of 30 on Moral dilemmas are supposed to elicit moral emotions
the MMSE. (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,
Lesion Analysis
2007), whereas nonmoral dilemmas are not (Greene et al.,
Lesion analysis was based on the most recent clinical CT or 2001). Typical examples of nonmoral dilemmas posed
MRI. The location and extent of each lesion were mapped questions about whether to buy a new television or to have
by using MRIcro software (Rorden & Brett, 2000). The le- your old television repaired for the same price, or whether
sions were manually drawn by a neurologist with experi- to travel by bus or train given certain time constraints.
ence in image analysis onto standard brain template from
the Montreal Neurological Institute, which is based on
Task Procedure
T1-weighted MRI scans, normalized to Talairach space.
This scan is distributed with SPM99 and has become a An IBM-compatible Pentium IV computer running E-Prime
popular template for normalization in functional brain software (Psychology Software Tools, 2002, Pittsburgh, PA)
imaging. For superimposing of the individual brain le- controlled the presentation of dilemmas, timing operation,
sions, the same MRIcro software was used. Figure 1 shows and behavioral data collection. Subjects sat in front of a
the extent and overlap of the brain lesions in the brain- computer screen (21-in. VGA monitor) in a quiet and dimly
damaged patients. Brodmannʼs areas (BA) affected in lit room. Each dilemma was presented as text through a
vmPFC group were areas 10, 11, 32 (subgenual portion), series of two screens. The first screen described the sce-
and 24, with region of maximal overlap occurring in nario and was presented for 45 sec. The second screen
BA 10 and 11. 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
Materials
by pushing the stranger to death?”). Participants indicated
Stimuli in the present study were 15 personal moral dilem- their judgments by pressing one of two different keys on
mas, 15 impersonal moral dilemmas, and 15 nonmoral di- the computer keyboard. There was no time limit. Partici-
lemmas, randomly selected from a battery of 60 dilemmas pants were told to respond as soon as they had reached
developed by Greene et al. (2001), and used in our pre- a decision. The intertrial interval, during which a blank

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 (Brodmannʼs
areas 10, 11, and 32).

Moretto et al. 1891

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.

screen was displayed, lasted for 20 sec in each trial, allow- on a second PC. Each testing session began with a 10-min
ing the psychophysiological response (see below) to return rest period during which the participantsʼ SCR acclimated
to baseline after each trial. to the environment, and the experimenter ensured a cor-
For all dilemmas being tested, (“appropriate”) affirma- rect attachment and conductance of the electrodes. Pre-
tive responses implied the maximization of overall conse- sentation of each dilemma was synchronized with the
quences (Greene, 2003), for instance, killing one instead sampling computer to the nearest millisecond. Further-
of five persons (in a moral dilemma), or buying a new tele- more, each time the subject pressed a response key, this
vision instead of repairing the old one for the same price action coincided with a mark on the SCR polygram. During
(in a nonmoral dilemma). However, only for moral dilem- acquisition of the psychophysiological data, the partici-
mas did “appropriate” responses result in moral violations. pants were asked to remain quiet and as still as possible
Note that “appropriate” and “inappropriate” is a value- to avoid confounding these measurements.
neutral description of what the participant said about the After acquisition, skin conductance values were trans-
action in the dilemma and not an evaluation of the partici- formed to microsiemens values using the AcqKnowledge
pantʼs decision. Both the number of “appropriate, affirma- software. Also, this software provides an extensive array
tive responses and response times (RTs; i.e., the time from of measurements that can be applied to the collected
the onset of the dilemmatic question to the moment a data. Raw skin conductance data were low-pass filtered
response was given)” were collected. Dilemmas were pre- to remove high-frequency noise. The slow downward drift
sented in random order in a single session that lasted ap- in baseline skin conductance level was removed using a
proximately 70 min. 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,
Psychophysiological Data Acquisition
such as loud sounds (i.e., hands clapping).
and Reduction
We used the skin conductance activity as a dependent
measure of emotional arousal and somatic state activation. RESULTS
For each participant, prewired Ag/AgCl electrodes (TSD203
Model; Biopac Systems, Goleta, CA), filled with isotonic Behavioral Data
hyposaturated conductant, were attached to the volar sur- The proportion of affirmative responses (e.g., utilitarian
face of the middle and index fingertip of the nondominant choices in the context of personal moral dilemmas) for
hand and held firmly in place with Velcro straps. Impor- each type of dilemma and each participant group were
tantly, doing so left the dominant hand free for behavioral computed (see Figure 2). The data were subjected to a
responses. The electrode pairs forming part of the input mixed-design ANOVA, with group (vmPFC, non-FC, HC)
circuit were excited by a constant voltage of 0.5 V (Fowles as a between-subject factor, and dilemma (personal, imper-
et al., 1981; Lykken & Venables, 1971) and the current sonal, nonmoral) as a within-subject factor. The ANOVA
change representing conductance was recorded using a yielded a significant main effect of group [F(2, 30) = 4.4,
DC amplifier (Biopac GSR100) with a gain factor of 5 μS/ V p < .05], as well as of dilemma [F(2, 30) = 6.3, p < .005].
and low-pass filter set at 10 Hz. The analog signal was digi- Critically, the two-way interaction between group and di-
tized using the MP-150 digital converter (Biopac Systems) lemma was significant [F(4, 60) = 2.6, p = .05]. Pair-
at a rate of 200 Hz and fed into AcqKnowledge 3.9 record- wise comparisons showed that both control groups gave
ing software (Biopac Systems). As subjects performed the fewer affirmative responses to personal (HC = 0.32, non-
moral judgment task seated in front of the computer, SCR FC = 0.30) as compared to impersonal (HC = 0.51, non-
was collected continuously and stored for off-line analysis FC = 0.57) and nonmoral dilemmas (HC = 0.52, non-FC =

1892 Journal of Cognitive Neuroscience Volume 22, Number 8

0.51; all ps < .05). By contrast, vmPFC patients made a mediately preceding each dilemma; (b) contemplation,
similar proportion of “appropriate,” affirmative responses the 45-sec time window during which participants viewed
across all types of dilemma (0.59, 053, and 0.57, for per- the dilemma; (c) decision, the time period comprised be-
sonal, impersonal, and nommoral dilemma, respectively; tween the presentation of the dilemmatic question and
all ps > .05). the emission of a response; (d) postresponse, the 5-sec
A more focused analysis on response patterns within time period following participantsʼ response. To examine
the personal moral dilemmas revealed that vmPFC pa- psychophysiological changes in more detail, the contem-
tients were more likely to endorse the “appropriate” (e.g., plation period was further divided into three consecutive
utilitarian) response than either comparison groups when epochs, lasting 15 sec each. SCRs were computed for each
high-conflict scenarios were presented (Kruskal–Wallis epoch of a trial as “area under the curve” (Naqvi & Bechara,
test, H = 11.9, df = 2, p < .01). In contrast, for low-conflict 2006; Vianna & Tranel, 2006; Damasio et al., 2000). The
personal scenarios, the frequency of selecting the affirma- “area under the curve” measurement is similar to the func-
tive response was negligible and with no significant dif- tion of an “integral” except that, instead of using zero as a
ference between vmPFC patients and control groups (H = baseline for integration, a straight line is drawn between
1.3, df = 2, p = .5). the endpoints of the selected area to function as the base-
The RT data (Figure 3) were also subjected to a mixed- line. The area is expressed in terms of amplitude units
design ANOVA with group (vmPFC, non-FC, HC) as a (microsiemens, μS) per time interval (sec). All SCRs were
between-subject factor, and dilemma (personal, impersonal, square-root-transformed to attain statistical normality.
nonmoral) and response (affirmative, negative) as within-
subject factors. As a violation of the ANOVA, assumption
Baseline SCRs
of sphericity was detected using the Mauchly sphericity
test and the Greenhouse–Geisser correction for repeated Skin conductance levels during the baseline period were
measures was applied. submitted to a mixed design ANOVA with group (vmPFC,
The analysis revealed a significant main effect of group non-FC, HC) as a between-subject factor, and dilemma (per-
[F(2, 30) = 5.4, p < .01], as well as a significant two-way sonal, impersonal, nonmoral) as a within-subject factor.
interaction between choice and dilemma [F(2, 60) = 5.9, Although baseline skin conductance level of vmPFC pa-
p < .01]. Moreover, the ANOVA yielded a marginally sig- tients was somewhat lower than control groups, the analysis
nificant three-way interaction [F(4, 60) = 2.6, p = .07]. did not reveal a significant main effect of group, or a sig-
Pairwise comparisons showed that healthy controls and nificant interaction between group and dilemma (F < 1 in
nonfrontal, control patients took longer to make affirma- both cases). Likewise, the main effect of dilemma was not
tive relative to negative responses in personal moral dilem- significant (F < 1).
mas (HC: 4996 vs. 3625 msec; non-FC: 8805 vs. 5709 msec;
both ps < .01), but not in impersonal moral dilemmas (HC:
Contemplation SCRs
3548 vs. 3654 msec; non-FC: 6352 vs. 6597; both ps > .5),
and in nonmoral dilemma (HC: 3837 vs. 3759 msec; non- Figure 4 shows mean SCRs elicited during each of three
FC: 6140 vs. 6496 msec; both ps > .5). In stark contrast, consecutive epochs of the contemplation period of per-
vmPFC patients showed similar RTs for affirmative and sonal, impersonal, and nonmoral dilemmas, separately
negative responses in either personal (5315 vs. 6341 msec), for each participant group and type of response (affirma-
impersonal (6937 vs. 7365 msec), and nonmoral dilemmas tive vs. negative response). Psychophysiological responses
(7725 vs. 7854 msec; all ps > .1). were subjected to a mixed-design ANOVA with group
(vmPFC, non-FC, HC) as a between-subject factor, and di-
lemma (personal, impersonal, nonmoral), epoch (I, II, III),
Psychophysiological Data
and response (affirmative, negative) as within-subject fac-
For analysis, each trial was divided off-line into four sepa- tors. The analysis revealed a significant main effect of di-
rate time periods: (a) baseline, the 15-sec time period im- lemma [F(2, 60) = 5.3, p < .01], indicating higher SCRs

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.

Moretto et al. 1893

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.

during contemplation of personal relative to impersonal comparisons using the Fisher LSD test, which is consid-
and nonmoral scenarios, as well as a highly significant effect ered the most powerful technique for post hoc tests in-
of response [F(1, 30) = 22.4, p < .0001], due to increased volving three groups (Cardinal & Aitken, 2006), revealed
levels of skin conductance for affirmative versus negative that both non-FC patients and healthy controls generated
responses. Also, there was a significant interaction be- larger SCRs during contemplation of personal moral di-
tween dilemma and response [F(2, 60) = 9.9, p < .001], lemmas that were associated with affirmative responses
and between group and response [F(1, 30) = 5.7, p < (e.g., utilitarian judgments) (all ps < .01); in contrast,
.01]. More important for the present purposes, however, vmPFC patients showed no differential skin conductance
the analysis showed a marginally significant three-way in- activity preceding affirmative and negative responses in
teraction between group, dilemma, and response [F(4, personal moral dilemmas ( p = .91).
60) = 2.4, p = .058], whereas the four-way interaction was For both impersonal and nonmoral dilemmas, ANOVAs
not significant [F(8, 120) = 0.9, p = .5]. showed that the factor group did not result in a main ef-
To uncover the source of the marginally significant fect; neither did it alter any of the interactions, suggesting
three-way interaction, separate ANOVAs were conducted that contemplation of impersonal and nonmoral scenarios
on contemplation SCRs (collapsing across epochs) for the resulted in similar skin conductance activity across all groups
different types of dilemma. For the personal dilemmas, of participants.
both the main effect of response [F(1, 30) = 19.4, p ≤ To ensure that our findings were not driven by group
.001] and the two-way interaction between group and re- differences in tonic level of electrodermal activity, we re-
sponse [F(2, 30) = 4.9, p < .01] were significant. Pairwise peated the main ANOVA with baseline skin conductance

1894 Journal of Cognitive Neuroscience Volume 22, Number 8

activity as a covariate. The previously (marginally) signifi- low tendency toward utilitarian judgment. One possibility
cant Group by Dilemma by Response interaction remained is that anticipatory SCRs, by marking a particular option–
significant [F(4, 58) = 2.9, p = .026], as did the Group by outcome pair with a negative tag, bias individuals to avoid
Response interaction [F(2, 29) = 5.5, p < .01]. The re- similar scenarios in the future (Bechara et al., 1996; Damasio,
sponse deficit in the vmPFC patients is, therefore, not a 1996).
function of lower baseline electrodermal activity. To investigate whether anticipatory skin conductance
activity was predictive of the type of choice on personal
moral dilemmas, a further analysis was performed. We
Decision SCRs computed an autonomic utilitarian index [(SCRs prior to
utilitarian choices − SCRs prior to nonutilitarian choices)/
Mean SCRs elicited during the 5-sec period following the
(SCRs prior to utilitarian choice + SCRs prior to nonutilitar-
dilemmatic question were subjected to a mixed-design
ian choices)] for each healthy control participant, and then
ANOVA, with group (vmPFC, non-FC, HC) as a between-
entered into a regression analysis with the percent of utili-
subject factor, and dilemma (personal, impersonal, nonmoral)
tarian choices made by each subject in response to per-
and choice (utilitarian, nonutilitarian) as within-subject
sonal moral dilemmas. Results showed that the autonomic
factors. Both the main factor of choice [F(1, 30) = 19.4,
utilitarian index correlated negatively with the proportion
p < .001] and the interaction between choice and dilemma
of utilitarian judgments (r = −.64, p < .005). Indeed, the
[F(2, 60) = 4.5, p < .01] were significant. In contrast, the
autonomic utilitarian index decreased linearly as the per-
three-way interaction was not significant [F(2, 60) = 1.4,
cent of utilitarian choices increased, indicating that low-
p = .2]. Nevertheless, for completeness, we also conducted
utilitarian participants exhibited higher skin conductance
planned comparisons. Particularly, we found that normal
activity prior to utilitarian judgments of personal moral di-
controls and non-FC patients generated larger SCRs prior
lemmas, whereas high-utilitarian participants showed the
to utilitarian as compared to nonutilitarian judgments
opposite pattern. By contrast, this was not the case for
in personal moral dilemma ( p < .05), whereas vmPFC
impersonal moral dilemmas (r = .10, p = .7), thereby re-
patients showed similar skin conductance activity regard-
vealing that utilitarian judgments were not related to skin
less of choice type ( p = .31). Again, no group difference
conductance activity for this type of moral dilemmas.
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. DISCUSSION
Recent findings from human lesion (Ciaramelli et al., 2007;
Koenigs et al., 2007) and brain imaging studies (Greene
Postresponse SCRs
et al., 2001, 2004) converge to suggest that medial pre-
Mean SCRs elicited during the 5-sec period following partici- frontal cortex constitutes a critical neural underpinning of
pantsʼ response were subjected to a mixed-design ANOVA, judgments about personal moral dilemmas, where one op-
with group (vmPFC, non-FC, HC) as a between-subject tion involves directly inflicting serious harm to other per-
factor, and dilemma (personal, impersonal, nonmoral) and sons. In particular, it has been found that vmPFC-lesioned
choice (utilitarian, nonutilitarian) as within-subject factors. patients, relative to healthy individuals and neurological
The main effect of choice was significant [F(1, 30) = 7.1, patients with brain damage in other cerebral regions, are
p < .05], indicating overall larger SCRs following utilitarian more likely to endorse personal moral violations in order
versus nonutilitarian choices. However, the factor group to maximize good consequences (i.e., the utilitarian re-
was not significant (F < 1), nor did it enter in any significant sponse). According to one account, this abnormally in-
interactions (all Fs < 1). creased utilitarian pattern of moral judgment would result
To sum up, the results from the ANOVAs revealed that, from impaired affective and intuitive processes, mediated
for healthy subjects and nonfrontal patients, SCRs were by vmPFC, which normally oppose deviations from moral
stronger during evaluation of personal moral dilemmas values and rules shared by a social group (Greene, 2007).
that subsequently attracted an affirmative (e.g., utilitarian) Although these results strongly suggest a causally neces-
response than during evaluation of personal moral dilem- sary role of emotions in morally relevant decision-making,
mas that subsequently attracted a negative (e.g., nonutili- a mechanistic account of how, and at which point, emo-
tarian) response. These individuals, on average, selected tional states subserved by vmPFC influence moral judg-
nonutilitarian over utilitarian choices in personal moral di- ment is still lacking (see Huebner, Dwyer, & Hauser, 2008
lemmas. In contrast, for vmPFC patients, who were more for a discussion).
inclined toward utilitarian judgment, SCRs did not change The present study was designed to examine the pattern
for personal moral dilemmas, subsequently attracting utili- of skin conductance changes, used as an autonomic index
tarian versus nonutilitarian choices. This finding relates of individualsʼ affective responses, associated with personal
increases in SCR during the anticipation of a utilitarian versus impersonal moral judgments, both in vmPFC pa-
choice (and therefore, a personal moral violation) with tients and control participants.

Moretto et al. 1895

 In complete agreement with previous data (Ciaramelli Importantly, in a now seminal series of studies, Bechara
et al., 2007; Koenigs et al., 2007), our present findings reveal et al. (1996, 1999), Bechara, Damasio, Tranel, and Damasio
that patients with vmPFC damage made significantly more (1997) and Damasio et al. (1990) have shown that vmPFC-
utilitarian choices in response to high-conflict personal lesioned patients perform poorly on a gambling task, and
moral scenarios, compared to patients with brain damage unlike normal controls, fail to show anticipatory SCRs im-
that spared vmPFC and to healthy controls. Moreover, pa- mediately before selecting a high-risk option (i.e., one of-
tients with vmPFC lesions were also faster than control fering immediate gain but a high probability of long-term
groups to approve personal moral violations. On the other monetary loss). These findings have led to a proposal that
hand, their behavior in low-conflict personal, impersonal, central representations of bodily states of arousal guide
and nonmoral dilemmas was comparable to that of controls, social behavior and bias decision-making, formulated as
both in terms of the quality of the choices they made and the “somatic marker hypothesis” (Bechara & Damasio,
in the time they needed to make their decisions, further 2005; Bechara et al., 1996; Damasio, 1994, 1996; Damasio
demonstrating the rather selective role played by vmPFC- et al., 1990). According to this hypothesis, the SCR would
mediated emotions on personal moral judgments (Young operate as an alarm signal that, by marking a specific
& Koenigs, 2007; Hauser, 2006). option–outcome combination with a negative tag, pro-
The psychophysiological data mirrored the behavioral motes the avoidance of similar options in the future. This
results: Whereas autonomic bodily signals during consid- interpretation of the SCR is also broadly consistent with
eration of impersonal and nonmoral dilemmas did not the observation of anticipatory SCRs in aversive condition-
differ across participant groups, skin conductance re- ing paradigms (Tabbert, Stark, Kirsch, & Vaitl, 2005; Büchel
cordings during contemplation of personal moral scenar- et al., 1998), and with the proposal that the SCR might rep-
ios differed considerably between patients with vmPFC resent a “somatic marker of erring” (Hajcak, McDonald, &
damage and control groups. Both healthy subjects and Simons, 2003, 2004).
brain-damaged control patients exhibited increased skin Our current finding of increased somatic arousal in con-
conductance activity several seconds before choosing the trol participants immediately before endorsing morally re-
utilitarian option in personal moral dilemmas, for instance, prehensible actions (in the context of personal dilemmas)
deciding that it would be appropriate to kill one person in is highly consistent with the anticipatory SCR obtained
order to save others. In striking contrast, vmPFC patients with Bechara gambling task. In keeping with the somatic
did not generate SCRs in anticipation of utilitarian choices marker hypothesis, anticipatory somatic states of arousal,
in personal moral dilemmas. These findings indicate pro- supported in part by circuits in vmPFC, may help forecast
found differences in the making of moral judgment be- the negative emotional consequences (e.g., shame, guilt
tween vmPFC patients and controls: In control groups, or remorse) of approving personal moral transgressions
emotional/somatic signals were critically recruited during (e.g., utilitarian judgments), thereby motivating individuals
moral judgment, and characterized the anticipation of per- to avoid actions that generate such negative somatic states
sonal moral violations. In contrast, no apparent emotional/ in subsequent choices. Thus, the SCR signal could not only
somatic response accompanied personal moral violations serve as an affective signal that alerts us to the moral rele-
in vmPFC patients. Importantly, somatic responses shaped vance of a rule transgression (particularly if that transgres-
personal moral judgment. A preliminary analysis showed a sion may cause serious harm to others), but also as a
negative correlation between anticipatory skin conduc- teaching signal aimed at decreasing the likelihood of mor-
tance activity and frequency of utilitarian responses in nor- ally impermissible behaviors. Accordingly, the absence
mal controls, such that individuals with higher SCRs of anticipatory SCRs in vmPFC patients may indicate that
before utilitarian choices were more reluctant to judge they fail to represent the affective expectations of highly
moral infractions as acceptable behaviors than those with aversive personal moral transgressions, thereby lacking
lower SCRs. One possibility, therefore, is that emotional a powerful biasing signal (e.g., a moral reinforcer) that
responses mark utilitarian choices in personal moral di- is critical for driving changes of behavior and compliance
lemmas with a negative tag, discouraging the selection of with moral values (Tangney et al., 2007; Amodio & Frith,
those options in future decisions. 2006; Frijda, 2005). This conclusion appears in accor-
Studies of patients with discrete brain lesions and, more dance with current theories maintaining that vmPFC is a
recently, functional imaging techniques have strongly im- critical neural substrate for representing potential posi-
plicated vmPFC in both generation and feedback represen- tive and negative action outcomes in order to promote ap-
tation of states of bodily arousal, indexed by SCRs, which proach/avoidance learning and behavior flexibility (Murray,
may influence cognition and bias motivational behavior OʼDoherty, & Schoenbaum, 2007; Montague, King-Casas,
(Nagai et al., 2004; Critchley, Mathias, & Dolan, 2001; & Cohen, 2006; Oya et al., 2005).
Damasio, Tranel, & Damasio, 1990). In several studies, The interpretation that we offer is compatible with re-
vmPFC patients often exhibit impaired autonomic arousal cent evidence from fMRI, showing that imagined socio-
and subjective feeling in response to emotionally charged moral transgressions associated with sentiments of guilt
events (Roberts et al., 2004; Blair & Cipolotti, 2000; Tranel elicited activation within medial sectors of prefrontal cortex
& Damasio, 1994; Damasio et al., 1990). (Zahn et al., 2009; Kédia, Berthoz, Wessa, Hilton, & Martinot,

1896 Journal of Cognitive Neuroscience Volume 22, Number 8

2008). Moreover, data from economic games indicate that anonymous reviewers for their valuable comments on an earlier
patients with vmPFC damage are abnormally insensitive to draft of the manuscript.
guilt in social and economic interactions (Krajbich, Adolphs, Reprint requests should be sent to Giuseppe di Pellegrino, Di-
Tranel, Denburg, & Camerer, 2009). Finally, our view is partimento di Psicologia, Università di Bologna, Viale Berti Pichat,
also in agreement with the finding that early damage to 5 - 40127 Bologna, Italy, or via e-mail: [email protected].
vmPFC can lead to severe deficits in moral sentiments,
including guilt, remorse, and empathy, as well as pro- Note
found impairments of moral reasoning (Anderson, Bechara,
1. Neurobehavioral consequences commonly observed follow-
Damasio, Tranel, & Damasio, 1999), thereby suggesting ing ACoA aneurysm rupture may include memory loss, confabula-
that emotional processing mediated by this area is develop- tion, decision-making deficits, and altered personality (see DeLuca
mentally necessary for the learning and acquisition of moral & Diamond, 1995, for a review). Many researchers in the field cur-
concepts. rently agree that damage to the basal forebrain primarily mediate
A different, but not necessarily mutually exclusive, ac- the memory loss, whereas damage to vmPFC is thought to under-
lie the personality changes and poor decision-making of ACoA
count of the present findings would instead invoke the patients (DeLuca & Chiaravalloti, 2002; Mavaddat, Kirkpatrick,
concepts of attention regulation rather than emotion Rogers, & Sahakian, 2000; Eslinger & Damasio, 1984). Future
and affective valuation of consequences (Botvinick, 2007; studies of patients with functional imaging and increased autopsy
Dawson et al., 2007). Indeed, SCR variability has been often data may help clarifying which structures are involved in produc-
used as an index of attention-related arousal (Boucsein, ing various aspects of the ACoA aneurysm syndrome.
1992). Notably, a recent study has shown elevation in skin
conductance immediately before actions associated with a
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