Supplementary Results

In line with numerous studies on pain processing84,85,212,523, high pain (contrast cHP_HP > cLP_LP) produced widespread activations in a distributed network often referred to as the pain matrix (Figure 23A, red areas; Table 5;). This included the bilateral posterior (PI) and middle insula (MI), extending further to the ventral portion of this region (VI). Other activations were observed in the middle (MCC) and anterior (ACC) portion of the cingulate cortex, the thalamus, as well as the dorsal postcentral gyrus (PCG), extending medially to the paracentral cortex, over and around somatosensory areas where the legs are represented. Figure 23A (green areas) and Table 5 provides a similar comparison for high disgust (contrast cHD_HD > cLP_LP), revealing strong activations bilaterally in the ventral insula (VI) and amygdala, extending to the piriform cortex (PirC). These effects accord with previous studies on disgust processing 488,498,246,524,525, specifically in the case of olfaction ^526,527. Furthermore, a bilateral portion of the ventral PCG was also activated, over and around somatosensory regions where the face (including the nose) is represented.

Furthermore, the main effect of Stimulus Modality (medium pain vs. medium disgust trials) led to similar results as those for the reference trials (see Figure 23B; Table 6), with medium pain recruiting the dorsal insula (both posterior and anterior portions), the mid anterior cingulate cortex, and the dorsomedial PCG, whereas medium disgust recruited more the ventral insula, amygdala, PirC, and ventrolateral portions of PCG.

109 2.6.2 Supplementary Figures

Figure 23 - Neural activity associated with pain and disgust stimulations during reference trials.

(A) Data from “reference trials”, for pain (red blobs), showing increased neural activity to highly (compared to low) unpleasant stimulations (i.e., cHP_HP > cLP_LP), and for disgust (green blobs), showing increased neural activity to highly (compared to low) unpleasant stimulations (cHD_HD > cLD_LD). Sagittal sections of the cingulate and insular cortex are also displayed to highlight effects in these regions. (B) Data from “Medium trials” for the main effect of Stimulus Modality, showing regions more sensitive to moderate pain, as opposed to disgust (MP > MD), and regions more sensitive to moderate disgust, as opposed to pain (MD > MP).

110 2.6.3 Supplementary Tables

Table 5 - Clusters of activation associated with pain and disgust stimulations of reference trials.

Reference trials: Pain (cHPLP - cLPLP)

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L, Left hemisphere; R, right hemisphere; M, medial activations. Activations clusters are corrected for multiple comparisons for the whole brain.

Table 6 - Clusters of activation associated with main effects of stimulus modality and cue unpleasantness of medium trials, and with consistent > inconsistent activations of disgust-specific medium trials.

Stimulus Modality main effect: Pain (MP - MD)

Region Side x y z t Cluster

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Stimulus Modality main effect: Disgust (MD - MP)

Region Side x y z t Cluster

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Putamen ^{L -30 -8 -2 4.24}

Pallidum L -24 -8 -2 4.06

Superior temporal pole ^{L -32 8 -24 3.67}

Inferior temporal gyrus ^{L -48 -54 -14 5.00}

Superior occipital gyrus ^{L -16 -82 24 5.22}

Middle occipital gyrus ^{L -38 -78 4 5.39}

Inferior occipital gyrus L -28 -84 -8 7.39

Fusiform gyrus ^{L -34 -40 -24 4.17}

Cerebellum ^{L -26 -52 -22 5.88}

Cuneus ^{M -6 -80 26 5.07}

Calcarine M -6 -84 10 7.01

Thalamus M 12 -12 4 5.42

Precentral gyrus ^{R 52 -10 44 7.44 1582 <0.001}

Postcentral gyrus (PCG) ^{R 66 -10 16 4.28}

Rolandic operculum R 58 -12 14 3.48

Middle frontal gyrus R 50 -4 52 5.34

Postcentral gyrus (PCG) ^{L -54 -14 44 6.91 877 <0.001}

Precentral gyrus ^{L -54 0 34 3.68}

Paracentral sulcus ^{M 8 -26 72 3.23 163 <0.05}

Supplementary motor area M 4 -6 56 4.61 156 <0.05

Cue Unpleasantness main effect (cH_M – cL_M)

Region Side x y z t Cluster

Cerebellum M 4 -66 -12 4.26 155 <0.05

Consistent > Inconsistent: Disgust-specific (cHD_MD > cLD_MD) > (cHP_MD > cLP_MD)

Region Side x y z t Cluster

Dorsal anterior insula (dAI) / IFG ^{R 32 30 -4 3.49 351 <0.001}

L, Left hemisphere; R, right hemisphere; M, medial activations. Activations clusters are corrected for multiple comparisons for the whole brain.

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3 Chapter 3

Does inappropriate behavior hurt or stink? Expectancy effects of pain and disgust on moral decisions.

Sharvit, G.

Lin, E.

Vuilleumier, P.

Corradi-Dell’Acqua, C.

(Under review).

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3.1 Abstract

Embodied theories of moral decision suggest that the evaluation of inappropriate conducts is often mediated by a representation of physical disgust. These theories are based on studies showing how disgusting stimuli can prime subsequent moral evaluations, in such a way that people’s choices are considered more despicable following a bad (but not good or neutral) tastes or smells. It is however possible that the effect described by previous studies does not reflect a re-enactment of physical sense of disgust specifically (as an embodied account would predict) but of negatively valenced feelings, elicited also by non-disgusting events such pain. To address this question, we conducted two experiments in which participants were asked to evaluate the appropriateness of conducts whilst expecting olfactory events which were either highly disgusting or neutral, or thermal events which were either highly painful or neutral. In both studies, participants were harsher in evaluating conducts whilst expecting highly disgusting, as opposed to control olfactory or highly painful, events. At the neural level, we found that the activity of the precuneus and posterior cingulate cortex was modulated by the appropriateness of others’ conducts when expecting highly disgusting events (but not when expecting olfactory control or highly painful stimuli). Finally, following the moral judgment, we analyzed participants’ reactions to the olfactory/thermal event that they were expecting. We found that highly disgusting events triggered enhanced electrodermal and neural response in the piriform cortex only after the evaluation of inappropriate (but not appropriate) conducts. Overall, our data prompt for a direct link between representation of inappropriate conducts and that of physical disgust, which does not extend to the case of pain. This supports embodied interpretations for moral cognition, and speak against accounts suggesting a major role of amodal dimensions such as unpleasantness.

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3.2 Introduction

Recent years have seen a proliferation of research investigating the psychological and neural processes underlying moral cognition and, specifically, the degree to which our evaluation of others’

conducts can be affected by current perceptual and emotional states.

The most popular experimental tool to investigate moral cognition is provided by dilemmas, i.e. short vignettes describing an individual confronted with the choice of whether or not to violate a norm (e.g., kill someone) to maximize community welfare (e.g., the life sacrificed will save five others). Through this paradigm, several studies highlighted the neural network underlying moral cognition – the, so-called, “moral brain” - which includes dorsal (DMPFC) and ventral (VMPFC) portions of the medial prefrontal cortex, the precuneus (PC), the posterior cingulate cortex (PCC), the temporoparietal-junction (TPJ) extending to the superior temporal sulcus (STS), and the amygdala (see531–533,452 for meta-analyses).

The previous line of research in moral cognition showed how individuals’ evaluations can be affected by factors which are intrinsic to the dilemmas, such as the number of people implicated^534,535, their relationship with the participant of the study534,536,537, or even if task was framed in such way that implicitly encourange participants to assume the point of view of the protagonist of the vignette (“would you, in this situation, choose this line of conduct?” vs. “to which extent is this line of conduct morally acceptable?”)^534,538. More interestingly, also extrinsic factors which are, at least in principle, unrelated to morality have been shown to affect individuals’ evaluations. For instance, moral judgments/choices can be biased by individuals’ personal hygiene, such as the cleanness of their hands⁵³⁹, or by the direct exposure to disgusting odors/tastes^479,468 (or the subsequent recall thereof⁵⁴⁰), or even the scent in the experimental room⁵⁴¹.

A common element between the different intrinsic and extrinsic factors that are known to modulate moral cognition relies in their ability change individuals’ emotional engagement during the evaluation process⁵⁴². Indeed, seminal theoretical perspectives posit that moral judgments are not always achieved through formal reasoning, but might result from intuitions generated by “gut” feelings^543,544, possibly linked with one’s current emotional and somatic state.

To our knowledge, there are two possible ways in which individuals’ emotional/somatic state might affect moral judgments. First, according to embodiment theories, conceptual/metaphorical representations of a given emotion are grounded on the same structures underlying direct affect^545–

548, with consequent somatic and physiological reactions (nausea, facial display, etc.)⁵⁴⁹. Specifically, embodied theories of morality posit that disgust has a major and specific role in moral cognition, as an embodied moral judgement^468–470. Indeed, there is evidence that moral disgust is a genuine form

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of disgust, which has an associative link with physical disgust. First, both adults and children call moral transgressions disgusting^471–473 and match them to disgusted facial expressions^473–475 even when the transgressions do not reference physical disgust. Second, moral transgressions result in a canonical facial expression^475,476, similar to that elicited by physical disgust and distaste⁴⁷⁵. Specifically, the upper lip raise in response to transgressions was found to be correlated with self-reported disgust, but not with other emotions (e.g. anger or contempt)⁴⁷⁵. Third, individuals with high (compared to those with low) sensitivity to physical disgust make more severe judgments about moral transgressions, an effect which is not accounted by other differences in negative traits⁴⁷⁷. Finally, it has been shown that inducing physical disgust or distaste can affect people’s moral evaluations, and vice versa479,468,478. For instance, participants made harsher moral judgments when subjected to a disgusting odor⁴⁶⁸ or a bitter taste⁴⁷⁹. Likewise, people find drinks more unpleasant after having observed immoral (as opposed to moral) behaviors⁴⁸⁰. Moreover, Wheatley and Haidt have reported that participants made harsher moral judgments following an induction of disgust feeling by hypnosis⁴⁷⁸. Within this embodiment framework, it is reasonable to predict that an evaluation of people’s conducts as

“morally disgusting” (i.e. extremely inappropriate) should be biased exclusively by physical disgust, but not by other kinds of affective/somatic experiences, even those aversive sensations (e.g., pain) which are as unpleasant as disgust.

Alternatively, moral evaluations might be modulated by amodal or supramodal properties of our emotional/somatic experience, such as unpleasantness or arousal, which are not specific to disgust.

In this perspective, most of the arguments linking moral cognition to physical disgust might as well be used to link moral cognition to the experience of pain. For instance, although morally-questionable conducts are often described as disgusting, in some cases they are described as “hurtful” (e.g., see the literature on social rejection/exclusion106,108,550). Furthermore, moral transgressions elicit facial expressions which are similar not only to the case of physical disgust, but also to the case of pain^487,551. A recent study showed that the neural responses to unfair behavior (although implemented through the Ultimatum Game task and not through dilemmas) in the insular and middle cingulate cortex were similar not only to those triggered by disgusting tastes, but also by painful electric shocks¹²⁷. Finally, although it has been repeatedly shown that physical disgust and moral processing can exert reciprocal causal influence, it has been argued that similar effects could be observed also by replacing disgust with a different experience of comparable unpleasantness or arousal^480,552.

In light of the two hypotheses reviewed above, we tested whether the link between physical disgust on moral judgments is modality-specific, or generalizes also the case of pain. To achieve this aim, we used a paradigm developed by our group in which participants experienced equally-unpleasant thermal pain and olfactory disgust after having been primed by an anticipatory cue⁵²⁰. In the time

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between the presentation of the cue and the subsequent stimulus, participants were asked to evaluate the appropriateness of people’s conducts as described in short vignette. The critical question would be to see whether the expectancy of two qualitatively different (and yet equally unpleasant) experiences such pain and disgust impact moral judgments in a comparable or differential way.

Experiment 3 investigated how and whether pain and disgust impact moral judgments looking at behavioral and physiological measures, whereas Experiment 4 tested their modulations on neural processing associated with moral coding.

3.3 Materials & Methods

3.3.1 Participants

We recruited a total of 47 participants. 22 (15 females; aged 18-39 mean 26.23 SD 4.88 years) took part to Experiment 3, whereas 25 (13 females; aged 18-33 mean 24.48 SD 4.19 years) took part in Experiment 4. All participants were native speakers of either French or English. They were right-handed, reported no history of neuropsychological or psychiatric disorders, and were sensitive to the odorants used in the present study. None had any history of neurological/psychiatric illness, reported any olfactory deficit. In addition, all participants taking part to Experiment 4 passed a screening for MRI-safety. Written informed consent was obtained from all subjects, who were naïve to the purpose of the experiment. The study was approved by the local ethics committee and conducted according to the declaration Helsinki.

3.3.2 Olfactory stimulation

Similarly to Experiments 1-2, odorants were delivered to the subjects’ nostrils by means of rubber cannulas connected to a computer-controlled, multi-channel, custom-built olfactometer. The olfactometer is able to reliably release various kinds of compounds over multiple trials, without contamination from one trial to the other, at known times, and without additional noise or tactile stimulation in the nose (see, Ischer et al., 2014 technical details for this apparatus). The odorous substances were diluted at variable concentrations in odorless dipropylene glycol. Odors were embedded in 1 l/min constant and filtered airstream. Two odorants provided by Firmenich, SA (Geneva) were selected on the basis of previous evaluations 500,501,519. Isovaleric acid (reminiscent of dirty socks) and Sclarymol (sweat) were chosen to elicit disgust in the participants. Each of these substances was diluted in five different concentrations (0.1%, 0.5%, 1%, 5% and 10% for Isovaleric acid and Sclarymol). In addition, shampoo (10%) and lavender (10%) odorants were also used to elicit positively-valenced sensation in participants. These positive odors were used in order to give to participants an olfactory relief from the disgusting odors and to reduce the occurrence of putative habituation or sensitization effects. On overall, our experimental set-up comprehended 12 olfactory

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stimuli (isovaleric acid and Sclarymol, each at 5 different concentrations, plus shampoo and lavender) and a 13^th odorless solution of dipropylene glycol that served as a control. In the main experiment, each participant was presented with 3 out of the possible 12 olfactory stimulations. These comprised one odorant expected to elicit disgust, at two different concentrations: low (unpleasantness ratings ~

− 5), and high (~ − 40). Additionally, a third odorant was expected to elicit a pleasant experience (> 0).

Those three odors were selected, at the individual level, on the basis of a pleasantness-rating task carried out at the beginning of the experimental session.

In this preselection task, all 12 odors (plus 13^th odorless control) were delivered to the participants as follows: each trial began with a 1 s fixation cross that was presented in the center of the computer screen; then the instruction “Breathe-out” was presented together with a numerical 3 s countdowns.

During the countdown, participants were instructed to expire and empty their lungs. When the countdown reached 0, participants had to breath in evenly while the text string “Breathe-in”

instruction was presented and the odorant delivered. This trial structure allowed to minimize the intra- and inter participant breathing pattern variability (see also Delplanque et al., 2009; Sharvit et al., 2015) and to synchronize the respiration cycle with the odorant delivery regardless of its nature.

After each stimulus, a visual analogic scale (VAS) was presented. Participants were asked to rate the degree of subjective unpleasantness/pleasantness evoked by the odorant by marking the corresponding position on the scale with a mouse device held in their right hand. The 13 stimuli (10 odors plus the control odorless solution) were presented twice in an equally distributed and pseudorandomized order. The olfactory-stimuli selection session lasted approximately 15 minutes.

3.3.3 Thermal stimulation

Thermal stimuli were delivered through a computer controlled thermal stimulator with an MRI-compatible 25 x 50 mm fluid-cooled Peltier probe (MSA, Thermotest), attached to participants’ leg.

For each participant, we selected two temperatures, each aimed at evoking comparable amount of unpleasantness (low and high) of one of the two odors selected for the same participant. These two temperatures were individually calibrated for each participant based on a brief thermal-stimuli selection session.

In line with Experiments 1-2, individual temperatures were determined through a modified double random staircase (DRS) algorithm aimed at identifying stimuli of comparable unpleasantness (measured with the same VAS as for the odorants selection session) to the highly unpleasant odor.

Our DRS procedure selected a given temperature on each experimental trial according to the previous response of the participant. Trials rated as more unpleasant than the given cut-off (selected in a subject-specific way, from ratings for the highly unpleasant odor) led to a subsequent lowered

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temperature in the next trial; whereas trials rated as less unpleasant than the given cut-off led to a subsequent higher temperature. This resulted in a sequence of temperatures that rapidly ascended towards, and subsequently converged around, a subjective unpleasantness threshold, which was in turn calculated as the average value of the first 4 temperatures leading to a direction change in the sequence. In order to avoid participants anticipating a systematic relationship between their rating and the subsequent temperature, two independent staircases were presented randomly. Initial thermal stimulations for the two staircases were 41°C and 43 °C. Within each staircase, stimulus temperatures increased or decreased with steps of 3°C, while smaller changes (1°C) occurred following direction flips in the sequence. None of our subjects was stimulated at temperature larger than 52°C.

The thermal stimuli were delivered in the following way: participants first saw a 1 s long fixation-cross, followed by the text string “Temperature is changing” and concomitant delivery of the heat stimulation. Each thermal event was composed of 3 s of rise time, 2 s of plateau at the target-temperature, and 3 s of return to baseline (37°C). The speed of the temperature rise and the temperature return was automatically adjusted according to the plateau in order to maintain both a rise time and a return time of approximately 3 s each. The unpleasantness scale was presented just after the 2 s of plateau stimulation, when the temperature started to return to baseline, and lasted until participant provided a response.

The present DRS approach was employed to determine temperatures eliciting two distinct levels of unpleasantness (corresponding to different levels of pain): low and high. This approach led to a highly unpleasant temperature, which varied on a participant-by-participant basis, but converged around the average value of 48.87°C (SD 1.50) for Experiment 3, and 47.15°C (SD 1.51) for Experiment 4. On the basis of this temperature, we selected one additional temperature associated with low unpleasantness, corresponding to an average value of 46.81°C (SD 1.61) for Experiment 3, and 44.68°C (SD 2.01) for Experiment 4. This session lasted approximately 10 minutes.

3.3.4 Dilemmas

For the purpose of this study, we created a database of 16 moral dilemmas and 16 non-moral (control) dilemmas, each of which was edited both in French and in English. The English version of the dilemmas were obtained from the same database of 44 stimuli used by Greene and colleagues (2001): in particular, the moral dilemmas corresponded to the “moral-personal” scenarios in Greene’s study, whereas the “non-moral” controls corresponded to the “neutral” scenarios. These dilemmas were translated ad hoc by a native speaker proficient in English. The original scenarios were also modified to incorporate cultural differences (e.g., changing “$” to “CHF”).

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In a pilot study, we asked proficient speakers in either French (20 volunteers: 12 females; aged 19–50 mean 28.8 SD 6.82 years) or English (37 volunteers: 19 females; aged 20-43 mean 28.81 SD 4.89) to evaluate each of the 44 (25 moral and 19 non-moral) dilemmas in their corresponding language. In particular, individuals taking part to the pilot study rated each dilemma according to the following dimensions. (1) “How much the course of action described in the story is appropriate for you?”;

participants marked the point corresponding to their judgment on a visual analog scale ranging from

“extremely inappropriate” to “extremely appropriate”. (2) “How emotionally engaged were you when reading the vignette?”; participants responded using a visual analog scale ranging from “not engaged at all” to “extremely engaged”. (3) “How comprehensible was the vignette?”; participants responded using a scale ranging from “extremely incomprehensible” to “extremely comprehensible”. The ratings were divided in three blocks, one for each question during which all 44 dilemmas were evaluated. The order of the blocks, and the order of the dilemmas within each block, was randomized across participants.

The data from these rating tasks were used to select 16 moral and 16 non-moral dilemmas, who displayed, in both their English and French formulation, the following properties: (a) moral dilemmas were associated with the lowest appropriateness ratings and with the highest emotional engagement ratings; (b) non-moral dilemmas were associated with the highest appropriateness ratings and the lowest emotional engagement ratings; (c) all dilemmas were associated with high comprehensibility ratings. Supplementary information (SI) Figure 32 reports the data associated with the selected 32 dilemmas, which show a clear dissociation between moral and non-moral scenarios (but nevertheless exhibit considerable variability within each category).

3.3.5 Experimental Setup 3.3.5.1 Task Design

The main experimental task consisted of 76 trials (see Figure 24A-B). On each trial, a 1.5 s predictive cue was presented and followed by an inter-stimulus interval (ISI) with a fixation cross at the screen center. In Experiment 3, this ISI had a fixed duration of 2 s, whereas in Experiment 4 the ISI duration

The main experimental task consisted of 76 trials (see Figure 24A-B). On each trial, a 1.5 s predictive cue was presented and followed by an inter-stimulus interval (ISI) with a fixation cross at the screen center. In Experiment 3, this ISI had a fixed duration of 2 s, whereas in Experiment 4 the ISI duration

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