Volume 222, 15 November 2020, 117251
Obeying orders reduces vicarious brain activation towards victims’ pain
Author links open overlay panelEmilie A.Caspar1†KalliopiIoumpa1†ChristianKeysers12‡ValeriaGazzola12‡Show morehttps://doi.org/10.1016/j.neuroimage.2020.117251Get rights and contentUnder a Creative Commons licenseopen access
•Participants inflict more shocks when obeying orders than when freely deciding.
•Empathy-related regions are less active when obeying orders compared to acting freely.
•Coercion reduced neurocognitive processes associated with guilt.
•Reduced empathy- and guilt-related activations could facilitate harming under orders.
Past historical events and experimental research have shown complying with the orders from an authority has a strong impact on people’s behaviour. However, the mechanisms underlying how obeying orders influences moral behaviours remain largely unknown. Here, we test the hypothesis that when male and female humans inflict a painful stimulation to another individual, their empathic response is reduced when this action complied with the order of an experimenter (coerced condition) in comparison with being free to decide to inflict that pain (free condition). We observed that even if participants knew that the shock intensity delivered to the ‘victim’ was exactly the same during coerced and free conditions, they rated the shocks as less painful in the coerced condition. MRI results further indicated that obeying orders reduced activity associated with witnessing the shocks to the victim in the ACC, insula/IFG, TPJ, MTG and dorsal striatum (including the caudate and the putamen) as well as neural signatures of vicarious pain in comparison with being free to decide. We also observed that participants felt less responsible and showed reduced activity in a multivariate neural guilt signature in the coerced than in the free condition, suggesting that this reduction of neural response associated with empathy could be linked to a reduction of felt responsibility and guilt. These results highlight that obeying orders has a measurable influence on how people perceive and process others’ pain. This may help explain how people’s willingness to perform moral transgressions is altered in coerced situations.
Many examples in the history of Mankind show that when people obey the orders from an authority, they are able to perform highly immoral acts towards others (e.g. Arendt, 1951, 1963, Herman and Chomsky, 1988). Even past experimental research, mainly by the work of Stanley Milgram (1963, 1974), showed that many people comply with coerced orders to inflict unbearable electric shock on a person for the sake of the experiment in which they were involved. However, the mechanisms underlying such drastic change in human behaviour during obedience acts remain largely unknown.
Humans, as other mammals, have the capacity to feel what others feel, namely, they have empathy. An extensive literature has shown that seeing another individual in pain triggers an empathic response in the observer (e.g. Keysers and Gazzola, 2014; Decety, 2011; Singer and Lamm, 2009; Krishnan et al., 2016). The seminal study of Singer et al. (2004) shows that experiencing painful stimulations and empathizing with the same pain delivered to others triggers an overlapping brain activity in the anterior insula (AI) and in the anterior cingulate cortex (ACC). These results, largely replicated (Fan et al., 2011; Lamm et al., 2011 for an overview), suggest that we share what others feel, at least in part, because we map their pain onto our own pain system (see Lamm and Majdandzic, 2015 for a critical review). The most widespread explanation for this phenomenon has been related to mirror neurons, which were initially shown to fire both when monkeys execute and observe an action (Gallese et al., 1996; Keysers, 2011), but which have recently been demonstrated to also exist in the ACC (Carillo et al., 2019). It has been argued that we generally do not inflict pain to our conspecifics because we would vicariously experience this pain ourselves (Waal and Preston, 2017; Meffert et al., 2013; Smith, 1759; Hein et al., 2016), and we have shown that deactivating the ACC in rats, where pain mirror neurons were found, reduces the emotional reactions to the pain of others (Carrillo et al., 2019) and prevents rats from choosing actions that prevent pain to other rats over actions that harm another rat (Hernandez-Lallement et al., 2020). We therefore hypothesize that if ‘simply’ obeying the orders of an authority allows humans to perform atrocities towards other humans, it could do so by reducing the inner empathic response towards the inflicted pain, which should lead to a measurable reduction of brain response in the abovementioned regions associated with empathy and pain ratings when witnessing pain delivered under coerced compared to free condition.
Indirect evidence for this hypothesis comes from a number of studies. Caspar et al. (2016) showed that both the sense of agency and the feeling of responsibility were reduced in a condition in which people were ordered by the experimenter to inflict either a financial or a physical pain to a ‘victim’ in comparison with a condition in which they were free to decide which action to execute. Several studies further suggested that losing the sense of responsibility for an observed pain reduces activity in the neural network associated with pain empathy (Cui et al., 2015; Koban et al., 2013; Lepron et al., 2015) and reduces feelings of guilt (Yu et al., 2020). However, those studies never explored the effect of receiving orders from an authority. Cui et al. (2015) and Koban et al. (2013) focused on errors that result in pain delivered to another individual. Lepron et al. (2015) showed that when participants are the executors (vs. mere eyewitnesses in the ‘observe’ condition) of painful outcomes delivered to another individual, empathic responses (as measured by facial electromyography and heart rate variability) increased. Interestingly, the authors did not find differences in the empathic response between a condition in which they could decide and execute the action and a condition in which they could only execute an action decided by the computer. However, the perception of being “under command” may strongly differ when the instructions come from a computer and when they come from a human, authoritative figure. Therefore, whether performing an action that causes pain to others under human command would lead to reduced empathic responses to that pain is still largely unknown. Here, we predict that receiving orders to deliver painful shocks will reduce empathy for that pain, even if participants are the authors of the actions. We hypothesize that this effect could be associated with the reduced experience of responsibility and guilt under command.
In the present paradigm, one out of two volunteers (the ‘agent’) was placed in the MRI scanner and was free to decide (abbreviated as ‘Free condition’) or received a coerced instruction (‘Coerced condition’) to deliver a real, mildly painful shock to the ‘victim’ for a small monetary gain to the agent (+€0.05). We expected to observe a reduced activity of the pain network, including the insula and the ACC, as well as a reduced perception of responsibility and guilt in the coerced condition in comparison with the free condition. We also expected that participants that show more activity in these pain regions while witnessing shocks would decide to deliver fewer shocks under the free condition. These results would help explain why people are less morally inhibited when complying with orders.
Because it is difficult to associate changes in brain activity in a single location such as the anterior insula or ACC with specific mental processes such as empathy or guilt (see Lieberman and Eisenberger, 2015 vs Wager et al., 2016 for a related debate about reverse inference), we also used three multivariate signatures that have been validated to scale quite selectively with perceiving other people’s pain (the vicarious pain signature, VPS, Krishnan et al., 2016), with feeling pain (the neurological pain signature, NPS, Wager et al., 2013) and with the feeling of interpersonal guilt (Yu et al., 2020).