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You Shouldn't Have: Your Brain on Others' Crimes

2008; Cell Press; Volume: 60; Issue: 5 Linguagem: Inglês

10.1016/j.neuron.2008.11.019

1097-4199

Johannes Haushofer, Ernst Fehr,

Free Will and Agency

Our legal system requires assigning responsibility for crimes and deciding on appropriate punishments. A new fMRI study by Buckholtz et al. in this issue of Neuron reveals that the right dorsolateral prefrontal cortex (rDLPFC) plays a key role in these cognitive processes. This finding sheds light on the neural mechanisms underlying moral judgment from a third-party perspective. Our legal system requires assigning responsibility for crimes and deciding on appropriate punishments. A new fMRI study by Buckholtz et al. in this issue of Neuron reveals that the right dorsolateral prefrontal cortex (rDLPFC) plays a key role in these cognitive processes. This finding sheds light on the neural mechanisms underlying moral judgment from a third-party perspective. Much recent research documents people's willingness to punish norm violations and to enforce social norms. This willingness also exists if the punishers derive no material benefit themselves, but instead incur costs (Henrich et al., 2001Henrich J. Boyd R. Bowles S. Camerer C. Fehr E. Gintis H. McElreath R. Am. Econ. Rev. 2001; 91: 73-78Crossref Scopus (1326) Google Scholar). Even unaffected third parties who merely observe a norm violation engage in costly norm enforcement (Fehr and Fischbacher, 2004Fehr E. Fischbacher U. Evol. Hum. Behav. 2004; 25: 63-87Abstract Full Text Full Text PDF Scopus (1066) Google Scholar). Modern legal systems are probably based on these deep human instincts, aiming primarily at retribution: offenders are jailed or executed to punish them for their transgressions, and only in the second instance to prevent future harm to society (Kant, 1999Kant I. Metaphysical Elements of Justice. Hackett Publishing, Indianapolis, IN1999Google Scholar, Whitman, 2003Whitman J.Q. Buffalo Crimial Law Review. 2003; 7: 85-107Crossref Google Scholar). Retributive punishment is thus a core element of contemporary justice. Judgment by third parties about punishment requires assigning responsibility for an offense that a perpetrator commits against a victim, judging the severity of that action, and finally selecting an appropriate punishment. Given the centrality of this process to the administration of justice, elucidating the cognitive and neural mechanisms underlying such judgments is of considerable interest. In this issue of Neuron, Buckholtz and colleagues (Buckholtz et al., 2008Buckholtz J.W. Asplund C.L. Dux P.E. Zald D.H. Gore J.C. Jones O.D. Marois R. Neuron. 2008; 60 (this issue): 930-940Abstract Full Text Full Text PDF PubMed Scopus (193) Google Scholar) take a step in this direction: using functional magnetic resonance imaging (fMRI), they examine which brain regions are activated when humans make judgments regarding the appropriate punishments for various violations. Specifically, participants in their study read vignettes describing hypothetical transgressions that a fictitious agent, "John," commits against another person. The stories were divided into three conditions: in the first, the "responsibility" (R) condition, the perpetrator was responsible for the negative outcome of his action against the victim; in the "diminished responsibility" (DR) condition, mitigating circumstances were present that reduced the protagonist's responsibility; and finally, the "no crime" (NC) condition consisted of stories that did not describe crimes. The participants had to make judgments regarding the degree of punishment that the offender should receive, on a scale from 1 to 9. The authors then proceeded to analyze the brain activation linked to these judgments. They contrasted activation in the "R" and "DR" conditions in order to identify neural correlates of responsibility. This contrast revealed a peak of activation in right doroslateral prefrontal cortex (rDLPFC). This activation did not simply reflect higher arousal resulting from reading the "R" compared to the "DR" stories, for two reasons: first, the stories were counterbalanced across subjects, so that the same stories appeared in the "R" condition for one-half of subjects and the "DR" condition for the other half of subjects, with the only difference being the responsibility allocation. More importantly, the results in the rDLPFC remained the same when the two conditions were matched for reported arousal. Interestingly, the same area in rDLPFC was activated in a second contrast between punished and nonpunished crimes from the "DR" condition. Thus, these findings suggest that rDLPFC might be involved in assigning responsibility for crimes or making judgments about appropriate punishments. However, rDLPFC did not exhibit a correlation between neural activation and punishment magnitude, suggesting that it does not directly underlie the decision on the amount of punishment. In contrast, there was some evidence that activation in amygdala and other emotion-related areas correlates with the degree of punishment subjects assign to the protagonist: higher punishment scores were associated with higher activation in these regions during the decision period. These findings complement a number of previous studies and shed new light on the role of right DLPFC in judgments involving the normative dimensions of social interactions. This region has previously been highlighted in a number of studies addressing questions similar to those studied by Buckholtz et al.: an early study (Sanfey et al., 2003Sanfey A.G. Rilling J.K. Aronson J.A. Nystrom L.E. Cohen J.D. Science. 2003; 300: 1755-1758Crossref PubMed Scopus (2050) Google Scholar) found increased activation in rDLPFC when subjects were involved in fairness judgments and decided whether to reject a low offer in an ultimatum game, compared to when they received a high offer. However, as in Buckholtz et al., the punishment decision was not correlated with activity in right DLPFC, i.e., subjects with higher DLPFC activation punished neither more nor less than those with less DLPFC activation. The work of Greene et al., 2004Greene J.D. Nystrom L.E. Engell A.D. Darley J.M. Cohen J.D. Neuron. 2004; 44: 389-400Abstract Full Text Full Text PDF PubMed Scopus (1464) Google Scholar suggests that this brain region is involved in normative evaluations involving conflicting moral goals. They presented participants with moral scenarios similar to the famous trolley dilemma (Thomson, 1976Thomson J.J. Monist. 1976; 59: 204-217Crossref PubMed Scopus (461) Google Scholar) and compared trials in which subjects acted in the interest of greater aggregate welfare (utilitarian decisions) at the expense of personal moral standards (e.g., killing one's child to keep its crying from raising the attention of enemy soldiers). Again this contrast showed activation in rDLPFC. The same region was also found to be active in another study by Spitzer et al., 2007Spitzer M. Fischbacher U. Herrnberger B. Gron G. Fehr E. Neuron. 2007; 56: 185-196Abstract Full Text Full Text PDF PubMed Scopus (351) Google Scholar involving social decision making: these authors scanned the first mover in a game similar to the ultimatum game, where this person can choose to transfer any amount of her endowment to another player, who then can punish the first mover for unfair transfer levels. The study found that rDLPFC was more active when the first player was threatened with punishment for making small transfers to the second player compared to a control treatment in which punishment was not an option. The punishment threat thus activates the rDLPFC in the player who faces the threat. Moreover, the activation in rDLPFC was the stronger the more subjects changed their behavior in the ultimatum game (when they faced the punishment threat) relative to the control treatment (when they did not face a threat). Finally, deactivating the rDLPFC with repetitive transcranial magnetic stimulation (TMS) reduced participants' ability to reject unfair offers in the ultimatum game, although participants' ability to judge these offers as unfair was not impaired (Knoch et al., 2006Knoch D. Pascual-Leone A. Meyer K. Treyer V. Fehr E. Science. 2006; 314: 829-832Crossref PubMed Scopus (661) Google Scholar). How does the new study fit together with the previous ones? To what extent is it possible to provide a unifying interpretation of the role of rDLPFC across all of these studies? The findings described above are all consistent with for the notion that rDLPFC is involved in inhibiting prepotent responses: rejecting a low ultimatum game offer (Sanfey et al., 2003Sanfey A.G. Rilling J.K. Aronson J.A. Nystrom L.E. Cohen J.D. Science. 2003; 300: 1755-1758Crossref PubMed Scopus (2050) Google Scholar) means losing money and thus requires overriding the impulse to accept the money; making utilitarian rather than emotion-driven moral decisions (Greene et al., 2004Greene J.D. Nystrom L.E. Engell A.D. Darley J.M. Cohen J.D. Neuron. 2004; 44: 389-400Abstract Full Text Full Text PDF PubMed Scopus (1464) Google Scholar) and resisting the impulse to make low transfers (Spitzer et al., 2007Spitzer M. Fischbacher U. Herrnberger B. Gron G. Fehr E. Neuron. 2007; 56: 185-196Abstract Full Text Full Text PDF PubMed Scopus (351) Google Scholar) also require the suppression of knee-jerk responses. The activation of rDLPFC in these studies is consistent with the view that rDLPFC is involved in overriding such responses. In addition, the TMS study (Knoch et al., 2006Knoch D. Pascual-Leone A. Meyer K. Treyer V. Fehr E. Science. 2006; 314: 829-832Crossref PubMed Scopus (661) Google Scholar) mentioned above even suggests a key causal role of rDLPFC for overriding prepotent impulses because if rTMS inhibits the recruitment of rDLPFC, subjects are less able to resist the temptation to accept unfair money offers. Is the new study by Buckholtz and colleagues consistent with this view of the role of rDLPFC? The crucial new element of this study is the fact that participants were instructed to determine "appropriate" judgments of punishment from a third-person perspective. Thus, participants acted like criminal judges; the fact that their punishment decisions correlated strongly with the prison sentences they deemed appropriate for the crimes in question attests to the fact that they saw themselves in this role. Inasmuch as judges are expected to act impartially and objectively, this task, too, requires the suppression of prepotent responses to the crimes described, to produce "just" and impartial punishments. Reading stories about severe crimes may well cause arousing emotional responses that may be associated with a strong desire to punish. Buckholtz et al. report, in fact, that right amygdala is strongly positively correlated with punishment judgments—a finding consistent with the role of this brain region in the representation of arousing emotional events. However, the demands of impartiality often require overriding these impulses in order to produce a reasonable judgment. The higher activation of rDLPFC in the R compared to the DR condition and during punished versus nonpunished trials is therefore consistent with a role for rDLPFC in the suppression of prepotent emotional reactions. Thus, the study of Buckholtz makes a valuable contribution in that it illustrates that third-person judgment situations, such as those used in their study, may rely on similar neural mechanisms as two-person economic and social exchanges. While it is difficult to draw reverse inferences about mental states based on brain activation (Poldrack, 2006Poldrack R.A. Trends Cogn. Sci. 2006; 10: 59-63Abstract Full Text Full Text PDF PubMed Scopus (1242) Google Scholar), one might speculate, based on this new study, that the mental processes motivating judicial verdicts involve the suppression of prepotent emotional reactions in favor of impartial and objective verdicts. Thus, this new result might, if confirmed by future studies, elucidate the neural source of judicial impartiality. The Neural Correlates of Third-Party PunishmentBuckholtz et al.NeuronDecember 10, 2008In BriefLegal decision-making in criminal contexts includes two essential functions performed by impartial "third parties:" assessing responsibility and determining an appropriate punishment. To explore the neural underpinnings of these processes, we scanned subjects with fMRI while they determined the appropriate punishment for crimes that varied in perpetrator responsibility and crime severity. Activity within regions linked to affective processing (amygdala, medial prefrontal and posterior cingulate cortex) predicted punishment magnitude for a range of criminal scenarios. Full-Text PDF Open Archive