Personal Moral Judgment Following Damage to Ventromedial Prefrontal Cortex
Personal Moral Judgment Following Damage to Ventromedial Prefrontal Cortex
Recent fMRI evidence has detected increased medial prefrontal activation during contemplation of personal moral dilemmas compared to impersonal ones, which suggests that this cortical region plays a role in personal moral judgment. However, functional imaging results cannot definitively establish that a brain area is necessary for a particular cognitive process. This requires evidence from lesion techniques, such as studies of human patients with focal brain damage. Here, we tested 7 patients with lesions in the ventromedial prefrontal cortex and 12 healthy individuals in personal moral dilemmas, impersonal moral dilemmas and non-moral dilemmas. Compared to normal controls, patients were more willing to judge personal moral violations as acceptable behaviors in personal moral dilemmas, and they did so more quickly. In contrast, their performance in impersonal and non-moral dilemmas was comparable to that of controls. These results indicate that the ventromedial prefrontal cortex is necessary to oppose personal moral violations, possibly by mediating anticipatory, self-focused, emotional reactions that may exert strong influence on moral choice and behavior.
Recent interest in social cognitive neuroscience has led to a growing body of research aimed at elucidating the neural and cognitive mechanisms that underlie human moral behavior (see for recent reviews Moll et al., 2005; Beer and Ochsner, 2006; Lieberman, 2006; McKinnon et al., 2006). Moral behavior refers to what individuals should do based on principles and judgments (i.e. moral values) shared with other members of their social environment. The initial foray into the neuroscience of moral behavior and reasoning came from the systematic examinations of changes in the social life of people with localized brain damage produced by accidents, strokes or neurological disease. Patients with lesions in the orbitofrontal and ventromedial prefrontal cortex have long been described as presenting high levels of aggressiveness, lack of concern for social and moral rules and irresponsibility (e.g. Eslinger and Damasio, 1985; Stuss et al., 1992; Damasio, 1994; Blair and Cipolotti, 2000), which suggests these brain areas are important neural correlates of moral behavior. Lesions of the same areas during childhood impair the development of moral knowledge and ethical judgment (Anderson et al., 1999), further suggesting that these brain regions are important neural correlates of moral behavior. Accordingly, functional imaging studies in healthy individuals involving moral judgment (Moll et al., 2002a; Heekeren et al., 2003) and moral reasoning (Greene et al., 2001; 2004; Borg et al., 2006) have detected consistent activations of the orbitofrontal and ventromedial prefrontal cortex, although activated regions encompass a more extended network of neural regions (see Moll et al., 2005 and references therein).
One crucial question concerns the specific mechanism by which these frontal regions promote behaviors that conform to, rather than violate, moral values and expectations shared by a social group. According to classical moral theories, moral behavior is a perfectly rational type of affair, governed by deliberative and high cognitive processing. A more recent view, however, emphasizes the role of intuitive and affective processes in social and ethical decision-making (Damasio, 1994; Greene et al., 2001).
Consistent with this latter view, Greene and colleagues have proposed that medial prefrontal areas might mediate strong negative emotional responses to moral violations, which prevent individuals from implementing such morally impermissible actions (Greene and Haidt, 2002). These emotions might be the by-product of (or, alternatively, evolved to promote) humans' intensely social nature, which relies on behaviors warranting the cohesion of social groups (Greene, 2003). In a series of fMRI experiments (Greene et al., 2001; 2004), the authors explored this possibility by studying healthy individuals who were considering moral dilemmas. Ethicists have called moral dilemmas situations in which a person faces a conflict between two (or more) opposing moral values or requirements. Specifically, Greene et al. (2001) compared individuals' performance on two different types of moral dilemmas, i.e. those involving 'personal' and those involving 'impersonal' moral judgments. A typical personal moral dilemma involves having to decide whether or not to push a stranger off of a footbridge in front of an oncoming trolley in order to save five people on the main track (i.e. the footbridge dilemma). In a quite similar situation, an impersonal moral dilemma involves having to decide whether or not to hit a switch that will turn the trolley to an alternate set of tracks, where it will kill one person instead of five (i.e. the trolley dilemma). In both types of dilemmas individuals are required to judge whether it is appropriate to incur in a moral violation (i.e. killing one person) in order to maximize overall consequences (i.e. saving five persons). However, whereas personal moral violations consist in (i) causing serious bodily harm (ii) to a human being (iii) through one's own agency (i.e. in such a way that the harm does not result from the deflection of an existing threat onto a different party), impersonal moral violations do not satisfy at least one of these criteria (e.g. #3 in the case of the trolley dilemma), and, therefore, may induce a less intense emotional experience in individuals (Greene et al., 2001).
Greene and colleagues found that medial prefrontal regions commonly associated with social/emotional processing (Damasio, 1994; Berthoz et al., 2002; Moll et al., 2002b; 2005), including the medial prefrontal gyrus and the posterior cingulate gyrus, were strongly activated while responding to personal, but not impersonal, moral dilemmas (Greene et al., 2001). Importantly, this medial prefrontal activation appeared to interfere with 'utilitarian' moral judgment: Individuals were slower to approve, compared to refuse, personal moral violations, consistent with the idea that the approval of a personal moral violation is in conflict with emotional intuitions, whereas its refusal is a rather automatic reaction (Greene and Haidt, 2002). This pattern of results was not detected for impersonal moral judgments or dilemmas with no moral connotation (non-moral dilemmas), suggesting these were mainly accomplished through logical reasoning, supported by dorsolateral prefrontal cortex (Greene et al., 2004), with relatively scarce contribution from processes dedicated to social cognition.
Although these neuroimaging studies have suggested a role of the medial prefrontal cortex in personal moral judgment, it is currently unclear whether this brain region is essential for determining normal moral behavior, or is co-activated with the crucial region, but contributes little, if anything. In this respect, a stronger case could be made if one uncovered patients with medial prefrontal lesions who show abnormal personal moral judgment. Thus, in order to integrate lesion data with the neuroimaging findings, in the present study we tested patients with focal ventromedial prefrontal damage and healthy control subjects in personal and impersonal moral dilemmas. Given that patients with ventromedial prefrontal damage may show deficits in decision-making independent of the moral content of the choice options (e.g. Mavaddat et al., 2000; Fellows and Farah, 2003; Fellows, 2006), we also included a set of non-moral dilemmas for comparison purposes. In order to make our results easily comparable with those by Greene and colleagues (Greene et al., 2001), we used the same dilemmas used by these researchers, although translated to Italian.
If medial prefrontal regions are implicated in opposing personal moral violations, then patients with lesions in this region should be more inclined than healthy controls to approve moral violations in personal moral dilemmas. In contrast, no performance difference was expected between patients and controls in impersonal and non-moral dilemmas, in which behavior is deemed to be less dependent on processing in medial prefrontal areas (Greene et al., 2001).
Recent fMRI evidence has detected increased medial prefrontal activation during contemplation of personal moral dilemmas compared to impersonal ones, which suggests that this cortical region plays a role in personal moral judgment. However, functional imaging results cannot definitively establish that a brain area is necessary for a particular cognitive process. This requires evidence from lesion techniques, such as studies of human patients with focal brain damage. Here, we tested 7 patients with lesions in the ventromedial prefrontal cortex and 12 healthy individuals in personal moral dilemmas, impersonal moral dilemmas and non-moral dilemmas. Compared to normal controls, patients were more willing to judge personal moral violations as acceptable behaviors in personal moral dilemmas, and they did so more quickly. In contrast, their performance in impersonal and non-moral dilemmas was comparable to that of controls. These results indicate that the ventromedial prefrontal cortex is necessary to oppose personal moral violations, possibly by mediating anticipatory, self-focused, emotional reactions that may exert strong influence on moral choice and behavior.
Recent interest in social cognitive neuroscience has led to a growing body of research aimed at elucidating the neural and cognitive mechanisms that underlie human moral behavior (see for recent reviews Moll et al., 2005; Beer and Ochsner, 2006; Lieberman, 2006; McKinnon et al., 2006). Moral behavior refers to what individuals should do based on principles and judgments (i.e. moral values) shared with other members of their social environment. The initial foray into the neuroscience of moral behavior and reasoning came from the systematic examinations of changes in the social life of people with localized brain damage produced by accidents, strokes or neurological disease. Patients with lesions in the orbitofrontal and ventromedial prefrontal cortex have long been described as presenting high levels of aggressiveness, lack of concern for social and moral rules and irresponsibility (e.g. Eslinger and Damasio, 1985; Stuss et al., 1992; Damasio, 1994; Blair and Cipolotti, 2000), which suggests these brain areas are important neural correlates of moral behavior. Lesions of the same areas during childhood impair the development of moral knowledge and ethical judgment (Anderson et al., 1999), further suggesting that these brain regions are important neural correlates of moral behavior. Accordingly, functional imaging studies in healthy individuals involving moral judgment (Moll et al., 2002a; Heekeren et al., 2003) and moral reasoning (Greene et al., 2001; 2004; Borg et al., 2006) have detected consistent activations of the orbitofrontal and ventromedial prefrontal cortex, although activated regions encompass a more extended network of neural regions (see Moll et al., 2005 and references therein).
One crucial question concerns the specific mechanism by which these frontal regions promote behaviors that conform to, rather than violate, moral values and expectations shared by a social group. According to classical moral theories, moral behavior is a perfectly rational type of affair, governed by deliberative and high cognitive processing. A more recent view, however, emphasizes the role of intuitive and affective processes in social and ethical decision-making (Damasio, 1994; Greene et al., 2001).
Consistent with this latter view, Greene and colleagues have proposed that medial prefrontal areas might mediate strong negative emotional responses to moral violations, which prevent individuals from implementing such morally impermissible actions (Greene and Haidt, 2002). These emotions might be the by-product of (or, alternatively, evolved to promote) humans' intensely social nature, which relies on behaviors warranting the cohesion of social groups (Greene, 2003). In a series of fMRI experiments (Greene et al., 2001; 2004), the authors explored this possibility by studying healthy individuals who were considering moral dilemmas. Ethicists have called moral dilemmas situations in which a person faces a conflict between two (or more) opposing moral values or requirements. Specifically, Greene et al. (2001) compared individuals' performance on two different types of moral dilemmas, i.e. those involving 'personal' and those involving 'impersonal' moral judgments. A typical personal moral dilemma involves having to decide whether or not to push a stranger off of a footbridge in front of an oncoming trolley in order to save five people on the main track (i.e. the footbridge dilemma). In a quite similar situation, an impersonal moral dilemma involves having to decide whether or not to hit a switch that will turn the trolley to an alternate set of tracks, where it will kill one person instead of five (i.e. the trolley dilemma). In both types of dilemmas individuals are required to judge whether it is appropriate to incur in a moral violation (i.e. killing one person) in order to maximize overall consequences (i.e. saving five persons). However, whereas personal moral violations consist in (i) causing serious bodily harm (ii) to a human being (iii) through one's own agency (i.e. in such a way that the harm does not result from the deflection of an existing threat onto a different party), impersonal moral violations do not satisfy at least one of these criteria (e.g. #3 in the case of the trolley dilemma), and, therefore, may induce a less intense emotional experience in individuals (Greene et al., 2001).
Greene and colleagues found that medial prefrontal regions commonly associated with social/emotional processing (Damasio, 1994; Berthoz et al., 2002; Moll et al., 2002b; 2005), including the medial prefrontal gyrus and the posterior cingulate gyrus, were strongly activated while responding to personal, but not impersonal, moral dilemmas (Greene et al., 2001). Importantly, this medial prefrontal activation appeared to interfere with 'utilitarian' moral judgment: Individuals were slower to approve, compared to refuse, personal moral violations, consistent with the idea that the approval of a personal moral violation is in conflict with emotional intuitions, whereas its refusal is a rather automatic reaction (Greene and Haidt, 2002). This pattern of results was not detected for impersonal moral judgments or dilemmas with no moral connotation (non-moral dilemmas), suggesting these were mainly accomplished through logical reasoning, supported by dorsolateral prefrontal cortex (Greene et al., 2004), with relatively scarce contribution from processes dedicated to social cognition.
Although these neuroimaging studies have suggested a role of the medial prefrontal cortex in personal moral judgment, it is currently unclear whether this brain region is essential for determining normal moral behavior, or is co-activated with the crucial region, but contributes little, if anything. In this respect, a stronger case could be made if one uncovered patients with medial prefrontal lesions who show abnormal personal moral judgment. Thus, in order to integrate lesion data with the neuroimaging findings, in the present study we tested patients with focal ventromedial prefrontal damage and healthy control subjects in personal and impersonal moral dilemmas. Given that patients with ventromedial prefrontal damage may show deficits in decision-making independent of the moral content of the choice options (e.g. Mavaddat et al., 2000; Fellows and Farah, 2003; Fellows, 2006), we also included a set of non-moral dilemmas for comparison purposes. In order to make our results easily comparable with those by Greene and colleagues (Greene et al., 2001), we used the same dilemmas used by these researchers, although translated to Italian.
If medial prefrontal regions are implicated in opposing personal moral violations, then patients with lesions in this region should be more inclined than healthy controls to approve moral violations in personal moral dilemmas. In contrast, no performance difference was expected between patients and controls in impersonal and non-moral dilemmas, in which behavior is deemed to be less dependent on processing in medial prefrontal areas (Greene et al., 2001).
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