The neural basis of implicit moral attitude—An IAT study using event-related fMRI
Introduction
Until relatively recently, most models of moral decision-making held a rationalist view (Kohlberg and Kramer, 1969, Piaget, 1932). Such models viewed moral reasoning as a conscious process; that is, it is attentional, effortful and controllable, and the reasoner is aware of what is going on (Bargh, 1994). However, recently, models stressing the role of emotion have become prevalent (Blair, 1995a, Blair, 1995b, Greene and Haidt, 2002 review; Haidt, 2001, Kagan and Lamb, 1987, Moll et al., 2003 review). Part of the reason for this theoretical transition has been data collected from clinical populations. Thus, patients with damage to the ventromedial frontal cortex show no impairment for many aspects of reasoning yet are impaired in their emotional responses (e.g., Damasio et al., 1990), their moral emotions (Eslinger et al., 1992, Eslinger and Damasio, 1985) and their moral behavior (Anderson et al., 1999, Blair and Cipolotti, 2000, Damasio, 1999, Eslinger and Damasio, 1985, Grafman et al., 1996). Similarly, individuals with psychopathy show no impairment in many aspects of non-emotional reasoning (see Blair, 2004). However, they are impaired in specific forms of emotional responding (Blair et al., 2001, Lykken, 1957), their moral emotions (Blair, 1995a, Blair, 1995b, Hare, 1991), their moral reasoning (Blair, 1995a, Blair, 1995b, Gray et al., 2003) and their moral behavior (Hare, 1991). By understanding the neuro-cognitive systems involved in moral reasoning, we may increase our understanding of these clinical conditions. To further this goal, we investigated the neural systems underlying moral reasoning performed in the context of a moral Implicit Associations Task.
Several recent studies have investigated the neural systems involved in moral reasoning (e.g., Greene et al., 2001, Greene et al., 2004, Heekeren et al., 2003, Heekeren et al., 2005, Moll et al., 2001, Moll et al., 2002a, Moll et al., 2002b). These studies have revealed the importance of medial orbitofrontal cortex (Greene et al., 2001, Greene et al., 2004, Heekeren et al., 2003, Heekeren et al., 2005, Moll et al., 2001, Moll et al., 2002a, Moll et al., 2002b), the cingulate gyrus (Greene et al., 2001, Moll et al., 2001, Moll et al., 2002a, Moll et al., 2002b), superior temporal sulcus (Heekeren et al., 2003, Heekeren et al., 2005, Moll et al., 2002a, Moll et al., 2002b) and the amygdala (Greene et al., 2004, Heekeren et al., 2005, Moll et al., 2002a, Moll et al., 2002b). However, the functional contributions of these regions remain relatively unclear.
The previous moral reasoning work has used varying methodologies such as making moral decisions based on text descriptions of ethical dilemmas (Greene et al., 2001), passive viewing pictures of moral violations (Moll et al., 2002a), judging sentence descriptions of behaviors as moral or immoral (Moll et al., 2002b, Heekeren et al., 2005) and making moral decisions (morally appropriate or not) versus semantic decisions (semantically correct or not) on sentences (Heekeren et al., 2003). One feature that these methodologies have in common is that they rely on explicit processing; the participant is asked to make an explicit judgment of a behavior (e.g., Greene et al., 2001, Greene et al., 2004, Heekeren et al., 2003, Heekeren et al., 2005, Moll et al., 2001). However, such measures are susceptible to voluntary control and allow a participant the ability to conceal their genuine attitudes. Moreover, recent work on moral reasoning has stressed its “automatic” nature (Greene and Haidt, 2002, Haidt, 2001).
One methodology that can be considered to assess an individual's automatic and implicit attitudes towards social stimuli is the Implicit Association Test (IAT; Greewald et al., 1998). This test measures the extent to which two target concepts (e.g., flower and insect) are associated with two attributes (e.g., good and bad). In contrast to verbal measures of self-report, the IAT relies on differentials in reaction times to index an individual's automatic attitudes. When the target concept (e.g., flower) is paired with an associated attribute (e.g., good), the participant's reaction times are faster than when it is paired with an attribute to which it is not associated (e.g., bad). The IAT can therefore be used to identify an individual's implicit attitudes, for example, to out-groups, regardless of the individual's wish to hide these attitudes (e.g., Greewald et al., 1998, Greenwald and Farnham, 2000). Recently, the IAT has been adapted to assess an individual's automatic attitudes to moral and immoral actions, even in individuals with psychopathy who might wish to conceal their attitude to these actions (Gray et al., 2003). Such studies reveal a reduced automatic “bad” attitude towards immoral actions in individuals with psychopathy relative to comparison populations.
Very little work has investigated the neural correlates of performance on the IAT. Phelps et al. (2000) found that the strength of an “automatic” amygdala response to racial out-groups predicted the level of IAT effect for a race-based task. However, this study did not examine neural correlates of performing the IAT task itself. Chee et al. (2000) examined the neural correlates of an IAT task involving the assessment of the association of two object categories (flower and insect) with the valenced attribute categories of “pleasant” and “unpleasant”. Chee et al. (2000) reported that performance on “incongruent” trials (trials where the same response is made for stimuli associated with differently valenced attributes; e.g., “flower” and “unpleasant”) was associated with significantly greater activity in ventrolateral (BA 47), dorsolateral (BA 9, 44) prefrontal cortex and anterior cingulate (BA 32). However, there has been no fMRI investigation of a morality IAT task.
In the current study, we aimed to determine regions involved in the performance of the morality IAT task. We predicted on the basis of prior fMRI data investigating moral reasoning (Greene et al., 2004, Heekeren et al., 2005, Moll et al., 2002a, Moll et al., 2002b) that the individual's automatic moral response (as indexed by an increased response to high intensity stimuli [interpersonal violence] relative to low intensity stimuli [vandalism]) would recruit the amygdala, superior temporal sulcus and medial orbital frontal cortex. In addition, we predicted on the basis of Chee's earlier study (Chee et al., 2000) that the IAT effect (as indexed by an increased response to incongruent trials rather than congruent trials) would be related to increased activity in ventrolateral prefrontal cortex and anterior cingulate.
Section snippets
Participants
Twenty healthy volunteers, 9 males and 11 females, between the ages of 20 to 36 participated in this study. All gave written informed consent to participate in the study, which was approved by the National Institute of Mental Health Institutional Review Board.
The morality implicit association task and experimental procedure
The stimuli consisted of 48 color photographic stimuli primarily selected from the International Affective Picture System (IAPS; Lang and Greenwald, 1985); several of the low intensity illegal items were taken from additional sources. As
Behavioral data
Fig. 1 depicts the participant's RTs by stimulus condition and congruence. The participants made few errors (1.62%), and RTs for these trials were not included in subsequent analyses. A 2 (Congruence: congruent vs. incongruent) × 2 (Stimulus intensity: High vs. Low) × 2 (Legality: Illegal vs. Legal) ANOVA was conducted on the data. This revealed significant main effects for congruence, stimulus intensity and legality. The subjects responded significantly faster in the congruent than in the
Discussion
The goal of the current study was to determine regions involved in the performance of the morality IAT task. Behaviorally, and in line with previous work using other types of IAT paradigm (e.g., Chee et al., 2000, Gray et al., 2003, Greewald et al., 1998), participants were significantly slower on incongruent (when categories of different valence shared the same key: e.g., moral transgressions and good animals) than on congruent trials (when categories of the same valence shared the same key:
References (85)
A cognitive developmental approach to morality: investigating the psychopath
Cognition
(1995)A cognitive developmental approach to morality: investigating the psychopath
Cognition
(1995)The roles of orbital frontal cortex in the modulation of antisocial behavior
Brain and Cognition
(2004)- et al.
Moral reasoning and conduct problems in children with emotional and behavioural difficulties
Pers. Individ. Differ.
(2001) - et al.
Conflict monitoring and anterior cingulate cortex: an update
Trends Cogn. Sci.
(2004) - et al.
Anterior cingulate cortex dysfunction in attention-deficit/hyperactivity disorder revealed by fMRI and counting Stroop
Biol. Psychiatry
(1999) - et al.
Cognitive and emotional influences in anterior cingulate cortex
Trends Cogn. Sci.
(2000) - et al.
Individuals with sociopathic behavior caused by frontal damage fail to respond automatically to social stimuli
Behav. Brain Res.
(1990) - et al.
Interaction between the amygdala and the medial temporal lobe memory system predicts better memory for emotional events
Neuron
(2004) - et al.
The effect of preceding context on inhibition: an event-related fMRI study
NeuroImage
(2002)
Parametric manipulation of conflict and response competition using rapid mixed-trial event-related functional MRI
NeuroImage
Dissociable executive functions in the dynamic control of behavior: inhibition, error detection, and correction
NeuroImage
How and where does moral judgment work?
Trends in Cognitive Sciences
The neural bases of cognitive conflict and control in moral judgment
Neuron
Influence of bodily harm on neural correlates of semantic and moral decision-making
NeuroImage
Neural correlates of rapid context-dependent reversal learning in a simple model of human social interaction
NeuroImage
Limbic activation and psychophysiologic responses to aversive visual stimuli. Interaction with cognitive task
Neuropsychopharmacology
Interdimensional interference in the Stroop effect: uncovering the cognitive and neural anatomy of attention
Trends Cogn. Sci.
Functional networks in emotional moral and nonmoral social judgments
NeuroImage
Norms with feeling: towards a psychological account of moral judgment
Cognition
Intentional false responding shares neural substrates with response conflict and cognitive control
NeuroImage
An event-related functional MRI study comparing interference effects in the Simon and Stroop tasks
Brain Res. Cogn. Brain Res.
Intact performance on an indirect measure of face bias following amygdala damage
Neuropsychologia
The role of the anterior cingulate cortex in conflict processing: evidence from reverse Stroop interference
NeuroImage
Monitoring and control of action by the frontal lobes
Neuron
Impairment of social and moral behavior related to early damage in human prefrontal cortex
Nat. Neurosci.
The four horsemen of automaticity: awareness, intention, efficiency, and control in social cognition
Bad is stronger than good
Rev. Gen. Psychol.
Emotion, decision making and the orbitofrontal cortex
Cereb. Cortex
Neurocognitive models of aggression, the antisocial personality disorders, and psychopathy
J. Neurol. Neurosurg. Psychiatry
Impaired social response reversal: a case of “acquired sociopathy”
Brain
Conflict monitoring vs. selection-for-action in anterior cingulate cortex
Nature
The counting Stroop: an interference task specialized for functional neuroimaging-validation study with functional MRI
Hum. Brain Mapp.
Anterior cingulate cortex, error detection, and the online monitoring of performance
Science
Sensitivity of prefrontal cortex to changes in target probability: a functional MRI study
Hum. Brain Mapp.
Dissociating striatal and hippocampal function developmentally with a stimulus–response compatibility task
J. Neurosci.
Dorsolateral prefrontal cortex and the implicit association of concepts and attributes
NeuroReport
Anterior cingulate and prefrontal cortex: who's in control?
Nat. Neurosci.
Defining the neural mechanisms of probabilistic reversal learning using event-related functional magnetic resonance imaging
J. Neurosci.
The Feeling of What Happens: Body and Emotion in the Making of Consciousness
Dissociable functions of the medial and lateral orbitofrontal cortex: evidence from neuroimaging studies
Cereb. Cortex
Severe disturbance of higher cognition after bilateral frontal lobe ablation: patient EVR
Neurology
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