Evidence for a different role of the ventral and dorsal medial prefrontal cortex for social reactive aggression: An interactive fMRI study
Introduction
The experience of being unjustly assaulted evokes the impulse to defend oneself and to respond aggressively to the offender. This type of reactive aggression contrasts with instrumental aggression which is purposeful and goal-directed (Berkowitz, 1993). The cognitive control of reactive aggressive impulses, important for social interaction (Siegel, 2004), is motivated by the anticipation of negative consequences and leads to avoidance behavior (Gray, 1982) and the mobilization of empathic feelings (Ohbuchi et al., 1993).
The prefrontal cortex (PFC) plays a central role in many aspects of social cognition (Rilling et al., 2002), including perspective taking (Frith and Frith, 1999), and also in the regulation of emotions such as aggression (for a review, see Blair, 2004). In particular, studies with patients with lesions of the ventral prefrontal lobe demonstrated impairment in identifying emotional expression using face or voice stimuli (Hornak et al., 1996) and deficits in representing the mental states of others when performing verbal tasks based on theory of mind (Stone et al., 1998, Mah et al., 2005). Additionally, lesions of the ventromedial prefrontal cortex disturb the control of reactive aggressive behavior (Grafman et al., 1996, Anderson et al., 1999) which might result in a similar behavior as in other psychopathic individuals (Blair and Cipolotti, 2000). Increased reactive aggressive behavior in subjects without brain lesions is often associated with prefrontal dysfunction (Volkow et al., 1995).
Imaging studies on facial perception demonstrated an increase of activation in the lateral ventral prefrontal areas during observation of angry and fearful facial expressions (Blair et al., 1999) and social norm violations (Berthoz et al., 2002; together with the medial PFC (mPFC)). Imaging studies on social interaction and emotional control identified at least two distinct areas within the mPFC involved in aggression and its control. Activation of the dorsal mPFC has been observed during cognitive regulation of emotional behavior (Ochsner et al., 2004a) and when subjects made judgments about another person’s emotional states (Ochsner et al., 2004b). In contrast, activity in the ventral mPFC has been associated with monitoring of one’s own feelings (Lane et al., 1997, Phan et al., 2004) and physiological changes that accompany a particular emotional response (Damasio, 1996).
The present study investigated the role of the PFC with functional magnetic resonance imaging (fMRI) in a paradigm provoking reactive aggression. We used a realistic, dynamic social interaction that involved being offended, retaliating and watching the opponent suffer. Subjects played a competitive reaction time task and, depending on the outcome, either received an aversive stimulus or administered one with an intensity of their choice to their opponent. Reactive aggression was induced by increasing the intensity of the aversive stimulus the subjects received over the course of the experiment. This paradigm was modified for usage in a social interactive imaging setting based on the experimental design from Taylor (1967), a design which reliably induces reactive aggressive behavior (Giancola and Zeichner, 1994). A modification in our paradigm was the reduction of number of winning trials during the course of the experiment. After each retaliation trial, subjects were shown a short video clip of the opponent receiving the aversive stimulus (see Fig. 1). By introducing a second person as a competitor and presenting his pain-related expressive behavior matching the intensity of the retaliation stimulus, we ensured that aggression control was induced. An event-related design that entailed anicipation of an offending aversive stimulation, retaliation and watching the opponent suffering was used to isolate functional brain activity associated with different aspects of aggression and its control. Specifically, we investigated the role of the mPFC during the interaction with an opponent. Additionally, we examined the relationship between brain activity during the different trial phases, skin conductance responses (SCR) as an indicator of autonomic arousal, and self-reported psychopathic personality traits. We hypothesized that the mPFC is critically involved in the regulation of reactive aggression (Taylor et al., 2003, Ochsner et al., 2004a) and that psychopathic personality traits correlating with a lack of peripheral physiological changes correspond with reduced activation within the mPFC. Lack of social affection in psychopathy was repeatedly found to be related to reduced processing of bodily signals during emotions (Damasio, 1996, Birbaumer et al., 2005; “somatic markers”).
Section snippets
Subjects
Sixteen healthy male subjects (mean age 28.6 years, standard deviation (SD) 6.5 years), recruited by advertisement in the local newspaper, participated in the fMRI experiment. Two subjects who reported doubts about the veracity of the opponent’s role were excluded from the analysis.
The study was approved by the Ethics Committee of the Medical Faculty of the University of Tübingen. Written informed consent was obtained according to the guidelines of the Declaration of Helsinki.
Experimental design
Before scanning,
Behavioral and peripheral physiological data
A multivariate analysis of variance (MANOVA) with repeated measurements testing for differences in aggressive feelings and intensity of the applied retaliation stimulus over the four experimental sessions revealed that both the intensity of the retaliation stimulus (F(3,36) = 2.86; p < 0.05; Fig. 2A) and aggressive feelings against their opponent (F(3,36) = 13.64; p < 0.001; Fig. 2B) increased significantly over the course of the experiment. Positive correlations were observed between the received
Discussion
This is the first imaging study that has induced reactive aggression in a social interactive setting by using a modified Taylor (Taylor, 1967) aggression paradigm. In the ventral mPFC, activation was stronger in less callous subjects pointing to the association with empathy. In contrast, the activation of the dorsal mPFC, correlating with revenge intensity, seemed to be related to cognitive operations during more intense social interaction processes. Furthermore, the present study confirms
Acknowledgments
We want to thank Dr. Susanne Leiberg for correction of the manuscript and Professor Tracy Trevorrov and Ranganatha Sitaram for help with the English editing. This study was supported by the DFG, SFB 437; F1.
References (55)
- et al.
Social perception from visual cues: role of the STS region
Trends Cogn. Sci.
(2000) The roles of the orbital frontal cortex in the modulation of antisocial behavior
Brain Cogn.
(2004)- et al.
Construct validation of a self-report psychopathy scale: does Levinson’s self-report psychopathy scale measure the same constructs as Hare’s psychopathy checklist revised?
Pers. Individ. Differ.
(2001) - et al.
A new SPM toolbox for combining probabilistic cytoarchitectonic maps and functional imaging data
NeuroImage
(2005) - et al.
Functional imaging of ‘theory of mind’
Trends Cogn. Sci.
(2003) - et al.
Imaging the intentional stance in a competitive game
NeuroImage
(2002) - et al.
Thresholding of statistical maps in functional neuroimaging using the false discovery rate
NeuroImage
(2002) - et al.
Face and voice expression identification in patients with emotional and behavioural changes following ventral frontal lobe damage
Neuropsychologia
(1996) - et al.
Differential role of the orbital frontal lobe in emotional versus cognitive perspective-taking
Neuropsychologia
(2006) - et al.
Neural circuitry underlying voluntary suppression of sadness
Biol. Psychiatry
(2003)
Differential cerebral activation during observation of expressive gestures and motor acts
Neuropsychologia
Abnormalities in emotion processing within cortical and subcortical regions in criminal psychopaths: evidence from a functional magnetic resonance imaging study using pictures with emotional content
Biol. Psychiatry
Attention to emotion modulates fMRI activity in human right superior temporal sulcus
Brain Res. Cogn. Brain Res.
Valid conjunction inference with the minimum statistic
NeuroImage
For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion
NeuroImage
Neural correlates of individual ratings of emotional salience: a trial-related fMRI study
NeuroImage
A neural basis for social cooperation
Neuron
Segregation of cognitive and emotional function in the prefrontal cortex: a stereotactic meta-analysis
NeuroImage
Subjective rating of emotionally salient stimuli modulates neural activity
NeuroImage
Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain
NeuroImage
Brain circuits involved in emotional learning in antisocial behavior and social phobia in humans
Neurosci. Lett.
Brain glucose metabolism in violent psychiatric patients: a preliminary study
Psychiatry Res.
Identification of emotional intonation evaluated by fMRI
NeuroImage
External validity of trivial experiments: the case of laboratory aggression
Rev. Gen. Psychol.
Impairment of social and moral behavior related to early damage in human prefrontal cortex
Nat. Neurosci.
Aggression: 1st Causes Consequences and Control
An fMRI study of intentional and unintentional (embarrassing) violations of social norms
Brain
Cited by (172)
Laboratory assessment of aggression: The Taylor Aggression Paradigm in adults with and without a disorder of impulsive aggression
2023, Journal of Psychiatric ResearchNutritional supplementation in the management of childhood/youth aggression: A systematic review
2023, Aggression and Violent BehaviorAmygdala connectivity and aggression
2023, Handbook of Clinical NeurologyEffect of subjective sleep quality on aggression: A two-year longitudinal and fMRI pilot study
2023, Biological Psychology
- 1
These authors contributed equally to the manuscript.