Brain Regions Influencing Implicit Violent Attitudes: A Lesion-Mapping Study

Abstract

Increased aggression is common after traumatic brain injuries and may persist after cognitive recovery. Maladaptive aggression and violence are associated with dysfunction in the prefrontal and temporal cortex, but such dysfunctional behaviors are typically measured by explicit scales and history. However, it is well known that answers on explicit scales on sensitive topics--such as aggressive thoughts and behaviors--may not reveal true tendencies. Here, we investigated the neural basis of implicit attitudes toward aggression in humans using a modified version of the Implicit Association Task (IAT) with a unique sample of 112 Vietnam War veterans who suffered penetrating brain injury and 33 healthy controls who also served in combat in Vietnam but had no history of brain injury. We hypothesized that dorsolateral prefrontal cortex (dlPFC) lesions, due to the crucial role of the dlPFC in response inhibition, could influence performance on the IAT. In addition, we investigated the causal contribution of specific brain areas to implicit attitudes toward violence. We found a more positive implicit attitude toward aggression among individuals with lesions to the dlPFC and inferior posterior temporal cortex (ipTC). Furthermore, executive functions were critically involved in regulating implicit attitudes toward violence and aggression. Our findings complement existing evidence on the neural basis of explicit aggression centered on the ventromedial prefrontal cortex. These findings highlight that dlPFC and ipTC play a causal role in modulating implicit attitudes about violence and are crucially involved in the pathogenesis of aggressive behavior.

Significance statement: Maladaptive aggression and violence can lead to interpersonal conflict and criminal behavior. Surprisingly little is known about implicit attitudes toward violence and aggression. Here, we used a range of techniques, including voxel-based lesion-symptom mapping, to examine the causal role of brain structures underpinning implicit attitudes toward aggression in a unique sample of combat veterans with traumatic brain injury. We found that damage to the dorsolateral prefrontal cortex (dlPFC) led to a more positive implicit attitude toward violence that under most normal situations would be considered inappropriate. These results suggest that treatments aimed at increasing cognitive control using cognitive behavioral therapies dependent on the intact dlPFC could treat aggressive and violent behavior.

Keywords: aggression; implicit attitudes; traumatic brain injury.

Figure 1.

Violence IAT design (a) and lesion analysis results (b–d). a, Violence IAT design. Participants completed five blocks, including one congruent and one incongruent condition. b, Lesion overlay of all 112 patients with focal penetrating traumatic brain injuries. The color indicates the number of patients with damage to a given voxel. The greatest lesion overlap is in red and the least lesion overlap is in blue. c, VLSM of violence IAT performance (D-score). Lesions within the left inferior posterior temporal cortex were associated with lower D-scores (i.e., more positive implicit attitude toward violence) on the violence IAT. The statistical map is corrected at 5% FDR, with minimum cluster size of 10 voxels. The color indicates the z-value: yellow represents the highest z-value and orange represents the lowest z-value. d, Conjunction and disjunction lesion overlay of the Violence IAT low and high score groups. Blue indicates regions associated with high D-score only (i.e., a less positive implicit attitude toward violence), yellow indicates regions associated with low D-score only (i.e., a more positive implicit attitude toward violence), and green indicates regions associated with both high and low D-score (i.e., overlapping regions of more and less positive implicit attitude toward violence). Patients with lower D-score (i.e., a more positive implicit attitude toward violence) sustained lesions that affected the left inferior posterior temporal cortex and bilateral dlPFC, whereas patients with higher D-scores (i.e., a less positive implicit attitude toward violence) had more lesions in the middle and superior orbitofrontal cortex. Only voxels with a minimum of four patients are displayed. All brain figures are in radiologic convention: the right hemisphere is on the reader's left.

Figure 2.

Group lesion overlays (a) and group analysis results (b, c). a, Lesion overlays of the dlPFC (BA46, BA9), vmPFC (BA10, BA11, BA25, and BA32), ipTC (BA20 and BA21), and other lesions group (no dlPFC, no vmPFC, no ipTC). Color bar indicates the number of patients with overlapping lesions in each voxel. The figure is in radiologic convention: the right hemisphere is on the reader's left. b, Average violence IAT D-scores for the five groups: dlPFC (n = 14), vmPFC (n = 19), ipTC (n = 13), and other lesions (n = 30) and HCs (n = 33). The dlPFC group had a lower violence D-score (i.e., a more positive implicit attitude toward violence) compared with the HC (p = 0.03), vmPFC (p = 0.05), and other lesions (p < 0.01) groups. The ipTC group had a lower violence D-score compared with the other lesions group (p < 0.01). Error bars indicate ± SEM. c, Results of the mediation analysis testing the relationship between dlPFC lesion, executive function (EF, verbal fluency), and implicit attitude toward violence (D-score). The diagram shows the coefficients ± SE of the path model significant at **p < 0.01 and *p < 0.05. ∧Indirect path coefficient (lower and upper limit of the confidence interval).