The Personality Dispositions and Resting-state Neural Correlates Associated With Aggressive Children

Qingqing Li; Mingyue Xiao; Shiqing Song; Yufei Huang; Ximei Chen; Yong Liu; Hong Chen

Disclosures

Soc Cogn Affect Neurosci. 2020;15(9):1004-1016. 

In This Article

Discussion

The present study aimed to investigate the relevance of personality and neuroanatomical factors for aggression in middle children. Aggression was negatively correlated with agreeableness and positively correlated with neuroticism. The whole-brain correlation analyses showed that higher aggression was linked to lower fALFF in the left temporal lobe including the STG, temporal pole and limbic area including the right PHG, the insula and the SMG in the left parietal lobe. Moreover, we found that physical and total aggressions were negatively associated with the rsFC between the right PHG and the right putamen. Analysis of the moderation effect of brain connectivity revealed that this right PHG-right putamen connectivity could moderate the influence of neuroticism on total aggression. In addition, no sex difference was found in the preferred subtypes of aggression. Moreover, imaging results showed that in girls, a lower fALFF in the SMG and a decreased SMG-STG connectivity were associated with higher indirect aggression, whereas in boys, a lower fALFF in the pre-central gyrus and post-central gyrus and a decreased rsFC between the pre-central gyrus and angular gyrus were associated with higher physical aggression.

Existing evidence suggests that neuroticism and agreeableness are the important predictors of aggressive behavior (Sharpe and Desai, 2001; Anderson, 2012; Brees et al., 2014). Consistent with previous findings, the present results showed that trait aggression is negatively correlated with agreeableness and positively correlated with neuroticism in middle children. Specifically, children with high levels of neuroticism had high scores in all aggression subtypes (verbal, physical, anger, etc.), and children with high levels of agreeableness reported lower anger, hostility and total aggression. Research has shown that children with high agreeableness have greater perspective-taking ability and empathic concern (Melchers et al., 2016) and tend to behave communally to reduce interpersonal conflict and maintain intragroup cooperation (Graziano et al., 1996; Mooradian et al., 2011), thus showing a low level of aggression propensity. Studies also indicate that children with high neuroticism tend to fall apart under stress, show greater concern about acceptance, become flustered and disorganized and experience more negative emotion such as anxiety, fearfulness and insecurity (Goldberg, 2001; Shiner and Caspi, 2003). When encountering problems, neurotic children easily become frustrated and upset and have difficulty calming themselves. These maladjusted psychological and social functions in children with neuroticism possibly activate and aggravate aggressive manifestations.

Previous studies have revealed an anatomically widespread neurological mechanism of aggression. Historically, the temporal lobe was the second major brain area to be associated with antisocial and aggressive behavior (Raine and Yang, 2006). The present results on the resting brain activity underlying aggression in children mostly implicate the left temporal regions. Neuroimaging studies show that the temporal cortex plays an important role in linking sensory experiences to emotions, and its dysfunction might trigger impulsive responses and aggression (Bufkin and Luttrell, 2005). More specifically, Koenigsberg et al. (2011) asked subjects to apply reappraisal strategies to regulate emotions associated with both social and non-social situations. They found that pictures depicting social content activated the STG areas, which are likely involved in social cognition. Moreover, increased activity in the STG was also reported in tasks involving social judgment such as attributing mental states (Grecucci et al., 2013; Buadesrotger et al., 2016) and thinking about the intentions of others (Schultz et al., 2003; Gallagher and Frith, 2004). Previous studies also indicate that maladaptive social information processing in children aged 10 to 12 years is associated with aggressive responses and hostile attributional bias in negative social situations (Choe et al., 2015). Additionally, clinical studies have documented that aggressiveness in patients with psychiatric disorders is related to functional and structural abnormalities in the temporal cortex (Raine et al., 2010; Amen et al., 2011) and in the STG (Goldstein et al., 2009; Sun et al., 2009). Thus, deactivation of the left STG may be related to impaired social judgment in aggressive children.

The present study also implicated clusters covering the SMG, temporal pole, and insula in child propensity for aggression. Previous studies revealed the SMG to be an important hub in the perception of socio-affective stimuli (Göttlich et al., 2017), in overcoming emotional egocentricity bias in social situations (Silani et al., 2013; Klasen et al., 2018), and in functionally supporting empathy (Shamay-Tsoory, 2011; Coll et al., 2017). Heberlein et al. (2004) found that the SMG is involved in observing gestures and in evaluating the emotions conveyed by socially significant interactions. This indicated that the SMG might play a role complementary to that of the mirror neuron system by providing access to the meaning of observed actions (Grosbras and Paus, 2005). Moreover, dysfunctions of the temporal–parietal junction, which encompass the SMG, have been shown to contribute to aggressive behavior (Harenski et al., 2014; Klasen et al., 2018). The engagement of the insula and the temporal pole is consistently reported in studies of the experience of emotion (Marie-Hélène and Tomás, 2006; Coccaro et al., 2011) and empathy (Carrington and Bailey, 2009; Philipp and Christina, 2009; Bernhardt and Singer, 2012).

Taken together with the STG results, regions of resting activity including the SMG, temporal pole and insula are important neurological mechanism of empathy (Frith and Tania, 2008; Overwalle and Baetens, 2009; Shamay-Tsoory, 2011). Empathy is the capacity to identify and understand another's thoughts, intentions and emotional states and has been proposed as a potential inhibitor of aggression (Feshbach, 1975; Hoffman, 2001). Empathy can promote pro-social behavior such as helping (Warden and Mackinnon, 2003; Eggum et al., 2011) and prevent antisocial behavior such as aggression and delinquency (Miller and Eisenberg, 1988; Jolliffe and Farrington, 2004). Research on aggression in child and adolescent samples has emphasized the role of empathy (Lovett and Sheffield, 2007; Pascualsagastizabal et al., 2019). Previous studies have shown that empathy is negatively associated with aggression in childhood aged 8 to 12 years (middle childhood) and that this association remains stable through adolescence (Lovett and Sheffield, 2007; Tampke et al., 2020). Problems of dysfunctional empathy among children are closely related to disruptive behavior and conduct disorders (Minet et al., 2010; Schwenck et al., 2012; Bons et al., 2013; Georgiou et al., 2019). The regions of brain deactivation observed in the present study might be related to poorer empathy and social judgment, which may cause children to respond with aggression (Bernhardt and Singer, 2012; Chester et al., 2014).

The association of the PHG with child physical aggression that we observed is consistent with it being an important hub within the medial temporal lobe, and an important part of the limbic system (Burwell, 2000; Eichenbaum and Lipton, 2008). Neuroimaging studies have revealed that the PHG is critical for behavioral inhibition (Peters and Christian, 2010, 2011), impulse control (Yang et al., 2010) and emotional regulation (Phillips et al., 2008). Additionally, the present study found that the rsFC of the right PHG with the right putamen was associated with total aggression, and that this rsFC further moderated the relationship between neuroticism and total aggression. Basal ganglia structures such as the putamen and caudate nucleus are implicated in the regulation of both simple and complex motor acts (Aouizerate et al., 2005; Chiang-Shan Ray et al., 2008). Abnormalities in these structures are suggested to be part of the pathophysiology of antisocial behavior (Glenn and Yaling, 2012). These results suggest that the PHG and its functional connectivity with the putamen could contribute to poor impulse control leading ultimately to aggression in children.

Previous studies indicate the presence of sex differences in the development trajectory and expression preferences of aggression. To be specific, in early and middle childhood, boys are more likely to use physical and overt aggression, whereas girls tend to use indirect and relational aggression (Cote et al., 2007; Fite et al., 2014). It has been shown that girls display higher levels of empathy and lower levels of aggression compared with boys (Mayberry and Espelage, 2007; Malti et al., 2009; Rieffe et al., 2016). However, our correlation analysis did not find any significant sex differences in the preferred subtypes of aggression. This result is consistent with other studies that found no sex differences in aggressive behaviors (Archer, 2004; Card et al., 2008). The brain imaging results by sex showed that in girls, deactivation of the SMG is associated with indirect and total aggression and that decreased functional connectivity between the SMG and the STG is associated with indirect aggression. These results suggest that in girls, aggression is likely associated with deficient empathy and social cognition (Gallagher and Frith, 2004; Koenigsberg et al., 2010; Grecucci et al., 2013; Göttlich et al., 2017). In boys, physical aggression was associated with activation of the pre-central and post-central gyri, and decreased rsFC between the pre-central gyrus and the angular gyrus, suggesting that aggression in boys is associated with poor inhibition of motor action and behavior execution (Kubler et al., 2006; Cheng et al., 2008; Blickenstorfer et al., 2009). These findings suggest the presence of sex differences in the neurodevelopmental mechanism of aggression in middle childhood.

For growing children, the ability to control impulses and empathize is critical for reducing aggressive intentions and behavior. However, we did not find any significant activity in the frontal area. The frontal cortex develops more slowly than do other brain regions, a process that continues well into late adolescence (Nitin et al., 2004; Sowell et al., 2004; Best and Miller, 2010; Meisel et al., 2019). In children, the relatively mature temporal, parietal and limbic regions, which are implicated in empathy and social cognition, play a more important role in restraining aggression than does the cognitive control ability by the frontal cortex (Decety and Michalska, 2011). The Dual Systems model (Casey et al., 2008; Steinberg, 2008; Luna and Wright, 2016) posit a rapidly developing socioemotional system and a gradually developing cognitive control system during individual development. The present study provided neurological evidence that in children, high aggressiveness and aggressive behavior are associated with regional deactivations in the socioemotional system. Moreover, the behavioral inhibition in children is more associated with the limbic PHG rather than with frontal cortex. Our results suggest that for middle children, the socioemotional system possibly plays an important role in the development of a propensity for aggression. The present results indicate that aggressiveness in children might be more related to impaired empathy and social cognition, which suggest that the key to prevention and intervention for aggressive children is to cultivate their ability and skills in empathy and social understanding.

This study has several potential limitations. First, this is the first rsfMRI study to investigate the neural basis of aggression in children, and the results therefore require verification in further studies. Second, common with the most recent resting-state studies (Choe et al., 2017; Fonzo et al., 2017; Samara et al., 2017), the design did not include a control for the participants' degree of compliance with the experimenter's instructions on conduct in the scanner, which is especially important for child participants. It should be noted that the calculation of fALFF is closely related to the time course of brain activity, and the elimination of bad time points can greatly change the final index. Therefore, a relatively lenient head motion criterion was adopted in this study rather than scrubbing the data. Third, we used child self-report measures of aggression propensity and personality traits, which might be influenced by the development of the child's self-concept. Future research should ideally include both child-report and parent-report measures to optimally assess aggressive behaviors in daily life. Fourth, the present study preliminarily found a moderating effect of functional connectivity on the relationship between neuroticism and aggression in children, and further studies are required to explore the mediating mechanisms among the brain, neuroticism and aggression.

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