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

Abstract and Introduction

Abstract

Despite aggression being detrimental to children's physical health, mental health and social development, the dispositional and neurological antecedents of aggression in the child are poorly understood. Here we examined the relationship between trait aggression as measured by Buss and Warren's Aggression Questionnaire and personality traits measured with Big Five Questionnaire for Children in 77 primary-school children and recorded resting-state brain activity (fractional amplitude of low-frequency fluctuations [fALFF]) and resting-state functional connectivity (rsFC) using functional magnetic resonance imaging. The present results showed that trait aggression was negatively correlated with agreeableness and positively correlated with neuroticism. The brain analyses showed that children with a higher propensity for aggression had a lower fALFF mainly in the left superior temporal gyrus, right parahippocampal gyrus and left supramarginal gyrus. Physical and total aggressions were negatively associated with rsFC between the right parahippocampal gyrus and the right putamen. Further analysis revealed that this rsFC could moderate the influence of neuroticism on total aggression. Moreover, the results suggest the presence of a sex difference in the neurodevelopmental mechanisms underlying aggression in middle childhood. Overall, our findings indicate that aggressive children have lower agreeableness and higher neuroticism, and the underlying neural systems are mainly implicated in social judgment and empathy.

Introduction

Aggression generally means actions intended to cause physical or psychological harm to another individual—an innate and evolutionarily conserved adaptation in social organisms for the protection of food, mating partners, progeny and territory (Anderson, 2012). Although aggression can yield competitive advantages, most forms of aggression in contemporary humans are maladaptive and produce a variety of negative social, physical and emotional consequences for perpetrators, victims and their families (Quanty, 2010; Beck et al., 2013; Dolenc et al., 2015; Coccaro et al., 2016).

Middle childhood is a period of dramatic advances in social, biological and cognitive functioning with significant developmental changes (Beauchaine, 2015; Woltering et al., 2016). It is also a critical time in the developmental trajectory of aggression (Piquero et al., 2012). Aggressive behaviors such as verbal aggression, interpersonal hostility and physical fighting are prevalent during childhood (Séguin and Zelazo, 2005). Arsenio and Lemerise (2001) indicated that aggressive children usually lack emotional and empathic responsiveness toward their victims. Studies on the association between empathy and aggression have shown that boys (i.e. 9–14 years of age) exhibit higher levels of aggression and lower empathy than do girls (Mayberry and Espelage, 2007; Malti et al., 2009; Rieffe et al., 2016). Moreover, to avoid sanctions by adults against overt aggression (i.e. direct threatening or physical hitting), children will adopt more subtle forms of aggression. For example, indirect and hostile behaviors such as rumor spreading or social exclusion are often used to harm others by threatening the peer relationship. Previous studies also suggest that boys and girls may differ in the subtypes of aggression that they utilize. Evidence shows that boys are more likely to use physical and overt aggression whereas girls tend to use relational aggression (Cote et al., 2007; Fite et al., 2014). However, some studies find no sex difference in aggression (Archer, 2004; Card et al., 2008). Obviously, these behaviors seriously affect children's physical health, mental health, academic progress and social adaptation (Heilbron and Prinstein, 2008; Wang et al., 2009). Although aggressive behaviors tend to decrease with age, a certain number of children retain cognitive and behavioral patterns of aggression that continue through the teen years and into adulthood. Investigation of the dispositional and neurological underpinnings of aggression is likely to enhance our understanding of this maladaptive process and guide the formulation of effective prevention and intervention programs (Horton et al., 2014; Thomson and Centifanti, 2017).

Differences in aggression in children are generally attributed to individual characteristics (e.g. neurobiological substrates, personality) and environmental influences (e.g. parenting style, exposure to violent media). Personality traits comprise the relatively stable pattern of an individual's typical emotions, attitudes and behaviors and have been considered the key predictive variables of aggression (Anderson and Huesmann, 2003; Jensen-Campbell et al., 2007; Anderson, 2012; Brees et al., 2014). Neuroticism, characterized as being easily upset and emotionally unstable, is positively related to anger and aggressive behaviors (Sharpe and Desai, 2001; Brees et al., 2014). Agreeableness, described as being good-natured, altruistic, trustful, sympathetic, and cooperative, is negatively related to self and peer-reported aggression and violence (Heaven, 1996; Gleason et al., 2004). Evidence from research on early and middle children has shown that high neuroticism and low agreeableness are closely associated with a propensity for aggression, including the subtypes of anger, relational and physical aggression and hostility (Goldberg, 2001; Shiner and Caspi, 2003). Gleason et al. (2004) linked the personality dimensions to aggression and found that agreeableness was negatively associated with both indirect and direct aggression in late childhood. Moreover, personality traits have been shown to moderate the associations between environmental influences and externalizing behaviors represented by aggressive behaviors (Yeh et al., 2011; Smack et al., 2015). Smack et al. (2015) indicate that in the context of negative parenting, children with high neuroticism and low agreeableness show higher rates of externalizing problem behaviors than do their low-neuroticism counterparts.

In addition to exploring personality traits, uncovering neural correlates is of great significance for understanding the occurrence and development of aggression. The neural basis of aggression has been investigated extensively both in humans and in non-human species (Nelson and Trainor, 2007). Functional and structural neuroimaging studies show that the biological mechanisms underlying aggressive behavior involve various regions and multiple neural pathways distributed in cortical and subcortical brain structures (Raine and Yang, 2006). The brain regions most important in executing and regulating aggression are the frontal and prefrontal areas, which functionally support executive and affective control (Kateri et al., 2010; Florian et al., 2011; Mckenna et al., 2017), empathy (Stuss et al., 2001) and emotional regulation (Bufkin and Luttrell, 2005; Hedy et al., 2008; Koenigsberg et al., 2010). Another region important for aggression is the temporal cortex, which was found to be reliably activated in emotional processing and regulation (Allison et al., 2000; Marie-Hélène and Tomás, 2006), in empathy (Carrington and Bailey, 2009), and in social cognition (Koenigsberg et al., 2011). Aggression is also associated with dysregulation of a cortico-limbic network (Davidson et al., 2000; Siever, 2015; Klasen et al., 2019). Specifically, the functioning of the prefrontal cortex-amygdala regulatory system seems to be central to successfully restraining impulsive aggression (Hoptman et al., 2010a). Aggression generally appears to involve many brain areas and cognitive functions, but these results are mainly derived from adolescent and adult samples. The present research aims to explore the relative importance of brain regions in regulating aggression among children.

Theoretical and empirical research suggests that the development of aggression is influenced by different factors at different growth stages. The Dual Systems Model (Steinberg, 2008) posits an imbalance between the development of the cognitive control system and that of the socioemotional system. Cognitive control depends on the maturity of the frontal and prefrontal cortices, and the development of these areas is slow, continuing into late adolescence (Casey et al., 2012; Duckworth and Steinberg, 2015; Meisel et al., 2019). Neuroimaging studies also indicate that children are more prone to interference and have greater difficulty in inhibiting inappropriate responses than do adults (Casey et al., 2000; Bunge et al., 2002). This deficient functioning of inhibitory control in children is mainly due to the immaturity of the frontal regions (Nitin et al., 2004; Casey et al., 2008; Laurence, 2010). Compared with the slowly developing cognitive control system, the socioemotional system, involving primary sensory cortices and the limbic subcortical regions, develops earlier and regulates impulsive behavior during early development (Mills et al., 2014; Shulman et al., 2016; Meisel et al., 2019). The superior temporal gyrus (STG) and supramarginal gyrus (SMG) of the socioemotional system are specifically implicated in social cognition and empathy (Gallagher and Frith, 2004; Koenigsberg et al., 2010; Grecucci et al., 2013; Göttlich et al., 2017) and have been found to be associated with aggressive impulsive behavior in children. Based on the Dual Systems Model and the development of aggression, we inferred that in the group of children, the neural correlates of the socioemotional system might play a relatively dominant role in establishing a propensity for aggression.

Despite the wealth of neuroimaging studies on aggression in adults and adolescents, to our knowledge, few studies have addressed the neural substrates of aggression in children, especially with the technique of resting-state functional magnetic resonance imaging (rsfMRI). Previous research has used mostly task-related functional magnetic resonance imaging (fMRI) designs to investigate the neurobiological substrates of individual aggression. However, based on the existing evidence, stable individual differences in personality are more clearly manifested in the overall brain structure and function. Thus, task-free designs may be advantageous for examining the brain bases of aggression (Telzer et al., 2018; Water et al., 2019). The rsfMRI is a reliable and frequently used task-free method of detecting intrinsic brain activity (Romero-Martínez et al., 2019). The two most popular measures of rsfMRI are: (i) the fractional amplitude of low-frequency fluctuations (fALFF), which reflects the regional properties of spontaneous brain activity and (ii) the resting-state functional connectivity (rsFC), which reflects the synchronization and functional connections between brain regions within specific neural circuits. Research has shown that the physiological noise irrelevant to brain activity found by the original ALFF approach is successfully suppressed with the fALFF approach, suggesting that this measure has greater sensitivity and specificity in detecting spontaneous brain activity (Zou et al., 2008; Zuo et al., 2010). Previous studies have used the fALFF and rsFC to detect a variety of neuropsychiatric disorders (Han et al., 2011; Hoptman et al., 2010b) and to uncover the neural mechanisms underlying human cognition, social behavior and personality in healthy populations (Cox et al., 2011; Kong et al., 2015; Wang et al., 2017). In light of the above findings, the present study was designed to investigate the neural mechanisms underlying aggression based on both the regional brain activations indexed by fALFF and the functional connectivities between brain regions indexed by rsFC.

In the present study, we examined, in primary-school children, the relationships between personality traits and aggression, and the intrinsic brain activity and functional connectivity associated with aggression. We hypothesized that in children, aggression is negatively associated with agreeableness and positively associated with neuroticism, and initially expected that the neural correlates of aggression would be found mostly in the temporal and limbic areas. We also investigated the relationships among personality, brain mechanisms and trait aggression in this population. Considering that previous research supports a role for sex differences in aggression, we also examined behavior and imaging outcomes by sex.

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