Suzanne Brugman

Out of control: Evidence for anterior insula involvement in motor impulsivity and reactive aggression

Inhibiting impulsive reactions while still defending ones vital resources is paramount to functional self-control and successful development in a social environment. However, this ability of successfully inhibiting, and thus controlling ones impulsivity, often fails, leading to consequences ranging from motor impulsivity to aggressive reactions following provocation. Although inhibitory failure represents the underlying mechanism, the neurocognition of social aggression and motor response inhibition have traditionally been investigated in separation. Here, we aimed to directly investigate and compare the neural mechanisms underlying the failure of inhibition across those different modalities of self-control. We used functional imaging to reveal the overlap in neural correlates between failed motor response inhibition (measured by a go/no-go task) and reactive aggression (measured by the Taylor aggression paradigm) in healthy males. The core overlap of neural correlates was located in the anterior insula, suggesting common anterior insula involvement in motor impulsivity as well as reactive aggression. This evidence regarding an overarching role of the anterior insula across different modalities of self-control enables an integrative perspective on insula function and a better integration of cognitive, social and emotional factors into a comprehensive model of impulsivity. Furthermore, it can eventually lead to a better understanding of clinical syndromes involving inhibitory deficits.

The role of right prefrontal and medial cortex in response inhibition: Interfering with action restraint and action cancellation using transcranial magnetic brain stimulation

The ability of inhibiting impulsive urges is paramount for human behavior. Such successful response inhibition has consistently been associated with activity in pFC. The current study aims to unravel the differential involvement of different areas within right pFC for successful action restraint versus action cancellation. These two conceptually different aspects of action inhibition were measured with a go/no-go task (action restraint) and a stop signal task (action cancellation). Localization of relevant prefrontal activation was based on fMRI data. Significant task-related activation during successful action restraint was localized for each participant individually in right anterior insula (rAI), right superior frontal gyrus, and pre-SMA. Activation during successful action cancellation was localized in rAI, right middle frontal gyrus, and pre-SMA. Subsequently, fMRI-guided continuous thetaburst stimulation was applied to these regions. Results showed that the disruption of neural activity in rAI reduced both the ability to restrain (go/no-go) and cancel (stop signal) responses. In contrast, continuous thetaburst stimulation-induced disruption of the right superior frontal gyrus specifically impaired the ability to restrain from responding (go/no-go), while leaving the ability for action cancellation largely intact. Stimulation applied to right middle frontal gyrus and pre-SMA did not affect inhibitory processing in neither of the two tasks. These findings provide a more comprehensive perspective on the role of pFC in inhibition and cognitive control. The results emphasize the role of inferior frontal regions for global inhibition, whereas superior frontal regions seem to be specifically relevant for successful action restraint.

Reducing proactive aggression through non-invasive brain stimulation

Aggressive behavior poses a threat to human collaboration and social safety. It is of utmost importance to identify the functional mechanisms underlying aggression and to develop potential interventions capable of reducing dysfunctional aggressive behavior already at a brain level. We here experimentally shifted fronto-cortical asymmetry to manipulate the underlying motivational emotional states in both male and female participants while assessing the behavioral effects on proactive and reactive aggression. Thirty-two healthy volunteers received either anodal transcranial direct current stimulation to increase neural activity within right dorsolateral prefrontal cortex, or sham stimulation. Aggressive behavior was measured with the Taylor Aggression Paradigm. We revealed a general gender effect, showing that men displayed more behavioral aggression than women. After the induction of right fronto-hemispheric dominance, proactive aggression was reduced in men. This study demonstrates that non-invasive brain stimulation can reduce aggression in men. This is a relevant and promising step to better understand how cortical brain states connect to impulsive actions and to examine the causal role of the prefrontal cortex in aggression. Ultimately, such findings could help to examine whether the brain can be a direct target for potential supportive interventions in clinical settings dealing with overly aggressive patients and/or violent offenders.

A network approach to response inhibition: dissociating functional connectivity of neural components involved in action restraint and action cancellation

The ability to inhibit action tendencies is vital for adaptive human behaviour. Various paradigms are supposed to assess action inhibition and are often used interchangeably. However, these paradigms are based on different conceptualizations (action restraint vs. action cancellation) and the question arises as to what extent different conceptualizations of inhibitory processing are mirrored in a distinct neural activation pattern. We used functional magnetic resonance imaging to investigate the neural correlates of action restraint vs. action cancellation. Analyses of local activity changes as well as network connectivity measures revealed a strong overlap of activation within a common action inhibition network including inferior frontal, pre‐supplementary motor and thalamic brain areas as well as the anterior cingulate cortex. Furthermore, our findings pointed to additional neural networks that are distinct for action restraint (i.e. right superior frontal gyrus, left middle frontal gyrus, and bilateral anterior cingulate cortex) and action cancellation (i.e. right middle frontal gyrus, posterior cingulate cortex, and parietal regions). Our connectivity analyses showed that different inhibitory modalities largely relied on a task‐independent global inhibition network within the brain. Furthermore, they suggested that the conceptually distinct inhibitory aspects of action restraint vs. action cancellation also activated additional specific brain regions in a task‐dependent manner. This has implications for the choice of tasks in an empirical setting, but is also relevant for various clinical contexts in which inhibition deficits are considered a diagnostic feature.

No effects of bilateral tDCS over inferior frontal gyrus on response inhibition and aggression

Response inhibition is defined as the capacity to adequately withdraw pre-planned responses. It has been shown that individuals with deficits in inhibiting pre-planned responses tend to display more aggressive behaviour. The prefrontal cortex is involved in both, response inhibition and aggression. While response inhibition is mostly associated with predominantly right prefrontal activity, the neural components underlying aggression seem to be left-lateralized. These differences in hemispheric dominance are conceptualized in cortical asymmetry theories on motivational direction, which assign avoidance motivation (relevant to inhibit responses) to the right and approach motivation (relevant for aggressive actions) to the left prefrontal cortex. The current study aimed to directly address the inverse relationship between response inhibition and aggression by assessing them within one experiment. Sixty-nine healthy participants underwent bilateral transcranial Direct Current Stimulation (tDCS) to the inferior frontal cortex. In one group we induced right-hemispheric fronto-cortical dominance by means of a combined right prefrontal anodal and left prefrontal cathodal tDCS montage. In a second group we induced left-hemispheric fronto-cortical dominance by means of a combined left prefrontal anodal and right prefrontal cathodal tDCS montage. A control group received sham stimulation. Response inhibition was assessed with a go/no-go task (GNGT) and aggression with the Taylor Aggression Paradigm (TAP). We revealed that participants with poorer performance in the GNGT displayed more aggression during the TAP. No effects of bilateral prefrontal tDCS on either response inhibition or aggression were observed. This is at odds with previous brain stimulation studies applying unilateral protocols. Our results failed to provide evidence in support of the prefrontal cortical asymmetry model in the domain of response inhibition and aggression. The absence of tDCS effects might also indicate that the methodological approach of shifting cortical asymmetry by means of bilateral tDCS protocols has failed.

The Role of the Insular Cortex in Retaliation.

The insular cortex has consistently been associated with various aspects of emotion regulation and social interaction, including anger processing and overt aggression. Aggression research distinguishes proactive or instrumental aggression from retaliation, i.e. aggression in response to provocation. Here, we investigated the specific role of the insular cortex during retaliation, employing a controlled behavioral aggression paradigm implementing different levels of provocation. Fifteen healthy male volunteers underwent whole brain functional magnetic resonance imaging (fMRI) to identify brain regions involved in interaction with either a provoking or a non-provoking opponent. FMRI group analyses were complemented by examining the parametric modulations of brain activity related to the individual level of displayed aggression. These analyses identified a hemispheric lateralization as well as an anatomical segregation of insular cortex with specifically the left posterior part being involved in retaliation. The left-lateralization of insular activity during retaliation is in accordance with evidence from electro-physiological studies, suggesting left-lateralized fronto-cortical dominance during anger processing and aggressive acts. The posterior localization of insular activity, on the other hand, suggests a spatial segregation within insular cortex with particularly the posterior part being involved in the processing of emotions that trigger intense bodily sensations and immediate action tendencies.

Cognitive predictors of violent incidents in forensic psychiatric inpatients

This study tested the predictive value of attentional bias, emotion recognition, automatic associations, and response inhibition, in the assessment of in-clinic violent incidents. Sixty-nine male forensic patients participated and completed an Emotional Stroop to measure attentional bias for threat and aggression, a Single Target - Implicit Association Task to assess automatic associations, a Graded Emotional Recognition Task to measure emotion recognition, and an Affective Go/NoGo to measure response inhibition. Violent incidents were derived from patient files and scored on severity level. The predictive value of level of psychopathy was tested with the Psychopathy Checklist - Revised (PCL-R). Generalized linear mixed model analyses showed that increased attention towards threat and aggression, difficulty recognizing sad faces and factor 2 of the PCL-R predicted the sum of violent incidents. Specifically, verbal aggression was predicted by increased attention towards threat and aggression, difficulty to recognize sad and happy faces, and PCL-R factor 2; physical aggression by decreased response inhibition, higher PCL-R factor 2 and lower PCL-R factor 1 scores; and aggression against property by difficulty recognizing angry faces. Findings indicate that cognitive tasks could be valuable in predicting aggression, thereby extending current knowledge on dynamic factors predicting aggressive behavior in forensic patients.

Examining the Reactive Proactive Questionnaire in adults in forensic and non-forensic settings: a variable- and person-based approach

The Reactive Proactive Questionnaire (RPQ) was originally developed to assess reactive and proactive aggressive behavior in children. Nevertheless, some studies have used the RPQ in adults. This study examines the reliability of the RPQ within an adult sample by investigating whether reactive and proactive aggression can be distinguished at a variable- and person-based level. Male adults from forensic samples (N = 237) and from the general population (N = 278) completed the RPQ questionnaire. Variable-based approaches, including factor analyses, were conducted to verify the two-factor model of the RPQ and to examine alternative factor solutions of the 23 items. Subsequently, a person-based approach, i.e., Latent Class Analysis (LCA), was executed to identify homogeneous classes of subjects with similar profiles of aggression in the observed data. The RPQ proved to have sufficient internal consistency. Multiple-factor models were examined, but the original two-factor model was statistically and theoretically considered as most solid and in line with previous research. The multi-level LCA identified three different classes of aggression severity (class 1 showed low aggressive behavior; class 2 subjects displayed modest aggression levels; and class 3 exhibited the highest level of aggressive behavior). In addition, class 1 and 2 showed more reactive than proactive aggression, whereas class 3 displayed comparable levels of reactive/proactive aggression. The RPQ appears to have clinical relevance for adult populations in the way that it can distinguish severity levels of aggression. Before the RPQ is implemented in adult populations, norm scores need to be developed. Aggr. Behav. 43:155-162, 2017.

Examining the reactive proactive questionnaire in adults in forensic and non-forensic settings

The Reactive Proactive Questionnaire (RPQ) was originally developed to assess reactive and proactive aggressive behavior in children. Nevertheless, some studies have used the RPQ in adults. This study examines the reliability of the RPQ within an adult sample by investigating whether reactive and proactive aggression can be distinguished at a variable- and person-based level. Male adults from forensic samples (N = 237) and from the general population (N = 278) completed the RPQ questionnaire. Variable-based approaches, including factor analyses, were conducted to verify the two-factor model of the RPQ and to examine alternative factor solutions of the 23 items. Subsequently, a person-based approach, i.e., Latent Class Analysis (LCA), was executed to identify homogeneous classes of subjects with similar profiles of aggression in the observed data. The RPQ proved to have sufficient internal consistency. Multiple-factor models were examined, but the original two-factor model was statistically and theoretically considered as most solid and in line with previous research. The multi-level LCA identified three different classes of aggression severity (class 1 showed low aggressive behavior; class 2 subjects displayed modest aggression levels; and class 3 exhibited the highest level of aggressive behavior). In addition, class 1 and 2 showed more reactive than proactive aggression, whereas class 3 displayed comparable levels of reactive/proactive aggression. The RPQ appears to have clinical relevance for adult populations in the way that it can distinguish severity levels of aggression. Before the RPQ is implemented in adult populations, norm scores need to be developed. Aggr. Behav. 43:155-162, 2017.

Approach and avoidance towards aggressive stimuli and its relation to reactive and proactive aggression

This study assessed the association between indirectly measured behavioural approach- and avoidance-related tendencies on the one hand, and reactive versus proactive aggression on the other hand. Reactive aggression (i.e. the impulsive, anger-driven aggression expressed in response to threatening stimuli) was differentiated from proactive aggression (i.e. the more controlled aggression motivated towards obtaining specific goals). A mixed sample of 118 patients and healthy controls filled out a self-report measure to assess their degree of reactive and proactive aggression, and then performed an Approach Avoidance Task in which they were asked to pull or push a joystick in response to a format-feature of a series of pictures, irrespective of their contents. The pictorial stimuli used in this task included attack-related scenes and angry faces, along with neutral, positive and negative control stimuli. The results were controlled for the level of personality disorder pathology, gender, and age. The findings indicated that reactive but not proactive aggression was related to the relative behavioural tendency to approach attack-related scenes, along with positive stimuli. These findings reflect the hyper-reactivity of the approach-related reward system in reactive aggression, and further our knowledge into the distinct correlates and precursors of reactive and proactive aggression.