Distinct neural bases of disruptive behavior and autism symptom severity in boys with autism spectrum disorder

Abstract

Background: Disruptive behavior in autism spectrum disorder (ASD) is an important clinical problem, but its neural basis remains poorly understood. The current research aims to better understand the neural underpinnings of disruptive behavior in ASD, while addressing whether the neural basis is shared with or separable from that of core ASD symptoms. Methods: Participants consisted of 48 male children and adolescents: 31 ASD (7 had high disruptive behavior) and 17 typically developing (TD) controls, well-matched on sex, age, and IQ. For ASD participants, autism symptom severity, disruptive behavior, anxiety symptoms, and ADHD symptoms were measured. All participants were scanned while viewing biological motion (BIO) and scrambled motion (SCR). Two fMRI contrasts were analyzed: social perception (BIO > SCR) and Default Mode Network (DMN) deactivation (fixation > BIO). Age and IQ were included as covariates of no interest in all analyses. Results: First, the between-group analyses on BIO > SCR showed that ASD is characterized by hypoactivation in the social perception circuitry, and ASD with high or low disruptive behavior exhibited similar patterns of hypoactivation. Second, the between-group analyses on fixation > BIO showed that ASD with high disruptive behavior exhibited more restricted and less DMN deactivation, when compared to ASD with low disruptive behavior or TD. Third, the within-ASD analyses showed that (a) autism symptom severity (but not disruptive behavior) was uniquely associated with less activation in the social perception regions including the posterior superior temporal sulcus and inferior frontal gyrus; (b) disruptive behavior (but not autism symptom severity) was uniquely associated with less DMN deactivation in the medial prefrontal cortex (MPFC) and lateral parietal cortex; and (c) anxiety symptoms mediated the link between disruptive behavior and less DMN deactivation in both anterior cingulate cortex (ACC) and MPFC, while ADHD symptoms mediated the link primarily in ACC. Conclusions: In boys with ASD, disruptive behavior has a neural basis in reduced DMN deactivation, which is distinct and separable from that of core ASD symptoms, with the latter characterized by hypoactivation in the social perception circuitry. These differential neurobiological markers may potentially serve as neural targets or predictors for interventions when treating disruptive behavior vs. core symptoms in ASD.

The neurobiological presentation of anxiety in autism spectrum disorder: A systematic review

“…Anxiety and disruptive behavior were positively correlated in the autism group. Furthermore, the link between disruptive behavior and default mode network activity in the autism group was partially mediated by anxiety symptoms for the anterior cingulate cortex and medial prefrontal cortex [Yang et al, ].…”

“…Positive and negative relations between anxiety and amygdala volume [Corbett et al, ; Juranek et al, ], and positive relations between anxiety and amygdala activity [Herrington et al, ; Kleinhans et al, ] have been found. Furthermore, although the work is limited to only three studies, sensory over‐responsivity and disruptive behaviors may play a role in the link between anxiety and brain activity in autism [Green et al, ; Green et al, ; Yang et al, ].…”

“…Furthermore, although the work is limited to only three studies, sensory over-responsivity and disruptive [Lord et al, 2002[Lord et al, , 2012; ADI-R, Autism Diagnostic Interview-Revised [Lord et al, 1994]; MASC, Multidimensional Anxiety Scale for Children [March, 2012]; CBCL, Child Behavior Checklist [Achenbach & Rescorla, 2001]; SCARED, Screen for Child Anxiety-Related Emotional Disorders [Birmaher et al, 1997]; SADS, Social Avoidance and Distress Scale [Watson & Friend, 1969]; BAI, Beck Anxiety Inventory [Wilson, de Beurs, Palmer, & Chambless, 1999]; CSI-4/ASI-4, Child/Adolescent Symptom Inventory-4 [Gadow & Sprafkin, 1998;]. behaviors may play a role in the link between anxiety and brain activity in autism [Green et al, 2015;Green et al, 2013;Yang et al, 2017].…”

Neural mechanisms of behavioral change in young adults with high‐functioning autism receiving virtual reality social cognition training: A pilot study

“…Scanning was performed on a Siemens MAGNETOM 3 Tesla Tim Trio scanner at the Yale Magnetic Resonance Research Center (for YCSC participants) or a Philips 3 Tesla MR system (for CBH‐UTD participants) within 1 week before and after the treatment. Details regarding the imaging parameters and individual‐level processing steps had been described in previous research [Yang et al, ,b). The participant‐level contrast of interest is BIO > SCR, which served as inputs for the subsequent mass univariate fMRI analyses.…”

“…We measured the pretreatment and posttreatment BOLD (blood oxygen level dependent) responses using a well-established biological motion fMRI task [Bjornsdotter, Wang, Pelphrey, & Kaiser, 2016;Kaiser et al, 2010;Ventola et al, 2015;Yang et al, 2016Yang et al, , 2017a. We selected this paradigm because it measures the neural activities of two key components of social information processing [Kaiser et al, 2010], namely, socioemotional and socio-cognitive processing, which correspond to the treatment targets of VR-SCT and the two behavioral measures of emotion recognition and theory of mind, respectively.…”