Basal Ganglia Functional Connectivity and Repetitive Behaviours in Children with Neurodevelopmental Disorders: Data from Pond Network

Background: Repetitive behaviour is a core feature of autism spectrum disorder (ASD), but exists along a continuum in other neurodevelopmental disorders (NDDs), such as obsessive-compulsive disorder (OCD) and attention-deficit/hyperactivity disorder (ADHD). It has been shown that structural and functional atypicalities of the basal ganglia (BG) are linked to the severity of repetitive behaviours, but little is known about the extent and how the BG network is linked to repetitive behaviours across disorders.

Objectives: In the present study, we compared BG network connectivity in resting-state fMRI across three groups of NDDs together, including typically developing population and correlated them with subjects’ repetitive behaviour scores.

Methods: Resting-state fMRI data and anatomical T1-weighted images on a Siemens 3T MRI were collected from 315 children and adolescents with NDDs and typically developing controls (TD) (ASD=151, ADHD=65, OCD=44, TD=55) (mean age/SD = 11.81/3.80). All resting-state volumes were corrected for slice-timing and head motion, smoothed, and bandpass filtered (0.01 and 0.2 Hz). Nuisance signals from white matter and CSF were regressed out. Volumes with a maximum displacement exceeding 2mm (less than one voxel) were omitted and data from participants who lost more than 1/3 of the volumes were excluded. The subcortical network connectivity was investigated using seed-based analysis with left and right putamen and caudate seeds using FSL’s FEAT program. Statistical images were thresholded using clusters determined by Z >2.3 and a corrected cluster significance threshold of p = 0.05. Subjects’ repetitive behaviours were assessed using Repetitive Behaviors Scale (RBS-R).

Results: The behavioural results indicated children with ASD and OCD showed significantly higher scores in repetitive behaviours than children with ADHD and TD (Mean/SD: ASD = 31.63/20.33; ADHD = 12.34/10.73; OCD = 26.27/20.08; TD = 2.62/5.54; F=42.18, p=0.00). All three groups of NDDs shared increased BG network connectivity overall in widespread regions of brain compared to the TD group. Subsequent pairwise comparisons between NDDs indicated that the increased patterns in BG network were slightly different across NDDs. Of those findings, the increased connectivity in BG network was found with the right anterior insula in ASD, but with cerebellum and primary somatosensory regions in OCD. Across all participants, connectivity strength of primary somatosensory region in the BG network was positively correlated with self-injurious and compulsive behaviour scores, while connectivity strength of the right anterior insula in the BG network was positively correlated all sub-scores and total score in RBS, except the self-injurious behaviour score.

Conclusions: The present study demonstrated that the NDD group shares increased BG network functional connectivity, suggesting underlying neural correlates of overlapped symptoms in repetitive behaviours across disorders. The patterns in increased BG network in each condition may reflect a variance in repetitive behaviours exiting along a continuum. Increased connectivity with primary somatosensory regions in the OCD group may be linked to more sameness and compulsive pattern of behaviours in their everyday routines and rituals. Increased connectivity with anterior insula in the ASD group implicates atypical interoceptive processing integrating external sensory stimuli with internal states, resulting in increased repetitive behaviours in this condition.