Magnetoencephalographic (MEG) brain activity during a mental flexibility task suggests some shared neurobiology in children with neurodevelopmental disorders

Alexandra Mogadam,Evdokia Anagnostou,Paul D Arnold,Elizabeth W Pang,Russell Schachar,Jason P Lerch,Anne E Keller

doi:10.1186/s11689-019-9280-2

Abstract

BackgroundChildren with neurodevelopmental disorders (NDDs) exhibit a shared phenotype that involves executive dysfunctions including impairments in mental flexibility (MF). It is of interest to understand if this phenotype stems from some shared neurobiology.MethodsTo investigate this possibility, we used magnetoencephalography (MEG) neuroimaging to compare brain activity in children (n = 88; 8–15 years) with autism spectrum disorders (ASD), attention deficit hyperactivity disorder (ADHD) and obsessive-compulsive disorder (OCD), as they completed a set-shifting/mental flexibility task.ResultsNeuroimaging results revealed a similar parietal activation profile across the NDD, groups suggesting a link to their shared phenotype. Differences in frontal activity differentiated the three clinical groups. Brain-behaviour analyses showed a link with repetitive behaviours suggesting shared dysfunction in the associative loop of the corticostriatal system.ConclusionOur study supports the notion that NDDs may exist along a complex phenotypic/biological continuum. All NDD groups showed a sustained parietal activity profile suggesting that they share a strong reliance on the posterior parietal cortices to complete the mental flexibility task; future studies could elucidate whether this is due to delayed brain development or compensatory functioning. The differences in frontal activity may play a role in differentiating the NDDs. The OCD group showed sustained prefrontal activity that may be reflective of hyperfrontality. The ASD group showed reduced frontal activation suggestive of frontal dysfunction and the ADHD group showed an extensive hypoactivity that included frontal and parietal regions. Brain-behaviour analyses showed a significant correlation with repetitive behaviours which may reflect dysfunction in the associative loop of the corticostriatal system, linked to inflexible behaviours.

Highlights

Neurodevelopmental disorders (NDDs) are a heterogeneous group of disorders, characterized by compromised central nervous system development and aberrant brain function [1,2,3]
For the measure of obsessive-compulsive behaviours captured by the trials with measures of obsession-compulsion (TOCS), we found that the peak latency in two frontal regions, the right superior frontal gyrus (SFG) [F (2,79) = 4.084, p = 0.021; adjusted R2 = 0.071; B = − 0.102, p = 0.008] and left inferior frontal gyrus (IFG) pars triangularis [F (2, 79) = 3.419, p = 0.038; adjusted R2 = 0.056; B = − 0.086, p = 0.015], was negatively related with TOCS score
In conclusion, while children with autism spectrum disorders (ASD), attention deficit hyperactivity disorder (ADHD) and obsessive-compulsive disorder (OCD) behaviourally share the same impairment in mental flexibility (MF), using MEG, we found a pattern of similarities and differences in the neurobiological bases supporting this executive function

Summary

Introduction

Neurodevelopmental disorders (NDDs) are a heterogeneous group of disorders, characterized by compromised central nervous system development and aberrant brain function [1,2,3]. The most common NDDs include autism spectrum disorders (ASD), attention deficit hyperactivity disorder (ADHD) and paediatric obsessive-compulsive disorder (OCD) While each of these NDDs has its own distinct clinical phenotype (i.e. social communication impairments and repetitive behaviours in ASD, dysfunctions in attention regulation and hyperactivity in ADHD, and impaired control of obsessive thoughts and behaviours in OCD [1]); they are often co-morbid [4] and share genetic [5,6,7], neurobiological [8] and cognitive-behavioural characteristics, such as impairments in social perception [9], rigidity and difficulties with attention. Mental flexibility comprises the ability to alter behavioural and thought patterns in response to environmental changes [10, 11] and is essential for adapting to changing surroundings, navigating social interactions and learning in academic and work environments This crucial cognitive function can be assessed using a set-shifting task, in which participants are asked to match stimuli, with matching criteria shifting every few trials. It is of interest to understand if this phenotype stems from some shared neurobiology

Methods

Results

Discussion

Conclusion