Default mode and fronto-parietal network associations with IQ development across childhood in autism

Abstract Background Intellectual disability affects approximately one third of individuals with autism spectrum disorder (autism). Yet, a major unresolved neurobiological question is what differentiates autistic individuals with and without intellectual disability. Intelligence quotients (IQs) are h...

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Main Authors: Joshua K. Lee, An Chuen Billy Cho, Derek S. Andrews, Sally Ozonoff, Sally J. Rogers, David G. Amaral, Marjorie Solomon, Christine Wu Nordahl
Format: Article
Language:English
Published: BMC 2022-09-01
Series:Journal of Neurodevelopmental Disorders
Subjects:
Online Access:https://doi.org/10.1186/s11689-022-09460-y
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author Joshua K. Lee
An Chuen Billy Cho
Derek S. Andrews
Sally Ozonoff
Sally J. Rogers
David G. Amaral
Marjorie Solomon
Christine Wu Nordahl
author_facet Joshua K. Lee
An Chuen Billy Cho
Derek S. Andrews
Sally Ozonoff
Sally J. Rogers
David G. Amaral
Marjorie Solomon
Christine Wu Nordahl
author_sort Joshua K. Lee
collection DOAJ
description Abstract Background Intellectual disability affects approximately one third of individuals with autism spectrum disorder (autism). Yet, a major unresolved neurobiological question is what differentiates autistic individuals with and without intellectual disability. Intelligence quotients (IQs) are highly variable during childhood. We previously identified three subgroups of autistic children with different trajectories of intellectual development from early (2–3½ years) to middle childhood (9–12 years): (a) persistently high: individuals whose IQs remained in the normal range; (b) persistently low: individuals whose IQs remained in the range of intellectual disability (IQ < 70); and (c) changers: individuals whose IQs began in the range of intellectual disability but increased to the normal IQ range. The frontoparietal (FPN) and default mode (DMN) networks have established links to intellectual functioning. Here, we tested whether brain regions within the FPN and DMN differed volumetrically between these IQ trajectory groups in early childhood. Methods We conducted multivariate distance matrix regression to examine the brain regions within the FPN (11 regions x 2 hemispheres) and the DMN (12 regions x 2 hemispheres) in 48 persistently high (18 female), 108 persistently low (32 female), and 109 changers (39 female) using structural MRI acquired at baseline. FPN and DMN regions were defined using networks identified in Smith et al. (Proc Natl Acad Sci U S A 106:13040–5, 2009). IQ trajectory groups were defined by IQ measurements from up to three time points spanning early to middle childhood (mean age time 1: 3.2 years; time 2: 5.4 years; time 3: 11.3 years). Results The changers group exhibited volumetric differences in the DMN compared to both the persistently low and persistently high groups at time 1. However, the persistently high group did not differ from the persistently low group, suggesting that DMN structure may be an early predictor for change in IQ trajectory. In contrast, the persistently high group exhibited differences in the FPN compared to both the persistently low and changers groups, suggesting differences related more to concurrent IQ and the absence of intellectual disability. Conclusions Within autism, volumetric differences of brain regions within the DMN in early childhood may differentiate individuals with persistently low IQ from those with low IQ that improves through childhood. Structural differences in brain networks between these three IQ-based subgroups highlight distinct neural underpinnings of these autism sub-phenotypes.
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spelling doaj.art-e123f563090e41538a13a5771811a4732022-12-22T03:16:40ZengBMCJournal of Neurodevelopmental Disorders1866-19471866-19552022-09-0114111010.1186/s11689-022-09460-yDefault mode and fronto-parietal network associations with IQ development across childhood in autismJoshua K. Lee0An Chuen Billy Cho1Derek S. Andrews2Sally Ozonoff3Sally J. Rogers4David G. Amaral5Marjorie Solomon6Christine Wu Nordahl7MIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineMIND Institute, University of California Davis School of MedicineAbstract Background Intellectual disability affects approximately one third of individuals with autism spectrum disorder (autism). Yet, a major unresolved neurobiological question is what differentiates autistic individuals with and without intellectual disability. Intelligence quotients (IQs) are highly variable during childhood. We previously identified three subgroups of autistic children with different trajectories of intellectual development from early (2–3½ years) to middle childhood (9–12 years): (a) persistently high: individuals whose IQs remained in the normal range; (b) persistently low: individuals whose IQs remained in the range of intellectual disability (IQ < 70); and (c) changers: individuals whose IQs began in the range of intellectual disability but increased to the normal IQ range. The frontoparietal (FPN) and default mode (DMN) networks have established links to intellectual functioning. Here, we tested whether brain regions within the FPN and DMN differed volumetrically between these IQ trajectory groups in early childhood. Methods We conducted multivariate distance matrix regression to examine the brain regions within the FPN (11 regions x 2 hemispheres) and the DMN (12 regions x 2 hemispheres) in 48 persistently high (18 female), 108 persistently low (32 female), and 109 changers (39 female) using structural MRI acquired at baseline. FPN and DMN regions were defined using networks identified in Smith et al. (Proc Natl Acad Sci U S A 106:13040–5, 2009). IQ trajectory groups were defined by IQ measurements from up to three time points spanning early to middle childhood (mean age time 1: 3.2 years; time 2: 5.4 years; time 3: 11.3 years). Results The changers group exhibited volumetric differences in the DMN compared to both the persistently low and persistently high groups at time 1. However, the persistently high group did not differ from the persistently low group, suggesting that DMN structure may be an early predictor for change in IQ trajectory. In contrast, the persistently high group exhibited differences in the FPN compared to both the persistently low and changers groups, suggesting differences related more to concurrent IQ and the absence of intellectual disability. Conclusions Within autism, volumetric differences of brain regions within the DMN in early childhood may differentiate individuals with persistently low IQ from those with low IQ that improves through childhood. Structural differences in brain networks between these three IQ-based subgroups highlight distinct neural underpinnings of these autism sub-phenotypes.https://doi.org/10.1186/s11689-022-09460-yAutism spectrum disorderIntellectual disabilityIQMRILongitudinalDefault mode
spellingShingle Joshua K. Lee
An Chuen Billy Cho
Derek S. Andrews
Sally Ozonoff
Sally J. Rogers
David G. Amaral
Marjorie Solomon
Christine Wu Nordahl
Default mode and fronto-parietal network associations with IQ development across childhood in autism
Journal of Neurodevelopmental Disorders
Autism spectrum disorder
Intellectual disability
IQ
MRI
Longitudinal
Default mode
title Default mode and fronto-parietal network associations with IQ development across childhood in autism
title_full Default mode and fronto-parietal network associations with IQ development across childhood in autism
title_fullStr Default mode and fronto-parietal network associations with IQ development across childhood in autism
title_full_unstemmed Default mode and fronto-parietal network associations with IQ development across childhood in autism
title_short Default mode and fronto-parietal network associations with IQ development across childhood in autism
title_sort default mode and fronto parietal network associations with iq development across childhood in autism
topic Autism spectrum disorder
Intellectual disability
IQ
MRI
Longitudinal
Default mode
url https://doi.org/10.1186/s11689-022-09460-y
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