Alterations in the inferior longitudinal fasciculus in autism and associations with visual processing: a diffusion-weighted MRI study

Abstract

BackgroundOne of the most reported neural features of autism spectrum disorder (ASD) is the alteration of multiple long-range white matter fiber tracts, as assessed by diffusion-weighted imaging and indexed by reduced fractional anisotropy (FA). Recent methodological advances, however, have shown that this same pattern of reduced FA may be an artifact resulting from excessive head motion and poorer data quality and that aberrant structural connectivity in children with ASD is confined to the right inferior longitudinal fasciculus (ILF). This study aimed at replicating the observation of reduced FA along the right ILF in ASD, while controlling for group differences in head motion and data quality. In addition, we explored associations between reduced FA in the right ILF and quantitative ASD characteristics, and the involvement of the right ILF in visual processing, which is known to be altered in ASD.MethodGlobal probabilistic tractography was performed on diffusion-weighted imaging data of 17 adolescent boys with ASD and 17 typically developing boys, matched for age, performance IQ, handedness, and data quality. Four tasks were administered to measure various aspects of visual information processing, together with questionnaires assessing ASD characteristics. Group differences were examined and the neural data were integrated with previously published findings using Bayesian statistics to quantify evidence for replication and to pool data and thus increase statistical power. (Partial) correlations were calculated to investigate associations between measures.ResultsThe ASD group showed consistently reduced FA only in the right ILF and slower performance on the visual search task. Bayesian statistics pooling data across studies confirmed that group differences in FA were confined to the right ILF only, with the evidence for altered FA in the left ILF being indecisive. Lower FA in the right ILF tended to covary with slower visual search and a more fragmented part-oriented processing style. Individual differences in FA of the right ILF were not reliably associated with the severity of ASD traits after controlling for clinical status.ConclusionOur findings support the growing evidence for reduced FA along a specific fiber tract in ASD, the right ILF.Electronic supplementary materialThe online version of this article (10.1186/s13229-018-0188-6) contains supplementary material, which is available to authorized users.

Functional Anatomy of the Inferior Longitudinal Fasciculus: From Historical Reports to Current Hypotheses

“…From a clinical perspective, this general finding fits very well with the fact that the right ILF is known to be a critical white matter tract for face and emotion processing (see above) and that impaired face and emotion recognition are neuropsychological markers of patients with ASD ( Dawson et al, 2004 ; Weigelt et al, 2012 ). The selective disruption of the right ILF in ASD was recently confirmed ( Boets et al, 2018 ). Interestingly, disruption to the ILF (as evidenced by lower FA) was correlated with slower performance in a visual search task.…”

Poly(I:C) Challenge Alters Brain Expression of Oligodendroglia-Related Genes of Adult Progeny in a Mouse Model of Maternal Immune Activation

“…Growing evidence suggests that functional disconnectivity within and across large-scale neural networks is a central hallmark of clinically overlapping neurodevelopmental disorders such as autism spectrum disorder (ASD) and schizophrenia (Sharma et al, 2017 ; van den Heuvel et al, 2017 ). Indeed, numerous studies by diffusion tensor imaging (DTI; Cheung et al, 2008 ; Nickel et al, 2017 ; Boets et al, 2018 ; d’Albis et al, 2018 ) and histopathology (Drakesmith et al, 2016 ; Aoki et al, 2017 ) have demonstrated regional deficits in the white matter volume, microstructural alterations in white matter tracts, and aberrant oligodendroglial features in patients with schizophrenia or ASD. Post-mortem microarray and quantitative real-time PCR (qRT-PCR) analysis have revealed a reduction in the expression of oligodendroglia-related genes in multiple brain regions of schizophrenic patients (Tkachev et al, 2003 ; Aberg et al, 2006 ; Sokolov, 2007 ) and children with ASD (Broek et al, 2014 ; Tian et al, 2017 ).…”

<p>Diffusion Tensor Imaging And Tractography In Autistic, Dysphasic, And Healthy Control Children</p>

“…While the right ILF seems to be crucial for efficient face and emotion recognition, abnormalities in the left ILF have been connected with poor decoding in reading and impaired lexical retrieval 11. ASD individuals with poor language skills display lower FA in the posterior part of the left ILF compared to ASD individuals with moderate to strong language skills 56.…”

“…Research into the IFOF has revealed its role in semantic processing and perception of facial expression 10. The ILF is involved in processing and modulating visual cues including facial recognition, and its disruption is associated with emotional difficulties in ASD 11,12. Recent research suggests that the UF may be involved in proper name retrieval, emotion recognition, and self-awareness 1…”