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. 2014 Jul 30;9(7):e103038.
doi: 10.1371/journal.pone.0103038. eCollection 2014.

Autism and Sensory Processing Disorders: Shared White Matter Disruption in Sensory Pathways but Divergent Connectivity in Social-Emotional Pathways

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Free PMC article

Autism and Sensory Processing Disorders: Shared White Matter Disruption in Sensory Pathways but Divergent Connectivity in Social-Emotional Pathways

Yi-Shin Chang et al. PLoS One. .
Free PMC article

Abstract

Over 90% of children with Autism Spectrum Disorders (ASD) demonstrate atypical sensory behaviors. In fact, hyper- or hyporeactivity to sensory input or unusual interest in sensory aspects of the environment is now included in the DSM-5 diagnostic criteria. However, there are children with sensory processing differences who do not meet an ASD diagnosis but do show atypical sensory behaviors to the same or greater degree as ASD children. We previously demonstrated that children with Sensory Processing Disorders (SPD) have impaired white matter microstructure, and that this white matter microstructural pathology correlates with atypical sensory behavior. In this study, we use diffusion tensor imaging (DTI) fiber tractography to evaluate the structural connectivity of specific white matter tracts in boys with ASD (n = 15) and boys with SPD (n = 16), relative to typically developing children (n = 23). We define white matter tracts using probabilistic streamline tractography and assess the strength of tract connectivity using mean fractional anisotropy. Both the SPD and ASD cohorts demonstrate decreased connectivity relative to controls in parieto-occipital tracts involved in sensory perception and multisensory integration. However, the ASD group alone shows impaired connectivity, relative to controls, in temporal tracts thought to subserve social-emotional processing. In addition to these group difference analyses, we take a dimensional approach to assessing the relationship between white matter connectivity and participant function. These correlational analyses reveal significant associations of white matter connectivity with auditory processing, working memory, social skills, and inattention across our three study groups. These findings help elucidate the roles of specific neural circuits in neurodevelopmental disorders, and begin to explore the dimensional relationship between critical cognitive functions and structural connectivity across affected and unaffected children.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interest exist.

Figures

Figure 1
Figure 1. Examples of each delineated tract for a representative subject.
Green masks represent frontal tracts, blue masks represent parietal-occipital tracts, and orange masks represent temporal tracts. The tracts are superimposed upon the T1 image, registered to diffusion space and with decreased opacity, of the representative subject.
Figure 2
Figure 2. Group differences between TDC, SPD, and ASD subjects in average FA within different temporal tracts.
Crossbars correspond to group averages. Green asterisks depict significant group differences between ASD and TDC subjects, and red asterisks depict significant group differences between SPD and TDC subjects, FDR corrected at p<0.05.
Figure 3
Figure 3. Group differences between TDC, SPD, and ASD subjects in average FA within different parietal-occipital tracts.
Crossbars correspond to group averages. Green asterisks depict significant group differences between ASD and TDC subjects, and red asterisks depict significant group differences between SPD and TDC subjects, FDR corrected at p<0.05.
Figure 4
Figure 4. Group differences between TDC, SPD, and ASD subjects in average FA within different frontal tracts.
Crossbars correspond to group averages. Green asterisks depict significant group differences between ASD and TDC subjects, and red asterisks depict significant group differences between SPD and TDC subjects, FDR corrected at p<0.05.
Figure 5
Figure 5. Combined-group associations between tract connectivity and WMI.
The two bilateral tracts demonstrating significant associations between FA and WMI after FDR correction are displayed. Optic radiation: r = 0.41, p = 0.003. PCR (occipital): r = 0.49, p<0.001. Results of unilateral and individual group correlations are displayed in Table 7.
Figure 6
Figure 6. Combined-group associations between tract connectivity and SCQ-social.
The two bilateral tracts demonstrating significant associations between FA and the social component of the SCQ after FDR correction are displayed. Fusiform-amygdala: r = −0.44, p<0.001. Fusiform-hippocampus: r = −0.39, p = 0.004. Results of unilateral and individual group correlations are displayed in Table 8.
Figure 7
Figure 7. Combined-group associations between tract connectivity and the inattention measure of the Sensory Profile.
The two bilateral tracts demonstrating significant associations between FA and the inattention measure of the Sensory Profile after FDR correction are displayed. Dorsal visual stream: r = 0.38, p = 0.006. PCR (occipital): r = 0.46, p<0.001. Results of unilateral and individual group correlations are displayed in Table 9.
Figure 8
Figure 8. Combined-group associations between tract connectivity and the auditory measure of the Sensory Profile.
The bilateral tract demonstrating significant associations between FA and the auditory measure of the Sensory Profile after FDR correction are displayed. PCR (occipital): r = 0.42, p = 0.002. Results of unilateral and individual group correlations are displayed in Table 10.
Figure 9
Figure 9. Average fraction of tract overlap.
Color intensity corresponds to the subject average of the fraction of the voxels of the tracts on the vertical axis that are contained within the tracts on the horizontal axis. Tracts that are more than one-third contained in any other tract are indicated by an asterisk on the vertical axis.

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