Abnormal white matter microstructure in children with sensory processing disorders

Julia P Owen, Elysa J Marco, Shivani Desai, Emily Fourie, Julia Harris, Susanna S Hill, Anne B Arnett, Pratik Mukherjee, Julia P Owen, Elysa J Marco, Shivani Desai, Emily Fourie, Julia Harris, Susanna S Hill, Anne B Arnett, Pratik Mukherjee

Abstract

Sensory processing disorders (SPD) affect 5-16% of school-aged children and can cause long-term deficits in intellectual and social development. Current theories of SPD implicate primary sensory cortical areas and higher-order multisensory integration (MSI) cortical regions. We investigate the role of white matter microstructural abnormalities in SPD using diffusion tensor imaging (DTI). DTI was acquired in 16 boys, 8-11 years old, with SPD and 24 age-, gender-, handedness- and IQ-matched neurotypical controls. Behavior was characterized using a parent report sensory behavior measure, the Sensory Profile. Fractional anisotropy (FA), mean diffusivity (MD) and radial diffusivity (RD) were calculated. Tract-based spatial statistics were used to detect significant group differences in white matter integrity and to determine if microstructural parameters were significantly correlated with behavioral measures. Significant decreases in FA and increases in MD and RD were found in the SPD cohort compared to controls, primarily involving posterior white matter including the posterior corpus callosum, posterior corona radiata and posterior thalamic radiations. Strong positive correlations were observed between FA of these posterior tracts and auditory, multisensory, and inattention scores (r = 0.51-0.78; p < 0.001) with strong negative correlations between RD and multisensory and inattention scores (r = - 0.61-0.71; p < 0.001). To our knowledge, this is the first study to demonstrate reduced white matter microstructural integrity in children with SPD. We find that the disrupted white matter microstructure predominantly involves posterior cerebral tracts and correlates strongly with atypical unimodal and multisensory integration behavior. These findings suggest abnormal white matter as a biological basis for SPD and may also distinguish SPD from overlapping clinical conditions such as autism and attention deficit hyperactivity disorder.

Keywords: Attention deficit hyperactivity disorder (ADHD); Autism; Brain development; Connectivity; Diffusion tensor imaging (DTI); Pediatrics.

Figures

Fig. 1
Fig. 1
Principal component analysis of Sensory Profile scores in SPD subjects and matched controls.
Fig. 2
Fig. 2
A–C demonstrates reduced FA in SPD in the posterior body of the corpus callosum and bilateral PTR. D–F demonstrates increased MD in the SPD patients in the lateral callosal fibers of the posterior body and splenium, bilateral PTR, including the optic radiations, right PCR, and right SLF. G–I shows increased RD in the posterior body and splenium, bilateral PTR, including the optic radiations, left ATR, and left forceps minor. The color scheme denotes TDC > SPD in blue and SPD > TDC in red and all images are presented in radiological convention (left hemisphere on right side of image).
Fig. 3
Fig. 3
Correlation of FA with auditory sensory score: The left column displays the clusters extracted from the statistical image for the correlation (p 

Fig. 4

Correlation of FA and RD…

Fig. 4

Correlation of FA and RD with multisensory score: The left column displays the…

Fig. 4
Correlation of FA and RD with multisensory score: The left column displays the clusters extracted from the statistical image for the correlation (p 

Fig. 5

Correlation of FA and RD…

Fig. 5

Correlation of FA and RD with inattention score: The left column displays the…

Fig. 5
Correlation of FA and RD with inattention score: The left column displays the clusters extracted from the statistical image for the correlation (p 

Fig. 6

Correlation of FA with tactile…

Fig. 6

Correlation of FA with tactile and visual sensory scores: The left column displays…

Fig. 6
Correlation of FA with tactile and visual sensory scores: The left column displays the clusters extracted from the statistical image for the correlation (p 
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References
    1. Ahn R.R., Miller L.J., Milberger S., McIntosh D.N. Prevalence of parents' perceptions of sensory processing disorders among kindergarten children. American Journal of Occupational Therapy. 2004;58:287–293. - PubMed
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Fig. 4
Fig. 4
Correlation of FA and RD with multisensory score: The left column displays the clusters extracted from the statistical image for the correlation (p 

Fig. 5

Correlation of FA and RD…

Fig. 5

Correlation of FA and RD with inattention score: The left column displays the…

Fig. 5
Correlation of FA and RD with inattention score: The left column displays the clusters extracted from the statistical image for the correlation (p 

Fig. 6

Correlation of FA with tactile…

Fig. 6

Correlation of FA with tactile and visual sensory scores: The left column displays…

Fig. 6
Correlation of FA with tactile and visual sensory scores: The left column displays the clusters extracted from the statistical image for the correlation (p 
Similar articles
Cited by
References
    1. Ahn R.R., Miller L.J., Milberger S., McIntosh D.N. Prevalence of parents' perceptions of sensory processing disorders among kindergarten children. American Journal of Occupational Therapy. 2004;58:287–293. - PubMed
    1. Baranek G.T., Roberts J.E., David F.J., Sideris J., Mirrett P.L., Hatton D.D., Bailey D.B., Jr. Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome. Physical & Occupational Therapy in Pediatrics. 2008;28:79–98. - PubMed
    1. Basser P.J., Mattiello J., LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophysical Journal. 1994;66:259–267. - PMC - PubMed
    1. Beaulieu C. The basis of anisotropic water diffusion in the nervous system — a technical review. NMR in Biomedicine. 2002;15:435–455. - PubMed
    1. Ben-Sasson A., Carter A.S., Briggs-Gowan M.J. Sensory over-responsivity in elementary school: prevalence and social–emotional correlates. Journal of Abnormal Child Psychology. 2009;37:705–716. - PMC - PubMed
Show all 36 references
Related information
LinkOut - more resources
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM

NCBI Literature Resources

MeSH PMC Bookshelf Disclaimer

The PubMed wordmark and PubMed logo are registered trademarks of the U.S. Department of Health and Human Services (HHS). Unauthorized use of these marks is strictly prohibited.

Follow NCBI
Fig. 5
Fig. 5
Correlation of FA and RD with inattention score: The left column displays the clusters extracted from the statistical image for the correlation (p 

Fig. 6

Correlation of FA with tactile…

Fig. 6

Correlation of FA with tactile and visual sensory scores: The left column displays…

Fig. 6
Correlation of FA with tactile and visual sensory scores: The left column displays the clusters extracted from the statistical image for the correlation (p 
Similar articles
Cited by
References
    1. Ahn R.R., Miller L.J., Milberger S., McIntosh D.N. Prevalence of parents' perceptions of sensory processing disorders among kindergarten children. American Journal of Occupational Therapy. 2004;58:287–293. - PubMed
    1. Baranek G.T., Roberts J.E., David F.J., Sideris J., Mirrett P.L., Hatton D.D., Bailey D.B., Jr. Developmental trajectories and correlates of sensory processing in young boys with fragile X syndrome. Physical & Occupational Therapy in Pediatrics. 2008;28:79–98. - PubMed
    1. Basser P.J., Mattiello J., LeBihan D. MR diffusion tensor spectroscopy and imaging. Biophysical Journal. 1994;66:259–267. - PMC - PubMed
    1. Beaulieu C. The basis of anisotropic water diffusion in the nervous system — a technical review. NMR in Biomedicine. 2002;15:435–455. - PubMed
    1. Ben-Sasson A., Carter A.S., Briggs-Gowan M.J. Sensory over-responsivity in elementary school: prevalence and social–emotional correlates. Journal of Abnormal Child Psychology. 2009;37:705–716. - PMC - PubMed
Show all 36 references
Related information
LinkOut - more resources
[x]
Cite
Copy Download .nbib
Format: AMA APA MLA NLM
Fig. 6
Fig. 6
Correlation of FA with tactile and visual sensory scores: The left column displays the clusters extracted from the statistical image for the correlation (p 

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