Skip to main content
Log in

Classification of Preschoolers with Low-Functioning Autism Spectrum Disorder Using Multimodal MRI Data

  • Original Paper
  • Published:
Journal of Autism and Developmental Disorders Aims and scope Submit manuscript

Abstract

Multimodal imaging studies targeting preschoolers and low-functioning autism spectrum disorder (ASD) patients are scarce. We applied machine learning classifiers to parameters from T1-weighted MRI and DTI data of 58 children with ASD (age 3–6 years) and 48 typically developing controls (TDC). Classification performance reached an accuracy, sensitivity, and specificity of 88.8%, 93.0%, and 83.8%, respectively. The most prominent features were the cortical thickness of the right inferior occipital gyrus, mean diffusivity of the middle cerebellar peduncle, and nodal efficiency of the left posterior cingulate gyrus. Machine learning-based analysis of MRI data was useful in distinguishing low-functioning ASD preschoolers from TDCs. Combination of T1 and DTI improved classification accuracy about 10%, and large-scale multi-modal MRI studies are warranted for external validation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abraham, A., Pedregosa, F., Eickenberg, M., Gervais, P., Mueller, A., Kossaifi, J., Gramfort, A., Thirion, B., & Varoquaux, G. (2014). Machine learning for neuroimaging with scikit-learn. Frontiers in Neuroinformatics, 8, 14. https://doi.org/10.3389/fninf.2014.00014

    Article  Google Scholar 

  • Akshoomoff, N., Lord, C., Lincoln, A. J., Courchesne, R. Y., Carper, R. A., Townsend, J., & Courchesne, E. (2004). Outcome classification of preschool children with autism spectrum disorders using MRI brain measures. Journal of the American Academy of Child and Adolescent Psychiatry, 43(3), 349–357. https://doi.org/10.1097/00004583-200403000-00018

    Article  Google Scholar 

  • Alloway, T. P. (2010). Working memory and executive function profiles of individuals with borderline intellectual functioning. Journal of Intellectual Disability Research, 54(5), 448–456. https://doi.org/10.1111/j.1365-2788.2010.01281.x

    Article  Google Scholar 

  • Ameis, S. H., & Catani, M. (2015). Altered white matter connectivity as a neural substrate for social impairment in Autism Spectrum Disorder. Cortex, 62, 158–181. https://doi.org/10.1016/j.cortex.2014.10.014

    Article  Google Scholar 

  • Andrews, D. S., Lee, J. K., Solomon, M., Rogers, S. J., Amaral, D. G., & Nordahl, C. W. (2019). A diffusion-weighted imaging tract-based spatial statistics study of autism spectrum disorder in preschool-aged children. Journal of Neurodevelopmental Disorders, 11(1), 32. https://doi.org/10.1186/s11689-019-9291-z

    Article  Google Scholar 

  • Baio, J., Wiggins, L., Christensen, D. L., Maenner, M. J., Daniels, J., Warren, Z., Kurzius-Spencer, M., Zahorodny, W., Rosenberg, C.R., White, T., & Dowling, N. F. (2018). Prevalence of autism spectrum disorder among children aged 8 years—Autism and developmental disabilities monitoring network, 11 sites, United States, 2014. MMWR Surveillance Summaries, 67(6), 1–23. https://doi.org/10.15585/mmwr.ss6706a1

    Article  Google Scholar 

  • Bullmore, E., & Sporns, O. (2009). Complex brain networks: Graph theoretical analysis of structural and functional systems. Nature Reviews Neuroscience, 10(3), 186–198. https://doi.org/10.1038/nrn2575

    Article  Google Scholar 

  • Cai, J., Hu, X., Guo, K., Yang, P., Situ, M., & Huang, Y. (2018). Increased left inferior temporal gyrus was found in both low function autism and high function autism. Front Psychiatry, 9, 542. https://doi.org/10.3389/fpsyt.2018.00542

    Article  Google Scholar 

  • Calderoni, S., Retico, A., Biagi, L., Tancredi, R., Muratori, F., & Tosetti, M. (2012). Female children with autism spectrum disorder: An insight from mass-univariate and pattern classification analyses. NeuroImage, 59(2), 1013–1022. https://doi.org/10.1016/j.neuroimage.2011.08.070

    Article  Google Scholar 

  • Chu, C., Hsu, A. L., Chou, K. H., Bandettini, P., Lin, C. P., Neuroimaging, A., & s. D. (2012). Does feature selection improve classification accuracy? Impact of sample size and feature selection on classification using anatomical magnetic resonance images. NeuroImage, 60(1), 59–70. https://doi.org/10.1016/j.neuroimage.2011.11.066

    Article  Google Scholar 

  • Collins, D. L., Neelin, P., Peters, T. M., & Evans, A. C. (1994). Automatic 3D intersubject registration of MR volumetric data in standardized Talairach space. Journal of Computer Assisted Tomography, 18(2), 192–205.

    Article  Google Scholar 

  • Committee on Drugs. American Academy of Pediatrics. (2002). Guidelines for monitoring and management of pediatric patients during and after sedation for diagnostic and therapeutic procedures: Addendum. Pediatrics, 110(4), 836–838. https://doi.org/10.1542/peds.110.4.836

    Article  Google Scholar 

  • Crippa, A., Del Vecchio, G., Busti Ceccarelli, S., Nobile, M., Arrigoni, F., & Brambilla, P. (2016). Cortico-cerebellar connectivity in autism spectrum disorder: What do we know so far? Front Psychiatry, 7, 20. https://doi.org/10.3389/fpsyt.2016.00020

    Article  Google Scholar 

  • Deshpande, G., Libero, L. E., Sreenivasan, K. R., Deshpande, H. D., & Kana, R. K. (2013). Identification of neural connectivity signatures of autism using machine learning. Frontiers in Human Neuroscience, 7, 670. https://doi.org/10.3389/fnhum.2013.00670

    Article  Google Scholar 

  • Di Martino, A., Yan, C. G., Li, Q., Denio, E., Castellanos, F. X., Alaerts, K., Anderson, J.S., Assaf, M., Bookheimer, S.Y., Dapretto, M., & Milham, M. P. (2014). The autism brain imaging data exchange: Towards a large-scale evaluation of the intrinsic brain architecture in autism. Molecular Psychiatry, 19(6), 659–667. https://doi.org/10.1038/mp.2013.78

    Article  Google Scholar 

  • Dietz, C., Swinkels, S. H., Buitelaar, J. K., Van Daalen, E., & Van Engeland, H. (2007). Stability and change of IQ scores in preschool children diagnosed with autism spectrum disorder. European Child and Adolescent Psychiatry, 16(6), 405–410.

    Article  Google Scholar 

  • Domes, G., Heinrichs, M., Kumbier, E., Grossmann, A., Hauenstein, K., & Herpertz, S. C. (2013). Effects of intranasal oxytocin on the neural basis of face processing in autism spectrum disorder. Biological Psychiatry, 74(3), 164–171. https://doi.org/10.1016/j.biopsych.2013.02.007

    Article  Google Scholar 

  • Erbetta, A., Bulgheroni, S., Contarino, V. E., Chiapparini, L., Esposito, S., Annunziata, S., & Riva, D. (2015). Low-functioning autism and nonsyndromic intellectual disability: Magnetic resonance imaging (MRI) findings. Journal of Child Neurology, 30(12), 1658–1664.

    Article  Google Scholar 

  • Flanagan, H. E., Smith, I. M., Vaillancourt, T., Duku, E., Szatmari, P., Bryson, S., Fombonne, E., Mirenda, P., Roberts, W., Volden, J., Waddell, C., Zwaigenbaum, L., Bennett, T., Elsabbagh, M., & Georgiades, S. (2015). Stability and change in the cognitive and adaptive behavior scores of preschoolers with autism spectrum disorder. J Autism Devel Disord, 45, 2691–2703.

    Article  Google Scholar 

  • Fortin, J. P., Cullen, N., Sheline, Y. I., Taylor, W. D., Aselcioglu, I., Cook, P. A., Adams, P., Cooper, C., Fava, M., McGrath, P.J., & Shinohara, R. T. (2018). Harmonization of cortical thickness measurements across scanners and sites. NeuroImage, 167, 104–120. https://doi.org/10.1016/j.neuroimage.2017.11.024

    Article  Google Scholar 

  • Fortin, J. P., Parker, D., Tunc, B., Watanabe, T., Elliott, M. A., Ruparel, K., & Shinohara, R. T. (2017). Harmonization of multi-site diffusion tensor imaging data. NeuroImage, 161, 149–170. https://doi.org/10.1016/j.neuroimage.2017.08.047

    Article  Google Scholar 

  • Gabrielsen, T. P., Anderson, J. S., Stephenson, K. G., Beck, J., King, J. B., Kellems, R., Top, D.N., Russell, N.C., Anderberg, E., Lundwall, R.A., & South, M. (2018). Functional MRI connectivity of children with autism and low verbal and cognitive performance. Molecular Autism, 9, 67. https://doi.org/10.1186/s13229-018-0248-y

    Article  Google Scholar 

  • Gilmore, J. H., Knickmeyer, R. C., & Gao, W. (2018). Imaging structural and functional brain development in early childhood. Nature Reviews Neuroscience, 19(3), 123–137. https://doi.org/10.1038/nrn.2018.1

    Article  Google Scholar 

  • Gori, I., Giuliano, A., Muratori, F., Saviozzi, I., Oliva, P., Tancredi, R., Cosenza, A., Tosetti, M., Calderoni, S., & Retico, A. (2015). Gray matter alterations in young children with autism spectrum disorders: Comparing morphometry at the voxel and regional level. Journal of Neuroimaging, 25(6), 866–874. https://doi.org/10.1111/jon.12280

    Article  Google Scholar 

  • Gotham, K., Pickles, A., & Lord, C. (2012). Trajectories of autism severity in children using standardized ADOS scores. Pediatrics, 130(5), e1278-1284. https://doi.org/10.1542/peds.2011-3668

    Article  Google Scholar 

  • Ho, S. Y., Phua, K., Wong, L., & Bin Goh, W. W. (2020). Extensions of the external validation for checking learned model interpretability and generalizability. Patterns. https://doi.org/10.1016/j.patter.2020.100129

    Article  Google Scholar 

  • Huang, Z. A., Zhu, Z., Yau, C. H., & Tan, K. C. (2020). Identifying autism spectrum disorder from resting-state fMRI using deep belief network. IEEE Transactions on Neural Networks and Learning Systems. https://doi.org/10.1109/TNNLS.2020.3007943

    Article  Google Scholar 

  • Im, K., Lee, J. M., Lyttelton, O., Kim, S. H., Evans, A. C., & Kim, S. I. (2008). Brain size and cortical structure in the adult human brain. Cerebral Cortex, 18(9), 2181–2191. https://doi.org/10.1093/cercor/bhm244

    Article  Google Scholar 

  • Im, K., Lee, J. M., Yoon, U., Shin, Y. W., Hong, S. B., Kim, I. Y., Kwon, J.S., & Kim, S. I. (2006). Fractal dimension in human cortical surface: Multiple regression analysis with cortical thickness, sulcal depth, and folding area. Human Brain Mapping, 27(12), 994–1003. https://doi.org/10.1002/hbm.20238

    Article  Google Scholar 

  • Ingalhalikar, M., Parker, D., Bloy, L., Roberts, T. P., & Verma, R. (2011). Diffusion based abnormality markers of pathology: Toward learned diagnostic prediction of ASD. NeuroImage, 57(3), 918–927. https://doi.org/10.1016/j.neuroimage.2011.05.023

    Article  Google Scholar 

  • Ingalhalikar, M., Parker, W. A., Bloy, L., Roberts, T. P., & Verma, R. (2014). Creating multimodal predictors using missing data: Classifying and subtyping autism spectrum disorder. Journal of Neuroscience Methods, 235, 1–9. https://doi.org/10.1016/j.jneumeth.2014.06.030

    Article  Google Scholar 

  • Isaksson, J., Tammimies, K., Neufeld, J., Cauvet, E., Lundin, K., Buitelaar, J. K., Loth, E., Murphy, D.G., Spooren, W., & group, E.-A. L. (2018). EU-AIMS Longitudinal European Autism Project (LEAP): The autism twin cohort. Molecular Autism, 9, 26. https://doi.org/10.1186/s13229-018-0212-x

    Article  Google Scholar 

  • Jiao, Y., Chen, R., Ke, X. Y., Chu, K. K., Lu, Z. H., & Herskovits, E. H. (2010). Predictive models of autism spectrum disorder based on brain regional cortical thickness. NeuroImage, 50(2), 589–599. https://doi.org/10.1016/j.neuroimage.2009.12.047

    Article  Google Scholar 

  • Kaufman, J., Birmaher, B., Brent, D., Rao, U., Flynn, C., Moreci, P., Williamson, D., & Ryan, N. (1997). Schedule for affective disorders and schizophrenia for school-age children-present and lifetime version (K-SADS-PL): Initial reliability and validity data. Journal of the American Academy of Child and Adolescent Psychiatry, 36(7), 980–988. https://doi.org/10.1097/00004583-199707000-00021

    Article  Google Scholar 

  • Kim, Y. S., Cheon, K. A., Kim, B. N., Chang, S. A., Yoo, H. J., Kim, J. W., Cho, S. C., Seo, D. H., Bae, M. O., So, Y. K., & Leventhal, B. (2004). The reliability and validity of kiddie-schedule for affective disorders and schizophrenia-present and lifetime version- Korean version (K-SADS-PL-K). Yonsei Medical Journal, 45(1), 81–89. https://doi.org/10.3349/ymj.2004.45.1.81

    Article  Google Scholar 

  • Lange, N., Travers, B. G., Bigler, E. D., Prigge, M. B., Froehlich, A. L., Nielsen, J. A., Cariello, A.N., Zielinski, B.A., Anderson, J.S., Fletcher, P.T., & Lainhart, J. E. (2015). Longitudinal volumetric brain changes in autism spectrum disorder ages 6–35 years. Autism Research, 8(1), 82–93. https://doi.org/10.1002/aur.1427

    Article  Google Scholar 

  • Lee, D. K., Yoon, U., Kwak, K., & Lee, J. M. (2015). Automated segmentation of cerebellum using brain mask and partial volume estimation map. Computational and Mathematical Methods in Medicine, 2015, 167489. https://doi.org/10.1155/2015/167489

    Article  Google Scholar 

  • Lee, J. K., Andrews, D. S., Ozonoff, S., Solomon, M., Rogers, S., Amaral, D. G., & Nordahl, C. W. (2020). Longitudinal evaluation of cerebral growth across childhood in boys and girls with autism spectrum disorder. Biological Psychiatry. https://doi.org/10.1016/j.biopsych.2020.10.014

    Article  Google Scholar 

  • Li, D., Karnath, H. O., & Xu, X. (2017). Candidate biomarkers in children with autism spectrum disorder: a review of MRI studies. Neuroscience Bulletin, 33(2), 219–237. https://doi.org/10.1007/s12264-017-0118-1

    Article  Google Scholar 

  • Li, S. J., Wang, Y., Qian, L., Liu, G., Liu, S. F., Zou, L. P., Zhang, J. S., Hu, N., Chen, X. Q., Yu, S. Y., & Ma, L. (2018). Alterations of white matter connectivity in preschool children with autism spectrum disorder. Radiology, 288(1), 209–217. https://doi.org/10.1148/radiol.2018170059

    Article  Google Scholar 

  • Libero, L. E., DeRamus, T. P., Lahti, A. C., Deshpande, G., & Kana, R. K. (2015). Multimodal neuroimaging based classification of autism spectrum disorder using anatomical, neurochemical, and white matter correlates. Cortex, 66, 46–59. https://doi.org/10.1016/j.cortex.2015.02.008

    Article  Google Scholar 

  • Lord, C., Risi, S., Lambrecht, L., Cook, E. H., Jr., Leventhal, B. L., DiLavore, P. C., Pickles, A., & Rutter, M. (2000). The autism diagnostic observation schedule-generic: A standard measure of social and communication deficits associated with the spectrum of autism. Journal of Autism and Developmental Disorders, 30(3), 205–223.

    Article  Google Scholar 

  • MacDonald, D., Kabani, N., Avis, D., & Evans, A. C. (2000). Automated 3-D extraction of inner and outer surfaces of cerebral cortex from MRI. NeuroImage, 12(3), 340–356. https://doi.org/10.1006/nimg.1999.0534

    Article  Google Scholar 

  • Maslov, S., & Sneppen, K. (2002). Specificity and stability in topology of protein networks. Science, 296(5569), 910–913. https://doi.org/10.1126/science.1065103

    Article  Google Scholar 

  • Mateos-Perez, J. M., Dadar, M., Lacalle-Aurioles, M., Iturria-Medina, Y., Zeighami, Y., & Evans, A. C. (2018). Structural neuroimaging as a clinical predictor: A review of machine learning applications. Neuroimage Clinical, 20, 506–522. https://doi.org/10.1016/j.nicl.2018.08.019

    Article  Google Scholar 

  • Moon, S. J., Hwang, J., Kana, R., Torous, J., & Kim, J. W. (2019). Accuracy of machine learning algorithms for the diagnosis of autism spectrum disorder: Systematic review and meta-analysis of brain magnetic resonance imaging studies. JMIR Mental Health, 6(12), e14108. https://doi.org/10.2196/14108

    Article  Google Scholar 

  • Nordahl, C. W., Mello, M., Shen, A. M., Shen, M. D., Vismara, L. A., Li, D., Harrington, K., Tanase, C., Goodlin-Jones, B., Rogers, S., & Amaral, D. G. (2016). Methods for acquiring MRI data in children with autism spectrum disorder and intellectual impairment without the use of sedation. Journal of Neurodevelopmental Disorders, 8, 20. https://doi.org/10.1186/s11689-016-9154-9

    Article  Google Scholar 

  • Oishi, K., Zilles, K., Amunts, K., Faria, A., Jiang, H., Li, X., Akhter, K., Hua, K., Woods, R., Toga, A.W., & Mori, S. (2008). Human brain white matter atlas: Identification and assignment of common anatomical structures in superficial white matter. NeuroImage, 43(3), 447–457. https://doi.org/10.1016/j.neuroimage.2008.07.009

    Article  Google Scholar 

  • Pagnozzi, A. M., Conti, E., Calderoni, S., Fripp, J., & Rose, S. E. (2018). A systematic review of structural MRI biomarkers in autism spectrum disorder: A machine learning perspective. International Journal of Developmental Neuroscience, 71, 68–82. https://doi.org/10.1016/j.ijdevneu.2018.08.010

    Article  Google Scholar 

  • Park, G., Kwak, K., Seo, S. W., & Lee, J. M. (2018). Automatic segmentation of corpus callosum in midsagittal based on bayesian inference consisting of sparse representation error and multi-atlas voting. Frontiers in Neuroscience, 12, 629. https://doi.org/10.3389/fnins.2018.00629

    Article  Google Scholar 

  • Park, K. S., Yoon, Y. H., Park, H. J., Kwon, K. U. (1996). Development of KEDI-WISC, individual intelligence test for Korean children. In. Seoul, Republic of Korea: Korean Educational Development Institute.

  • Patenaude, B., Smith, S. M., Kennedy, D. N., & Jenkinson, M. (2011). A Bayesian model of shape and appearance for subcortical brain segmentation. NeuroImage, 56(3), 907–922. https://doi.org/10.1016/j.neuroimage.2011.02.046

    Article  Google Scholar 

  • Payabvash, S., Palacios, E. M., Owen, J. P., Wang, M. B., Tavassoli, T., Gerdes, M., Brandes-Aitken, A., Cuneo, D., Marco, E. J., & Mukherjee, P. (2019). White matter connectome edge density in children with autism spectrum disorders: Potential imaging biomarkers using machine-learning models. Brain Connect, 9(2), 209–220. https://doi.org/10.1089/brain.2018.0658

    Article  Google Scholar 

  • Pedregosa, F., Varoquaux, G., Gramfort, A., Michel, V., Thirion, B., Grisel, O., Blondel, M., Prettenhofer, P., Weiss, R., Dubourg, V., & Duchesnay, E. (2011). Scikit-learn: Machine learning in python. Journal of Machine Learning Research, 12, 2825–2830.

    Google Scholar 

  • Pierce, K., Haist, F., Sedaghat, F., & Courchesne, E. (2004). The brain response to personally familiar faces in autism: Findings of fusiform activity and beyond. Brain, 127(Pt 12), 2703–2716. https://doi.org/10.1093/brain/awh289

    Article  Google Scholar 

  • Pierce, K., Muller, R. A., Ambrose, J., Allen, G., & Courchesne, E. (2001). Face processing occurs outside the fusiform “face area” in autism: Evidence from functional MRI. Brain, 124(Pt 10), 2059–2073. https://doi.org/10.1093/brain/124.10.2059

    Article  Google Scholar 

  • Qin, B., Wang, L., Zhang, Y., Cai, J., Chen, J., & Li, T. (2018). Enhanced topological network efficiency in preschool autism spectrum disorder: A diffusion tensor imaging study. Front Psychiatry, 9, 278. https://doi.org/10.3389/fpsyt.2018.00278

    Article  Google Scholar 

  • Qureshi, M. N., Min, B., Jo, H. J., & Lee, B. (2016). Multiclass classification for the differential diagnosis on the ADHD subtypes using recursive feature elimination and hierarchical extreme learning machine: Structural MRI study. PLoS ONE, 11(8), e0160697. https://doi.org/10.1371/journal.pone.0160697

    Article  Google Scholar 

  • Reiter, M. A., Mash, L. E., Linke, A. C., Fong, C. H., Fishman, I., & Muller, R. A. (2019). Distinct patterns of atypical functional connectivity in lower-functioning autism. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(3), 251–259. https://doi.org/10.1016/j.bpsc.2018.08.009

    Article  Google Scholar 

  • Robbins, S., Evans, A. C., Collins, D. L., & Whitesides, S. (2004). Tuning and comparing spatial normalization methods. Medical Image Analysis, 8(3), 311–323. https://doi.org/10.1016/j.media.2004.06.009

    Article  Google Scholar 

  • Rubinov, M., & Sporns, O. (2010). Complex network measures of brain connectivity: Uses and interpretations. NeuroImage, 52(3), 1059–1069. https://doi.org/10.1016/j.neuroimage.2009.10.003

    Article  Google Scholar 

  • Shen, M. D., Li, D. D., Keown, C. L., Lee, A., Johnson, R. T., Angkustsiri, K., Rogers, S.J., Müller, R.A., Amaral, D.G., & Nordahl, C. W. (2016). Functional connectivity of the amygdala is disrupted in preschool-aged children with autism spectrum disorder. Journal of the American Academy of Child and Adolescent Psychiatry, 55(9), 817–824. https://doi.org/10.1016/j.jaac.2016.05.020

    Article  Google Scholar 

  • Shin, M. S., & Cho, S. C. (2010). The Korean Leiter International Performance Scale—Revised (K-Leiter-R). Seoul: Hakjisa.

  • Shukla, D. K., Keehn, B., Lincoln, A. J., & Muller, R. A. (2010). White matter compromise of callosal and subcortical fiber tracts in children with autism spectrum disorder: A diffusion tensor imaging study. J Am Acad Child Adolesc Psychiatry, 49(12), 1269–1278, 1278 e1261–1262. https://doi.org/10.1016/j.jaac.2010.08.018

  • Sivaswamy, L., Kumar, A., Rajan, D., Behen, M., Muzik, O., Chugani, D., & Chugani, H. (2010). A diffusion tensor imaging study of the cerebellar pathways in children with autism spectrum disorder. Journal of Child Neurology, 25(10), 1223–1231. https://doi.org/10.1177/0883073809358765

    Article  Google Scholar 

  • Sled, J. G., Zijdenbos, A. P., & Evans, A. C. (1998). A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Transactions on Medical Imaging, 17(1), 87–97. https://doi.org/10.1109/42.668698

    Article  Google Scholar 

  • Smith, S. M. (2002). Fast robust automated brain extraction. Human Brain Mapping, 17(3), 143–155. https://doi.org/10.1002/hbm.10062

    Article  Google Scholar 

  • Tamm, L., Day, H. A., & Duncan, A. (2021). Comparison of adaptive functioning measures in adolescents with autism spectrum disorder without intellectual disability. Journal of Autism and Developmental Disorders. https://doi.org/10.1007/s10803-021-05013-9

    Article  Google Scholar 

  • Turesky, T. K., Vanderauwera, J., & Gaab, N. (2021). Imaging the rapidly developing brain: Current challenges for MRI studies in the first five years of life. Developmental Cognitive Neuroscience, 47, 100893. https://doi.org/10.1016/j.dcn.2020.100893

    Article  Google Scholar 

  • Turner, L. M., Stone, W. L., Pozdol, S. L., & Coonrod, E. E. (2006). Follow-up of children with autism spectrum disorders from age 2 to age 9. Autism, 10(3), 243–265.

    Article  Google Scholar 

  • Tziraki, M., Garg, S., Harrison, E., Wright, N. B., Hawkes, R., Akhtar, K., Green, J., & Stivaros, S. (2021). A neuroimaging preparation protocol tailored for autism. Autism Research, 14(1), 65–74. https://doi.org/10.1002/aur.2427

    Article  Google Scholar 

  • Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., Mazoyer, B., & Joliot, M. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289. https://doi.org/10.1006/nimg.2001.0978

    Article  Google Scholar 

  • Vade, A., Sukhani, R., Dolenga, M., & Habisohn-Schuck, C. (1995). Chloral hydrate sedation of children undergoing CT and MR imaging: Safety as judged by American Academy of Pediatrics guidelines. AJR. American Journal of Roentgenology, 165(4), 905–909. https://doi.org/10.2214/ajr.165.4.7676990

    Article  Google Scholar 

  • van’t Hof, M., Tisseur, C., van Berckelear-Onnes, I., van Nieuwenhuyzen, A., Daniels, A. M., Deen, M., Hoek, H. W., & Ester, W. A. (2021). Age at autism spectrum disorder diagnosis: A systematic review and meta-analysis from 2012 to 2019. Autism, 25(4), 862–873. https://doi.org/10.1177/1362361320971107

    Article  Google Scholar 

  • Wook Yoo, S., Han, C. E., Shin, J. S., Won Seo, S., Na, D. L., Kaiser, M., Jeong, Y., & Seong, J. K. (2015). A network flow-based analysis of cognitive reserve in normal ageing and Alzheimer’s disease. Science and Reports, 5, 10057. https://doi.org/10.1038/srep10057

    Article  Google Scholar 

  • Xiao, X., Fang, H., Wu, J., Xiao, C., Xiao, T., Qian, L., Liang, F., Xiao, Z., Chu, K. K., & Ke, X. (2017). Diagnostic model generated by MRI-derived brain features in toddlers with autism spectrum disorder. Autism Research, 10(4), 620–630. https://doi.org/10.1002/aur.1711

    Article  Google Scholar 

  • Yang, J. J., Yoon, U., Yun, H. J., Im, K., Choi, Y. Y., Lee, K. H., Park, H., Hough, M. G., & Lee, J. M. (2013). Prediction for human intelligence using morphometric characteristics of cortical surface: Partial least square analysis. Neuroscience, 246, 351–361. https://doi.org/10.1016/j.neuroscience.2013.04.051

    Article  Google Scholar 

  • Yeh, F. C., Verstynen, T. D., Wang, Y., Fernandez-Miranda, J. C., & Tseng, W. Y. (2013). Deterministic diffusion fiber tracking improved by quantitative anisotropy. PLoS ONE, 8(11), e80713. https://doi.org/10.1371/journal.pone.0080713

    Article  Google Scholar 

  • Zhou, Y., Yu, F., & Duong, T. (2014). Multiparametric MRI characterization and prediction in autism spectrum disorder using graph theory and machine learning. PLoS ONE, 9(6), e90405. https://doi.org/10.1371/journal.pone.0090405

    Article  Google Scholar 

  • Zhuang, H., Liu, R., Wu, C., Meng, Z., Wang, D., Liu, D., Liu, M., & Li, Y. (2019). Multimodal classification of drug-naive first-episode schizophrenia combining anatomical, diffusion and resting state functional resonance imaging. Neuroscience Letters, 705, 87–93. https://doi.org/10.1016/j.neulet.2019.04.039

    Article  Google Scholar 

  • Zijdenbos, A. P., Forghani, R., & Evans, A. C. (2002). Automatic “pipeline” analysis of 3-D MRI data for clinical trials: Application to multiple sclerosis. IEEE Transactions on Medical Imaging, 21(10), 1280–1291. https://doi.org/10.1109/TMI.2002.806283

    Article  Google Scholar 

  • Zilles, K., Armstrong, E., Schleicher, A., & Kretschmann, H. J. (1988). The human pattern of gyrification in the cerebral cortex. Anatomy and Embryology (Berlin), 179(2), 173–179. https://doi.org/10.1007/BF00304699

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the National Research Foundation (NRF) funded by the Korean Government (MSIT) (2019M3E5D1A01069345 to J-IK and 2020M3E5D9080787 to B-NK), by the Korea Health Technology R&D Project through the Korea Health Industry Development Institute (KHIDI) and Korea Dementia Research Center (KDRC), funded by the Ministry of Health & Welfare and Ministry of Science and ICT, Republic of Korea (No.HU20C0198 to J-ML), and the Technology Innovation Program (Industrial Strategic Technology Development Program) funded by the Ministry of Trade, Industry, and Energy (20002769 to B-NK, Development of Next Generation Platform for Diagnosis and Therapeutic of Attention Deficit Hyperactivity Disorder and Intellectual Disability based on Big Data).

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception, design, material preparation and data collection. Analysis were performed by Sungkyu Bang and Jin-Ju Yang. The first draft of the manuscript was written by Johanna Inhyang Kim, Sungkyu Bang and Jin-Ju Yang. All authors read, commented on and approved the final manuscript. Jong-Min Lee and Bung-Nyun Kim supervised the whole process.

Corresponding authors

Correspondence to Jong-Min Lee or Bung-Nyun Kim.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 727 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kim, J.I., Bang, S., Yang, JJ. et al. Classification of Preschoolers with Low-Functioning Autism Spectrum Disorder Using Multimodal MRI Data. J Autism Dev Disord 53, 25–37 (2023). https://doi.org/10.1007/s10803-021-05368-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10803-021-05368-z

Keywords

Navigation