Skip to main content

Advertisement

Log in

Decreased Functional and Structural Connectivity is Associated with Core Symptom Improvement in Children with Autism Spectrum Disorder After Mini-basketball Training Program

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

Abstract

Exercise intervention has been proven helpful to ameliorate core symptoms of Autism Spectrum Disorder (ASD). However, the underlying mechanisms are not fully understood. In this study, we carried out a 12-week mini-basketball training program (MBTP) on ASD children and examined the changes of brain functional and structural networks before and after exercise intervention. We applied individual-based method to construct functional network and structural morphological network, and investigated their alterations following MBTP as well as their associations with the change in core symptom. Structural MRI and resting-state functional MRI data were obtained from 58 ASD children aged 3–12 years (experiment group: n = 32, control group: n = 26). ASD children who received MBTP intervention showed several distinguishable alternations compared to the control without special intervention. These included decreased functional connectivity within the sensorimotor network (SM) and between SM and the salience network, decreased morphological connectivity strength in a cortical-cortical network centered on the left inferior temporal gyrus, and a subcortical–cortical network centered on the left caudate. Particularly, the aforementioned functional and structural changes induced by MBTP were associated with core symptoms of ASD. Our findings suggested that MBTP intervention could be an effective approach to improve core symptoms in ASD children, decrease connectivity in both structure and function networks, and may drive the brain change towards normal-like neuroanatomy.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Alexander-Bloch, A., Giedd, J. N., & Bullmore, E. (2013). Imaging structural co-variance between human brain regions. Nature Reviews Neuroscience, 14(5), 322–336.

    Article  PubMed  PubMed Central  Google Scholar 

  • American Psychiatric Association. (2013). Diagnostic and statistical manual of mental disorders: DSM-5™ (5th ed., pp. xliv–947). American Psychiatric Publishing, Inc.

    Book  Google Scholar 

  • Benjamini, Y., & Hochberg, Y. (1995). Controlling the false discovery rate: A practical and powerful approach to multiple testing. Journal of the Royal Statistical Society: Series B (Methodological), 57(1), 289–300.

    Google Scholar 

  • Botev, Z. I., Grotowski, J. F., & Kroese, D. P. (2010). Kernel density estimation via diffusion. The Annals of Statistics, 38(5), 2916.

    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. Frontiers in Psychiatry, 9, 542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cai, K., Yu, Q., Herold, F., Liu, Z., Wang, J., Zhu, L., Xiong, X., Chen, A., Müller, P., Kramer, A. F., Müller, N. G., & Zou, L. (2020). Mini-basketball training program improves social communication and white matter integrity in children with autism. Brain Sciences, 10(11), 803.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cardon, G. J., Hepburn, S., & Rojas, D. C. (2017). Structural covariance of sensory networks, the cerebellum, and amygdala in autism spectrum disorder. Frontiers in Neurology, 8, 615.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, H., Uddin, L. Q., Duan, X., Zheng, J., Long, Z., Zhang, Y., Guo, X., Zhang, Y., Zhao, J., & Chen, H. (2017). Shared atypical default mode and salience network functional connectivity between autism and schizophrenia. Autism Research, 10(11), 1776–1786.

    Article  PubMed  PubMed Central  Google Scholar 

  • Cote, C. J., & Wilson, S. (2016). Guidelines for monitoring and management of pediatric patients before, during, and after sedation for diagnostic and therapeutic procedures: Update 2016. Pediatric Dentistry, 38(4), 13E-39E.

    Google Scholar 

  • Cummings, K. K., Lawrence, K. E., Hernandez, L. M., Wood, E. T., Bookheimer, S. Y., Dapretto, M., & Green, S. A. (2020). Sex differences in salience network connectivity and its relationship to sensory over-responsivity in youth with autism spectrum disorder. Autism Research, 13(9), 1489–1500.

    Article  PubMed  PubMed Central  Google Scholar 

  • Douaud, G., Smith, S., Jenkinson, M., Behrens, T., Johansen-Berg, H., Vickers, J., James, S., Voets, N., Watkins, K., Matthews, P. M., & James, A. (2007). Anatomically related grey and white matter abnormalities in adolescent-onset schizophrenia. Brain, 130(9), 2375–2386.

    Article  PubMed  Google Scholar 

  • Duan, X., Wang, R., Xiao, J., Li, Y., Huang, X., Guo, X., Cao, J., He, L., He, C., Ling, Z., Shan, X., Chen, H., Kang, X., & Chen, H. (2020). Subcortical structural covariance in young children with autism spectrum disorder. Progress in Neuro-Psychopharmacology and Biological Psychiatry, 99, 109874.

    Article  PubMed  Google Scholar 

  • Fan, Y., Li, L., Peng, Y., Li, H., Guo, J., Li, M., Yang, S., Yao, M., Zhao, J., Liu, H., Liao, W., Guo, X., Han, S., Cui, Q., Duan, X., Xu, Y., Zhang, Y., & Chen, H. (2021). Individual-specific functional connectome biomarkers predict schizophrenia positive symptoms during adolescent brain maturation. Human Brain Mapping, 42(5), 1475–1484.

    Article  Google Scholar 

  • Fetta, A., Carati, E., Moneti, L., Pignataro, V., Angotti, M., Bardasi, M. C., Cordelli, D. M., Franzoni, E., & Parmeggiani, A. (2021). Relationship between sensory alterations and repetitive behaviours in children with autism spectrum disorders: A parents’ questionnaire based study. Brain Sciences, 11(4), 484.

    Article  PubMed  PubMed Central  Google Scholar 

  • Green, S. A., Hernandez, L., Bookheimer, S. Y., & Dapretto, M. (2016). Salience network connectivity in autism is related to brain and behavioral markers of sensory overresponsivity. Journal of the American Academy of Child & Adolescent Psychiatry, 55(7), 618-626e1.

    Article  Google Scholar 

  • Harlalka, V., Bapi, R. S., Vinod, P. K., & Roy, D. (2018). Age, disease, and their interaction effects on intrinsic connectivity of children and adolescents in autism spectrum disorder using functional connectomics. Brain Connectivity, 8(7), 407–419.

    Article  PubMed  Google Scholar 

  • He, C., Cortes, J. M., Kang, X., Cao, J., Chen, H., Guo, X., Wang, R., Kong, L., Huang, X., Xiao, J., Shan, X., Feng, R., Chen, H., & Duan, X. (2021). Individual-based morphological brain network organization and its association with autistic symptoms in young children with autism spectrum disorder. Human Brain Mapping, 42(10), 3282–3294.

    Article  PubMed  PubMed Central  Google Scholar 

  • Healy, S., Nacario, A., Braithwaite, R. E., & Hopper, C. (2018). The effect of physical activity interventions on youth with autism spectrum disorder: A meta-analysis: Physical activity interventions. Autism Research, 11(6), 818–833.

    Article  PubMed  Google Scholar 

  • Hillis, A. E. (2014). Inability to empathize: Brain lesions that disrupt sharing and understanding another’s emotions. Brain, 137(4), 981–997.

    Article  PubMed  Google Scholar 

  • Howells, K., Sivaratnam, C., Lindor, E., Hyde, C., McGillivray, J., Whitehouse, A., & Rinehart, N. (2020). Can participation in a community organized football program improve social, behavioural functioning and communication in children with autism spectrum disorder? A pilot study. Journal of Autism and Developmental Disorders, 50(10), 3714–3727.

    Article  PubMed  Google Scholar 

  • Howells, K., Sivaratnam, C., May, T., Lindor, E., McGillivray, J., & Rinehart, N. (2019). Efficacy of group-based organised physical activity participation for Social outcomes in children with autism spectrum disorder: A systematic review and meta-analysis. Journal of Autism and Developmental Disorders, 49(8), 3290–3308.

    Article  PubMed  Google Scholar 

  • Hynes, J., & Block, M. (2022). Effects of physical activity on social, behavioral, and cognitive skills in children and young adults with autism spectrum disorder: A systematic review of the literature. Review Journal of Autism and Developmental Disorders, 1–22.

  • Khundrakpam, B. S., Lewis, J. D., Zhao, L., Chouinard-Decorte, F., & Evans, A. C. (2016). Brain connectivity in normally developing children and adolescents. Neuroimage, 134, 192–203.

    Article  PubMed  Google Scholar 

  • Kim, D., Lee, J. Y., Jeong, B. C., Ahn, J., Kim, J. I., Lee, E. S., Kim, H., Lee, H. J., & Han, C. E. (2021). Overconnectivity of the right Heschl’s and inferior temporal gyrus correlates with symptom severity in preschoolers with autism spectrum disorder. Autism Research, 14(11), 2314–2329.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kong, X., Wang, X., Huang, L., Pu, Y., Yang, Z., Dang, X., Zhen, Z., & Liu, J. (2014). Measuring individual morphological relationship of cortical regions. Journal of Neuroscience Methods, 237, 103–107.

    Article  PubMed  Google Scholar 

  • Lan, Z., Xu, S., Yu, X., Yu, Z., Li, M., Chen, F., Liu, Y., Wang, T., Wu, Y., Gan, Y., & Jiang, G. (2022). Functional connectivity underlying symptoms in preschool boys with autism: A resting-state functional magnetic resonance imaging study. Frontiers in Neuroscience, 16, 844821.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lewis, J. D., Evans, A. C., Pruett, J. R., Botteron, K., Zwaigenbaum, L., Estes, A., Gerig, G., Collins, L., Kostopoulos, P., McKinstry, R., Dager, S., Paterson, S., Schultz, R. T., Styner, M., Hazlett, H., & Piven, J. (2014). Network inefficiencies in autism spectrum disorder at 24 months. Translational Psychiatry, 4(5), e388–e388.

    Article  PubMed  PubMed Central  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., Guo, S. L., Li, K., He, M. W., Wu, H. T., Qiu, J. X., Zhang, L., Wang, Y. L., Lou, X., & Ma, L. (2018). Alterations of white matter connectivity in preschool children with autism spectrum disorder. Radiology, 288(1), 209–217.

    Article  PubMed  Google Scholar 

  • Many, Y. A., Berkenstadt, H., & Henkin, Y. (2022). The safety and efficacy of a nurse-led sedation service using chloral hydrate for auditory brainstem response testing. Journal of Pediatric Nursing, 63, e143–e148.

    Article  PubMed  Google Scholar 

  • Maximo, J. O., & Kana, R. K. (2019). Aberrant deep connectivity in autism: A cortico-subcortical functional connectivity magnetic resonance imaging study: Cortico-subcortical connectivity in ASD. Autism Research, 12(3), 384–400.

    Article  PubMed  Google Scholar 

  • Mueller, S., Wang, D., Fox, M. D., Yeo, B. T. T., Sepulcre, J., Sabuncu, M. R., Shafee, R., Lu, J., & Liu, H. (2013). Individual variability in functional connectivity architecture of the human brain. Neuron, 77(3), 586–595.

    Article  PubMed  PubMed Central  Google Scholar 

  • Oldehinkel, M., Mennes, M., Marquand, A., Charman, T., Tillmann, J., Ecker, C., Dell’Acqua, F., Brandeis, D., Banaschewski, T., Baumeister, S., Moessnang, C., Baron-Cohen, S., Holt, R., Bölte, S., Durston, S., Kundu, P., Lombardo, M. V., Spooren, W., Loth, E., & Zwiers, M. P. (2019). Altered connectivity between cerebellum, visual, and sensory-motor networks in autism spectrum disorder: Results from the EU-AIMS longitudinal European autism project. Biological Psychiatry: Cognitive Neuroscience and Neuroimaging, 4(3), 260–270.

    PubMed  Google Scholar 

  • Pan, C. Y. (2010). Effects of water exercise swimming program on aquatic skills and social behaviors in children with autism spectrum disorders. Autism, 14(1), 9–28.

    Article  PubMed  Google Scholar 

  • Rudie, J. D., Brown, J. A., Beck-Pancer, D., Hernandez, L. M., Dennis, E. L., Thompson, P. M., Bookheimer, S. Y., & Dapretto, M. (2013). Altered functional and structural brain network organization in autism. NeuroImage: Clinical, 2, 79–94.

    Article  Google Scholar 

  • Stein, D. J., Costa, D. L. C., Lochner, C., Miguel, E. C., Reddy, Y. C. J., Shavitt, R. G., van den Heuvel, O. A., & Simpson, H. B. (2019). Obsessive–compulsive disorder. Nature Reviews Disease Primers, 5(1), 52.

    Article  PubMed  PubMed Central  Google Scholar 

  • Supekar, K., Uddin, L. Q., Khouzam, A., Phillips, J., Gaillard, W. D., Kenworthy, L. E., Yerys, B. E., Vaidya, C. J., & Menon, V. (2013). Brain hyperconnectivity in children with autism and its links to Social deficits. Cell Reports, 5(3), 738–747.

    Article  PubMed  Google Scholar 

  • Thomas Yeo, B. T., Krienen, F. M., Sepulcre, J., Sabuncu, M. R., Lashkari, D., Hollinshead, M., Roffman, J. L., Smoller, J. W., Zöllei, L., Polimeni, J. R., Fischl, B., Liu, H., & Buckner, R. L. (2011). The organization of the human cerebral cortex estimated by intrinsic functional connectivity. Journal of Neurophysiology, 106(3), 1125–1165.

    Article  PubMed Central  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.

    Article  PubMed  Google Scholar 

  • Uddin, L. Q., Supekar, K., Lynch, C. J., Khouzam, A., Phillips, J., Feinstein, C., Ryali, S., & Menon, V. (2013). Salience network–based classification and prediction of symptom severity in children with autism. JAMA Psychiatry, 70(8), 869.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, D., Buckner, R. L., Fox, M. D., Holt, D. J., Holmes, A. J., Stoecklein, S., Langs, G., Pan, R., Qian, T., Li, K., Baker, J. T., Stufflebeam, S. M., Wang, K., Wang, X., Hong, B., & Liu, H. (2015a). Parcellating cortical functional networks in individuals. Nature Neuroscience, 18(12), 1853–1860.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, D., Li, M., Wang, M., Schoeppe, F., Ren, J., Chen, H., Öngür, D., Brady, R. O., Baker, J. T., & Liu, H. (2020a). Individual-specific functional connectivity markers track dimensional and categorical features of psychotic Illness. Molecular Psychiatry, 25(9), 2119–2129.

    Article  PubMed  Google Scholar 

  • Wang, H., Jin, X., Zhang, Y., & Wang, J. (2016). Single-subject morphological brain networks: Connectivity mapping, topological characterization and test–retest reliability. Brain and Behavior, 6(4), e00448.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, J. G., Cai, K. L., Liu, Z. M., Herold, F., Zou, L., Zhu, L. N., Xiong, X., & Chen, A. G. (2020b). Effects of mini-basketball training program on executive functions and core symptoms among preschool children with autism spectrum disorders. Brain Sciences, 10(5), 263.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, J., Wang, X., Wang, R., Duan, X., Chen, H., He, C., Zhai, J., Wu, L., & Chen, H. (2021). Atypical resting-state functional connectivity of Intra/Inter-Sensory networks is related to symptom severity in young boys with autism spectrum disorder. Frontiers in Physiology, 12, 626338.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, J., Wang, X., Xia, M., Liao, X., Evans, A., & He, Y. (2015b). GRETNA: A graph theoretical network analysis toolbox for imaging connectomics. Frontiers in Human Neuroscience, 9, 386.

    PubMed  PubMed Central  Google Scholar 

  • Woolrich, M. W., Ripley, B. D., Brady, M., & Smith, S. M. (2001). Temporal autocorrelation in univariate linear modeling of FMRI data. Neuroimage, 14(6), 1370–1386.

    Article  PubMed  Google Scholar 

  • Yarkoni, T., Poldrack, R. A., Nichols, T. E., Van Essen, D. C., & Wager, T. D. (2011). Large-scale automated synthesis of human functional neuroimaging data. Nature Methods, 8(8), 665–670.

  • Yu, H., Qu, H., Chen, A., Du, Y., Liu, Z., & Wang, W. (2021). Alteration of effective connectivity in the default mode network of autism after an intervention. Frontiers in Neuroscience, 15, 796437.

    Article  PubMed  PubMed Central  Google Scholar 

  • Zalesky, A., Fornito, A., & Bullmore, E. T. (2010). Network-based statistic: Identifying differences in brain networks. Neuroimage, 53(4), 1197–1207.

    Article  PubMed  Google Scholar 

  • Zuo, C., Wang, D., Tao, F., & Wang, Y. (2019). Changes in the development of subcortical structures in autism spectrum disorder. Neuroreport, 30(16), 1062–1067.

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by Science and Technology Planning Project of Liaoning Province (no. 2022JH2/10700002); The fifth “333 Project” scientific research funding project of Jiangsu Province (BRA2019283); Scientific research and practice innovation Project of Jiangsu Province (3161).

Author information

Authors and Affiliations

Authors

Contributions

DZ and ZL contributed equally to this study. DZ conducted data analysis and drafted the manuscript; ZL provided clinical expertise, data collection and the manuscript correction; AC designed and conducted mini-basketball training program; HL designed the data analysis pipeline and drafted the manuscript; KC contributed to MRI data collection; DZ, YZ, LL, FC, HL contributed to data analysis and interpretation of result; HX contributed to the figure; GG helped revise the grammar and some expressions to make the manuscript easier to read. All authors provided critical revision of the manuscript. All authors approved the final manuscript.

Corresponding authors

Correspondence to Huanjie Li or Aiguo Chen.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest.

Ethical Approval

The study with quasi-experimental design was conducted between October and December 2018 in Yangzhou, China. Approval letters have been received from both the Ethics Committee of Yangzhou Maternal and Child Health Hospital (No. 201806001) and the Ethics and Human Protection Committee of the Affiliated Hospital of Yangzhou University. Meanwhile, this study was registered with the Chinese Clinical Trial Registry (ChiCTR1900024973) on 5 August 2019, prior to the beginning of experiments.

Informed Consent

Informed consent was obtained from all individual participants included in the study.

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 material 1 (DOCX 401.2 kb)

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zhou, D., Liu, Z., Gong, G. et al. Decreased Functional and Structural Connectivity is Associated with Core Symptom Improvement in Children with Autism Spectrum Disorder After Mini-basketball Training Program. J Autism Dev Disord (2023). https://doi.org/10.1007/s10803-023-06160-x

Download citation

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10803-023-06160-x

Keywords

Navigation