A multi-parameter resting-state functional magnetic resonance imaging study of brain intrinsic activity in attention deficit hyperactivity disorder children_Journal of Biomedical Engineering

Authors：

ZHOU Jiaxiu ¹ , GAO Yingxue ² , BU Xuan ² , LI Hailong ² , LIANG Yan ³ , CHEN Hong ³ , WANG Meihao ⁴ , LIN Feifei ⁵ ,  YANG Chuang ³ , HUANG Xiaoqi ²

1. Department of Psychology, Shenzhen Children's Hospital, Shenzhen, Guangdong 518038, P.R.China;
2. Huaxi MR Research Center (HMRRC), Department of Radiology, West China Hospital, Sichuan University, Chengdu 610041, P.R.China;
3. Mental Health Department, the First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325000, P.R.China;
4. Radiology Department, the First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325000, P.R.China;
5. Radiology Department, Shenzhen Children's Hospital, Shenzhen, Guangdong 518038, P.R.China;

Corresponding author：

YANG Chuang, Email: dryangchuang@163.com

Keywords：

attention-deficit/hyperactivity disorder; functional magnetic resonance imaging; regional homogeneity; degree centrality; voxel-mirrored homotopic connectivity

DOI：

10.7507/1001-5515.201801001

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A great number of studies have demonstrated functional abnormalities in children with attention-deficit/hyperactivity disorder (ADHD), although conflicting results have also been reported. And few studies analyzed homotopic functional connectivity between hemispheres. In this study, resting-state functional magnetic resonance imaging (MRI) data were recorded from 45 medication-naïve ADHD children and 26 healthy controls. The regional homogeneity (ReHo), degree centrality (DC) and voxel-mirrored homotopic connectivity (VMHC) values were compared between the two groups to depict the intrinsic brain activities. We found that ADHD children exhibited significantly lower ReHo and DC values in the right middle frontal gyrus and the two values correlated with each other; moreover, lower VMHC values were found in the bilateral occipital lobes of ADHD children, which was negatively related with anxiety scores of Conners' Parent Rating Scale (CPRS-R) and positively related with completed categories of Wisconsin Card Sorting Test (WCST). Our results might suggest that less spontaneous neuronal activities of the right middle frontal gyrus and the bilateral occipital lobes in ADHD children.

Citation： ZHOU Jiaxiu, GAO Yingxue, BU Xuan, LI Hailong, LIANG Yan, CHEN Hong, WANG Meihao, LIN Feifei, YANG Chuang, HUANG Xiaoqi. A multi-parameter resting-state functional magnetic resonance imaging study of brain intrinsic activity in attention deficit hyperactivity disorder children. Journal of Biomedical Engineering, 2018, 35(3): 415-420. doi: 10.7507/1001-5515.201801001 Copy

1.	Barkley R A, Biederman J. Toward a broader definition of the age-of-onset criterion for attention-deficit hyperactivity disorder. J Am Acad Child Adolesc Psychiatry, 1997, 36(9): 1204-1210.
2.	Polanczyk G, de Lima M S, Horta B L, et al. The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry, 2007, 164(6): 942-948.
3.	童连, 史慧静, 臧嘉捷. 中国儿童ADHD流行状况Meta分析. 中国公共卫生, 2013, 29(9): 1279-1283.
4.	Faraone S V, Biederman J, Mick E. The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies. Psychol Med, 2006, 36(2): 159-165.
5.	Castellanos F X, Aoki Y. Intrinsic functional connectivity in attention-deficit/hyperactivity disorder: A science in development. Biol Psychiatry Cogn Neurosci Neuroimaging, 2016, 1(3): 253-261.
6.	郭润蒲, 杜亚松. 注意缺陷多动障碍相关脑网络结构及功能磁共振研究进展. 中国神经精神疾病杂志, 2016, 42(9): 556-559.
7.	Barkhof F, Haller S, Rombouts S A. Resting-state functional MR imaging: a new window to the brain. Radiology, 2014, 272(1): 29-49.
8.	Beckmann C F, Deluca M, Devlin J T, et al. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci, 2005, 360(1457): 1001-1013.
9.	Zuo X N, Ehmke R, Mennes M, et al. Network centrality in the human functional connectome. Cereb Cortex, 2012, 22(8): 1862-1875.
10.	Zuo X N, Kelly C, Di Martino A, et al. Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci, 2010, 30(45): 15034-15043.
11.	Park B Y, Hong J, Lee S H, et al. Functional connectivity of child and adolescent attention deficit hyperactivity disorder patients: correlation with IQ. Front Hum Neurosci, 2016, 10: 565.
12.	Park B Y, Park H. Connectivity differences between adult male and female patients with attention deficit hyperactivity disorder according to resting-state functional MRI. Neural Regen Res, 2016, 11(1): 119-125.
13.	Di Martino A, Zuo X N, Kelly C, et al. Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biol Psychiatry, 2013, 74(8): 623-632.
14.	Zhu Chaozhe, Zang Yufeng, Cao Qingjiu, et al. Fisher discriminative analysis of resting-state brain function for attention-deficit/hyperactivity disorder. Neuroimage, 2008, 40(1): 110-120.
15.	Yang Hong, Wu Qizhu, Guo Lanting, et al. Abnormal spontaneous brain activity in medication-naïve ADHD children: a resting state fMRI study. Neurosci Lett, 2011, 502(2): 89-93.
16.	Zang Yufeng, He Yong, Zhu Chaozhe, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev, 2007, 29(2): 83-91.
17.	Zang Yufeng, Jiang Tianzi, Lu Yingli, et al. Regional homogeneity approach to fMRI data analysis. Neuroimage, 2004, 22(1): 394-400.
18.	An Li, Cao Qingjiu, Sui Manqiu, et al. Local synchronization and amplitude of the fluctuation of spontaneous brain activity in attention-deficit/hyperactivity disorder: a resting-state fMRI study. Neurosci Bull, 2013, 29(5): 603-613.
19.	Cheng Wei, Ji Xiaoxi, Zhang Jie, et al. Individual classification of ADHD patients by integrating multiscale neuroimaging markers and advanced pattern recognition techniques. Front Syst Neurosci, 2012, 6: 58.
20.	Liu Dongqiang, Yan Chaogan, Ren Juejing, et al. Using coherence to measure regional homogeneity of resting-state FMRI signal. Front Syst Neurosci, 2010, 4: 24.
21.	An Li, Cao Xiaohua, Cao Qingjiu, et al. Methylphenidate normalizes resting-state brain dysfunction in boys with attention deficit hyperactivity disorder. Neuropsychopharmacology, 2013, 38(7): 1287-1295.
22.	Cao Qingjiu, Zang Yufeng, Sun Li, et al. Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study. Neuroreport, 2006, 17(10): 1033-1036.
23.	Alonso Bde D, Hidalgo Tobón S, Dies Suarez P, et al. A multi-methodological MR resting state network analysis to assess the changes in brain physiology of children with ADHD. PLoS One, 2014, 9(6): e99119.
24.	Yan Chaogan, Yang Zhen, Colcombe S J, et al. Concordance among indices of intrinsic brain function: Insights from inter-individual variation and temporal dynamics. Sci Bull, 2017, 62(23): 1572-1584.
25.	Yu Xiaoyan, Yuan Binke, Cao Qingjiu, et al. Frequency-specific abnormalities in regional homogeneity among children with attention deficit hyperactivity disorder: a resting-state fMRI study. Sci Bull, 2016, 61(9): 682-692.
26.	杨润许, 丁凯景, 刘瑞湘, 等. 注意缺陷多动障碍儿童的静息态脑功能磁共振研究. 中国当代儿科杂志, 2013, 15(9): 723-727.
27.	Golestani A M, Goodyear B G. Regions of interest for resting-state fMRI analysis determined by inter-voxel cross-correlation. NeuroImage, 2011, 56(1): 246-251.
28.	Zhang Jie, Kendrick K M, LU Guangming, et al. The fault Lies on the other side: altered brain functional connectivity in psychiatric disorders is mainly caused by counterpart regions in the opposite hemisphere. Cereb Cortex, 2015, 25(10): 3475-3486.
29.	Chen Lizhou, Hu Xinyu, Ouyang Luo, et al. A systematic review and meta-analysis of tract-based spatial statistics studies regarding attention-deficit/hyperactivity disorder. Neurosci Biobehav Rev, 2016, 68: 838-847.

1. Barkley R A, Biederman J. Toward a broader definition of the age-of-onset criterion for attention-deficit hyperactivity disorder. J Am Acad Child Adolesc Psychiatry, 1997, 36(9): 1204-1210.
2. Polanczyk G, de Lima M S, Horta B L, et al. The worldwide prevalence of ADHD: a systematic review and metaregression analysis. Am J Psychiatry, 2007, 164(6): 942-948.
3. 童连, 史慧静, 臧嘉捷. 中国儿童ADHD流行状况Meta分析. 中国公共卫生, 2013, 29(9): 1279-1283.
4. Faraone S V, Biederman J, Mick E. The age-dependent decline of attention deficit hyperactivity disorder: a meta-analysis of follow-up studies. Psychol Med, 2006, 36(2): 159-165.
5. Castellanos F X, Aoki Y. Intrinsic functional connectivity in attention-deficit/hyperactivity disorder: A science in development. Biol Psychiatry Cogn Neurosci Neuroimaging, 2016, 1(3): 253-261.
6. 郭润蒲, 杜亚松. 注意缺陷多动障碍相关脑网络结构及功能磁共振研究进展. 中国神经精神疾病杂志, 2016, 42(9): 556-559.
7. Barkhof F, Haller S, Rombouts S A. Resting-state functional MR imaging: a new window to the brain. Radiology, 2014, 272(1): 29-49.
8. Beckmann C F, Deluca M, Devlin J T, et al. Investigations into resting-state connectivity using independent component analysis. Philos Trans R Soc Lond B Biol Sci, 2005, 360(1457): 1001-1013.
9. Zuo X N, Ehmke R, Mennes M, et al. Network centrality in the human functional connectome. Cereb Cortex, 2012, 22(8): 1862-1875.
10. Zuo X N, Kelly C, Di Martino A, et al. Growing together and growing apart: regional and sex differences in the lifespan developmental trajectories of functional homotopy. J Neurosci, 2010, 30(45): 15034-15043.
11. Park B Y, Hong J, Lee S H, et al. Functional connectivity of child and adolescent attention deficit hyperactivity disorder patients: correlation with IQ. Front Hum Neurosci, 2016, 10: 565.
12. Park B Y, Park H. Connectivity differences between adult male and female patients with attention deficit hyperactivity disorder according to resting-state functional MRI. Neural Regen Res, 2016, 11(1): 119-125.
13. Di Martino A, Zuo X N, Kelly C, et al. Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder. Biol Psychiatry, 2013, 74(8): 623-632.
14. Zhu Chaozhe, Zang Yufeng, Cao Qingjiu, et al. Fisher discriminative analysis of resting-state brain function for attention-deficit/hyperactivity disorder. Neuroimage, 2008, 40(1): 110-120.
15. Yang Hong, Wu Qizhu, Guo Lanting, et al. Abnormal spontaneous brain activity in medication-naïve ADHD children: a resting state fMRI study. Neurosci Lett, 2011, 502(2): 89-93.
16. Zang Yufeng, He Yong, Zhu Chaozhe, et al. Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev, 2007, 29(2): 83-91.
17. Zang Yufeng, Jiang Tianzi, Lu Yingli, et al. Regional homogeneity approach to fMRI data analysis. Neuroimage, 2004, 22(1): 394-400.
18. An Li, Cao Qingjiu, Sui Manqiu, et al. Local synchronization and amplitude of the fluctuation of spontaneous brain activity in attention-deficit/hyperactivity disorder: a resting-state fMRI study. Neurosci Bull, 2013, 29(5): 603-613.
19. Cheng Wei, Ji Xiaoxi, Zhang Jie, et al. Individual classification of ADHD patients by integrating multiscale neuroimaging markers and advanced pattern recognition techniques. Front Syst Neurosci, 2012, 6: 58.
20. Liu Dongqiang, Yan Chaogan, Ren Juejing, et al. Using coherence to measure regional homogeneity of resting-state FMRI signal. Front Syst Neurosci, 2010, 4: 24.
21. An Li, Cao Xiaohua, Cao Qingjiu, et al. Methylphenidate normalizes resting-state brain dysfunction in boys with attention deficit hyperactivity disorder. Neuropsychopharmacology, 2013, 38(7): 1287-1295.
22. Cao Qingjiu, Zang Yufeng, Sun Li, et al. Abnormal neural activity in children with attention deficit hyperactivity disorder: a resting-state functional magnetic resonance imaging study. Neuroreport, 2006, 17(10): 1033-1036.
23. Alonso Bde D, Hidalgo Tobón S, Dies Suarez P, et al. A multi-methodological MR resting state network analysis to assess the changes in brain physiology of children with ADHD. PLoS One, 2014, 9(6): e99119.
24. Yan Chaogan, Yang Zhen, Colcombe S J, et al. Concordance among indices of intrinsic brain function: Insights from inter-individual variation and temporal dynamics. Sci Bull, 2017, 62(23): 1572-1584.
25. Yu Xiaoyan, Yuan Binke, Cao Qingjiu, et al. Frequency-specific abnormalities in regional homogeneity among children with attention deficit hyperactivity disorder: a resting-state fMRI study. Sci Bull, 2016, 61(9): 682-692.
26. 杨润许, 丁凯景, 刘瑞湘, 等. 注意缺陷多动障碍儿童的静息态脑功能磁共振研究. 中国当代儿科杂志, 2013, 15(9): 723-727.
27. Golestani A M, Goodyear B G. Regions of interest for resting-state fMRI analysis determined by inter-voxel cross-correlation. NeuroImage, 2011, 56(1): 246-251.
28. Zhang Jie, Kendrick K M, LU Guangming, et al. The fault Lies on the other side: altered brain functional connectivity in psychiatric disorders is mainly caused by counterpart regions in the opposite hemisphere. Cereb Cortex, 2015, 25(10): 3475-3486.
29. Chen Lizhou, Hu Xinyu, Ouyang Luo, et al. A systematic review and meta-analysis of tract-based spatial statistics studies regarding attention-deficit/hyperactivity disorder. Neurosci Biobehav Rev, 2016, 68: 838-847.

Journal of Biomedical Engineering

A multi-parameter resting-state functional magnetic resonance imaging study of brain intrinsic activity in attention deficit hyperactivity disorder children

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