Exploring white matter functional networks in children with attention-deficit/hyperactivity disorder

Brain Communications - Tập 2 Số 2 - 2020
Xuan Bu1,2, Kaili Liang1,2, Qingxia Lin3, Yingxue Gao1,2, Andan Qian4, Hong Chen3, Wanying Chen3, Meihao Wang4, Chuang Yang3, Xiaoqi Huang1,2
1Huaxi MR Research Center (HMRRC), Functional and Molecular Imaging Key Laboratory of Sichuan Province, Department of Radiology, West China Hospital of Sichuan University, Chengdu, Sichuan 610041, China
2Psychoradiology Research Unit of the Chinese Academy of Medical Sciences (2018RU011), West China Hospital of Sichuan University, Chengdu, Sichuan 610041, China
3Department of Psychiatry, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325003, China
4Department of Radiology, The First Affiliated Hospital of Wenzhou Medical University, Wenzhou, Zhejiang 325003, China

Tóm tắt

AbstractAttention-deficit/hyperactivity disorder has been identified to involve the impairment of large-scale functional networks within grey matter, and recent studies have suggested that white matter, which also encodes neural activity, can manifest intrinsic functional organization similar to that of grey matter. However, the alterations in white matter functional networks in attention-deficit/hyperactivity disorder remain unknown. We recruited a total of 99 children, including 66 drug-naive patients and 33 typically developing controls aged from 6 to 14, to characterize the alterations in functional networks within white matter in drug-naive children with attention-deficit/hyperactivity disorder. Using clustering analysis, resting-state functional MRI data in the white matter were parsed into different networks. Intrinsic activity within each network and connectivity between networks and the associations between network activity strength and clinical symptoms were assessed. We identified eight distinct white matter functional networks: the default mode network, the somatomotor network, the dorsal attention network, the ventral attention network, the visual network, the deep frontoparietal network, the deep frontal network and the inferior corticospinal-posterior cerebellum network. The default mode, somatomotor, dorsal attention and ventral attention networks showed lower spontaneous neural activity in patients. In particular, the default mode network and the somatomotor network largely showed higher connectivity with other networks, which correlated with more severe hyperactive behaviour, while the dorsal and ventral attention networks mainly had lower connectivity with other networks, which correlated with poor attention performance. In conclusion, there are two distinct patterns of white matter functional networks in children with attention-deficit/hyperactivity disorder, with one being the hyperactivity-related hot networks including default mode network and somatomotor network and the other being inattention-related cold networks including dorsal attention and ventral attention network. These results extended upon our understanding of brain functional networks in attention-deficit/hyperactivity disorder from the perspective of white matter dysfunction.

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Tài liệu tham khảo

American Psychiatric Association, 2013, Diagnostic and statistical manual of mental disorders, 5th edn, 10.1176/appi.books.9780890425596

Bu, 2019, Quantitative tractography reveals changes in the corticospinal tract in drug-naive children with attention-deficit/hyperactivity disorder, J Psychiatry Neurosci, 45, 190024

Carmona, 2015, Sensation-to-cognition cortical streams in attention-deficit/hyperactivity disorder, Hum Brain Mapp, 36, 2544, 10.1002/hbm.22790

Castellanos, 2012, Large-scale brain systems in ADHD: beyond the prefrontal-striatal model, Trends Cogn Sci, 16, 17, 10.1016/j.tics.2011.11.007

Conners, 1998, The revised Conners' Parent Rating Scale (CPRS-R): factor structure, reliability, and criterion validity, J Abnorm Child Psychol, 26, 257, 10.1023/A:1022602400621

Cortese, 2012, Toward systems neuroscience of ADHD: a meta-analysis of 55 fMRI studies, Am J Psychiatry, 169, 1038, 10.1176/appi.ajp.2012.11101521

Cubillo, 2012, A review of fronto-striatal and fronto-cortical brain abnormalities in children and adults with attention deficit hyperactivity disorder (ADHD) and new evidence for dysfunction in adults with ADHD during motivation and attention, Cortex, 48, 194, 10.1016/j.cortex.2011.04.007

de Lacy, 2018, Novel in silico multivariate mapping of intrinsic and anticorrelated connectivity to neurocognitive functional maps supports the maturational hypothesis of ADHD, Hum Brain Mapp, 39, 3449, 10.1002/hbm.24187

Desikan, 2006, An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest, Neuroimage, 31, 968, 10.1016/j.neuroimage.2006.01.021

Di Martino, 2013, Shared and distinct intrinsic functional network centrality in autism and attention-deficit/hyperactivity disorder, Biol Psychiatry, 74, 623, 10.1016/j.biopsych.2013.02.011

Ding, 2018, Detection of synchronous brain activity in white matter tracts at rest and under functional loading, Proc Natl Acad Sci USA, 115, 595, 10.1073/pnas.1711567115

Ding, 2013, Spatio-temporal correlation tensors reveal functional structure in human brain, PLoS One, 8, e82107, 10.1371/journal.pone.0082107

Ding, 2016, Visualizing functional pathways in the human brain using correlation tensors and magnetic resonance imaging, Magn Reson Imaging, 34, 8, 10.1016/j.mri.2015.10.003

Fair, 2010, Atypical default network connectivity in youth with attention-deficit/hyperactivity disorder, Biol Psychiatry, 68, 1084, 10.1016/j.biopsych.2010.07.003

Faraone, 2015, Attention-deficit/hyperactivity disorder, Nat Rev Dis Primers, 1, 15020, 10.1038/nrdp.2015.20

Gallo, 2016, Moving towards causality in attention-deficit hyperactivity disorder: overview of neural and genetic mechanisms, Lancet Psychiatry, 3, 555, 10.1016/S2215-0366(16)00096-1

Gao, 2019, Impairments of large-scale functional networks in attention-deficit/hyperactivity disorder: a meta-analysis of resting-state functional connectivity, Psychol Med, 1

Gawryluk, 2014, Does functional MRI detect activation in white matter? A review of emerging evidence, issues, and future directions, Front Neurosci, 8, 239, 10.3389/fnins.2014.00239

Gong, 1994, The Wechsler Intelligence Scale for Children Revised in China(C-WISC), Chin J Clin Psychol, 1, 1

Hart, 2013, Meta-analysis of functional magnetic resonance imaging studies of inhibition and attention in attention-deficit/hyperactivity disorder: exploring task-specific, stimulant medication, and age effects, JAMA Psychiatry, 70, 185, 10.1001/jamapsychiatry.2013.277

Helenius, 2011, Impaired engagement of the ventral attentional pathway in ADHD, Neuropsychologia, 49, 1889, 10.1016/j.neuropsychologia.2011.03.014

Hong, 2014, Connectomic disturbances in attention-deficit/hyperactivity disorder: a whole-brain tractography analysis, Biol Psychiatry, 76, 656, 10.1016/j.biopsych.2013.12.013

Huang, 2018, Voxel-wise detection of functional networks in white matter, Neuroimage, 183, 544, 10.1016/j.neuroimage.2018.08.049

Jiang, 2019, White-matter functional networks changes in patients with schizophrenia, Neuroimage, 190, 172, 10.1016/j.neuroimage.2018.04.018

Jiang, 2019, Dysfunctional white-matter networks in medicated and unmedicated benign epilepsy with centrotemporal spikes, Hum Brain Mapp, 40, 3113, 10.1002/hbm.24584

Ji, 2017, Low-frequency blood oxygen level-dependent fluctuations in the brain white matter: more than just noise, Sci Bull, 62, 656, 10.1016/j.scib.2017.03.021

Kaufman, 2000, K-SADS-PL, J Am Acad Child Adolesc Psychiatry, 39, 1208, 10.1097/00004583-200010000-00002

Kessler, 2014, Modality-spanning deficits in attention-deficit/hyperactivity disorder in functional networks, gray matter, and white matter, J Neurosci, 34, 16555, 10.1523/JNEUROSCI.3156-14.2014

Konrad, 2010, Is the ADHD brain wired differently? A review on structural and functional connectivity in attention deficit hyperactivity disorder, Hum Brain Mapp, 31, 904, 10.1002/hbm.21058

Li, 2019, Exploring the functional connectome in white matter, Hum Brain Mapp, 40, 4331, 10.1002/hbm.24705

Li, 2019, Characterization of the hemodynamic response function in white matter tracts for event-related fMRI, Nat Commun, 10, 1140, 10.1038/s41467-019-09076-2

Marussich, 2017, Mapping white-matter functional organization at rest and during naturalistic visual perception, Neuroimage, 146, 1128, 10.1016/j.neuroimage.2016.10.005

McCarthy, 2013, Attention network hypoconnectivity with default and affective network hyperconnectivity in adults diagnosed with attention-deficit/hyperactivity disorder in childhood, JAMA Psychiatry, 70, 1329, 10.1001/jamapsychiatry.2013.2174

McLeod, 2016, Atypical within- and between-hemisphere motor network functional connections in children with developmental coordination disorder and attention-deficit/hyperactivity disorder, Neuroimage Clin, 12, 157, 10.1016/j.nicl.2016.06.019

O'Halloran, 2018, Neural circuitry underlying sustained attention in healthy adolescents and in ADHD symptomatology, Neuroimage, 169, 395, 10.1016/j.neuroimage.2017.12.030

Peer, 2017, Evidence for functional networks within the human brain's white matter, J Neurosci, 37, 6394, 10.1523/JNEUROSCI.3872-16.2017

Posner, 2016, Increased default mode network connectivity in individuals at high familial risk for depression, Neuropsychopharmacology, 41, 1759, 10.1038/npp.2015.342

Posner, 2014, Connecting the dots: a review of resting connectivity MRI studies in attention-deficit/hyperactivity disorder, Neuropsychol Rev, 24, 3, 10.1007/s11065-014-9251-z

Posner, 2017, Increased functional connectivity between the default mode and salience networks in unmedicated adults with obsessive-compulsive disorder, Hum Brain Mapp, 38, 678, 10.1002/hbm.23408

Power, 2012, Spurious but systematic correlations in functional connectivity MRI networks arise from subject motion, NeuroImage, 59, 2142, 10.1016/j.neuroimage.2011.10.018

Power, 2014, Methods to detect, characterize, and remove motion artifact in resting state fMRI, NeuroImage, 84, 320, 10.1016/j.neuroimage.2013.08.048

Proal, 2011, Brain gray matter deficits at 33-year follow-up in adults with attention-deficit/hyperactivity disorder established in childhood, Arch Gen Psychiatry, 68, 1122, 10.1001/archgenpsychiatry.2011.117

Qiu, 2012, Inattention and hyperactivity predict alterations in specific neural circuits among 6-year-old boys, J Am Acad Child Adolesc Psychiatry, 51, 632, 10.1016/j.jaac.2012.02.017

Samea, 2019, Brain alterations in children/adolescents with ADHD revisited: a neuroimaging meta-analysis of 96 structural and functional studies, Neurosci Biobehav Rev, 100, 1, 10.1016/j.neubiorev.2019.02.011

Sidlauskaite, 2016, Default mode network abnormalities during state switching in attention deficit hyperactivity disorder, Psychol Med, 46, 519, 10.1017/S0033291715002019

Silk, 2009, White-matter abnormalities in attention deficit hyperactivity disorder: a diffusion tensor imaging study, Hum Brain Mapp, 30, 2757, 10.1002/hbm.20703

Sonuga-Barke, 2007, Spontaneous attentional fluctuations in impaired states and pathological conditions: a neurobiological hypothesis, Neurosci Biobehav Rev, 31, 977, 10.1016/j.neubiorev.2007.02.005

Su, 2001, Norms of the Conners parent symptom questionnaire in Chinese urban children, Chin J Clin Psychol, 9, 241

Tinius, 2003, The integrated visual and auditory continuous performance test as a neuropsychological measure, Arch Clin Neuropsychol, 18, 439, 10.1093/arclin/18.5.439

Valera, 2010, Neural substrates of impaired sensorimotor timing in adult attention-deficit/hyperactivity disorder, Biol Psychiatry, 68, 359, 10.1016/j.biopsych.2010.05.012

Wang, 2009, Altered small-world brain functional networks in children with attention-deficit/hyperactivity disorder, Hum Brain Mapp, 30, 638, 10.1002/hbm.20530

Wu, 2017, Functional connectivity and activity of white matter in somatosensory pathways under tactile stimulations, Neuroimage, 152, 371, 10.1016/j.neuroimage.2017.02.074

Wu, 2014, White matter tract integrity of frontostriatal circuit in attention deficit hyperactivity disorder: association with attention performance and symptoms, Hum Brain Mapp, 35, 199, 10.1002/hbm.22169

Yan, 2013, A comprehensive assessment of regional variation in the impact of head micromovements on functional connectomics, NeuroImage, 76, 183, 10.1016/j.neuroimage.2013.03.004

Yeo, 2011, The organization of the human cerebral cortex estimated by intrinsic functional connectivity, J Neurophysiol, 106, 1125, 10.1152/jn.00338.2011

Yerys, 2019, Functional connectivity of frontoparietal and salience/ventral attention networks have independent associations with co-occurring attention-deficit/hyperactivity disorder symptoms in children with autism, Biol Psychiatry Cogn Neurosci Neuroimaging, 4, 343

Zhu, 2008, Fisher discriminative analysis of resting-state brain function for attention-deficit/hyperactivity disorder, Neuroimage, 40, 110, 10.1016/j.neuroimage.2007.11.029

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