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 ORCID:

Bin HU

https://orcid.org/0000-0003-3514-5413

Jing ZHANG

https://orcid.org/0000-0002-1678-5688

Zhijun YAO

https://orcid.org/0000-0003-0057-0831

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Journal of Zhejiang University SCIENCE B 2024 Vol.25 No.10 P.857-877

http://doi.org/10.1631/jzus.B2300401


Aberrant dynamic functional connectivity of thalamocortical circuitry in major depressive disorder


Author(s):  Weihao ZHENG, Qin ZHANG, Ziyang ZHAO, Pengfei ZHANG, Leilei ZHAO, Xiaomin WANG, Songyu YANG, Jing ZHANG, Zhijun YAO, Bin HU

Affiliation(s):  Gansu Provincial Key Laboratory of Wearable Computing, School of Information Science and Engineering, Lanzhou University,Lanzhou730000,China; more

Corresponding email(s):   bh@lzu.edu.cn, yaozj@lzu.edu.cn, ery_zhangjing@lzu.edu.cn

Key Words:  Major depressive disorder, Resting-state functional magnetic resonance imaging, Thalamocortical circuitry, Dynamic functional connectivity, Dynamic laterality


Weihao ZHENG, Qin ZHANG, Ziyang ZHAO, Pengfei ZHANG, Leilei ZHAO, Xiaomin WANG, Songyu YANG, Jing ZHANG, Zhijun YAO, Bin HU. Aberrant dynamic functional connectivity of thalamocortical circuitry in major depressive disorder[J]. Journal of Zhejiang University Science B, 2024, 25(10): 857-877.

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author="Weihao ZHENG, Qin ZHANG, Ziyang ZHAO, Pengfei ZHANG, Leilei ZHAO, Xiaomin WANG, Songyu YANG, Jing ZHANG, Zhijun YAO, Bin HU",
journal="Journal of Zhejiang University Science B",
volume="25",
number="10",
pages="857-877",
year="2024",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2300401"
}

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%A Weihao ZHENG
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%A Leilei ZHAO
%A Xiaomin WANG
%A Songyu YANG
%A Jing ZHANG
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A1 - Ziyang ZHAO
A1 - Pengfei ZHANG
A1 - Leilei ZHAO
A1 - Xiaomin WANG
A1 - Songyu YANG
A1 - Jing ZHANG
A1 - Zhijun YAO
A1 - Bin HU
J0 - Journal of Zhejiang University Science B
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IS - 10
SP - 857
EP - 877
%@ 1673-1581
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PB - Zhejiang University Press & Springer
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DOI - 10.1631/jzus.B2300401


Abstract: 
thalamocortical circuitry has a substantial impact on emotion and cognition. Previous studies have demonstrated alterations in thalamocortical functional connectivity (FC), characterized by region-dependent hypo- or hyper-connectivity, among individuals with major depressive disorder (MDD). However, the dynamical reconfiguration of the thalamocortical system over time and potential abnormalities in dynamic thalamocortical connectivity associated with MDD remain unclear. Hence, we analyzed dynamic FC (dFC) between ten thalamic subregions and seven cortical subnetworks from resting-state functional magnetic resonance images of 48 patients with MDD and 57 healthy controls (HCs) to investigate time-varying changes in thalamocortical FC in patients with MDD. Moreover, dynamic laterality analysis was conducted to examine the changes in functional lateralization of the thalamocortical system over time. Correlations between the dynamic measures of thalamocortical FC and clinical assessment were also calculated. We identified four dynamic states of thalamocortical circuitry wherein patients with MDD exhibited decreased fractional time and reduced transitions within a negative connectivity state that showed strong correlations with primary cortical networks, compared with the HCs. In addition, MDD patients also exhibited increased fluctuations in functional laterality in the thalamocortical system across the scan duration. The thalamo-subnetwork analysis unveiled abnormal dFC variability involving higher-order cortical networks in the MDD cohort. Significant correlations were found between increased dFC variability with dorsal attention and default mode networks and the severity of symptoms. Our study comprehensively investigated the pattern of alteration of the thalamocortical dFC in MDD patients. The heterogeneous alterations of dFC between the thalamus and both primary and higher-order cortical networks may help characterize the deficits of sensory and cognitive processing in MDD.

重度抑郁障碍患者丘脑皮层环路的动态功能连接异常

郑炜豪1,张芹1,赵子阳1,张鹏飞2,3,4,赵磊磊1,王晓敏1,杨淞宇1,张静2,3,4,姚志军1,胡斌1,5,6,7
1甘肃省可穿戴装备重点实验室,兰州大学信息科学与工程学院,中国兰州市,730000
2兰州大学第二临床医学院,中国兰州市,730030
3兰州大学第二医院核磁共振科,中国兰州市,730030
4甘肃省功能及分子影像临床医学研究中心,中国兰州市,730030
5北京理工大学医学技术学院,中国北京市,100081
6中国科学院脑科学与智能技术卓越创新中心,中国科学院神经科学研究所,中国上海市,200031
7中国科学院半导体研究所 兰州大学认知神经传感技术联合研究中心,中国兰州市,730000
摘要:丘脑皮层环路对情绪和认知具有重大影响。研究表明,重度抑郁障碍患者存在丘脑皮层功能连接异常,主要表现为区域依赖性的低连接或超连接。然而,重度抑郁障碍患者丘脑皮层环路动态功能连接的潜在异常目前尚不清楚。因此,基于48名重度抑郁障碍患者和57名健康对照的静息态功能磁共振成像数据,本研究评估了10个丘脑亚区和大脑皮层之间的动态功能连接变化,进而探究重度抑郁障碍患者丘脑皮层环路的动态交互模式。利用动态偏侧性分析探究了丘脑皮层系统的功能偏侧性随时间的动态变化。此外,还计算了丘脑皮层环路的动态功能连接特征与临床量表评分之间的相关性。本研究确定了4个反复出现的丘脑皮层功能连接状态。与健康对照组相比,重度抑郁障碍患者在与初级皮层网络具有较强负相关的连接状态下,时间分数和状态转换概率显著降低。此外,重度抑郁障碍患者丘脑皮层系统的功能偏侧性表现出更大的波动。丘脑-子网络分析进一步发现重度抑郁障碍患者中丘脑与高阶皮层网络之间连接的变异性异常增加,并且与背侧注意网络和默认模式网络相关的丘脑皮层功能连接变异性与患者的症状严重程度之间存在显著的相关性。本研究综合探究了重度抑郁障碍患者丘脑皮层环路的动态功能连接变化模式。研究结果表明,丘脑与初级和高阶皮层网络之间动态功能连接的异质性改变可能有助于表征重度抑郁障碍患者的感觉和认知处理缺陷。

关键词:重度抑郁障碍;静息态功能磁共振成像;丘脑皮层环路;动态功能连接;动态偏侧性

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Reference

[1]AggarwalCC,HinneburgA,KeimDA,2001.On the surprising behavior of distance metrics in high dimensional space.Database Theory—ICDT 2001, Berlin, Heidelberg. Springer Berlin Heidelberg, p.420-434.

[2]AllenEA,DamarajuE,PlisSM,et al.,2014.Tracking whole-brain connectivity dynamics in the resting state.Cereb Cortex,24(3):663-676.

[3]ArbabshiraniMR,DamarajuE,PhlypoR,et al.,2014.Impact of autocorrelation on functional connectivity.NeuroImage,102(Part2):294-308.

[4]AvantsB,TustisonNJ,SongG,2009.Advanced Normalization Tools: V1.0. Insight J, July-December.

[5]BehrensTEJ,Johansen-BergH,WoolrichMW,et al.,2003.Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging.Nat Neurosci,6(7):750-757.

[6]BosDJ,OranjeB,AchterbergM,et al.,2017.Structural and functional connectivity in children and adolescents with and without attention deficit/hyperactivity disorder.J Child Psychol Psychiatry,58(7):810-818.

[7]BrownEC,ClarkDL,HasselS,et al.,2017.Thalamocortical connectivity in major depressive disorder.J Affect Disord,217:125-131.

[8]BruderGE,StewartJW,McGrathPJ,2017.Right brain, left brain in depressive disorders: clinical and theoretical implications of behavioral, electrophysiological and neuroimaging findings.Neurosci Biobehav Rev,78:178-191.

[9]CalhounVD,MillerR,PearlsonG,et al.,2014.The chronnectome: time-varying connectivity networks as the next frontier in fMRI data discovery.Neuron,84(2):262-274.

[10]ChenFF,LvXY,FangJL,et al.,2021.Body-mind relaxation meditation modulates the thalamocortical functional connectivity in major depressive disorder: a preliminary resting-state fMRI study.Transl Psychiatry,11:546.

[11]ChenQL,BeatyRE,CuiZX,et al.,2019.Brain hemispheric involvement in visuospatial and verbal divergent thinking.NeuroImage,202:116065.

[12]ChenSY,LangleyJ,ChenXC,et al.,2016.Spatiotemporal modeling of brain dynamics using resting-state functional magnetic resonance imaging with Gaussian Hidden Markov model.Brain Connect,6(4):326-334.

[13]ChoeAS,NebelMB,BarberAD,et al.,2017.Comparing test-retest reliability of dynamic functional connectivity methods.NeuroImage,158:155-175.

[14]ChoiJ,JeongB,LeeSW,et al.,2013.Aberrant development of functional connectivity among resting state-related functional networks in medication-naive ADHD children.PLoS ONE,8(12):e83516.

[15]DingYD,YangR,YanCG,et al.,2021.Disrupted hemispheric connectivity specialization in patients with major depressive disorder: evidence from the REST-meta-MDD Project.J Affect Disord,284:217-228.

[16]DoronKW,BassettDS,GazzanigaMS,2012.Dynamic network structure of interhemispheric coordination.Proc Natl Acad Sci USA,109(46):18661-18668.

[17]DuHH,ShenX,DuXY,et al.,2022.Altered visual cortical excitability is associated with psychopathological symptoms in major depressive disorder.Front Psychiatry,13:844434.

[18]DupireA,KantP,MonsN,et al.,2013.A role for anterior thalamic nuclei in affective cognition: interaction with environmental conditions.Hippocampus,23(5):392-404.

[19]FischlB,2012.FreeSurfer.NeuroImage,62(2):774-781.

[20]FoxMD,SnyderAZ,VincentJL,et al.,2005.The human brain is intrinsically organized into dynamic, anticorrelated functional networks.Proc Natl Acad Sci USA,102(27):9673-9678.

[21]FoxMD,ZhangDY,SnyderAZ,et al.,2009.The global signal and observed anticorrelated resting state brain networks.J Neurophysiol,101(6):3270-3283.

[22]GotlibIH,JonidesJ,BuschkuehlM,et al.,2011.Memory for affectively valenced and neutral stimuli in depression: evidence from a novel matching task.Cognit Emotion,25(7):1246-1254.

[23]GrohA,KriegerP,MeaseRA,et al.,2018.Acute and chronic pain processing in the thalamocortical system of humans and animal models.Neuroscience,387:58-71.

[24]GüntürkünO,StröckensF,OcklenburgS,2020.Brain lateralization: a comparative perspective.Physiol Rev,100(3):1019-1063.

[25]HakimdavoodiH,AmirmazlaghaniM,2020.Using autoregressive-dynamic conditional correlation model with residual analysis to extract dynamic functional connectivity.J Neural Eng,17(3):035008.

[26]HamiltonJP,ChenMC,WaughCE,et al.,2015.Distinctive and common neural underpinnings of major depression, social anxiety, and their comorbidity.Soc Cogn Affect Neurosci,10(4):552-560.

[27]HamiltonM,1967.Development of a rating scale for primary depressive illness.Br J Soc Clin Psychol,6(4):278-296.

[28]HutchisonRM,WomelsdorfT,GatiJS,et al.,2013.Resting-state networks show dynamic functional connectivity in awake humans and anesthetized macaques.Hum Brain Mapp,34(9):2154-2177.

[29]IglesiasJE,InsaustiR,Lerma-UsabiagaG,et al.,2018.A probabilistic atlas of the human thalamic nuclei combining ex vivo MRI and histology.NeuroImage,183:314-326.

[30]KaiserRH,Andrews-HannaJR,WagerTD,et al.,2015.Large-scale network dysfunction in major depressive disorder: a meta-analysis of resting-state functional connectivity.JAMA Psychiatry,72(6):603-611.

[31]KangLJ,ZhangAX,SunN,et al.,2018.Functional connectivity between the thalamus and the primary somatosensory cortex in major depressive disorder: a resting-state fMRI study.BMC Psychiatry,18:339.

[32]KlingnerCM,LangbeinK,DietzekM,et al.,2014.Thalamocortical connectivity during resting state in schizophrenia.Eur Arch Psychiatry Clin Neurosci,264(2):111-119.

[33]KongQM,QiaoH,LiuCZ,et al.,2018.Aberrant intrinsic functional connectivity in thalamo-cortical networks in major depressive disorder.CNS Neurosci Ther,24(11):1063-1072.

[34]LenoskiB,BaxterLC,KaramLJ,et al.,2008.On the perform

[35]ance of autocorrelation estimation algorithms for fMRI analysis.IEEE J Sel Top Signal Process,2(6):828-838.

[36]LindquistMA,XuYT,NebelMB,et al.,2014.Evaluating dynamic bivariate correlations in resting-state fMRI: a comparison study and a new approach.NeuroImage,101:531-546.

[37]LiuF,WangYF,LiML,et al.,2017.Dynamic functional network connectivity in idiopathic generalized epilepsy with generalized tonic-clonic seizure.Hum Brain Mapp,38(2):957-973.

[38]LiuPH,TuHW,ZhangAX,et al.,2021.Brain functional alterations in MDD patients with somatic symptoms: a resting-state fMRI study.J Affect Disord,295:788-796.

[39]LiuX,ZhangNY,ChangC,et al.,2018.Co-activation patterns in resting-state fMRI signals.NeuroImage,180:485-494.

[40]LlinásRR,ParéD,1991.Of dreaming and wakefulness.Neuroscience,44(3):521-535.

[41]LlinásRR,RibaryU,JeanmonodD,et al.,1999.Thalamocortical dysrhythmia: a neurological and neuropsychiatric syndrome characterized by magnetoencephalography.Proc Natl Acad Sci USA,96(26):15222-15227.

[42]LlinásRR,UrbanoFJ,LeznikE,et al.,2005.Rhythmic and dysrhythmic thalamocortical dynamics: GABA systems and the edge effect.Trends Neurosci,28(6):325-333.

[43]LongYC,CaoHY,YanCG,et al.,2020.Altered resting-state dynamic functional brain networks in major depressive disorder: findings from the REST-meta-MDD consortium.NeuroImage Clin,26:102163.

[44]LuFM,ChenYC,CuiQ,et al.,2023.Shared and distinct patterns of dynamic functional connectivity variability of thalamo-cortical circuit in bipolar depression and major depressive disorder.Cereb Cortex,33(11):6681-6692.

[45]LuiS,WuQZ,QiuLH,et al.,2011.Resting-state functional connectivity in treatment-resistant depression.Am J Psychiatry,168(6):642-648.

[46]LundTE,MadsenKH,SidarosK,et al.,2006.Non-white noise in fMRI: does modelling have an impact?NeuroImage,29(1):54-66.

[47]McLeodKR,LangevinLM,GoodyearBG,et al.,2014.Functional connectivity of neural motor networks is disrupted in children with developmental coordination disorder and attention-deficit/hyperactivity disorder.NeuroImage Clin,4:566-575.

[48]MillerKD,PintoDJ,SimonsDJ,2001.Processing in layer 4 of the neocortical circuit: new insights from visual and somatosensory cortex.Curr Opin Neurobiol,11(4):‍488-497.

[49]MurataY,ColonneseMT,2018.Thalamus controls development and expression of arousal states in visual cortex.J Neurosci,38(41):8772-8786.

[50]OtteC,GoldSM,PenninxBW,et al.,2016.Major depressive disorder.Nat Rev Dis Primers,2:16065.

[51]PrattJA,MorrisBJ,2015.The thalamic reticular nucleus: a functional hub for thalamocortical network dysfunction in schizophrenia and a target for drug discovery.J Psychopharmacol,29(2):127-137.

[52]PurdonPL,WeisskoffRM,1998.Effect of temporal autocorrelation due to physiological noise and stimulus paradigm on voxel-level false-positive rates in fMRI.Hum Brain Mapp,6(4):239-249.

[53]RosenAFG,RoalfDR,RuparelK,et al.,2018.Quantitative assessment of structural image quality.NeuroImage,169:407-418.

[54]SaalmannYB,2014.Intralaminar and medial thalamic influence on cortical synchrony, information transmission and cognition.Front Syst Neurosci,8:83.

[55]SacchetMD,HoTC,ConnollyCG,et al.,2016.Large-scale hypoconnectivity between resting-state functional networks in unmedicated adolescent major depressive disorder.Neuropsychopharmacology,41(12):2951-2960.

[56]SanacoraG,TreccaniG,PopoliM,2012.Towards a glutamate hypothesis of depression: an emerging frontier of neuropsychopharmacology for mood disorders.Neuropharmacology,62(1):63-77.

[57]SchaeferA,KongR,GordonEM,et al.,2018.Local-global parcellation of the human cerebral cortex from intrinsic functional connectivity MRI.Cereb Cortex,28(9):‍3095-3114.

[58]SendiMSE,ZendehrouhE,SuiJ,et al.,2021.Abnormal dynamic functional network connectivity estimated from default mode network predicts symptom severity in major depressive disorder.Brain Connect,11(10):838-849.

[59]ShermanSM,2007.The thalamus is more than just a relay.Curr Opin Neurobiol,17(4):417-422.

[60]ShineJM,2019.Neuromodulatory influences on integration and segregation in the brain.Trends Cogn Sci,23(7):‍572-583.

[61]SteinerL,FederspielA,SlavovaN,et al.,2020.Functional topography of the thalamo-cortical system during development and its relation to cognition.NeuroImage,223:117361.

[62]SteriadeM,2001.Impact of network activities on neuronal properties in corticothalamic systems.J Neurophysiol,86(1):1-39.

[63]SunWZ,TanZC,MenshBD,et al.,2016.Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs.Nat Neurosci,19(2):308-315.

[64]Sweeney-ReedCM,BuentjenL,VogesJ,et al.,2021.The role of the anterior nuclei of the thalamus in human memory processing.Neurosci Biobehav Rev,126:146-158.

[65]TadayonnejadR,YangSL,KumarA,et al.,2015.Clinical, cognitive, and functional connectivity correlations of resting-state intrinsic brain activity alterations in unmedicated depression.J Affect Disord,172:241-250.

[66]VaccarinoAL,SillsTL,EvansKR,et al.,2009.Multiple pain complaints in patients with major depressive disorder.Psychosom Med,71(2):159-162.

[67]WangR,LiuMX,ChengXH,et al.,2021.Segregation, integration, and balance of large-scale resting brain networks configure different cognitive abilities.Proc Natl Acad Sci USA,118(23):e2022288118.

[68]WeelandCJ,VriendC,van der WerfY,et al.,2022a.Thalamic subregions and obsessive-compulsive symptoms in 2,500 children from the general population.J Am Acad Child Adolesc Psychiatry,61(2):321-330.

[69]WeelandCJ,KasprzakS,de JoodeNT,et al.,2022b.The thalamus and its subnuclei—a gateway to obsessive-compulsive disorder.Transl Psychiatry,12:70.

[70]WeiQ,BaiTJ,BrownEC,et al.,2020.Thalamocortical connectivity in electroconvulsive therapy for major depressive disorder.J Affect Disord,264:163-171.

[71]WilliamsJBW,1988.A structured interview guide for the Hamilton Depression Rating Scale.Arch Gen Psychiatry,45(8):742-747.

[72]WuXR,KongXZ,VatanseverD,et al.,2022.Dynamic changes in brain lateralization correlate with human cognitive performance.PLoS Biol,20(3):e3001560.

[73]XueSW,WangD,TanZ,et al.,2019.Disrupted brain entropy and functional connectivity patterns of thalamic subregions in major depressive disorder.Neuropsychiatr Dis Treat,15:2629-2638.

[74]YanCG,ZangYF,2010.DPARSF: a MATLAB toolbox for “pipeline” data analysis of resting-state fMRI.Front Syst Neurosci,4:13.

[75]YaoZJ,ShiJ,ZhangZ,et al.,2019a.Altered dynamic functional connectivity in weakly-connected state in major depressive disorder.Clin Neurophysiol,130(11):2096-2104.

[76]YaoZJ,ZouY,ZhengWH,et al.,2019b.Structural alterations of the brain preceded functional alterations in major depressive disorder patients: evidence from multimodal connectivity.J Affect Disord,253:107-117.

[77]YuYM,ZhengWH,TanXF,et al.,2021.Microstructural profiles of thalamus and thalamocortical connectivity in patients with disorder of consciousness.J Neurosci Res,99(12):3261-3273.

[78]YuanR,DiX,TaylorPA,et al.,2016.Functional topography of the thalamocortical system in human.Brain Struct Funct,221(4):1971-1984.

[79]ZhangDY,SnyderAZ,ShimonyJS,et al.,2010.Noninvasive functional and structural connectivity mapping of the human thalamocortical system.Cereb Cortex,20(5):‍1187-1194.

[80]ZhaoZY,ZhangYH,ChenN,et al.,2022.Altered temporal reachability highlights the role of sensory perception systems in major depressive disorder.Prog Neuropsychopharmacol Biol Psychiatry,112:110426.

[81]ZhengWH,TanXF,LiuTT,et al.,2021.Individualized thalamic parcellation reveals alterations in shape and microstructure of thalamic nuclei in patients with disorder of consciousness.Cereb Cortex Commun,2(2):tgab024.

[82]ZhiDM,CalhounVD,LvLX,et al.,2018.Aberrant dynamic functional network connectivity and graph properties in major depressive disorder.Front Psychiatry,9:339.

[83]ZhuFR,LiuF,GuoWB,et al.,2018.Disrupted asymmetry of inter- and intra-hemispheric functional connectivity in patients with drug-naive, first-episode schizophrenia and their unaffected siblings.eBioMedicine,36:429-435.

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