The development of brain functional connectivity networks revealed by resting-state functional magnetic resonance imaging
|
摘要
Previous studies on brain functional connectivity networks in children have mainly focused on changes in function in specific brain regions, as opposed to whole brain connectivity in healthy children. By analyzing the independent components of activation and network connectivity between brain regions, we examined brain activity status and development trends in children aged 3 and 5 years. These data could provide a reference for brain function rehabilitation in children with illness or abnormal function. We acquired functional magnetic resonance images from 15 3-year-old children and 15 5-year-old children under natural sleep conditions. The participants were recruited from five kindergartens in the Nanshan District of Shenzhen City, China. The parents of the participants signed an informed consent form with the premise that they had been fully informed regarding the experimental protocol. We used masked independent component analysis and BrainNet Viewer software to explore the independent components of the brain and correlation connections between brain regions. We identified seven independent components in the two groups of children, including the executive control network, the dorsal attention network, the default mode network, the left frontoparietal network, the right frontoparietal network, the salience network, and the motor network. In the default mode network, the posterior cingulate cortex, medial frontal gyrus, and inferior parietal lobule were activated in both 3-and 5-year-old children, supporting the "three-brain region theory" of the default mode network. In the frontoparietal network, the frontal and parietal gyri were activated in the two groups of children, and functional connectivity was strengthened in 5-year-olds compared with 3-year-olds, although the nodes and network connections were not yet mature. The high-correlation network connections in the default mode networks and dorsal attention networks had been significantly strengthened in 5-year-olds vs. 3-year-olds. Further, the salience network in the 3-year-old children included an activated insula/inferior frontal gyrus-anterior cingulate cortex network circuit and an activated thalamus-parahippocampal-posterior cingulate cortex-subcortical regions network circuit. By the age of 5 years, nodes and high-correlation network connections(edges) were reduced in the salience network. Overall, activation of the dorsal attention network, default mode network, left frontoparietal network, and right frontoparietal network increased(the volume of activation increased, the signals strengthened, and the high-correlation connections increased and strengthened) in 5-year-olds compared with 3-year-olds, but activation in some brain nodes weakened or disappeared in the salience network, and the network connections(edges) were reduced. Between the ages of 3 and 5 years, we observed a tendency for function in some brain regions to be strengthened and for the generalization of activation to be reduced, indicating that specialization begins to develop at this time. The study protocol was approved by the local ethics committee of the Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences in China with approval No. SIAT-IRB-131115-H0075 on November 15, 2013.
Previous studies on brain functional connectivity networks in children have mainly focused on changes in function in specific brain regions, as opposed to whole brain connectivity in healthy children. By analyzing the independent components of activation and network connectivity between brain regions, we examined brain activity status and development trends in children aged 3 and 5 years. These data could provide a reference for brain function rehabilitation in children with illness or abnormal function. We acquired functional magnetic resonance images from 15 3-year-old children and 15 5-year-old children under natural sleep conditions. The participants were recruited from five kindergartens in the Nanshan District of Shenzhen City, China. The parents of the participants signed an informed consent form with the premise that they had been fully informed regarding the experimental protocol. We used masked independent component analysis and BrainNet Viewer software to explore the independent components of the brain and correlation connections between brain regions. We identified seven independent components in the two groups of children, including the executive control network, the dorsal attention network, the default mode network, the left frontoparietal network, the right frontoparietal network, the salience network, and the motor network. In the default mode network, the posterior cingulate cortex, medial frontal gyrus, and inferior parietal lobule were activated in both 3-and 5-year-old children, supporting the "three-brain region theory" of the default mode network. In the frontoparietal network, the frontal and parietal gyri were activated in the two groups of children, and functional connectivity was strengthened in 5-year-olds compared with 3-year-olds, although the nodes and network connections were not yet mature. The high-correlation network connections in the default mode networks and dorsal attention networks had been significantly strengthened in 5-year-olds vs. 3-year-olds. Further, the salience network in the 3-year-old children included an activated insula/inferior frontal gyrus-anterior cingulate cortex network circuit and an activated thalamus-parahippocampal-posterior cingulate cortex-subcortical regions network circuit. By the age of 5 years, nodes and high-correlation network connections(edges) were reduced in the salience network. Overall, activation of the dorsal attention network, default mode network, left frontoparietal network, and right frontoparietal network increased(the volume of activation increased, the signals strengthened, and the high-correlation connections increased and strengthened) in 5-year-olds compared with 3-year-olds, but activation in some brain nodes weakened or disappeared in the salience network, and the network connections(edges) were reduced. Between the ages of 3 and 5 years, we observed a tendency for function in some brain regions to be strengthened and for the generalization of activation to be reduced, indicating that specialization begins to develop at this time. The study protocol was approved by the local ethics committee of the Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences in China with approval No. SIAT-IRB-131115-H0075 on November 15, 2013.
Previous studies on brain functional connectivity networks in children have mainly focused on changes in function in specific brain regions, as opposed to whole brain connectivity in healthy children. By analyzing the independent components of activation and network connectivity between brain regions, we examined brain activity status and development trends in children aged 3 and 5 years. These data could provide a reference for brain function rehabilitation in children with illness or abnormal function. We acquired functional magnetic resonance images from 15 3-year-old children and 15 5-year-old children under natural sleep conditions. The participants were recruited from five kindergartens in the Nanshan District of Shenzhen City, China. The parents of the participants signed an informed consent form with the premise that they had been fully informed regarding the experimental protocol. We used masked independent component analysis and BrainNet Viewer software to explore the independent components of the brain and correlation connections between brain regions. We identified seven independent components in the two groups of children, including the executive control network, the dorsal attention network, the default mode network, the left frontoparietal network, the right frontoparietal network, the salience network, and the motor network. In the default mode network, the posterior cingulate cortex, medial frontal gyrus, and inferior parietal lobule were activated in both 3-and 5-year-old children, supporting the "three-brain region theory" of the default mode network. In the frontoparietal network, the frontal and parietal gyri were activated in the two groups of children, and functional connectivity was strengthened in 5-year-olds compared with 3-year-olds, although the nodes and network connections were not yet mature. The high-correlation network connections in the default mode networks and dorsal attention networks had been significantly strengthened in 5-year-olds vs. 3-year-olds. Further, the salience network in the 3-year-old children included an activated insula/inferior frontal gyrus-anterior cingulate cortex network circuit and an activated thalamus-parahippocampal-posterior cingulate cortex-subcortical regions network circuit. By the age of 5 years, nodes and high-correlation network connections(edges) were reduced in the salience network. Overall, activation of the dorsal attention network, default mode network, left frontoparietal network, and right frontoparietal network increased(the volume of activation increased, the signals strengthened, and the high-correlation connections increased and strengthened) in 5-year-olds compared with 3-year-olds, but activation in some brain nodes weakened or disappeared in the salience network, and the network connections(edges) were reduced. Between the ages of 3 and 5 years, we observed a tendency for function in some brain regions to be strengthened and for the generalization of activation to be reduced, indicating that specialization begins to develop at this time. The study protocol was approved by the local ethics committee of the Shenzhen Institute of Advanced Technology, Chinese Academy of Sciences in China with approval No. SIAT-IRB-131115-H0075 on November 15, 2013.
引文
Bi XA,Zhao J,Xu Q,Sun Q,Wang Z(2018)Abnormal functional connectivity of resting state network detection based on linear ica analysis in autism spectrum disorder.Front Physiol 9:475.
Biswal B,Yetkin FZ,Haughton VM,Hyde JS(1995)Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.Magn Reson Med 34:537-541.
Buclkner RL,Andrews-Hanna JR,Schacter DL(2008)The brain's default network:anatomy,function,and relevance to disease.Ann N Y Acad Sci U S A1124:1-38.
Corbetta M,Shulman GL(2002)Control of goal-directed and stimulus-driven attention in the brain.Nat Rev Neurosci 3:201-215.
Cox RW(2012)AFNI:what a long strange trip it's been.Neuroimage 62:743-747.
Damaraju E,Caprihan A,Lowe JR,Allen EA,Calhoun VD,Phillips JP(2014)Functional connectivity in the developing brain:a longitudinal study from 4to 9 months of age.Neuroimage 84:169-180.
de Bie HM,Boersma M,Adriaanse S,Veltman DJ,Wink AM,Roosendaal SD,Barkhof F,Stam CJ,Oostrom KJ,Delemarre-van de Waal HA,Sanz-Arigita EJ(2012)Resting-state networks in awake five-to eight-year old children.Hum Brain Mapp 33:1189-1201.
Deng Z,Chandrasekaran B,Wang S,Wong PC(2016)Resting-state low-frequency fluctuations reflect individual differences in spoken language learning.Cortex 76:63-78.
Doria V,Beckmann CF,Arichi T,Merchant N,Groppo M,Turkheimer FE,Counsell SJ,Murgasova M,Aljabar p,Nunes RG,Larkman DJ,Rees G,Edwards AD(2010)Emergence of resting state networks in the preterm human brain.Proc Natl Acad Sci U S A 107:20015-20020.
Dosenbach NU,Fair DA,Miezin FM,Cohen AL,Wenger KK,Dosenbach RA,Fox MD,Snyder AZ,Vincent JL,Raichle ME,Schlaggar BL,Petersen SE(2007)Distinct brain networks for adaptive and stable task control in humans.Proc Natl Acad Sci U S A 104:11073-11078.
Fair DA,Cohen AL,Dosenbach NU,Church JA,Miezin FM,Barch DM,Raichle ME,Petersen SE,Schlaggar BL(2008)The maturing architecture of the brain's default network.Proc Natl Acad Sci U S A 105:4028-4032.
Farrant K,Uddin LQ(2015)Asymmetric development of dorsal and ventral attention networks in the human brain.Dev Cogn Neurosci 12:165-174.
Fox MD,Snyder AZ,Vincent JL,Corbetta M,Van Essen DC,Raichle ME(2005)The human brain is intrinsically organized into dynamic,anticorrelated functional networks.Proc Natl Acad Sci U S A 102:9673-9678.
Gao W,Zhu H,Giovanello KS,Smith JK,Shen D,Gilmore JH,Lin W(2009)Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects.Proc Natl Acad Sci U S A 106:6790-6795.
Gomot M,Bernard FA,Davis MH,Belmonte MK,Ashwin C,Bullmore ET,Baron-Cohen S(2006)Change detection in children with autism:an auditory event-related fMRI study.Neuroimage 29:475-484.
Grossmann T,Striano T,Friederici AD(2007)Developmental changes in infants'processing of happy and angry facial expressions:a neurobehavioral study.Brain Cogn 64:30-41.
Jafri MJ,Pearlson GD,Stevens M,Calhoun VD(2008)A method for functional network connectivity among spatially independent resting-state components in schizophrenia.Neuroimage 39:1666-1681.
Jiang P,Vuontela V,Tokariev M,Lin H,Aronen ET,Ma Y,Carlson S(2018)Functional connectivity of intrinsic cognitive networks during resting state and task performance in preadolescent children.PLoS One 13:e0205690.
Konishi Y,Taga G,Yamada H,Hirasawa K(2002)Functional brain imaging using fMRI and optical topography in infancy.Sleep Med 3:S41-S43.
Lee MH,Smyser CD,Shimony JS(2013)Resting-state fMRI:a review of methods and clinical applications.AJNR Am J Neuroradiol 34:1866-1872.
Lenneberg EH(1967)Biological Foundation of Language.New York:Wiley,USA.
Lin W,Wu H,Liu Y,Lv D,Yang L(2017)A CCA and ICA-based mixture model for identifying major depression disorder.IEEE Trans Med Imaging 36:745-756.
Margolis AE,Pagliaccio D,Thomas L,Banker S,Marsh R(2018)Salience network connectivity and social processing in children with nonverbal learning disability or autism spectrum disorder.Neuropsychology doi:10.1037/neu0000494.
Moher Alsady T,Blessing EM,Beissner F(2016)MICA-A toolbox for masked independent component analysis of fMRI data.Hum Brain Mapp 37:3544-3556.
Mostert JC,Shumskaya E,Mennes M,Onnink AM,Hoogman M,Kan CC,Arias Vasquez A,Buitelaar J,Franke B,Norris DG(2016)Characterising resting-state functional connectivity in a large sample of adults with ADHD.Prog Neuropsychopharmacol Biol Psychiatry 67:82-91.
Muetzel RL,Blanken LM,Thijssen S,van der Lugt A,Jaddoe VW,Verhulst FC,Tiemeier H,White T(2016)Resting-state networks in 6-to-10 year old children.Hum Brain Mapp 37:4286-4300.
Nomi JS,Uddin LQ(2015)Developmental changes in large-scale network connectivity in autism.Neuroimage Clin 7:732-741.
Penfield W,Roberts L(1959)Speech and Brain Mechanisms.New Jersey:Princeton University Press,USA.
Raichle ME(2015)The brain's default mode network.Annu Rev Neurosci38:433-447.
Raichle ME,MacLeod AM,Snyder AZ,Powers WJ,Gusnard DA,Shulman GL(2001)A default mode of brain function.Proc Natl Acad Sci U S A 98:676-682.
Rohr CS,Arora A,Cho IYK,Katlariwala P,Dimond D,Dewey D,Bray S(2018)Functional network integration and attention skills in young children.Dev Cogn Neurosci 30:200-211.
Thomason ME,Dennis EL,Joshi AA,Joshi SH,Dinov ID,Chang C,Henry ML,Johnson RF,Thompson PM,Toga AW,Glover GH,Van Horn JD,Gotlib IH(2011)Resting-state fMRI can reliably map neural networks in children.Neuroimage 55:165-175.
Wang Y,Li Y,Wang H,Chen Y,Huang W(2017)Altered default mode network on resting-state fmri in children with infantile spasms.Front Neurol 8:209.
Xia M,Wang J,He Y(2013)BrainNet Viewer:a network visualization tool for human brain connectomics.PLoS One 8:e68910.
Xiao Y,Zhai H,Friederici AD,Jia F(2016)The development of the intrinsic functional connectivity of default network subsystems from age 3 to 5.Brain Imaging Behav 10:50-59.
Zhang H,Zuo XN,Ma SY,Zang YF,Milham MP,Zhu CZ(2010)Subject order-independent group ICA(SOI-GICA)for functional MRI data analysis.Neuroimage 51:1414-1424.
Biswal B,Yetkin FZ,Haughton VM,Hyde JS(1995)Functional connectivity in the motor cortex of resting human brain using echo-planar MRI.Magn Reson Med 34:537-541.
Buclkner RL,Andrews-Hanna JR,Schacter DL(2008)The brain's default network:anatomy,function,and relevance to disease.Ann N Y Acad Sci U S A1124:1-38.
Corbetta M,Shulman GL(2002)Control of goal-directed and stimulus-driven attention in the brain.Nat Rev Neurosci 3:201-215.
Cox RW(2012)AFNI:what a long strange trip it's been.Neuroimage 62:743-747.
Damaraju E,Caprihan A,Lowe JR,Allen EA,Calhoun VD,Phillips JP(2014)Functional connectivity in the developing brain:a longitudinal study from 4to 9 months of age.Neuroimage 84:169-180.
de Bie HM,Boersma M,Adriaanse S,Veltman DJ,Wink AM,Roosendaal SD,Barkhof F,Stam CJ,Oostrom KJ,Delemarre-van de Waal HA,Sanz-Arigita EJ(2012)Resting-state networks in awake five-to eight-year old children.Hum Brain Mapp 33:1189-1201.
Deng Z,Chandrasekaran B,Wang S,Wong PC(2016)Resting-state low-frequency fluctuations reflect individual differences in spoken language learning.Cortex 76:63-78.
Doria V,Beckmann CF,Arichi T,Merchant N,Groppo M,Turkheimer FE,Counsell SJ,Murgasova M,Aljabar p,Nunes RG,Larkman DJ,Rees G,Edwards AD(2010)Emergence of resting state networks in the preterm human brain.Proc Natl Acad Sci U S A 107:20015-20020.
Dosenbach NU,Fair DA,Miezin FM,Cohen AL,Wenger KK,Dosenbach RA,Fox MD,Snyder AZ,Vincent JL,Raichle ME,Schlaggar BL,Petersen SE(2007)Distinct brain networks for adaptive and stable task control in humans.Proc Natl Acad Sci U S A 104:11073-11078.
Fair DA,Cohen AL,Dosenbach NU,Church JA,Miezin FM,Barch DM,Raichle ME,Petersen SE,Schlaggar BL(2008)The maturing architecture of the brain's default network.Proc Natl Acad Sci U S A 105:4028-4032.
Farrant K,Uddin LQ(2015)Asymmetric development of dorsal and ventral attention networks in the human brain.Dev Cogn Neurosci 12:165-174.
Fox MD,Snyder AZ,Vincent JL,Corbetta M,Van Essen DC,Raichle ME(2005)The human brain is intrinsically organized into dynamic,anticorrelated functional networks.Proc Natl Acad Sci U S A 102:9673-9678.
Gao W,Zhu H,Giovanello KS,Smith JK,Shen D,Gilmore JH,Lin W(2009)Evidence on the emergence of the brain's default network from 2-week-old to 2-year-old healthy pediatric subjects.Proc Natl Acad Sci U S A 106:6790-6795.
Gomot M,Bernard FA,Davis MH,Belmonte MK,Ashwin C,Bullmore ET,Baron-Cohen S(2006)Change detection in children with autism:an auditory event-related fMRI study.Neuroimage 29:475-484.
Grossmann T,Striano T,Friederici AD(2007)Developmental changes in infants'processing of happy and angry facial expressions:a neurobehavioral study.Brain Cogn 64:30-41.
Jafri MJ,Pearlson GD,Stevens M,Calhoun VD(2008)A method for functional network connectivity among spatially independent resting-state components in schizophrenia.Neuroimage 39:1666-1681.
Jiang P,Vuontela V,Tokariev M,Lin H,Aronen ET,Ma Y,Carlson S(2018)Functional connectivity of intrinsic cognitive networks during resting state and task performance in preadolescent children.PLoS One 13:e0205690.
Konishi Y,Taga G,Yamada H,Hirasawa K(2002)Functional brain imaging using fMRI and optical topography in infancy.Sleep Med 3:S41-S43.
Lee MH,Smyser CD,Shimony JS(2013)Resting-state fMRI:a review of methods and clinical applications.AJNR Am J Neuroradiol 34:1866-1872.
Lenneberg EH(1967)Biological Foundation of Language.New York:Wiley,USA.
Lin W,Wu H,Liu Y,Lv D,Yang L(2017)A CCA and ICA-based mixture model for identifying major depression disorder.IEEE Trans Med Imaging 36:745-756.
Margolis AE,Pagliaccio D,Thomas L,Banker S,Marsh R(2018)Salience network connectivity and social processing in children with nonverbal learning disability or autism spectrum disorder.Neuropsychology doi:10.1037/neu0000494.
Moher Alsady T,Blessing EM,Beissner F(2016)MICA-A toolbox for masked independent component analysis of fMRI data.Hum Brain Mapp 37:3544-3556.
Mostert JC,Shumskaya E,Mennes M,Onnink AM,Hoogman M,Kan CC,Arias Vasquez A,Buitelaar J,Franke B,Norris DG(2016)Characterising resting-state functional connectivity in a large sample of adults with ADHD.Prog Neuropsychopharmacol Biol Psychiatry 67:82-91.
Muetzel RL,Blanken LM,Thijssen S,van der Lugt A,Jaddoe VW,Verhulst FC,Tiemeier H,White T(2016)Resting-state networks in 6-to-10 year old children.Hum Brain Mapp 37:4286-4300.
Nomi JS,Uddin LQ(2015)Developmental changes in large-scale network connectivity in autism.Neuroimage Clin 7:732-741.
Penfield W,Roberts L(1959)Speech and Brain Mechanisms.New Jersey:Princeton University Press,USA.
Raichle ME(2015)The brain's default mode network.Annu Rev Neurosci38:433-447.
Raichle ME,MacLeod AM,Snyder AZ,Powers WJ,Gusnard DA,Shulman GL(2001)A default mode of brain function.Proc Natl Acad Sci U S A 98:676-682.
Rohr CS,Arora A,Cho IYK,Katlariwala P,Dimond D,Dewey D,Bray S(2018)Functional network integration and attention skills in young children.Dev Cogn Neurosci 30:200-211.
Thomason ME,Dennis EL,Joshi AA,Joshi SH,Dinov ID,Chang C,Henry ML,Johnson RF,Thompson PM,Toga AW,Glover GH,Van Horn JD,Gotlib IH(2011)Resting-state fMRI can reliably map neural networks in children.Neuroimage 55:165-175.
Wang Y,Li Y,Wang H,Chen Y,Huang W(2017)Altered default mode network on resting-state fmri in children with infantile spasms.Front Neurol 8:209.
Xia M,Wang J,He Y(2013)BrainNet Viewer:a network visualization tool for human brain connectomics.PLoS One 8:e68910.
Xiao Y,Zhai H,Friederici AD,Jia F(2016)The development of the intrinsic functional connectivity of default network subsystems from age 3 to 5.Brain Imaging Behav 10:50-59.
Zhang H,Zuo XN,Ma SY,Zang YF,Milham MP,Zhu CZ(2010)Subject order-independent group ICA(SOI-GICA)for functional MRI data analysis.Neuroimage 51:1414-1424.