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Published in: Brain Structure and Function 6/2022

06-06-2022 | Original Article

Functional individual variability development of the neonatal brain

Authors: Wenjian Gao, Ziyi Huang, Wenfei Ou, Xiaoqian Tang, Wanying Lv, Jingxin Nie

Published in: Brain Structure and Function | Issue 6/2022

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Abstract

Individual variability in cognition and behavior results from the differences in brain structure and function that have already emerged before birth. However, little is known about individual variability in brain functional architecture at local level in neonates which is of great significance to explore owing to largely undeveloped long-range functional connectivity and segregated functions in early brain development. To address this, resting-state fMRI data of 163 neonates ranged from 32 to 45 postconceptional weeks (PCW) were used in this study, and various functional features including functional parcellation similarity, local brain activity and local functional connectivity were used to characterize individual functional variability. We observed significantly higher local functional individual variability in superior parietal, sensorimotor, and visual cortex, and lower variability in the frontal, insula and cingulate cortex relative to other regions within each hemisphere. The mean local functional individual variability significantly increased with age, and the age effect was found larger in brain regions such as the occipital, temporal, prefrontal and parietal cortex. Our findings promote the understanding of brain plasticity and regional differential maturation in the early stage.
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Literature
go back to reference Batalle D, Edwards AD, O’Muircheartaigh J (2018) Annual research review: not just a small adult brain: understanding later neurodevelopment through imaging the neonatal brain. J Child Psychol Psychiatry 59(4):350–371PubMedCrossRef Batalle D, Edwards AD, O’Muircheartaigh J (2018) Annual research review: not just a small adult brain: understanding later neurodevelopment through imaging the neonatal brain. J Child Psychol Psychiatry 59(4):350–371PubMedCrossRef
go back to reference Boerwinkle VL, Cediel EG, Mirea L, Williams K, Kerrigan JF, Lam S et al (2019) Network-targeted approach and postoperative resting-state functional magnetic resonance imaging are associated with seizure outcome. Ann Neurol 86(3):344–356PubMedCrossRef Boerwinkle VL, Cediel EG, Mirea L, Williams K, Kerrigan JF, Lam S et al (2019) Network-targeted approach and postoperative resting-state functional magnetic resonance imaging are associated with seizure outcome. Ann Neurol 86(3):344–356PubMedCrossRef
go back to reference Bouyssi-Kobar M, De Asis-Cruz J, Murnick J, Chang T, Limperopoulos C (2019) Altered functional brain network integration, segregation, and modularity in infants born very preterm at term-equivalent age. J Pediatr 213(13–21):e11 Bouyssi-Kobar M, De Asis-Cruz J, Murnick J, Chang T, Limperopoulos C (2019) Altered functional brain network integration, segregation, and modularity in infants born very preterm at term-equivalent age. J Pediatr 213(13–21):e11
go back to reference Burkhalter A (1993) Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex 3(5):476–487PubMedCrossRef Burkhalter A (1993) Development of forward and feedback connections between areas V1 and V2 of human visual cortex. Cereb Cortex 3(5):476–487PubMedCrossRef
go back to reference Cao M, He Y, Dai Z, Liao X, Jeon T, Ouyang M et al (2017a) Early development of functional network segregation revealed by connectomic analysis of the preterm human brain. Cereb Cortex 27(3):1949–1963PubMed Cao M, He Y, Dai Z, Liao X, Jeon T, Ouyang M et al (2017a) Early development of functional network segregation revealed by connectomic analysis of the preterm human brain. Cereb Cortex 27(3):1949–1963PubMed
go back to reference Cao M, He Y, Dai Z, Liao X, Jeon T, Ouyang M et al (2017b) Early development of functional network segregation revealed by connectomic analysis of the preterm human brain. Cereb Cortex 27(3):1949–1963PubMed Cao M, He Y, Dai Z, Liao X, Jeon T, Ouyang M et al (2017b) Early development of functional network segregation revealed by connectomic analysis of the preterm human brain. Cereb Cortex 27(3):1949–1963PubMed
go back to reference Craddock RC, James GA, Holtzheimer PE III, Hu XP, Mayberg HS (2012) A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum Brain Mapp 33(8):1914–1928PubMedCrossRef Craddock RC, James GA, Holtzheimer PE III, Hu XP, Mayberg HS (2012) A whole brain fMRI atlas generated via spatially constrained spectral clustering. Hum Brain Mapp 33(8):1914–1928PubMedCrossRef
go back to reference Doria V, Beckmann CF, Arichi T, Merchant N, Groppo M, Turkheimer FE et al (2010) Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci 107(46):20015–20020PubMedPubMedCentralCrossRef Doria V, Beckmann CF, Arichi T, Merchant N, Groppo M, Turkheimer FE et al (2010) Emergence of resting state networks in the preterm human brain. Proc Natl Acad Sci 107(46):20015–20020PubMedPubMedCentralCrossRef
go back to reference Drysdale AT, Grosenick L, Downar J, Dunlop K, Mansouri F, Meng Y et al (2017) Resting-state connectivity biomarkers define neurophysiological subtypes of depression. Nat Med 23(1):28–38PubMedCrossRef Drysdale AT, Grosenick L, Downar J, Dunlop K, Mansouri F, Meng Y et al (2017) Resting-state connectivity biomarkers define neurophysiological subtypes of depression. Nat Med 23(1):28–38PubMedCrossRef
go back to reference Fitzgibbon SP, Harrison SJ, Jenkinson M, Baxter L, Robinson EC, Bastiani M et al (2020) The developing Human Connectome Project (dHCP) automated resting-state functional processing framework for newborn infants. Neuroimage 223:117303PubMedCrossRef Fitzgibbon SP, Harrison SJ, Jenkinson M, Baxter L, Robinson EC, Bastiani M et al (2020) The developing Human Connectome Project (dHCP) automated resting-state functional processing framework for newborn infants. Neuroimage 223:117303PubMedCrossRef
go back to reference Gao W, Elton A, Zhu H, Alcauter S, Smith JK, Gilmore JH, Lin W (2014) Intersubject variability of and genetic effects on the brain’s functional connectivity during infancy. J Neurosci 34(34):11288–11296PubMedPubMedCentralCrossRef Gao W, Elton A, Zhu H, Alcauter S, Smith JK, Gilmore JH, Lin W (2014) Intersubject variability of and genetic effects on the brain’s functional connectivity during infancy. J Neurosci 34(34):11288–11296PubMedPubMedCentralCrossRef
go back to reference Gao W, Alcauter S, Elton A, Hernandez-Castillo CR, Smith JK, Ramirez J, Lin W (2015) Functional network development during the first year: relative sequence and socioeconomic correlations. Cereb Cortex 25(9):2919–2928PubMedCrossRef Gao W, Alcauter S, Elton A, Hernandez-Castillo CR, Smith JK, Ramirez J, Lin W (2015) Functional network development during the first year: relative sequence and socioeconomic correlations. Cereb Cortex 25(9):2919–2928PubMedCrossRef
go back to reference Geerligs L, Tsvetanov KA, Henson RN (2017) Challenges in measuring individual differences in functional connectivity using fMRI: the case of healthy aging. Hum Brain Mapp 38(8):4125–4156PubMedPubMedCentralCrossRef Geerligs L, Tsvetanov KA, Henson RN (2017) Challenges in measuring individual differences in functional connectivity using fMRI: the case of healthy aging. Hum Brain Mapp 38(8):4125–4156PubMedPubMedCentralCrossRef
go back to reference Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ et al (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci 107(44):19067–19072PubMedPubMedCentralCrossRef Hagmann P, Sporns O, Madan N, Cammoun L, Pienaar R, Wedeen VJ et al (2010) White matter maturation reshapes structural connectivity in the late developing human brain. Proc Natl Acad Sci 107(44):19067–19072PubMedPubMedCentralCrossRef
go back to reference Horovitz SG, Fukunaga M, de Zwart JA, van Gelderen P, Fulton SC, Balkin TJ, Duyn JH (2008) Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum Brain Mapp 29(6):671–682PubMedCrossRef Horovitz SG, Fukunaga M, de Zwart JA, van Gelderen P, Fulton SC, Balkin TJ, Duyn JH (2008) Low frequency BOLD fluctuations during resting wakefulness and light sleep: a simultaneous EEG-fMRI study. Hum Brain Mapp 29(6):671–682PubMedCrossRef
go back to reference Horovitz SG, Braun AR, Carr WS, Picchioni D, Balkin TJ, Fukunaga M, Duyn JH (2009) Decoupling of the brain’s default mode network during deep sleep. Proc Natl Acad Sci 106(27):11376–11381PubMedPubMedCentralCrossRef Horovitz SG, Braun AR, Carr WS, Picchioni D, Balkin TJ, Fukunaga M, Duyn JH (2009) Decoupling of the brain’s default mode network during deep sleep. Proc Natl Acad Sci 106(27):11376–11381PubMedPubMedCentralCrossRef
go back to reference Huang H, Shu N, Mishra V, Jeon T, Chalak L, Wang ZJ et al (2015) Development of human brain structural networks through infancy and childhood. Cereb Cortex 25(5):1389–1404PubMedCrossRef Huang H, Shu N, Mishra V, Jeon T, Chalak L, Wang ZJ et al (2015) Development of human brain structural networks through infancy and childhood. Cereb Cortex 25(5):1389–1404PubMedCrossRef
go back to reference Keunen K, Counsell SJ, Benders MJ (2017) The emergence of functional architecture during early brain development. Neuroimage 160:2–14PubMedCrossRef Keunen K, Counsell SJ, Benders MJ (2017) The emergence of functional architecture during early brain development. Neuroimage 160:2–14PubMedCrossRef
go back to reference Kostović I, Jovanov-Milošević N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Paper presented at the seminars in fetal and neonatal medicine Kostović I, Jovanov-Milošević N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Paper presented at the seminars in fetal and neonatal medicine
go back to reference Kostović I, Judaš M (2006) Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants. Dev Med Child Neurol 48(5):388–393PubMedCrossRef Kostović I, Judaš M (2006) Prolonged coexistence of transient and permanent circuitry elements in the developing cerebral cortex of fetuses and preterm infants. Dev Med Child Neurol 48(5):388–393PubMedCrossRef
go back to reference Liu W-C, Flax JF, Guise KG, Sukul V, Benasich AA (2008) Functional connectivity of the sensorimotor area in naturally sleeping infants. Brain Res 1223:42–49PubMedCrossRef Liu W-C, Flax JF, Guise KG, Sukul V, Benasich AA (2008) Functional connectivity of the sensorimotor area in naturally sleeping infants. Brain Res 1223:42–49PubMedCrossRef
go back to reference Ma L, Tian L, Hu T, Jiang T, Zuo N (2021) Development of individual variability in brain functional connectivity and capability across the adult lifespan. Cereb Cortex 31:3925PubMedCrossRef Ma L, Tian L, Hu T, Jiang T, Zuo N (2021) Development of individual variability in brain functional connectivity and capability across the adult lifespan. Cereb Cortex 31:3925PubMedCrossRef
go back to reference Makropoulos A, Robinson EC, Schuh A, Wright R, Fitzgibbon S, Bozek J et al (2018) The developing human connectome project: a minimal processing pipeline for neonatal cortical surface reconstruction. Neuroimage 173:88–112PubMedCrossRef Makropoulos A, Robinson EC, Schuh A, Wright R, Fitzgibbon S, Bozek J et al (2018) The developing human connectome project: a minimal processing pipeline for neonatal cortical surface reconstruction. Neuroimage 173:88–112PubMedCrossRef
go back to reference Mueller S, Wang D, Fox MD, Yeo BT, Sepulcre J, Sabuncu MR et al (2013) Individual variability in functional connectivity architecture of the human brain. Neuron 77(3):586–595PubMedPubMedCentralCrossRef Mueller S, Wang D, Fox MD, Yeo BT, Sepulcre J, Sabuncu MR et al (2013) Individual variability in functional connectivity architecture of the human brain. Neuron 77(3):586–595PubMedPubMedCentralCrossRef
go back to reference Rajasilta O, Tuulari JJ, Björnsdotter M, Scheinin NM, Lehtola SJ, Saunavaara J et al (2020) Resting-state networks of the neonate brain identified using independent component analysis. Dev Neurobiol 80(3–4):111–125PubMedCrossRef Rajasilta O, Tuulari JJ, Björnsdotter M, Scheinin NM, Lehtola SJ, Saunavaara J et al (2020) Resting-state networks of the neonate brain identified using independent component analysis. Dev Neurobiol 80(3–4):111–125PubMedCrossRef
go back to reference Sepulcre J, Liu H, Talukdar T, Martincorena I, Yeo BT, Buckner RL (2010) The organization of local and distant functional connectivity in the human brain. PLoS Comput Biol 6(6):e1000808PubMedPubMedCentralCrossRef Sepulcre J, Liu H, Talukdar T, Martincorena I, Yeo BT, Buckner RL (2010) The organization of local and distant functional connectivity in the human brain. PLoS Comput Biol 6(6):e1000808PubMedPubMedCentralCrossRef
go back to reference Shi J, Malik J (2000) Normalized cuts and image segmentation. IEEE Trans Pattern Anal Mach Intell 22(8):888–905CrossRef Shi J, Malik J (2000) Normalized cuts and image segmentation. IEEE Trans Pattern Anal Mach Intell 22(8):888–905CrossRef
go back to reference Shi F, Salzwedel AP, Lin W, Gilmore JH, Gao W (2018) Functional brain parcellations of the infant brain and the associated developmental trends. Cereb Cortex 28(4):1358–1368PubMedCrossRef Shi F, Salzwedel AP, Lin W, Gilmore JH, Gao W (2018) Functional brain parcellations of the infant brain and the associated developmental trends. Cereb Cortex 28(4):1358–1368PubMedCrossRef
go back to reference Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62(1):1–35PubMedCrossRef Sidman RL, Rakic P (1973) Neuronal migration, with special reference to developing human brain: a review. Brain Res 62(1):1–35PubMedCrossRef
go back to reference Smyser CD, Snyder AZ, Neil JJ (2011) Functional connectivity MRI in infants: exploration of the functional organization of the developing brain. Neuroimage 56(3):1437–1452PubMedCrossRef Smyser CD, Snyder AZ, Neil JJ (2011) Functional connectivity MRI in infants: exploration of the functional organization of the developing brain. Neuroimage 56(3):1437–1452PubMedCrossRef
go back to reference Smyser CD, Neil JJ (2015) Use of resting-state functional MRI to study brain development and injury in neonates. Paper presented at the Seminars in Perinatology Smyser CD, Neil JJ (2015) Use of resting-state functional MRI to study brain development and injury in neonates. Paper presented at the Seminars in Perinatology
go back to reference Stoecklein S, Hilgendorff A, Li M, Förster K, Flemmer AW, Galiè F et al (2020) Variable functional connectivity architecture of the preterm human brain: impact of developmental cortical expansion and maturation. Proc Natl Acad Sci 117(2):1201–1206PubMedCrossRef Stoecklein S, Hilgendorff A, Li M, Förster K, Flemmer AW, Galiè F et al (2020) Variable functional connectivity architecture of the preterm human brain: impact of developmental cortical expansion and maturation. Proc Natl Acad Sci 117(2):1201–1206PubMedCrossRef
go back to reference Thomason ME, Grove LE, Lozon TA Jr, Vila AM, Ye Y, Nye MJ et al (2015) Age-related increases in long-range connectivity in fetal functional neural connectivity networks in utero. Dev Cogn Neurosci 11:96–104PubMedCrossRef Thomason ME, Grove LE, Lozon TA Jr, Vila AM, Ye Y, Nye MJ et al (2015) Age-related increases in long-range connectivity in fetal functional neural connectivity networks in utero. Dev Cogn Neurosci 11:96–104PubMedCrossRef
go back to reference Vértes PE, Bullmore ET (2015) Annual research review: growth connectomics–the organization and reorganization of brain networks during normal and abnormal development. J Child Psychol Psychiatry 56(3):299–320PubMedCrossRef Vértes PE, Bullmore ET (2015) Annual research review: growth connectomics–the organization and reorganization of brain networks during normal and abnormal development. J Child Psychol Psychiatry 56(3):299–320PubMedCrossRef
go back to reference Wang Q, Xu Y, Zhao T, Xu Z, He Y, Liao X (2021) Individual uniqueness in the neonatal functional connectome. Cereb Cortex 31:3701PubMedCrossRef Wang Q, Xu Y, Zhao T, Xu Z, He Y, Liao X (2021) Individual uniqueness in the neonatal functional connectome. Cereb Cortex 31:3701PubMedCrossRef
go back to reference Xu Y, Cao M, Liao X, Xia M, Wang X, Jeon T et al (2019) Development and emergence of individual variability in the functional connectivity architecture of the preterm human brain. Cereb Cortex 29(10):4208–4222PubMedCrossRef Xu Y, Cao M, Liao X, Xia M, Wang X, Jeon T et al (2019) Development and emergence of individual variability in the functional connectivity architecture of the preterm human brain. Cereb Cortex 29(10):4208–4222PubMedCrossRef
go back to reference Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M et al (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol Yeo BT, Krienen FM, Sepulcre J, Sabuncu MR, Lashkari D, Hollinshead M et al (2011) The organization of the human cerebral cortex estimated by intrinsic functional connectivity. J Neurophysiol
go back to reference Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22(1):394–400PubMedCrossRef Zang Y, Jiang T, Lu Y, He Y, Tian L (2004) Regional homogeneity approach to fMRI data analysis. Neuroimage 22(1):394–400PubMedCrossRef
go back to reference Zang Y, He Y, Zhu C, Cao Q, Sui M-Q, Liang M et al (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 29(2):83–91PubMedCrossRef Zang Y, He Y, Zhu C, Cao Q, Sui M-Q, Liang M et al (2007) Altered baseline brain activity in children with ADHD revealed by resting-state functional MRI. Brain Dev 29(2):83–91PubMedCrossRef
go back to reference Zhang H, Shen D, Lin W (2019) Resting-state functional MRI studies on infant brains: a decade of gap-filling efforts. Neuroimage 185:664–684PubMedCrossRef Zhang H, Shen D, Lin W (2019) Resting-state functional MRI studies on infant brains: a decade of gap-filling efforts. Neuroimage 185:664–684PubMedCrossRef
go back to reference Zhao J, Tang C, Nie J (2020) Functional parcellation of individual cerebral cortex based on functional mri. Neuroinformatics 18(2):295–306PubMedCrossRef Zhao J, Tang C, Nie J (2020) Functional parcellation of individual cerebral cortex based on functional mri. Neuroinformatics 18(2):295–306PubMedCrossRef
go back to reference Zou Q-H, Zhu C-Z, Yang Y, Zuo X-N, Long X-Y, Cao Q-J et al (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172(1):137–141PubMedPubMedCentralCrossRef Zou Q-H, Zhu C-Z, Yang Y, Zuo X-N, Long X-Y, Cao Q-J et al (2008) An improved approach to detection of amplitude of low-frequency fluctuation (ALFF) for resting-state fMRI: fractional ALFF. J Neurosci Methods 172(1):137–141PubMedPubMedCentralCrossRef
go back to reference Zuo X-N, He Y, Betzel RF, Colcombe S, Sporns O, Milham MP (2017) Human connectomics across the life span. Trends Cogn Sci 21(1):32–45PubMedCrossRef Zuo X-N, He Y, Betzel RF, Colcombe S, Sporns O, Milham MP (2017) Human connectomics across the life span. Trends Cogn Sci 21(1):32–45PubMedCrossRef
Metadata
Title
Functional individual variability development of the neonatal brain
Authors
Wenjian Gao
Ziyi Huang
Wenfei Ou
Xiaoqian Tang
Wanying Lv
Jingxin Nie
Publication date
06-06-2022
Publisher
Springer Berlin Heidelberg
Published in
Brain Structure and Function / Issue 6/2022
Print ISSN: 1863-2653
Electronic ISSN: 1863-2661
DOI
https://doi.org/10.1007/s00429-022-02516-8

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