Preterm birth alters neonatal, functional rich club organization

Brain Structure and Function

Volumn 221, Issue 6, 2016, Pages 3211-3222

  Scheinost, Dustin ^a   Kwon, Soo Hyun ^a   Shen, Xilin ^a   Lacadie, Cheryl ^a   Schneider, Karen C ^a   Dai, Feng ^a   Ment, Laura R ^a   Constable, R Todd ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Connectivity; Neonate; Network theory; Preterm birth; Rich club

Indexed keywords

ARTICLE; BIRTH WEIGHT; BRAIN DEVELOPMENT; BRAIN FUNCTION; BRAIN REGION; BRAIN SIZE; CLINICAL ARTICLE; CONNECTOME; CONTROLLED STUDY; FEMALE; FUNCTIONAL MAGNETIC RESONANCE IMAGING; FUNCTIONAL NEUROIMAGING; HUMAN; LUNG DYSPLASIA; MALE; NERVE CELL NETWORK; NEWBORN; NEWBORN SEPSIS; PREMATURE LABOR; PREMATURITY; PRIORITY JOURNAL; RETROLENTAL FIBROPLASIA; RICH CLUB ORGANIZATION; SENSORIMOTOR INTEGRATION; TERM BIRTH; BRAIN; BRAIN MAPPING; IMAGE PROCESSING; NERVE TRACT; NUCLEAR MAGNETIC RESONANCE IMAGING; PATHOPHYSIOLOGY; PROCEDURES;

BRAIN; BRAIN MAPPING; FEMALE; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; INFANT, NEWBORN; INFANT, PREMATURE; MAGNETIC RESONANCE IMAGING; MALE; NEURAL PATHWAYS;

EID: 84940859070     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-015-1096-6     Document Type: Article

References (45)

1. Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26(1):63–72
2. Back SA, Miller SP (2014) Brain injury in premature neonates: a primary cerebral dysmaturation disorder? Ann Neurol 75(4):469–486. doi:10.1002/ana.24132
3. Ball G, Aljabar P, Zebari S, Tusor N, Arichi T, Merchant N, Robinson EC, Ogundipe E, Rueckert D, Edwards AD, Counsell SJ (2014) Rich-club organization of the newborn human brain. Proc Natl Acad Sci USA 111(20):7456–7461. doi:10.1073/pnas.1324118111
4. Bauer SC, Msall ME (2010) Optimizing neurodevelopmental outcomes after prematurity: lessons in neuroprotection and early intervention. Minerva Pediatr 62(5):485–497 (R15103597 [pii])
5. Beck S, Wojdyla D, Say L, Betran AP, Merialdi M, Requejo JH, Rubens C, Menon R, Van Look PF (2010) The worldwide incidence of preterm birth: a systematic review of maternal mortality and morbidity. Bull World Health Organ 88(1):31–38. doi:10.2471/BLT.08.062554
6. Brown CJ, Miller SP, Booth BG, Andrews S, Chau V, Poskitt KJ, Hamarneh G (2014) Structural network analysis of brain development in young preterm neonates. Neuroimage 101:667–680. doi:10.1016/j.neuroimage.2014.07.030
7. Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10(3):186–198. doi:10.1038/nrn2575
8. Cole MW, Reynolds JR, Power JD, Repovs G, Anticevic A, Braver TS (2013) Multi-task connectivity reveals flexible hubs for adaptive task control. Nat Neurosci 16(9):1348–1355. doi:10.1038/nn.3470
9. Colizza V, Flammini A, Serrano MA, Vespignani A (2006) Detecting rich-club ordering in complex networks. Nat Phys 2(2):110–115
10. Constable R.T., Vohr B.R., Scheinost D., Benjamin J.R., Fulbright R.K., Lacadie C., Schneider K.C., Katz K.H., Zhang H., Papademetris X., Ment L.R. A left cerebellar pathway mediates language in prematurely-born young adults. Neuroimage 64(1)2013,pp:371–378.
11. Crossley NA, Mechelli A, Scott J, Carletti F, Fox PT, McGuire P, Bullmore ET (2014) The hubs of the human connectome are generally implicated in the anatomy of brain disorders. Brain 137(Pt 8):2382–2395. doi:10.1093/brain/awu132
12. 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 USA 107(46):20015–20020. doi:10.1073/pnas.1007921107
13. Finn E.S.,Shen X., Holahan J.M., Scheinost D., Lacadie C., Papademetris X., Shaywitz S.E, Shaywitz B.A, Constable R.T. Disruption of functional networks in dyslexia: a whole-brain, data-driven analysis of connectivity.Biological Psychiatry 76(5) 2014,pp.397-404
14. Foster-Cohen SH, Friesen MD, Champion PR, Woodward LJ (2010) High prevalence/low severity language delay in preschool children born very preterm. J Dev Behav Pediatr 31(8):658–667. doi:10.1097/DBP.0b013e3181e5ab7e
15. Gilmore JH, Lin W, Prastawa MW, Looney CB, Vetsa YS, Knickmeyer RC, Evans DD, Smith JK, Hamer RM, Lieberman JA, Gerig G (2007) Regional gray matter growth, sexual dimorphism, and cerebral asymmetry in the neonatal brain. J Neurosci 27(6):1255–1260. doi:10.1523/JNEUROSCI.3339-06.2007
16. Grayson DS, Ray S, Carpenter S, Iyer S, Dias TG, Stevens C, Nigg JT, Fair DA (2014) Structural and functional rich club organization of the brain in children and adults. PLoS One 9(2):e88297. doi:10.1371/journal.pone.0088297
17. Joshi A, Scheinost D, Okuda H, Belhachemi D, Murphy I, Staib LH, Papademetris X (2011) Unified framework for development, deployment and robust testing of neuroimaging algorithms. Neuroinformatics 9(1):69–84. doi:10.1007/s12021-010-9092-8
18. Kim DJ, Davis EP, Sandman CA, Sporns O, O’Donnell BF, Buss C, Hetrick WP (2014) Longer gestation is associated with more efficient brain networks in preadolescent children. Neuroimage 100C:619–627. doi:10.1016/j.neuroimage.2014.06.048
19. Komitova M, Xenos D, Salmaso N, Tran KM, Brand T, Schwartz ML, Ment L, Vaccarino FM (2013) Hypoxia-induced developmental delays of inhibitory interneurons are reversed by environmental enrichment in the postnatal mouse forebrain. J Neurosci 33(33):13375–13387. doi:10.1523/JNEUROSCI.5286-12.2013
20. Kostović I, Jovanov-Milosević N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med 11(6):415–422. doi:10.1016/j.siny.2006.07.001
21. Kwon SH, Scheinost D, Lacadie C, Benjamin J, Myers EH, Qiu M, Schneider KC, Rothman DL, Constable RT, Ment LR (2014a) GABA, resting-state connectivity and the developing brain. Neonatology 106(2):149–155. doi:10.1159/000362433
22. Kwon S.H., Scheinost D., Lacadie C., Sze G., Schneider K.C., Dai F., Constable R.T., Ment L.R.Adaptive mechanisms of developing brain: cerebral lateralization in the prematurely-born.Neuroimage 108C,2015,pp:144–150.
23. Nishida M, Makris N, Kennedy DN, Vangel M, Fischl B, Krishnamoorthy KS, Caviness VS, Grant PE (2006) Detailed semiautomated MRI based morphometry of the neonatal brain: preliminary results. Neuroimage 32(3):1041–1049. doi:10.1016/j.neuroimage.2006.05.020
24. Opsahl T, Colizza V, Panzarasa P, Ramasco JJ (2008) Prominence and control: the weighted rich-club effect. Phys Rev Lett 101(16):168702
25. Pandit AS, Robinson E, Aljabar P, Ball G, Gousias IS, Wang Z, Hajnal JV, Rueckert D, Counsell SJ, Montana G, Edwards AD (2014) Whole-brain mapping of structural connectivity in infants reveals altered connection strength associated with growth and preterm birth. Cereb Cortex 24(9):2324–2333. doi:10.1093/cercor/bht086
26. Pritchard VE, Bora S, Austin NC, Levin KJ, Woodward LJ (2014) Identifying very preterm children at educational risk using a school readiness framework. Pediatrics 134(3):e825–e832. doi:10.1542/peds.2013-3865
27. Ray S, Miller M, Karalunas S, Robertson C, Grayson DS, Cary RP, Hawkey E, Painter JG, Kriz D, Fombonne E, Nigg JT, Fair DA (2014) Structural and functional connectivity of the human brain in autism spectrum disorders and attention-deficit/hyperactivity disorder: a rich club-organization study. Hum Brain Mapp. doi:10.1002/hbm.22603
28. Rubinov M, Sporns O (2010) Complex network measures of brain connectivity: uses and interpretations. Neuroimage 52(3):1059–1069
29. Salvan P, Walsh SF, Allin MP, Walshe M, Murray RM, Bhattacharyya S, McGuire P, Williams SC, Nosarti C (2013) Road work on memory lane-Functional and structural alterations to the learning and memory circuit in adults born very preterm. Neuroimage. doi:10.1016/j.neuroimage.2013.12.031
30. Saunders DE, Thompson C, Gunny R, Jones R, Cox T, Chong WK (2007) Magnetic resonance imaging protocols for paediatric neuroradiology. Pediatr Radiol 37(8):789–797. doi:10.1007/s00247-007-0462-9
31. Scheinost D, Benjamin J, Lacadie CM, Vohr B, Schneider KC, Ment LR, Papademetris X, Constable RT (2012) The intrinsic connectivity distribution: a novel contrast measure reflecting voxel level functional connectivity. Neuroimage. doi:10.1016/j.neuroimage.2012.05.073
32. Scheinost D, Lacadie C, Vohr BR, Schneider KC, Papademetris X, Constable RT, Ment LR (2014) Cerebral lateralization is protective in the very prematurely born. Cereb Cortex. doi:10.1093/cercor/bht430
33. Shen X, Tokoglu F, Papademetris X, Constable RT (2013) Groupwise whole-brain parcellation from resting-state fMRI data for network node identification. Neuroimage 82:403–415. doi:10.1016/j.neuroimage.2013.05.081
34. Smyser CD, Inder TE, Shimony JS, Hill JE, Degnan AJ, Snyder AZ, Neil JJ (2010) longitudinal analysis of neural network development in preterm infants. Cereb Cortex. doi:10.1093/cercor/bhq035
35. Smyser CD, Snyder AZ, Shimony JS, Blazey TM, Inder TE, Neil JJ (2013) Effects of white matter injury on resting state fMRI measures in prematurely born infants. PLoS One 8(7):e68098. doi:10.1371/journal.pone.0068098
36. Smyser CD, Snyder AZ, Shimony JS, Mitra A, Inder TE, Neil JJ (2014) Resting-state network complexity and magnitude are reduced in prematurely born infants. Cereb Cortex. doi:10.1093/cercor/bhu251
37. Spann MN, Bansal R, Rosen TS, Peterson BS (2014) Morphological features of the neonatal brain support development of subsequent cognitive, language, and motor abilities. Hum Brain Mapp 35(9):4459–4474. doi:10.1002/hbm.22487
38. Sporns O (2013) Network attributes for segregation and integration in the human brain. Curr Opin Neurobiol 23(2):162–171. doi:10.1016/j.conb.2012.11.015
39. Towlson EK, Vértes PE, Ahnert SE, Schafer WR, Bullmore ET (2013) The rich club of the C. elegans neuronal connectome. J Neurosci 33(15):6380–6387. doi:10.1523/JNEUROSCI.3784-12.2013
40. van den Heuvel MP, Sporns O (2011) Rich-club organization of the human connectome. J Neurosci 31(44):15775–15786. doi:10.1523/JNEUROSCI.3539-11.2011
41. van den Heuvel MP, Sporns O, Collin G, Scheewe T, Mandl RC, Cahn W, Goni J, Hulshoff Pol HE, Kahn RS (2013) Abnormal rich club organization and functional brain dynamics in schizophrenia. JAMA Psychiatry 70(8):783–792. doi:10.1001/jamapsychiatry.2013.1328
42. van den Heuvel MP, Kersbergen KJ, de Reus MA, Keunen K, Kahn RS, Groenendaal F, de Vries LS, Benders MJ (2014) The neonatal connectome during preterm brain development. Cereb Cortex. doi:10.1093/cercor/bhu095
43. Van Dijk KR, Sabuncu MR, Buckner RL (2012) The influence of head motion on intrinsic functional connectivity MRI. Neuroimage 59(1):431–438. doi:10.1016/j.neuroimage.2011.07.044
44. White TP, Symington I, Castellanos NP, Brittain PJ, Froudist Walsh S, Nam KW, Sato JR, Allin MP, Shergill SS, Murray RM, Williams SC, Nosarti C (2014) Dysconnectivity of neurocognitive networks at rest in very-preterm born adults. Neuroimage Clin 4:352–365. doi:10.1016/j.nicl.2014.01.005
45. Wilke M, Hauser TK, Krageloh-Mann I, Lidzba K (2014) Specific impairment of functional connectivity between language regions in former early preterms. Hum Brain Mapp 35(7):3372–3384. doi:10.1002/hbm.22408