Maturation of preterm newborn brains: a fMRI–DTI study of auditory processing of linguistic stimuli and white matter development

Brain Structure and Function

Volumn 220, Issue 6, 2015, Pages 3733-3751

  Baldoli, Cristina ^a,b   Scola, Elisa ^a,b   Della Rosa, Pasquale Antony ^c   Pontesilli, Silvia ^a,b   Longaretti, Roberta ^a,b   Poloniato, Antonella ^a   Scotti, Roberta ^a,b   Blasi, Valeria ^a,b   Cirillo, Sara ^a,b   Iadanza, Antonella ^a,b   Rovelli, Rosanna ^a   Barera, Graziano ^a   Scifo, Paola ^a,b  

^a SAN RAFFAELE HOSPITAL   (Italy)

^b VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^c INSTITUTE OF MOLECULAR BIOIMAGING AND PHYSIOLOGY   (Italy)

Author keywords

Brain; Development; DTI; fMRI; Preterm; Subplate

Indexed keywords

ARCUATE FASCICULUS; ARTERIAL OXYGEN SATURATION; ARTICLE; ARTIFACT; BOLD SIGNAL; BRAIN MATURATION; CAPSULA INTERNA; CLINICAL ARTICLE; CONTROLLED STUDY; DIFFUSION TENSOR IMAGING; ELECTROENCEPHALOGRAM; EYE HAND COORDINATION; FEMALE; FRACTIONAL ANISOTROPY; FUNCTIONAL MAGNETIC RESONANCE IMAGING; HEARING; HUMAN; IMAGE PROCESSING; IMAGE QUALITY; INFERIOR FRONTAL GYRUS; INFERIOR LONGITUDINAL FASCICULUS; LANGUAGE ABILITY; LANGUAGE TEST; MALE; NEUROPSYCHOLOGICAL TEST; NEWBORN; NUCLEAR MAGNETIC RESONANCE IMAGING; OCCIPITAL CORTEX; PREMATURITY; PRIORITY JOURNAL; SOCIAL EVOLUTION; SUPERIOR LONGITUDINAL FASCICULUS; SUPERIOR TEMPORAL GYRUS; SUPRAMARGINAL GYRUS; THALAMOCORTICAL TRACT; WHITE MATTER; ANATOMY AND HISTOLOGY; AUDITORY STIMULATION; BRAIN; BRAIN MAPPING; DIFFUSION WEIGHTED IMAGING; GROWTH, DEVELOPMENT AND AGING; INFANT; LINGUISTICS; PHYSIOLOGY; SPEECH PERCEPTION;

ACOUSTIC STIMULATION; BRAIN; BRAIN MAPPING; DIFFUSION MAGNETIC RESONANCE IMAGING; DIFFUSION TENSOR IMAGING; FEMALE; HUMANS; INFANT; INFANT, NEWBORN; INFANT, PREMATURE; LINGUISTICS; MALE; NEUROPSYCHOLOGICAL TESTS; SPEECH PERCEPTION; WHITE MATTER;

EID: 84942370461     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-014-0887-5     Document Type: Article

References (97)

1. Altman NR, Bernal B (2001) Brain activation in sedated children: auditory and visual functional MR imaging. Radiology 221(1):56–63
2. Anderson AW, Marois R, Colson ER, Peterson BS, Duncan CC, Ehrenkranz RA, Schneider KC, Gore JC, Ment LR (2001) Neonatal auditory activation detected by functional magnetic resonance imaging. Magn Reson Imaging 19(1):1–5
3. Arichi T, Moraux A, Melendez A, Doria V, Groppo M, Merchant N, Combs S, Burdet E, Larkman DJ, Counsell SJ, Beckmann CF, Edwards AD (2010) Somatosensory cortical activation identified by functional MRI in preterm and term infants. Neuroimage 49(3):2063–2071
4. Arichi T, Fagiolo G, Varela M, Melendez-Calderon A, Allievi A, Merchant N, Tusor N, Counsell SJ, Burdet E, Beckmann CF, Edwards AD (2012) Development of BOLD signal hemodynamic responses in the human brain. Neuroimage 63(2):663–673
5. Aylward GP (2002) Cognitive and neuropsychological outcomes: more than IQ scores. Ment Retard Dev Disabil Res Rev 8(4):234–240
6. Ball G, Srinivasan L, Aljabar P, Counsell SJ, Durighel G, Hajnal JV, Rutherford MA, Edwards AD (2013) Development of cortical microstructure in the preterm human brain. Proc Natl Acad Sci USA 110(23):9541–9546
7. Barre N, Morgan A, Doyle LW, Anderson PJ (2011) Language abilities in children who were very preterm and/or very low birth weight: a meta-analysis. J Pediatr 158(5):766–774
8. Bhutta AT, Cleves MA, Casey PH, Cradock MM, Anand KJ (2002) Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA 288:728–737
9. Brauer J, Neumann J, Friederici AD (2008) Temporal dynamics of perisylvian activation during language processing in children and adults. Neuroimage 41(4):1484–1492
10. Brauer J, Anwander A, Friederici AD (2011) Neuroanatomical prerequisites for language functions in the maturing brain. Cereb Cortex 21(2):459–466
11. Caravale B, Tozzi C, Albino G, Vicari S (2005) Cognitive development in low risk preterm infants at 3–4 years of life. Arch Dis Child Fetal Neonatal Ed 90(6):F474–F479
12. Catani M, Thiebaut de Schotten M (2008) A diffusion tensor imaging tractography atlas for virtual in vivo dissections. Cortex 44:1105–1132
13. Challis JR, Lye SJ, Gibb W, Whittle W, Patel F, Alfaidy N (2001) Understanding preterm labor. Ann NY Acad Sci 943:225–234
14. Chaudhary T, Walch E, Herold B, Metze B, Lejeune A, Burkhardt F, Buhrer C (2013) Predictive and concurrent validity of standardized neurodevelopmental examinations by the Griffiths scales and Bayley scales of infant development II. Klin Padiatr 225(1):8–12
15. Chi JG, Dooling EC, Gilles FH (1977) Gyral development of the human brain. Ann Neurol 1(1):86–93
16. Chugani HT, Phelps ME, Mazziotta JC (1987) Positron emission tomography study of human brain functional development. Ann Neurol 22(4):487–497
17. Dall’oglio AM, Rossiello B, Coletti MF, Bultrini M, De Marchis C, Rava L, Caselli C, Paris S, Cuttini M (2010) Do healthy preterm children need neuropsychological follow-up? Preschool outcomes compared with term peers. Dev Med Child Neurol 52(10):955–961
18. Dehaene-Lambertz G (2000) Cerebral specialization for speech and non-speech stimuli in infants. J Cogn Neurosci 12(3):449–460
19. Dehaene-Lambertz G, Dehaene S, Hertz-Pannier L (2002) Functional neuroimaging of speech perception in infants. Science 298(5600):2013–2015
20. Dehaene-Lambertz G, Pallier C, Serniclaes W, Sprenger-Charolles L, Jobert A, Dehaene S (2005) Neural correlates of switching from auditory to speech perception. Neuroimage 24(1):21–33
21. Dehaene-Lambertz G, Hertz-Pannier L, Dubois J (2006) Nature and nurture in language acquisition: anatomical and functional brain-imaging studies in infants. Trends Neurosci 29(7):367–373
22. Draper ES, Manktelow B, Field DJ, James D (1999) Prediction of survival for preterm births by weight and gestational age: retrospective population based study. BMJ 319(7217):1093–1097
23. Fransson P, Skiöld B, Horsch S, Nordell A, Blennow M, Lagercrantz H, Aden U (2007) Resting-state networks in the infant brain. Proc Natl Acad Sci USA 104(39):15531–15536
24. Fransson P, Skiöld B, Engström M, Hallberg B, Mosskin M, Aden U, Lagercrantz H, Blennow M (2009) Spontaneous brain activity in the newborn brain during natural sleep—an fMRI study in infants born at full term. Pediatr Res 66(3):301–305
25. Fransson P, Aden U, Blennow M, Lagercrantz H (2011) The functional architecture of the infant brain as revealed by resting-state fMRI. Cereb Cortex 21(1):145–154
26. Friederici AD, Brauer J, Lohmann G (2011) Maturation of the language network: from inter- to intrahemispheric connectivities. PLoS ONE 6(6):e20726
27. Friston KJ, Ashburner JT, Kiebel SJ, Nichols TE, Penny WD (2011) Statistical parametric mapping: the analysis of functional brain images. Academic Press, London
28. Gaillard WD, Grandin CB, Xu B (2001) Developmental aspects of pediatric fMRI: considerations for image acquisition, analysis, and interpretation. Neuroimage 13(2):239–249
29. Ghosh A, Shatz CJ (1994) Segregation of geniculocortical afferents during the critical period: a role for subplate neurons. J Neurosci 14(6):3862–3880
30. Graziani LJ, Katz L, Cracco Q, Cracco JB, Weitzman ED (1974) The maturation and interrelationship of EEF patterns and auditory evoked response in premature infants. Electroencephalogr Clin Neurophysiol 36(4):367–375
31. Grimmer I, Metze BC, Walch E, Scholz T, Buhrer C (2010) Predicting neurodevelopmental impairment in preterm infants by standardized neurological assessments at 6 and 12 months corrected age. Acta Paediatr 99(4):526–530
32. Hack M, Flannery DJ, Schluchter M, Cartar L, Borawski E, Klein N (2002) Outcomes in young adulthood for very-low-birth-weight infants. N Engl J Med 346(3):149–157
33. Hermoye L, Saint-Martin C, Cosnard G, Lee SK, Kim J, Nassogne MC, Menten R, Clapuyt P, Donohue PK, Hua K, Wakana S, Jiang H, van Zijl PC, Mori S (2006) Pediatric diffusion tensor imaging: normal database and observation of the white matter maturation in early childhood. Neuroimage 29(2):493–504
34. Holland SK, Vannest J, Mecoli M, Jacola LM, Tillema JM, Karunanayaka PR, Schmithorst VJ, Yuan W, Plante E, Byars AW (2007) Functional MRI of language lateralization during development in children. Int J Audiol 46(9):533–551
35. Hope PL, Gould SJ, Howard S, Hamilton PA, Costello AM, Reynolds EO (1988) Precision of ultrasound diagnosis of pathologically verified lesions in the brains of very preterm infants. Dev Med Child Neurol 30(4):457–471
36. Huang H, Xue R, Zhang J, Ren T, Richards LJ, Yarowsky P, Miller MI, Mori S (2009) Anatomical characterization of human fetal brain development with diffusion tensor magnetic resonance imaging. J Neurosci 29(13):4263–4273
37. Huntley M (1996) The Griffiths Mental Development Scales—Revised: birth to 2 years. Hogrefe, Oxford
38. Huppi PS, Dubois J (2006) Diffusion tensor imaging of brain development. Semin Fetal Neonatal Med 11(6):489–497
39. Huppi PS, Maier SE, Peled S, Zientara GP, Barnes PD, Jolesz FA, Volpe JJ (1998) Microstructural development of human newborn cerebral white matter assessed in vivo by diffusion tensor magnetic resonance imaging. Pediatr Res 44(4):584–590
40. Huppi PS, Murphy B, Maier SE, Zientara GP, Inder TE, Barnes PD, Kikinis R, Jolesz FA, Volpe JJ (2001) Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107(3):455–460
41. Jardri R, Pins D, Houfflin-Debarge V, Chaffiotte C, Rocourt N, Pruvo JP, Steinling M, Delion P, Thomas P (2008) Fetal cortical activation to sound at 33 weeks of gestation: a functional MRI study. Neuroimage 42(1):10–18
42. Judas M, Sedmak G, Kostovic I (2013) The significance of the subplate for evolution and developmental plasticity of the human brain. Front Hum Neurosci 7:423. doi:10.3389/fnhum.2013.00423
43. Kasprian G, Langs G, Brugger PC, Bittner M, Weber M, Arantes M, Prayer D (2011) The prenatal origin of hemispheric asymmetry: an in utero neuroimaging study. Cereb Cortex 21(5):1076–1083
44. Koay CG, Chang LC, Carew JD, Pierpaoli C, Basser PJ (2006) A unifying theoretical and algorithmic framework for least squares methods of estimation in diffusion tensor imaging. J Magn Reson 182(1):115–125
45. Kostovic I, Jovanov-Milosevic N (2006) The development of cerebral connections during the first 20–45 weeks’ gestation. Semin Fetal Neonatal Med 11(6):415–422
46. Kostovic I, Judas M (2010) The development of the subplate and thalamocortical connections in the human foetal brain. Acta Paediatr 99(8):1119–1127
47. Kostovic I, Rakic P (1990) Developmental history of the transient subplate zone in the visual and somatosensory cortex of the macaque monkey and human brain. J Comp Neurol 297(3):441–470
48. Kozberg MG, Chen BR, DeLeo SE, Bouchard MB, Hillman EM (2013) Resolving the transition from negative to positive blood oxygen level-dependent responses in the developing brain. Proc Natl Acad Sci USA 110(11):4380–4385
49. Kuban KC, Leviton A (1994) Cerebral palsy. N Engl J Med 330(3):188–195
50. Kuklisova-Murgasova M, Aljabar P, Srinivasan L, Counsell SJ, Doria V, Serag A, Gousias IS, Boardman JP, Rutherford MA, Edwards AD, Hajnal JV, Rueckert D (2011) A dynamic 4D probabilistic atlas of the developing brain. Neuroimage 54(4):2750–2763
51. Lawrence EJ, McGuire PK, Allin M, Walshe M, Giampietro V, Murray RM, Rifkin L, Nosarti C (2010) The very preterm brain in young adulthood: the neural correlates of verbal paired associate learning. J Pediatr 156:889–895
52. Liu Y, Baleriaux D, Kavec M, Metens T, Absil J, Denolin V, Pardou A, Avni F, Van Bogaert P, Aeby A (2010) Structural asymmetries in motor and language networks in a population of healthy preterm neonates at term equivalent age: a diffusion tensor imaging and probabilistic tractography study. Neuroimage 51(2):783–788
53. Mahmoudzadeh M, Dehaene-Lambertz G, Fournier M, Kongolo G, Goudjil S, Dubois J, Grebe R, Wallois F (2013) Syllabic discrimination in premature human infants prior to complete formation of cortical layers. Proc Natl Acad Sci USA 110(12):4846–4851
54. Marlow N (2004) Neurocognitive outcome after very preterm birth. Arch Dis Child Fetal Neonatal Ed 89(3):F224–F228
55. Ment LR, Vohr B, Allan W, Katz KH, Schneider KC, Westerveld M, Duncan CC, Makuch RW (2003) Change in cognitive function over time in very low-birth-weight infants. JAMA 289(6):705–711
56. Miller SP, Vigneron DB, Henry RG, Bohland MA, Ceppi-Cozzio C, Hoffman C, Newton N, Partridge JC, Ferriero DM, Barkovich AJ (2002) Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J Magn Reson Imaging 16(6):621–632
57. Miller JH, McKinstry RC, Philip JV, Mukherjee P, Neil JJ (2003) Diffusion-tensor MR imaging of normal brain maturation: a guide to structural development and myelination. AJR Am J Roentgenol 180(3):851–859
58. Mohammadi S, Moller HE, Kugel H, Muller DK, Deppe M (2010) Correcting eddy current and motion effects by affine whole-brain registrations: evaluation of three-dimensional distortions and comparison with slicewise correction. Magn Reson Med 64:1047–1056
59. Mohammadi S, Keller SS, Glauche V, Kugel H, Jansen A, Hutton C, Flšel A, Deppe M (2012) The influence of spatial registration on detection of cerebral asymmetries using voxel-based statistics of fractional anisotropy images and TBSS. PLoS ONE 7(6):e3685
60. Molliver ME, Kostovic I, Van der Loos H (1973) The development of synapses in cerebral cortex of the human foetus. Brain Res 50:403–407
61. Morita T, Kochiyama T, Yamada H, Konishi Y, Yonekura Y, Matsumura M, Sadato N (2000) Difference in the metabolic response to photic stimulation of the lateral geniculate nucleus and the primary visual cortex of infants: a fMRI study. Neurosci Res 38(1):63–70
62. Mukherjee P, Miller JH, Shimony JS, Conturo TE, Lee BC, Almli CR, McKinstry RC (2001) Normal brain maturation during childhood: developmental trends characterized with diffusion-tensor MR imaging. Radiology 221(2):349–358
63. Mukherjee P, Miller JH, Shimony JS, Philip JV, Nehra D, Snyder AZ, Conturo TE, Neil JJ, McKinstry RC (2002) Diffusion-tensor MR imaging of gray and white matter development during normal human brain maturation. AJNR Am J Neuroradiol 23(9):1445–1456
64. Myers EH, Hampson M, Vohr B, Lacadie C, Frost SJ, Pugh KR, Katz KH, Schneider KC, Makuch RW, Constable RT, Ment LR (2010) Functional connectivity to a right hemisphere language center in prematurely born adolescents. Neuroimage 51(4):1445–1452
65. Narberhaus A, Lawrence E, Allin MP, Walshe M, McGuire P, Rifkin L, Murray R, Nosarti C (2009) Neural substrates of visual paired associates in young adults with a history of very preterm birth: alterations in fronto-parieto-occipital networks and caudate nucleus. Neuroimage 47:1884–1893
66. Neil JJ, Shiran SI, McKinstry RC, Schefft GL, Snyder AZ, Almli CR, Akbudak E, Aronovitz JA, Miller JP, Lee BC, Conturo TE (1998) Normal brain in human newborns: apparent diffusion coefficient and diffusion anisotropy measured by using diffusion tensor MR imaging. Radiology 209(1):57–66
67. Neil J, Miller J, Mukherjee P, Huppi PS (2002) Diffusion tensor imaging of normal and injured developing human brain—a technical review. NMR Biomed 15(7–8):543–552
68. Nosarti C, Shergill SS, Allin MP, Walshe M, Rifkin L, Murray RM, McGuire PK (2009) Neural substrates of letter fluency processing in young adults who were born very preterm: alterations in frontal and striatal regions. Neuroimage 47:1904–1913
69. Olesen PJ, Nagy Z, Westerberg H, Klingberg T (2003) Combined analysis of DTI and fMRI data reveals a joint maturation of white and grey matter in a fronto-parietal network. Brain Res Cogn Brain Res 18(1):48–57
70. Partridge SC, Mukherjee P, Henry RG, Miller SP, Berman JI, Jin H, Lu Y, Glenn OA, Ferriero DM, Barkovich AJ, Vigneron DB (2004) Diffusion tensor imaging: serial quantitation of white matter tract maturity in premature newborns. Neuroimage 22(3):1302–1314
71. Perani D, Saccuman MC, Scifo P, Spada D, Andreolli G, Rovelli R, Baldoli C, Koelsch S (2010) Functional specializations for music processing in the human newborn brain. Proc Natl Acad Sci USA 107(10):4758–4763
72. Perani D, Saccuman MC, Scifo P, Anwander A, Spada D, Baldoli C, Poloniato A, Lohmann G, Friederici AD (2011) Neural language networks at birth. Proc Natl Acad Sci USA 108(38):16056–16061
73. Peterson BS, Vohr B, Kane MJ, Whalen DH, Schneider KC, Katz KH, Zhang H, Duncan CC, Makuch R, Gore JC, Ment LR (2002) A functional magnetic resonance imaging study of language processing and its cognitive correlates in prematurely born children. Pediatrics 110(6):1153–1162
74. Repka MX (2002) Ophthalmological problems of the premature infant. Ment Retard Dev Disabil Res Rev 8(4):249–257
75. Rushe TM, Rifkin L, Stewart AL, Townsend JP, Roth SC, Wyatt JS, Murray RM (2001) Neuropsychological outcome at adolescence of very preterm birth and its relation to brain structure. Dev Med Child Neurol 43(4):226–233
76. Salvan P, Froudist Walsh S, Allin MP, Walshe M, Murray RM, Bhattacharyya S, McGuire PK, Williams SC, Nosarti C (2014) 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
77. Schafer RJ, Lacadie C, Vohr B, Kesler SR, Katz KH, Schneider KC, Pugh KR, Makuch RW, Reiss AL, Constable RT, Ment LR (2009) Alterations in functional connectivity for language in prematurely born adolescents. Brain 132(Pt 3):661–670
78. Schapiro MB, Schmithorst VJ, Wilke M, Byars AW, Strawsburg RH, Holland SK (2004) BOLD fMRI signal increases with age in selected brain regions in children. NeuroReport 15(17):2575–2578
79. Schneider JF, Il’yasov KA, Hennig J, Martin E (2004) Fast quantitative diffusion-tensor imaging of cerebral white matter from the neonatal period to adolescence. Neuroradiology 46(4):258–266
80. Seghier ML, Lazeyras F, Huppi PS (2006) Functional MRI of the newborn. Semin Fetal Neonatal Med 6:479–488
81. Serag A, Aljabar P, Ball G, Counsell SJ, Boardman JP, Rutherford MA, Edwards AD, Hajnal JV, Rueckert D (2012) Construction of a consistent high-definition spatio-temporal atlas of the developing brain using adaptive kernel regression. Neuroimage 59(3):2255–2265
82. Smith GC, Gutovich J (2011) Neonatal intensive care unit stress is associated with brain development in preterm infants. Ann Neurol 70(4):541–549
83. 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 20(12):2852–2862
84. Stoelhorst GM, Rijken M, Martens SE, Brand R, den Ouden AL, Wit JM, Veen S, Follow-Up Project on Prematurity (2005) Changes in neonatology: comparison of two cohorts of very preterm infants (gestational age <32 weeks): the project on preterm and small for gestational age infants 1983 and the Leiden follow-up project on prematurity 1996–1997. Pediatrics 115(2):396–405
85. Szaflarski JP, Holland SK, Schmithorst VJ, Byars AW (2006) fMRI study of language lateralization in children and adults. Hum Brain Mapp 27(3):202–212
86. Thomas M, Karmiloff-Smith A (2002) Are developmental disorders like cases of adult brain damage? Implications from connectionist modelling. Behav Brain Sci 25:727–750
87. Tin W, Wariyar U, Hey E (1997) Changing prognosis for babies of less than 28 weeks’ gestation in the north of England between 1983 and 1994. Northern Neonatal Network. BMJ 314(7074):107–111
88. van Kooij BJ, de Vries LS, Ball G, van Haastert IC, Benders MJ, Groenendaal F, Counsell SJ (2012) Neonatal tract-based spatial statistics findings and outcome in preterm infants. AJNR Am J Neuroradiol 33(1):188–194
89. Vannest J, Karunanayaka PR, Schmithorst VJ, Szaflarski JP, Holland SK (2009) Language networks in children: evidence from functional MRI studies. AJR Am J Roentgenol 192(5):1190–1196
90. Volpe JJ (2003) Cerebral white matter injury of the premature infant—more common than you think. Pediatrics 112(1 Pt 1):176–180
91. Volpe JJ (2005) Encephalopathy of prematurity includes neuronal abnormalities. Pediatrics 116(1):221–225
92. Walch E, Chaudhary T, Herold B, Obladen M (2009) Parental bilingualism is associated with slower cognitive development in very low birth weight infants. Early Hum Dev 85(7):449–454
93. Wen SW, Smith G, Yang Q, Walker M (2004) Epidemiology of preterm birth and neonatal outcome. Semin Fetal Neonatal Med 9(6):429–435
94. Wilke M, Hauser TK, Krägeloh-Mann I, Lidzba K (2014) Specific impairment of functional connectivity between language regions in former early preterms. Hum Brain Mapp 35(7):3199–3215
95. Witelson SF, Pallie W (1973) Left hemisphere specialization for language in the newborn. Neuroanatomical evidence of asymmetry. Brain 96(3):641–646
96. Yamada H, Sadato N, Konishi Y, Kimura K, Tanaka M, Yonekura Y, Ishii Y (1997) A rapid brain metabolic change in infants detected by fMRI. NeuroReport 8(17):3775–3778
97. Yu VY (2000) Developmental outcome of extremely preterm infants. Am J Perinatol 17(2):57–61