Controversies in preterm brain injury

Neurobiology of Disease

Volumn 92, Issue Part A, 2016, Pages 90-101

  Penn, Anna A ^a   Gressens, Pierre ^b,d   Fleiss, Bobbi ^b,d   Back, Stephen A ^c   Gallo, Vittorio ^a  

^a GEORGE WASHINGTON UNIVERSITY SCHOOL OF MEDICINE AND HEALTH SCIENCES   (United States)

^b UNIVERSITÉ PARIS DESCARTES   (France)

^c OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^d KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Brain development; Neuroimaging; Preterm brain injury; White matter injury

Indexed keywords

3ALPHA HYDROXY 5ALPHA PREGNAN 20 ONE; BARBITURIC ACID DERIVATIVE; BENZODIAZEPINE DERIVATIVE; BETAMETHASONE; CASPASE 3; DEXAMETHASONE; DIAZEPAM; EPIDERMAL GROWTH FACTOR; EPIDERMAL GROWTH FACTOR RECEPTOR; ERYTHROPOIETIN; FIBROBLAST GROWTH FACTOR; FIBROBLAST GROWTH FACTOR 1; FIBROBLAST GROWTH FACTOR 2; GLIAL FIBRILLARY ACIDIC PROTEIN; HYDROCORTISONE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INDOMETACIN; MIDAZOLAM; NARCOTIC AGENT; STEROID HORMONE; THYROID HORMONE;

AXON; BLOOD BRAIN BARRIER; BRAIN BLOOD FLOW; BRAIN FUNCTION; BRAIN GROWTH; BRAIN INJURY; BRAIN SIZE; CELL LOSS; CONNECTOME; DEVELOPMENTAL DISORDER; DIFFERENTIAL DIAGNOSIS; GRAY MATTER; HUMAN; HYPOXIC ISCHEMIC ENCEPHALOPATHY; INFANTILE SPASM; NERVOUS SYSTEM DEVELOPMENT; NEUROTRANSMISSION; NONHUMAN; OLIGODENDROGLIA; PATHOPHYSIOLOGY; PREMATURITY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; RISK FACTOR; WHITE MATTER; ANIMAL; BRAIN; DIAGNOSTIC IMAGING; EMBRYOLOGY;

ANIMALS; BRAIN; BRAIN INJURIES; HUMANS;

EID: 84979072415     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2015.10.012     Document Type: Review

References (149)

1. Agarwal, R., Chiswick, M.L., Rimmer, S., Taylor, G.M., McNally, R.J., Alston, R.D., D'Souza, S.W., Antenatal steroids are associated with a reduction in the incidence of cerebral white matter lesions in very low birthweight infants. Arch. Dis. Child. Fetal Neonatal Ed. 86:2 (2002), F96–F101.
2. Aguirre, A., Rubio, M.E., Gallo, V., Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467:7313 (2010), 323–327.
3. Alix, J.J., Fern, R., Glutamate receptor-mediated ischemic injury of premyelinated central axons. Ann. Neurol. 66:5 (2009), 682–693.
4. Alix, J.J., Zammit, C., Riddle, A., Meshul, C.K., Back, S.A., Valentino, M., Fern, R., Central axons preparing to myelinate are highly sensitive [corrected] to ischemic injury. Ann. Neurol. 72:6 (2012), 936–951.
5. Andiman, S.E., Haynes, R.L., Trachtenberg, F.L., Billiards, S.S., Folkerth, R.D., Volpe, J.J., Kinney, H.C., The cerebral cortex overlying periventricular leukomalacia: analysis of pyramidal neurons. Brain Pathol. 20:4 (2010), 803–814.
6. Back, S.A., Perinatal white matter injury: the changing spectrum of pathology and emerging insights into pathogenetic mechanisms. Ment. Retard. Dev. Disabil. Res. Rev. 12:2 (2006), 129–140.
7. Back, S.A., Miller, S.P., Brain injury in premature neonates: A primary cerebral dysmaturation disorder?. Ann. Neurol. 75:4 (2014), 469–486.
8. Back, S.A., Rosenberg, P.A., Pathophysiology of glia in perinatal white matter injury. Glia 62:11 (2014), 1790–1815.
9. Back, S.A., Tuohy, T.M., Chen, H., Wallingford, N., Craig, A., Struve, J., Luo, N.L., Banine, F., Liu, Y., Chang, A., Trapp, B.D., Bebo, B.F. Jr., Rao, M.S., Sherman, L.S., Hyaluronan accumulates in demyelinated lesions and inhibits oligodendrocyte progenitor maturation. Nat. Med. 11:9 (2005), 966–972.
10. Back, S.A., Riddle, A., Dean, J., Hohimer, A.R., The instrumented fetal sheep as a model of cerebral white matter injury in the premature infant. Neurotherapeutics 9:2 (2012), 359–370.
11. Ball, G., Boardman, J.P., Rueckert, D., Aljabar, P., Arichi, T., Merchant, N., Gousias, I.S., Edwards, A.D., Counsell, S.J., The effect of preterm birth on thalamic and cortical development. Cereb. Cortex 22:5 (2012), 1016–1024.
12. Ball, G., Srinivasan, L., Aljabar, P., Counsell, S.J., Durighel, G., Hajnal, J.V., Rutherford, M.A., Edwards, A.D., Development of cortical microstructure in the preterm human brain. Proc. Natl. Acad. Sci. U. S. A. 110:23 (2013), 9541–9546.
13. Ballabh, P., Pathogenesis and prevention of intraventricular hemorrhage. Clin. Perinatol. 41:1 (2014), 47–67.
14. Bellu, R., de Waal, K.A., Zanini, R., Opioids for neonates receiving mechanical ventilation. Cochrane Database Syst. Rev., 1, 2008, CD004212.
15. Bennet, L., Davidson, J.O., Koome, M., Gunn, A.J., Glucocorticoids and preterm hypoxic–ischemic brain injury: the good and the bad. J. Pregnancy, 2012, 2012, 751694.
16. Berbel, P., Navarro, D., Auso, E., Varea, E., Rodriguez, A.E., Ballesta, J.J., Salinas, M., Flores, E., Faura, C.C., de Escobar, G.M., Role of late maternal thyroid hormones in cerebral cortex development: an experimental model for human prematurity. Cereb. Cortex 20:6 (2010), 1462–1475.
17. Bodeau-Livinec, F., Marlow, N., Ancel, P.Y., Kurinczuk, J.J., Costeloe, K., Kaminski, M., Impact of intensive care practices on short-term and long-term outcomes for extremely preterm infants: comparison between the British Isles and France. Pediatrics 122:5 (2008), e1014–e1021.
18. Bora, S., Pritchard, V.E., Chen, Z., Inder, T.E., Woodward, L.J., Neonatal cerebral morphometry and later risk of persistent inattention/hyperactivity in children born very preterm. J. Child Psychol. Psychiatry 55:7 (2014), 828–838.
19. Brines, M.L., Ghezzi, P., Keenan, S., Agnello, D., de Lanerolle, N.C., Cerami, C., Itri, L.M., Cerami, A., Erythropoietin crosses the blood–brain barrier to protect against experimental brain injury. Proc. Natl. Acad. Sci. U. S. A. 97:19 (2000), 10526–10531.
20. Brown, N.C., Inder, T.E., Bear, M.J., Hunt, R.W., Anderson, P.J., Doyle, L.W., Neurobehavior at term and white and gray matter abnormalities in very preterm infants. J. Pediatr. 155:1 (2009), 32–38 (38 e31).
21. Brummelte, S., Grunau, R.E., Chau, V., Poskitt, K.J., Brant, R., Vinall, J., Gover, A., Synnes, A.R., Miller, S.P., Procedural pain and brain development in premature newborns. Ann. Neurol. 71:3 (2012), 385–396.
22. Brunton, P.J., Russell, J.A., Hirst, J.J., Allopregnanolone in the brain: protecting pregnancy and birth outcomes. Prog. Neurobiol. 113 (2014), 106–136.
23. Buser, J.R., Maire, J., Riddle, A., Gong, X., Nguyen, T., Nelson, K., Luo, N.L., Ren, J., Struve, J., Sherman, L.S., Miller, S.P., Chau, V., Hendson, G., Ballabh, P., Grafe, M.R., Back, S.A., Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann. Neurol. 71:1 (2012), 93–109.
24. Bystron, I., Molnar, Z., Otellin, V., Blakemore, C., Tangential networks of precocious neurons and early axonal outgrowth in the embryonic human forebrain. J. Neurosci. 25:11 (2005), 2781–2792.
25. Cellot, G., Cherubini, E., Functional role of ambient GABA in refining neuronal circuits early in postnatal development. Front Neural Circuits, 7, 2013, 136.
26. Chapman, K., Holmes, M., Seckl, J., 11beta-hydroxysteroid dehydrogenases: intracellular gate-keepers of tissue glucocorticoid action. Physiol. Rev. 93:3 (2013), 1139–1206.
27. Cioni, G., D'Acunto, G., Guzzetta, A., Perinatal brain damage in children: neuroplasticity, early intervention, and molecular mechanisms of recovery. Prog. Brain Res. 189 (2011), 139–154.
28. 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 (2013), 371–378.
29. Counsell, S.J., Boardman, J.P., Differential brain growth in the infant born preterm: current knowledge and future developments from brain imaging. Semin. Fetal Neonatal Med. 10:5 (2005), 403–410.
30. Cunningham, C.L., Martinez-Cerdeno, V., Noctor, S.C., Microglia regulate the number of neural precursor cells in the developing cerebral cortex. J. Neurosci. 33:10 (2013), 4216–4233.
31. Curristin, S.M., Cao, A., Stewart, W.B., Zhang, H., Madri, J.A., Morrow, J.S., Ment, L.R., Disrupted synaptic development in the hypoxic newborn brain. Proc. Natl. Acad. Sci. U. S. A. 99:24 (2002), 15729–15734.
32. Dammann, O., Leviton, A., Intermittent or sustained systemic inflammation and the preterm brain. Pediatr. Res. 75:3 (2014), 376–380.
33. Dean, J.M., McClendon, E., Hansen, K., Azimi-Zonooz, A., Chen, K., Riddle, A., Gong, X., Sharifnia, E., Hagen, M., Ahmad, T., Leigland, L.A., Hohimer, A.R., Kroenke, C.D., Back, S.A., Prenatal cerebral ischemia disrupts MRI-defined cortical microstructure through disturbances in neuronal arborization. Sci. Transl. Med., 5(168), 2013, 168ra167.
34. Dhuria, S.V., Hanson, L.R., Frey, W.H. 2nd, Intranasal delivery to the central nervous system: mechanisms and experimental considerations. J. Pharm. Sci. 99:4 (2010), 1654–1673.
35. Doesburg, S.M., Chau, C.M., Cheung, T.P., Moiseev, A., Ribary, U., Herdman, A.T., Miller, S.P., Cepeda, I.L., Synnes, A., Grunau, R.E., Neonatal pain-related stress, functional cortical activity and visual-perceptual abilities in school-age children born at extremely low gestational age. Pain 154:10 (2013), 1946–1952.
36. Doria, V., Arichi, T., Edwards, D.A., Magnetic resonance imaging of the preterm infant brain. Curr. Pediatr. Rev. 10:1 (2014), 48–55.
37. Doyle, L.W., Ehrenkranz, R.A., Halliday, H.L., Dexamethasone treatment in the first week of life for preventing bronchopulmonary dysplasia in preterm infants: a systematic review. Neonatology 98:3 (2010), 217–224.
38. Drobyshevsky, A., Jiang, R., Lin, L., Derrick, M., Luo, K., Back, S.A., Tan, S., Unmyelinated axon loss with postnatal hypertonia after fetal hypoxia. Ann. Neurol. 75:4 (2014), 533–541.
39. Durrmeyer, X., Vutskits, L., Anand, K.J., Rimensberger, P.C., Use of analgesic and sedative drugs in the NICU: integrating clinical trials and laboratory data. Pediatr. Res. 67:2 (2010), 117–127.
40. Fagel, D.M., Ganat, Y., Cheng, E., Silbereis, J., Ohkubo, Y., Ment, L.R., Vaccarino, F.M., Fgfr1 is required for cortical regeneration and repair after perinatal hypoxia. J. Neurosci. 29:4 (2009), 1202–1211.
41. Fancy, S.P., Harrington, E.P., Yuen, T.J., Silbereis, J.C., Zhao, C., Baranzini, S.E., Bruce, C.C., Otero, J.J., Huang, E.J., Nusse, R., Franklin, R.J., Rowitch, D.H., Axin2 as regulatory and therapeutic target in newborn brain injury and remyelination. Nat. Neurosci. 14:8 (2011), 1009–1016.
42. Favrais, G., van de Looij, Y., Fleiss, B., Ramanantsoa, N., Bonnin, P., Stoltenburg-Didinger, G., Lacaud, A., Saliba, E., Dammann, O., Gallego, J., Sizonenko, S., Hagberg, H., Lelievre, V., Gressens, P., Systemic inflammation disrupts the developmental program of white matter. Ann. Neurol. 70:4 (2011), 550–565.
43. Feigenson, K., Reid, M., See, J., Crenshaw, E.B. 3rd, Grinspan, J.B., Wnt signaling is sufficient to perturb oligodendrocyte maturation. Mol. Cell. Neurosci. 42:3 (2009), 255–265.
44. Fernandez, E.F., Watterberg, K.L., Relative adrenal insufficiency in the preterm and term infant. J. Perinatol. 29:Suppl. 2 (2009), S44–S49.
45. Fino, E., Yuste, R., Dense inhibitory connectivity in neocortex. Neuron 69:6 (2011), 1188–1203.
46. Gallo, V., Deneen, B., Glial development: the crossroads of regeneration and repair in the CNS. Neuron 83:2 (2014), 283–308.
47. Ganat, Y., Soni, S., Chacon, M., Schwartz, M.L., Vaccarino, F.M., Chronic hypoxia up-regulates fibroblast growth factor ligands in the perinatal brain and induces fibroblast growth factor-responsive radial glial cells in the sub-ependymal zone. Neuroscience 112:4 (2002), 977–991.
48. Ghosh, A., Shatz, C.J., A role for subplate neurons in the patterning of connections from thalamus to neocortex. Development 117:3 (1993), 1031–1047.
49. Ghosh, A., Shatz, C.J., Segregation of geniculocortical afferents during the critical period: a role for subplate neurons. J. Neurosci. 14:6 (1994), 3862–3880.
50. Gonzalez-Perez, O., Alvarez-Buylla, A., Oligodendrogenesis in the subventricular zone and the role of epidermal growth factor. Brain Res. Rev. 67:1–2 (2011), 147–156.
51. Guardia Clausi, M., Paez, P.M., Campagnoni, A.T., Pasquini, L.A., Pasquini, J.M., Intranasal administration of aTf protects and repairs the neonatal white matter after a cerebral hypoxic–ischemic event. Glia 60:10 (2012), 1540–1554.
52. Gustafsson, M.V., Zheng, X., Pereira, T., Gradin, K., Jin, S., Lundkvist, J., Ruas, J.L., Poellinger, L., Lendahl, U., Bondesson, M., Hypoxia requires notch signaling to maintain the undifferentiated cell state. Dev. Cell 9:5 (2005), 617–628.
53. Haynes, R.L., Billiards, S.S., Borenstein, N.S., Volpe, J.J., Kinney, H.C., Diffuse axonal injury in periventricular leukomalacia as determined by apoptotic marker fractin. Pediatr. Res. 63:6 (2008), 656–661.
54. Hill, M., Parizek, A., Bicikova, M., Havlikova, H., Klak, J., Fait, T., Cibula, D., Hampl, R., Cegan, A., Sulcova, J., Starka, L., Neuroactive steroids, their precursors, and polar conjugates during parturition and postpartum in maternal and umbilical blood: 1. Identification and simultaneous determination of pregnanolone isomers. J Steroid Biochem Mol Biol 75:4–5 (2000), 237–244.
55. Hirst, J.J., Kelleher, M.A., Walker, D.W., Palliser, H.K., Neuroactive steroids in pregnancy: key regulatory and protective roles in the foetal brain. J Steroid Biochem Mol Biol 139 (2014), 144–153.
56. Hoerder-Suabedissen, A., Molnar, Z., Development, evolution and pathology of neocortical subplate neurons. Nat. Rev. Neurosci. 16:3 (2015), 133–146.
57. Hu, S., Sheng, W.S., Lokensgard, J.R., Peterson, P.K., Morphine induces apoptosis of human microglia and neurons. Neuropharmacology 42:6 (2002), 829–836.
58. Huppi, P.S., Murphy, B., Maier, S.E., Zientara, G.P., Inder, T.E., Barnes, P.D., Kikinis, R., Jolesz, F.A., Volpe, J.J., Microstructural brain development after perinatal cerebral white matter injury assessed by diffusion tensor magnetic resonance imaging. Pediatrics 107:3 (2001), 455–460.
59. Iai, M., Takashima, S., Thalamocortical development of parvalbumin neurons in normal and periventricular leukomalacia brains. Neuropediatrics 30:1 (1999), 14–18.
60. Jablonska, B., Scafidi, J., Aguirre, A., Vaccarino, F., Nguyen, V., Borok, E., Horvath, T.L., Rowitch, D.H., Gallo, V., Oligodendrocyte regeneration after neonatal hypoxia requires FoxO1-mediated p27Kip1 expression. J. Neurosci. 32:42 (2012), 14775–14793.
61. Juul, S.E., McPherson, R.J., Bauer, L.A., Ledbetter, K.J., Gleason, C.A., Mayock, D.E., A phase I/II trial of high-dose erythropoietin in extremely low birth weight infants: pharmacokinetics and safety. Pediatrics 122:2 (2008), 383–391.
62. Kanold, P.O., Shatz, C.J., Subplate neurons regulate maturation of cortical inhibition and outcome of ocular dominance plasticity. Neuron 51:5 (2006), 627–638.
63. Kelleher, M.A., Palliser, H.K., Walker, D.W., Hirst, J.J., Sex-dependent effect of a low neurosteroid environment and intrauterine growth restriction on foetal guinea pig brain development. J Endocrinol 208:3 (2011), 301–309.
64. Kersbergen, K.J., de Vries, L.S., van Kooij, B.J., Isgum, I., Rademaker, K.J., van Bel, F., Huppi, P.S., Dubois, J., Groenendaal, F., Benders, M.J., Hydrocortisone treatment for bronchopulmonary dysplasia and brain volumes in preterm infants. J. Pediatr. 163:3 (2013), 666–671 e661.
65. Khalife, N., Glover, V., Taanila, A., Ebeling, H., Jarvelin, M.R., Rodriguez, A., Prenatal glucocorticoid treatment and later mental health in children and adolescents. PLoS One, 8(11), 2013, e81394.
66. Kinney, H.C., Haynes, R.L., Xu, G., Andiman, S.E., Folkerth, R.D., Sleeper, L.A., Volpe, J.J., Neuron deficit in the white matter and subplate in periventricular leukomalacia. Ann. Neurol. 71:3 (2012), 397–406.
67. Komitova, M., Xenos, D., Salmaso, N., Tran, K.M., Brand, T., Schwartz, M.L., Ment, L., Vaccarino, F.M., Hypoxia-induced developmental delays of inhibitory interneurons are reversed by environmental enrichment in the postnatal mouse forebrain. J. Neurosci. 33:33 (2013), 13375–13387.
68. Kuban, K.C., O'Shea, T.M., Allred, E.N., Paneth, N., Hirtz, D., Fichorova, R.N., Leviton, A., Investigators, E.S., Systemic inflammation and cerebral palsy risk in extremely preterm infants. J. Child Neurol. 29:12 (2014), 1692–1698.
69. Kuzumaki, N., Ikegami, D., Tamura, R., Hareyama, N., Imai, S., Narita, M., Torigoe, K., Niikura, K., Takeshima, H., Ando, T., Igarashi, K., Kanno, J., Ushijima, T., Suzuki, T., Narita, M., Hippocampal epigenetic modification at the brain-derived neurotrophic factor gene induced by an enriched environment. Hippocampus 21:2 (2011), 127–132.
70. Kwon, S.H., Scheinost, D., Lacadie, C., Benjamin, J., Myers, E.H., Qiu, M., Schneider, K.C., Rothman, D.L., Constable, R.T., Ment, L.R., GABA, resting-state connectivity and the developing brain. Neonatology 106:2 (2014), 149–155.
71. Laviola, G., Hannan, A.J., Macri, S., Solinas, M., Jaber, M., Effects of enriched environment on animal models of neurodegenerative diseases and psychiatric disorders. Neurobiol. Dis. 31:2 (2008), 159–168.
72. Lee, W., Morgan, B.R., Shroff, M.M., Sled, J.G., Taylor, M.J., The development of regional functional connectivity in preterm infants into early childhood. Neuroradiology 55:Suppl. 2 (2013), 105–111.
73. Lester, B.M., Hawes, K., Abar, B., Sullivan, M., Miller, R., Bigsby, R., Laptook, A., Salisbury, A., Taub, M., Lagasse, L.L., Padbury, J.F., Single-family room care and neurobehavioral and medical outcomes in preterm infants. Pediatrics 134:4 (2014), 754–760.
74. Lubsen, J., Vohr, B., Myers, E., Hampson, M., Lacadie, C., Schneider, K.C., Katz, K.H., Constable, R.T., Ment, L.R., Microstructural and functional connectivity in the developing preterm brain. Semin. Perinatol. 35:1 (2011), 34–43.
75. Lucas-Thompson, R., Townsend, E.L., Gunnar, M.R., Georgieff, M.K., Guiang, S.F., Ciffuentes, R.F., Lussky, R.C., Davis, E.P., Developmental changes in the responses of preterm infants to a painful stressor. Infant Behav Dev 31:4 (2008), 614–623.
76. Malik, S., Vinukonda, G., Vose, L.R., Diamond, D., Bhimavarapu, B.B., Hu, F., Zia, M.T., Hevner, R., Zecevic, N., Ballabh, P., Neurogenesis continues in the third trimester of pregnancy and is suppressed by premature birth. J. Neurosci. 33:2 (2013), 411–423.
77. McAdams, R.M., McPherson, R.J., Mayock, D.E., Juul, S.E., Outcomes of extremely low birth weight infants given early high-dose erythropoietin. J. Perinatol. 33:3 (2013), 226–230.
78. McClain, C.R., Sim, F.J., Goldman, S.A., Pleiotrophin suppression of receptor protein tyrosine phosphatase-beta/zeta maintains the self-renewal competence of fetal human oligodendrocyte progenitor cells. J. Neurosci. 32:43 (2012), 15066–15075.
79. McClendon, E., Chen, K., Gong, X., Sharifnia, E., Hagen, M., Cai, V., Shaver, D.C., Riddle, A., Dean, J.M., Gunn, A.J., Mohr, C., Kaplan, J.S., Rossi, D.J., Kroenke, C.D., Hohimer, A.R., Back, S.A., Prenatal cerebral ischemia triggers dysmaturation of caudate projection neurons. Ann Neurol. 75:4 (2014), 508–524.
80. McClure, M.M., Riddle, A., Manese, M., Luo, N.L., Rorvik, D.A., Kelly, K.A., Barlow, C.H., Kelly, J.J., Vinecore, K., Roberts, C.T., Hohimer, A.R., Back, S.A., Cerebral blood flow heterogeneity in preterm sheep: lack of physiologic support for vascular boundary zones in fetal cerebral white matter. J. Cereb. Blood Flow Metab. 28:5 (2008), 995–1008.
81. McConnell, S.K., Ghosh, A., Shatz, C.J., Subplate neurons pioneer the first axon pathway from the cerebral cortex. Science 245:4921 (1989), 978–982.
82. McConnell, S.K., Ghosh, A., Shatz, C.J., Subplate pioneers and the formation of descending connections from cerebral cortex. J. Neurosci. 14:4 (1994), 1892–1907.
83. McQuillen, P.S., Sheldon, R.A., Shatz, C.J., Ferriero, D.M., Selective vulnerability of subplate neurons after early neonatal hypoxia–ischemia. J. Neurosci. 23:8 (2003), 3308–3315.
84. Mellon, S.H., Neurosteroid regulation of central nervous system development. Pharmacol. Ther. 116:1 (2007), 107–124.
85. Ment, L.R., Vohr, B.R., Preterm birth and the developing brain. Lancet Neurol. 7:5 (2008), 378–379.
86. Ment, L.R., Schwartz, M., Makuch, R.W., Stewart, W.B., Association of chronic sublethal hypoxia with ventriculomegaly in the developing rat brain. Brain Res. Dev. Brain Res. 111:2 (1998), 197–203.
87. Ment, L.R., Vohr, B., Allan, W., Katz, K.H., Schneider, K.C., Westerveld, M., Duncan, C.C., Makuch, R.W., Change in cognitive function over time in very low-birth-weight infants. JAMA 289:6 (2003), 705–711.
88. Ment, L.R., Vohr, B.R., Makuch, R.W., Westerveld, M., Katz, K.H., Schneider, K.C., Duncan, C.C., Ehrenkranz, R., Oh, W., Philip, A.G., Scott, D.T., Allan, W.C., Prevention of intraventricular hemorrhage by indomethacin in male preterm infants. J. Pediatr. 145:6 (2004), 832–834.
89. Ment, L.R., Hirtz, D., Huppi, P.S., Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol. 8:11 (2009), 1042–1055.
90. Miller, S.P., Ferriero, D.M., From selective vulnerability to connectivity: insights from newborn brain imaging. Trends Neurosci. 32:9 (2009), 496–505.
91. Miller, S.P., Vigneron, D.B., Henry, R.G., Bohland, M.A., Ceppi-Cozzio, C., Hoffman, C., Newton, N., Partridge, J.C., Ferriero, D.M., Barkovich, A.J., Serial quantitative diffusion tensor MRI of the premature brain: development in newborns with and without injury. J. Magn. Reson. Imaging 16:6 (2002), 621–632.
92. Mullen, K.M., Vohr, B.R., Katz, K.H., Schneider, K.C., Lacadie, C., Hampson, M., Makuch, R.W., Reiss, A.L., Constable, R.T., Ment, L.R., Preterm birth results in alterations in neural connectivity at age 16 years. NeuroImage 54:4 (2011), 2563–2570.
93. Myers, E.H., Hampson, M., Vohr, B., Lacadie, C., Frost, S.J., Pugh, K.R., Katz, K.H., Schneider, K.C., Makuch, R.W., Constable, R.T., Ment, L.R., Functional connectivity to a right hemisphere language center in prematurely born adolescents. NeuroImage 51:4 (2010), 1445–1452.
94. Nave, K.A., Werner, H.B., Myelination of the nervous system: mechanisms and functions. Annu. Rev. Cell Dev. Biol. 30 (2014), 503–533.
95. Ng, S.M., Turner, M.A., Gamble, C., Didi, M., Victor, S., Atkinson, J., Sluming, V., Parkes, L.M., Tietze, A., Abernethy, L.J., Weindling, A.M., Effect of thyroxine on brain microstructure in extremely premature babies: magnetic resonance imaging findings in the TIPIT study. Pediatr. Radiol. 44:8 (2014), 987–996.
96. O'Gorman, R.L., Bucher, H.U., Held, U., Koller, B.M., Huppi, P.S., Hagmann, C.F., Swiss, E.P.O.N.T.G., Tract-based spatial statistics to assess the neuroprotective effect of early erythropoietin on white matter development in preterm infants. Brain 138:Pt 2 (2015), 388–397.
97. Ohls, R.K., Kamath-Rayne, B.D., Christensen, R.D., Wiedmeier, S.E., Rosenberg, A., Fuller, J., Lacy, C.B., Roohi, M., Lambert, D.K., Burnett, J.J., Pruckler, B., Peceny, H., Cannon, D.C., Lowe, J.R., Cognitive outcomes of preterm infants randomized to darbepoetin, erythropoietin, or placebo. Pediatrics 133:6 (2014), 1023–1030.
98. Osborn, D.A., Hunt, R.W., Postnatal thyroid hormones for preterm infants with transient hypothyroxinaemia. Cochrane Database Syst. Rev., 1, 2007, CD005945.
99. Osborn, D.A., Hunt, R.W., Prophylactic postnatal thyroid hormones for prevention of morbidity and mortality in preterm infants. Cochrane Database Syst. Rev., 1, 2007, CD005948.
100. Paolicelli, R.C., Bolasco, G., Pagani, F., Maggi, L., Scianni, M., Panzanelli, P., Giustetto, M., Ferreira, T.A., Guiducci, E., Dumas, L., Ragozzino, D., Gross, C.T., Synaptic pruning by microglia is necessary for normal brain development. Science 333:6048 (2011), 1456–1458.
101. Partridge, S.C., Mukherjee, P., Berman, J.I., Henry, R.G., Miller, S.P., Lu, Y., Glenn, O.A., Ferriero, D.M., Barkovich, A.J., Vigneron, D.B., Tractography-based quantitation of diffusion tensor imaging parameters in white matter tracts of preterm newborns. J. Magn. Reson. Imaging 22:4 (2005), 467–474.
102. Patel, J., Landers, K., Li, H., Mortimer, R.H., Richard, K., Thyroid hormones and fetal neurological development. J. Endocrinol. 209:1 (2011), 1–8.
103. Patz, S., Grabert, J., Gorba, T., Wirth, M.J., Wahle, P., Parvalbumin expression in visual cortical interneurons depends on neuronal activity and TrkB ligands during an Early period of postnatal development. Cereb. Cortex 14:3 (2004), 342–351.
104. Peterson, B.S., Anderson, A.W., Ehrenkranz, R., Staib, L.H., Tageldin, M., Colson, E., Gore, J.C., Duncan, C.C., Makuch, R., Ment, L.R., Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics 111:5 Pt 1 (2003), 939–948.
105. Pierson, C.R., Folkerth, R.D., Billiards, S.S., Trachtenberg, F.L., Drinkwater, M.E., Volpe, J.J., Kinney, H.C., Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol. 114:6 (2007), 619–631.
106. Pineda, R.G., Neil, J., Dierker, D., Smyser, C.D., Wallendorf, M., Kidokoro, H., Reynolds, L.C., Walker, S., Rogers, C., Mathur, A.M., Van Essen, D.C., Inder, T., Alterations in brain structure and neurodevelopmental outcome in preterm infants hospitalized in different neonatal intensive care unit environments. J. Pediatr. 164:1 (2014), 52–60 e52.
107. Rademaker, K.J., Rijpert, M., Uiterwaal, C.S., Lieftink, A.F., van Bel, F., Grobbee, D.E., de Vries, L.S., Groenendaal, F., Neonatal hydrocortisone treatment related to 1 H-MRS of the hippocampus and short-term memory at school age in preterm born children. Pediatr. Res. 59:2 (2006), 309–313.
108. Ranger, M., Grunau, R.E., Early repetitive pain in preterm infants in relation to the developing brain. Pain Manag. 4:1 (2014), 57–67.
109. Ranger, M., Chau, C.M., Garg, A., Woodward, T.S., Beg, M.F., Bjornson, B., Poskitt, K., Fitzpatrick, K., Synnes, A.R., Miller, S.P., Grunau, R.E., Neonatal pain-related stress predicts cortical thickness at age 7 years in children born very preterm. PLoS One, 8(10), 2013, e76702.
110. Rash, B.G., Tomasi, S., Lim, H.D., Suh, C.Y., Vaccarino, F.M., Cortical gyrification induced by fibroblast growth factor 2 in the mouse brain. J. Neurosci. 33:26 (2013), 10802–10814.
111. Reidy, N., Morgan, A., Thompson, D.K., Inder, T.E., Doyle, L.W., Anderson, P.J., Impaired language abilities and white matter abnormalities in children born very preterm and/or very low birth weight. J. Pediatr. 162:4 (2013), 719–724.
112. Reynolds, R.M., Programming effects of glucocorticoids. Clin. Obstet. Gynecol. 56:3 (2013), 602–609.
113. Riddle, A., Maire, J., Gong, X., Chen, K.X., Kroenke, C.D., Hohimer, A.R., Back, S.A., Differential susceptibility to axonopathy in necrotic and non-necrotic perinatal white matter injury. Stroke 43:1 (2012), 178–184.
114. Robinson, S., Li, Q., Dechant, A., Cohen, M.L., Neonatal loss of gamma-aminobutyric acid pathway expression after human perinatal brain injury. J. Neurosurg. 104:6 Suppl (2006), 396–408.
115. Rousset, C.I., Chalon, S., Cantagrel, S., Bodard, S., Andres, C., Gressens, P., Saliba, E., Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr. Res. 59:3 (2006), 428–433.
116. Salmaso, N., Silbereis, J., Komitova, M., Mitchell, P., Chapman, K., Ment, L.R., Schwartz, M.L., Vaccarino, F.M., Environmental enrichment increases the GFAP + stem cell pool and reverses hypoxia-induced cognitive deficits in juvenile mice. J. Neurosci. 32:26 (2012), 8930–8939.
117. Salmaso, N., Jablonska, B., Scafidi, J., Vaccarino, F.M., Gallo, V., Neurobiology of premature brain injury. Nat. Neurosci. 17:3 (2014), 341–346.
118. Scafidi, J., Fagel, D.M., Ment, L.R., Vaccarino, F.M., Modeling premature brain injury and recovery. Int. J. Dev. Neurosci. 27:8 (2009), 863–871.
119. Scafidi, J., Hammond, T.R., Scafidi, S., Ritter, J., Jablonska, B., Roncal, M., Szigeti-Buck, K., Coman, D., Huang, Y., McCarter, R.J. Jr., Hyder, F., Horvath, T.L., Gallo, V., Intranasal epidermal growth factor treatment rescues neonatal brain injury. Nature 506:7487 (2014), 230–234.
120. Schafer, R.J., Lacadie, C., Vohr, B., Kesler, S.R., Katz, K.H., Schneider, K.C., Pugh, K.R., Makuch, R.W., Reiss, A.L., Constable, R.T., Ment, L.R., Alterations in functional connectivity for language in prematurely born adolescents. Brain 132:Pt 3 (2009), 661–670.
121. Schang, A.L., Gressens, P., Fleiss, B., Revisiting thyroid hormone treatment to prevent brain damage of prematurity. J. Neurosci. Res. 92:12 (2014), 1609–1610.
122. Schang, A.L., Van Steenwinckel, J., Chevenne, D., Alkmark, M., Hagberg, H., Gressens, P., Fleiss, B., Failure of thyroid hormone treatment to prevent inflammation-induced white matter injury in the immature brain. Brain Behav. Immun. 37 (2014), 95–102.
123. Schumacher, M., Mattern, C., Ghoumari, A., Oudinet, J.P., Liere, P., Labombarda, F., Sitruk-Ware, R., De Nicola, A.F., Guennoun, R., Revisiting the roles of progesterone and allopregnanolone in the nervous system: resurgence of the progesterone receptors. Prog. Neurobiol. 113 (2014), 6–39.
124. Schwaller, B., Tetko, I.V., Tandon, P., Silveira, D.C., Vreugdenhil, M., Henzi, T., Potier, M.C., Celio, M.R., Villa, A.E., Parvalbumin deficiency affects network properties resulting in increased susceptibility to epileptic seizures. Mol. Cell. Neurosci. 25:4 (2004), 650–663.
125. Seo, J.H., Yu, J.H., Suh, H., Kim, M.S., Cho, S.R., Fibroblast growth factor-2 induced by enriched environment enhances angiogenesis and motor function in chronic hypoxic–ischemic brain injury. PLoS One, 8(9), 2013, e74405.
126. Smith, G.C., Gutovich, J., Smyser, C., Pineda, R., Newnham, C., Tjoeng, T.H., Vavasseur, C., Wallendorf, M., Neil, J., Inder, T., Neonatal intensive care unit stress is associated with brain development in preterm infants. Ann. Neurol. 70:4 (2011), 541–549.
127. Smyser, C.D., Inder, T.E., Shimony, J.S., Hill, J.E., Degnan, A.J., Snyder, A.Z., Neil, J.J., Longitudinal analysis of neural network development in preterm infants. Cereb. Cortex 20:12 (2010), 2852–2862.
128. Smyser, C.D., Snyder, A.Z., Shimony, J.S., Blazey, T.M., Inder, T.E., Neil, J.J., Effects of white matter injury on resting state fMRI measures in prematurely born infants. PLoS One, 8(7), 2013, e68098.
129. Soul, J.S., Hammer, P.E., Tsuji, M., Saul, J.P., Bassan, H., Limperopoulos, C., Disalvo, D.N., Moore, M., Akins, P., Ringer, S., Volpe, J.J., Trachtenberg, F., du Plessis, A.J., Fluctuating pressure-passivity is common in the cerebral circulation of sick premature infants. Pediatr. Res. 61:4 (2007), 467–473.
130. Spittle, A.J., Orton, J., Doyle, L.W., Boyd, R., Early developmental intervention programs post hospital discharge to prevent motor and cognitive impairments in preterm infants. Cochrane Database Syst. Rev., 2, 2007, CD005495.
131. Tam, E.W., Chau, V., Ferriero, D.M., Barkovich, A.J., Poskitt, K.J., Studholme, C., Fok, E.D., Grunau, R.E., Glidden, D.V., Miller, S.P., Preterm cerebellar growth impairment after postnatal exposure to glucocorticoids. Sci. Transl. Med., 3(105), 2011, 105ra105.
132. Traudt, C.M., Juul, S.E., Erythropoietin as a neuroprotectant for neonatal brain injury: animal models. Methods Mol. Biol. 982 (2013), 113–126.
133. Tsai, P.T., Ohab, J.J., Kertesz, N., Groszer, M., Matter, C., Gao, J., Liu, X., Wu, H., Carmichael, S.T., A critical role of erythropoietin receptor in neurogenesis and post-stroke recovery. J. Neurosci. 26:4 (2006), 1269–1274.
134. Ueno, M., Fujita, Y., Tanaka, T., Nakamura, Y., Kikuta, J., Ishii, M., Yamashita, T., Layer V cortical neurons require microglial support for survival during postnatal development. Nat. Neurosci. 16:5 (2013), 543–551.
135. Vaccarino, F.M., Schwartz, M.L., Raballo, R., Rhee, J., Lyn-Cook, R., Fibroblast growth factor signaling regulates growth and morphogenesis at multiple steps during brain development. Curr. Top. Dev. Biol. 46 (1999), 179–200.
136. van den Heuvel, M.P., Kersbergen, K.J., de Reus, M.A., Keunen, K., Kahn, R.S., Groenendaal, F., de Vries, L.S., Benders, M.J., The neonatal connectome during preterm brain development. Cereb. Cortex 25:9 (2015), 3000–3013.
137. van Praag, H., Kempermann, G., Gage, F.H., Neural consequences of environmental enrichment. Nat. Rev. Neurosci. 1:3 (2000), 191–198.
138. Verney, C., Monier, A., Fallet-Bianco, C., Gressens, P., Early microglial colonization of the human forebrain and possible involvement in periventricular white-matter injury of preterm infants. J. Anat. 217:4 (2010), 436–448.
139. Verney, C., Pogledic, I., Biran, V., Adle-Biassette, H., Fallet-Bianco, C., Gressens, P., Microglial reaction in axonal crossroads is a hallmark of noncystic periventricular white matter injury in very preterm infants. J. Neuropathol. Exp. Neurol. 71:3 (2012), 251–264.
140. Vinall, J., Grunau, R.E., Impact of repeated procedural pain-related stress in infants born very preterm. Pediatr. Res. 75:5 (2014), 584–587.
141. Vinall, J., Grunau, R.E., Brant, R., Chau, V., Poskitt, K.J., Synnes, A.R., Miller, S.P., Slower postnatal growth is associated with delayed cerebral cortical maturation in preterm newborns. Sci. Transl. Med., 5(168), 2013, 168ra168.
142. Volpe, J.J., Subplate neurons—missing link in brain injury of the premature infant?. Pediatrics 97:1 (1996), 112–113.
143. Vose, L.R., Vinukonda, G., Jo, S., Miry, O., Diamond, D., Korumilli, R., Arshad, A., Zia, M.T., Hu, F., Kayton, R.J., La Gamma, E.F., Bansal, R., Bianco, A.C., Ballabh, P., Treatment with thyroxine restores myelination and clinical recovery after intraventricular hemorrhage. J. Neurosci. 33:44 (2013), 17232–17246.
144. Wang, J.M., Singh, C., Liu, L., Irwin, R.W., Chen, S., Chung, E.J., Thompson, R.F., Brinton, R.D., Allopregnanolone reverses neurogenic and cognitive deficits in mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U. S. A. 107:14 (2010), 6498–6503.
145. Wong, H.S., Edwards, P., Nature or nurture: a systematic review of the effect of socio-economic status on the developmental and cognitive outcomes of children born preterm. Matern. Child Health J. 17:9 (2013), 1689–1700.
146. Wu, Y.W., Gonzalez, F.F., Erythropoietin: a novel therapy for hypoxic–ischaemic encephalopathy?. Dev. Med. Child Neurol. 57:Suppl. 3 (2015), 34–39.
147. Yawno, T., Yan, E.B., Walker, D.W., Hirst, J.J., Inhibition of neurosteroid synthesis increases asphyxia-induced brain injury in the late gestation fetal sheep. Neuroscience 146:4 (2007), 1726–1733.
148. Yawno, T., Hirst, J.J., Castillo-Melendez, M., Walker, D.W., Role of neurosteroids in regulating cell death and proliferation in the late gestation fetal brain. Neuroscience 163:3 (2009), 838–847.
149. Ye, F., Chen, Y., Hoang, T., Montgomery, R.L., Zhao, X.H., Bu, H., Hu, T., Taketo, M.M., van Es, J.H., Clevers, H., Hsieh, J., Bassel-Duby, R., Olson, E.N., Lu, Q.R., HDAC1 and HDAC2 regulate oligodendrocyte differentiation by disrupting the beta-catenin-TCF interaction. Nat. Neurosci. 12:7 (2009), 829–838.