Seminars in Perinatology
Volume 34, Issue 1 , Pages 93-101 , February 2010

Advanced Neuroimaging Techniques: Their Role in the Development of Future Fetal and Neonatal Neuroprotection

  • Catherine Limperopoulos, PhD

      Affiliations

    • Corresponding Author InformationAddress reprint requests to Catherine Limperopoulos, PhD, Montreal Children's Hospital, Pediatric Neurology, 2300 Tupper St A-334, Montreal, Quebec, Canada H3H 1P3

References 

  1. Toga AW, Thompson PM, Sowell ER. Mapping brain maturation. Trends Neurosci. 2006;29:148–159
  2. Krageloh-Mann I. Imaging of early brain injury and cortical plasticity. Exp Neurol. 2004;190(suppl 1):S84–S90
  3. Huppi PS, Warfield S, Kikinis R, et al. Quantitative magnetic resonance imaging of brain development in premature and mature newborns. Ann Neurol. 1998;43:224–235
  4. Hubel DH, Wiesel TN. Receptive fields of cells in striate cortex of very young, visually inexperienced kittens. J Neurophysiol. 1963;26:994–1002
  5. Wiesel TN, Hubel DH. Comparison of the effects of unilateral and bilateral eye closure on cortical unit responses in kittens. J Neurophysiol. 1965;28:1029–1040
  6. Wiesel TN, Hubel DH. Extent of recovery from the effects of visual deprivation in kittens. J Neurophysiol. 1965;28:1060–1072
  7. Johnston MV. Clinical disorders of brain plasticity. Brain Dev. 2004;26:73–80
  8. Johnston MV, Nishimura A, Harum K, et al. Sculpting the developing brain. Adv Pediatr. 2001;48:1–38
  9. Raff MC, Barres BA, Burne JF, et al. Programmed cell death and the control of cell survival: Lessons from the nervous system. Science. 1993;262:695–700
  10. Faverjon S, Silveira DC, Fu DD, et al. Beneficial effects of enriched environment following status epilepticus in immature rats. Neurology. 2002;59:1356–1364
  11. Giza CC, Griesbach GS, Hovda DA. Experience-dependent behavioral plasticity is disturbed following traumatic injury to the immature brain. Behav Brain Res. 2005;157:11–22
  12. Kolb B, Gibb R. Environmental enrichment and cortical injury: Behavioral and anatomical consequences of frontal cortex lesions. Cereb Cortex. 1991;1:189–198
  13. Kolb B, Elliott W. Recovery from early cortical damage in rats. II (Effects of experience on anatomy and behavior following frontal lesions at 1 or 5 days of age). Behav Brain Res. 1987;26:47–56
  14. Tees RC, Buhrmann K, Hanley J. The effect of early experience on water maze spatial learning and memory in rats. Dev Psychobiol. 1990;23:427–439
  15. Malkasian DR, Diamond MC. The effects of environmental manipulation on the morphology of the neonate rat brain. Int J Neurosci. 1971;2:161–169
  16. van Gool WA, Mirmiran M, van Haaren F. Spatial memory and visual evoked potentials in young and old rats after housing in an enriched environment. Behav Neural Biol. 1985;44:454–469
  17. Venable N, Pinto-Hamuy T, Arraztoa JA, et al. Greater efficacy of preweaning than postweaning environmental enrichment on maze learning in adult rats. Behav Brain Res. 1988;31:89–92
  18. McDonald J, Johnston M. Physiological and pathophysiological roles of excitatory amino acids during central nervous system development. Brain Res Rev. 1990;15:41–70
  19. Ikonomidou C, Bittigau P, Koch C, et al. Neurotransmitters and apoptosis in the developing brain. Biochem Pharmacol. 2001;62:401–405
  20. Nakajima W, Ishida A, Lange MS, et al. Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat. J Neurosci. 2000;20:7994–8004
  21. Escalona SK. Babies at double hazard: Early development of infants at biologic and social risk. Pediatrics. 1982;70:670–676
  22. Gilles FH, Leviton A, Golden JA, et al. Groups of histopathologic abnormalities in brains of very low birthweight infants. J Neuropathol Exp Neurol. 1998;57:1026–1034
  23. Jensen FE. Developmental factors regulating susceptibility to perinatal brain injury and seizures. Curr Opin Pediatr. 2006;18:628–633
  24. Pasternak JF, Predey TA, Mikhael MA. Neonatal asphyxia: Vulnerability of basal ganglia, thalamus, and brainstem. Pediatr Neurol. 1991;7:147–149
  25. Barkovich AJ. MR and CT evaluation of profound neonatal and infantile asphyxia. AJNR Am J Neuroradiol. 1993;13:959–972discussion 973-955
  26. Back SA, Gan X, Li Y, et al. Maturation-dependent vulnerability of oligodendrocytes to oxidative stress-induced death caused by glutathione depletion. J Neurosci. 1998;18:6241–6253
  27. Kinney HC, Back SA. Human oligodendroglial development: Relationship to periventricular leukomalacia. Semin Pediatr Neurol. 1998;5:180–189
  28. Volpe JJ. Subplate neurons—Missing link in brain injury of the premature infant?. Pediatrics. 1996;97:112–113
  29. Miller SP, Ferriero DM. From selective vulnerability to connectivity: Insights from newborn brain imaging. Trends Neurosci. 2009;32:496–505
  30. Volpe JJ. Encephalopathy of prematurity includes neuronal abnormalities. Pediatrics. 2005;116:221–225
  31. Volpe JJ. Brain injury in premature infants: A complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2009;8:110–124
  32. Shankaran S, Laptook A. Challenge of conducting trials of neuroprotection in the asphyxiated term infant. Semin Perinatol. 2003;27:320–332
  33. Gunn AJ, Gluckman PD, Gunn TR. Selective head cooling in newborn infants after perinatal asphyxia: A safety study. Pediatrics. 1998;102:885–892
  34. Battin MR, Dezoete JA, Gunn TR, et al. Neurodevelopmental outcome of infants treated with head cooling and mild hypothermia after perinatal asphyxia. Pediatrics. 2001;107:480–484
  35. Tsuji M, Saul JP, du Plessis A, et al. Cerebral intravascular oxygenation correlates with mean arterial pressure in critically ill premature infants. Pediatrics. 2000;106:625–632
  36. Soul JS, Hammer PE, Tsuji M, et al. Fluctuating pressure-passivity is common in the cerebral circulation of sick premature infants. Pediatr Res. 2007;61:467–473
  37. Lou HC. Autoregulation of cerebral blood flow and brain lesions in newborn infants. Lancet. 1998;352:1406
  38. Als H, Duffy FH, McAnulty GB, et al. Early experience alters brain function and structure. Pediatrics. 2004;113:846–857
  39. Limperopoulos C, Gauvreau KK, O'Leary H, et al. Cerebral hemodynamic changes during intensive care of preterm infants. Pediatrics. 2008;122:e1006–e1013
  40. Mosca F, Colnaghi M, Lattanzio M, et al. Closed versus open endotracheal suctioning in preterm infants: Effects on cerebral oxygenation and blood volume. Biol Neonate. 1997;72:9–14
  41. Segar JL, Merrill DC, Chapleau MW, et al. Hemodynamic changes during endotracheal suctioning are mediated by increased autonomic activity. Pediatr Res. 1993;33:649–652
  42. Danford DA, Miske S, Headley J, et al. Effects of routine care procedures on transcutaneous oxygen in neonates: A quantitative approach. Arch Dis Child. 1983;58:20–23
  43. Stevens B, McGrath P, Gibbins S, et al. Determining behavioural and physiological responses to pain in infants at risk for neurological impairment. Pain. 2007;127:94–102
  44. Gibbins S, Stevens B, Beyene J, et al. Pain behaviours in extremely low gestational age infants. Early Hum Dev. 2008;84:451–458
  45. Wolfberg AJ, Robinson JN, Mulkern R, et al. Identification of fetal cerebral lactate using magnetic resonance spectroscopy. Am J Obstet Gynecol. 2007;196:e9–e11
  46. Azpurua H, Alvarado A, Mayobre F, et al. Metabolic assessment of the brain using proton magnetic resonance spectroscopy in a growth-restricted human fetus: Case report. Am J Perinatol. 2008;25:305–309
  47. Limperopoulos C, Tworetzky W, McElhinney DB, et al: Brain volume and metabolism in fetuses with congenital heart disease: Evaluation with quantitative magnetic resonance imaging and spectroscopy. Circulation (in press)
  48. Dautry C, Vaufrey F, Brouillet E, et al. Early N-acetylaspartate depletion is a marker of neuronal dysfunction in rats and primates chronically treated with the mitochondrial toxin 3-nitropropionic acid. J Cereb Blood Flow Metab. 2000;20:789–799
  49. Demougeot C, Garnier P, Mossiat C, et al. N-acetylaspartate, a marker of both cellular dysfunction and neuronal loss: Its relevance to studies of acute brain injury. J Neurochem. 2001;77:408–415
  50. Girard N, Fogliarini C, Viola A, et al. MRS of normal and impaired fetal brain development. Eur J Radiol. 2006;57:217–225
  51. Seghier ML, Lazeyras F, Huppi PS. Functional MRI of the newborn. Semin Fetal Neonatal Med. 2006;11:479–488
  52. Heep A, Scheef L, Jankowski J, et al. Functional magnetic resonance imaging of the sensorimotor system in preterm infants. Pediatrics. 2009;123:294–300
  53. Lin W, Zhu Q, Gao W, et al. Functional connectivity MR imaging reveals cortical functional connectivity in the developing brain. AJNR Am J Neuroradiol. 2008;29:1883–1889
  54. Arichi T, Moraux A, Melendez A, et al: Somatosensory cortical activation identified by functional MRI in preterm and term infants. Neuroimage (in press)
  55. Fransson P, Skiold B, Engstrom M, et al. Spontaneous brain activity in the newborn brain during natural sleep—An fMRI study in infants born at full term. Pediatr Res. 2009;66:301–305
  56. Buehler DM, Als H, Duffy FH, et al. Effectiveness of individualized developmental care for low-risk preterm infants: Behavioral and electrophysiologic evidence. Pediatrics. 1995;96:923–932
  57. Anand KJ, Scalzo FM. Can adverse neonatal experiences alter brain development and subsequent behavior?. Biol Neonate. 2000;77:69–82
  58. Als H. Reading the premature infant. In:  Goldsen E editors. Developmental Interventions in the Neonatal Intensive Care Nursery. New York, NY: Oxford University Press; 1999;p. 18–85
  59. Als H, Lawhon G, Duffy FH, et al. Individualized developmental care for the very low-birth-weight preterm infant. JAMA. 1994;272:853–858
  60. Meek JH, Firbank M, Elwell CE, et al. Regional hemodynamic responses to visual stimulation in awake infants. Pediatr Res. 1998;43:840–843
  61. Shah AR, Kurth CD, Gwiazdowski SG, et al. Fluctuations in cerebral oxygenation and blood volume during endotracheal suctioning in premature infants. J Pediatr. 1992;120:769–774
  62. Azzopardi DV, Strohm B, Edwards AD, et al. Moderate hypothermia to treat perinatal asphyxial encephalopathy. N Engl J Med. 2009;361:1349–1358
  63. Shankaran S, Laptook AR, Ehrenkranz RA, et al. Whole-body hypothermia for neonates with hypoxic-ischemic encephalopathy. N Engl J Med. 2005;353:1574–1584
  64. Amess PN, Penrice J, Cady EB, et al. Mild hypothermia after severe transient hypoxia-ischemia reduces the delayed rise in cerebral lactate in the newborn piglet. Pediatr Res. 1997;41:803–808
  65. Groenendaal F, Veenhoven RH, van der Grond J, et al. Cerebral lactate and N-acetyl-aspartate/choline ratios in asphyxiated full-term neonates demonstrated in vivo using proton magnetic resonance spectroscopy. Pediatr Res. 1994;35:148–151
  66. Hanrahan JD, Sargentoni J, Azzopardi D, et al. Cerebral metabolism within 18 hours of birth asphyxia: A proton magnetic resonance spectroscopy study. Pediatr Res. 1996;39:584–590
  67. Penrice J, Lorek A, Cady EB, et al. Proton magnetic resonance spectroscopy of the brain during acute hypoxia-ischemia and delayed cerebral energy failure in the newborn piglet. Pediatr Res. 1997;41:795–802
  68. Penrice J, Thoresen M, Lorek A, et al. Mild hypothermia following severe hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Early Hum Dev. 1994;39:146A
  69. Thoresen M, Penrice J, Lorek A, et al. Mild hypothermia after severe transient hypoxia-ischemia ameliorates delayed cerebral energy failure in the newborn piglet. Pediatr Res. 1995;37:667–670
  70. Schlaug G, Benfield A, Baird AE, et al. The ischemic penumbra: Operationally defined by diffusion and perfusion MRI. Neurology. 1999;53:1528–1537
  71. Kidwell CS, Saver JL, Mattiello J, et al. Diffusion-perfusion MR evaluation of perihematomal injury in hyperacute intracerebral hemorrhage. Neurology. 2001;57:1611–1617
  72. Paiva FF, Tannus A, Silva AC. Measurement of cerebral perfusion territories using arterial spin labelling. NMR Biomed. 2007;20:633–642
  73. Petersen ET, Zimine I, Ho YC, et al. Non-invasive measurement of perfusion: A critical review of arterial spin labelling techniques. Br J Radiol. 2006;79:688–701
  74. Buckley EM, Cook NM, Durduran T, et al. Cerebral hemodynamics in preterm infants during positional intervention measured with diffuse correlation spectroscopy and transcranial Doppler ultrasound. Opt Express. 2009;17:12571–12581
  75. Woodward LJ, Anderson PJ, Austin NC, et al. Neonatal MRI to predict neurodevelopmental outcomes in preterm infants. N Engl J Med. 2006;355:685–694
  76. Nanba Y, Matsui K, Aida N, et al. Magnetic resonance imaging regional T1 abnormalities at term accurately predict motor outcome in preterm infants. Pediatrics. 2007;120:e10–e19
  77. Rutherford MA, Pennock JM, Counsell SJ, et al. Abnormal magnetic resonance signal in the internal capsule predicts poor neurodevelopmental outcome in infants with hypoxic-ischemic encephalopathy. Pediatrics. 1998;102:323–328
  78. Cowan FM, de Vries LS. The internal capsule in neonatal imaging. Semin Fetal Neonatal Med. 2005;10:461–474
  79. Roelants-van Rijn AM, Nikkels PG, Groenendaal F, et al. Neonatal diffusion-weighted MR imaging: Relation with histopathology or follow-up MR examination. Neuropediatrics. 2001;32:286–294
  80. Bassi L, Ricci D, Volzone A, et al. Probabilistic diffusion tractography of the optic radiations and visual function in preterm infants at term equivalent age. Brain. 2008;131:573–582
  81. Berman JI, Mukherjee P, Partridge SC, et al. Quantitative diffusion tensor MRI fiber tractography of sensorimotor white matter development in premature infants. Neuroimage. 2005;27:862–871
  82. Partridge SC, Mukherjee P, Henry RG, et al. Diffusion tensor imaging: Serial quantitation of white matter tract maturity in premature newborns. Neuroimage. 2004;22:1302–1314
  83. Malik GK, Trivedi R, Gupta RK, et al. Serial quantitative diffusion tensor MRI of the term neonates with hypoxic-ischemic encephalopathy (HIE). Neuropediatrics. 2006;37:337–343
  84. Counsell SJ, Allsop JM, Harrison MC, et al. Diffusion-weighted imaging of the brain in preterm infants with focal and diffuse white matter abnormality. Pediatrics. 2003;112:1–7
  85. Krishnan ML, Dyet LE, Boardman JP, et al. Relationship between white matter apparent diffusion coefficients in preterm infants at term-equivalent age and developmental outcome at 2 years. Pediatrics. 2007;120:e604–e609
  86. Arzoumanian Y, Mirmiran M, Barnes PD, et al. Diffusion tensor brain imaging findings at term-equivalent age may predict neurologic abnormalities in low birth weight preterm infants. AJNR Am J Neuroradiol. 2003;24:1646–1653
  87. Rose J, Mirmiran M, Butler EE, et al. Neonatal microstructural development of the internal capsule on diffusion tensor imaging correlates with severity of gait and motor deficits. Dev Med Child Neurol. 2007;49:745–750
  88. Limperopoulos C, Soul JS, Gauvreau K, et al. Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics. 2005;115:688–695
  89. Thompson DK, Warfield SK, Carlin JB, et al. Perinatal risk factors altering regional brain structure in the preterm infant. Brain. 2007;130:667–677
  90. Mewes AU, Huppi PS, Als H, et al. Regional brain development in serial magnetic resonance imaging of low-risk preterm infants. Pediatrics. 2006;118:23–33
  91. Peterson BS, Anderson AW, Ehrenkranz R, et al. Regional brain volumes and their later neurodevelopmental correlates in term and preterm infants. Pediatrics. 2003;111:939–948
  92. Peterson BS, Vohr B, Staib LH, et al. Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA. 2000;284:1939–1947
  93. Nosarti C, Giouroukou E, Healy E, et al. Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome. Brain. 2008;131:205–217
  94. Tzarouchi LC, Astrakas LG, Xydis V, et al. Age-related grey matter changes in preterm infants: An MRI study. Neuroimage. 2009;47:1148–1153
  95. Kesler SR, Reiss AL, Vohr B, et al. Brain volume reductions within multiple cognitive systems in male preterm children at age twelve. J Pediatr. 2008;152:513–520520.e511
  96. Boardman JP, Counsell SJ, Rueckert D, et al. Early growth in brain volume is preserved in the majority of preterm infants. Ann Neurol. 2007;62:185–192
  97. Dubois J, Benders M, Borradori-Tolsa C, et al. Primary cortical folding in the human newborn: An early marker of later functional development. Brain. 2008;131:2028–2041
  98. Dubois J, Benders M, Cachia A, et al. Mapping the early cortical folding process in the preterm newborn brain. Cereb Cortex. 2008;18:1444–1454
  99. Ramenghi LA, Fumagalli M, Righini A, et al. Magnetic resonance imaging assessment of brain maturation in preterm neonates with punctate white matter lesions. Neuroradiology. 2007;49:161–167
  100. Granziera C, Schmahmann JD, Hadjikhani N, et al. Diffusion spectrum imaging shows the structural basis of functional cerebellar circuits in the human cerebellum in vivo. PLoS One. 2009;4:e5101
  101. Wedeen VJ, Wang RP, Schmahmann JD, et al. Diffusion spectrum magnetic resonance imaging (DSI) tractography of crossing fibers. Neuroimage. 2008;41:1267–1277
  102. Limperopoulos C, Soul JS, Haidar H, et al. Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics. 2005;116:844–850
  103. Rollins NK, Wen TS, Dominguez R. Crossed cerebellar atrophy in children: A neurologic sequela of extreme prematurity. Pediatr Radiol. 1995;25(suppl 1):S20–S25
  104. Niimura K, Chugani DC, Muzik O, et al. Cerebellar reorganization following cortical injury in humans: Effects of lesion size and age. Neurology. 1999;52:792–797
  105. Fair DA, Cohen AL, Dosenbach NU, et al. The maturing architecture of the brain's default network. Proc Natl Acad Sci USA. 2008;105:4028–4032
  106. Fransson P, Skiold B, Horsch S, et al. Resting-state networks in the infant brain. Proc Natl Acad Sci USA. 2007;104:15531–15536
  107. Bonnier C. Evaluation of early stimulation programs for enhancing brain development. Acta Paediatr. 2008;97:853–858
  108. Berger SE, Holt-Turner I, Cupoli JM, et al. Caring for the graduate from the neonatal intensive care unit: At home, in the office, and in the community. Pediatr Clin North Am. 1998;45:701–712
  109. Orton J, Spittle A, Doyle L, et al. Do early intervention programmes improve cognitive and motor outcomes for preterm infants after discharge? (A systematic review). Dev Med Child Neurol. 2009;51:851–859
  110. Mathur AM, Neil JJ, McKinstry RC, et al. Transport, monitoring, and successful brain MR imaging in unsedated neonates. Pediatr Radiol. 2008;38:260–264
  111. Almli CR, Rivkin MJ, McKinstry RC Brain Development Cooperative Group. The NIH MRI study of normal brain development (objective-2): Newborns, infants, toddlers, and preschoolers. Neuroimage. 2007;35:308–325

 This study was supported in part by the Canadian Institutes of Health Research. Dr Limperopoulos is supported by the Canada Research Chairs Program, Canada Research Chair in Brain and Development.

 Catherine Limperopoulos is a Canada Research Chair in Brain and Child Development, Assistant Professor, Departments of Neurology and Neurosurgery, School of Physical and Occupational Therapy in Pediatrics; McGill University, Montreal, Quebec, Canada; Fetal-Neonatal Neurology Research Group, Department of Neurology, Children's Hospital Boston and Harvard Medical School, Boston, Massachusetts.

PII: S0146-0005(09)00099-8

doi: 10.1053/j.semperi.2009.12.001

Seminars in Perinatology
Volume 34, Issue 1 , Pages 93-101 , February 2010