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Neural Plasticity
Volume 2016, Article ID 4901014, 16 pages
http://dx.doi.org/10.1155/2016/4901014
Review Article

Plasticity in the Neonatal Brain following Hypoxic-Ischaemic Injury

UCL Institute for Women’s Health, Maternal & Fetal Medicine, Perinatal Brain Repair Group, London WC1E 6HX, UK

Received 13 November 2015; Revised 12 January 2016; Accepted 7 February 2016

Academic Editor: Zygmunt Galdzicki

Copyright © 2016 Eridan Rocha-Ferreira and Mariya Hristova. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. J. J. Kurinczuk, M. White-Koning, and N. Badawi, “Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy,” Early Human Development, vol. 86, no. 6, pp. 329–338, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. J. E. Lawn, S. Cousens, and J. Zupan, “4 Million neonatal deaths: when? Where? Why?” The Lancet, vol. 365, no. 9462, pp. 891–900, 2005. View at Publisher · View at Google Scholar
  3. J. E. Lawn, K. Kerber, C. Enweronu-Laryea, and S. Cousens, “3.6 million neonatal deaths-what is progressing and what is not?” Seminars in Perinatology, vol. 34, no. 6, pp. 371–386, 2010. View at Publisher · View at Google Scholar · View at Scopus
  4. H. B. Sarnat and M. S. Sarnat, “Neonatal encephalopathy following fetal distress. A clinical and electroencephalographic study,” Archives of Neurology, vol. 33, no. 10, pp. 696–705, 1976. View at Publisher · View at Google Scholar · View at Scopus
  5. R. D. Sanders, H. J. Manning, N. J. Robertson et al., “Preconditioning and postinsult therapies for perinatal hypoxic-ischemic injury at term,” Anesthesiology, vol. 113, no. 1, pp. 233–249, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. R. C. Vannucci, “Experimental biology of cerebral hypoxia-ischemia: relation to perinatal brain damage,” Pediatric Research, vol. 27, no. 4, part 1, pp. 317–326, 1990. View at Publisher · View at Google Scholar · View at Scopus
  7. A. Jensen and R. Berger, “Fetal circulatory responses to oxygen lack,” Journal of Developmental Physiology, vol. 16, no. 4, pp. 181–207, 1991. View at Google Scholar · View at Scopus
  8. A. J. Gunn, J. T. Parer, E. C. Mallard, C. E. Williams, and P. D. Gluckman, “Cerebral histologic and electrocorticographic changes after asphyxia in fetal sheep,” Pediatric Research, vol. 31, no. 5, pp. 486–491, 1992. View at Publisher · View at Google Scholar · View at Scopus
  9. A. Jensen, Y. Garnier, and R. Berger, “Dynamics of fetal circulatory responses to hypoxia and asphyxia,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 84, no. 2, pp. 155–172, 1999. View at Publisher · View at Google Scholar · View at Scopus
  10. T. King and J. Parer, “The physiology of fetal heart rate patterns and perinatal asphyxia,” Journal of Perinatal and Neonatal Nursing, vol. 14, no. 3, pp. 19–103, 2000. View at Publisher · View at Google Scholar · View at Scopus
  11. K.-A. Hossmann, “Viability thresholds and the penumbra of focal ischemia,” Annals of Neurology, vol. 36, no. 4, pp. 557–565, 1994. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Locatelli, M. Incerti, A. Ghidini, M. Greco, E. Villa, and G. Paterlini, “Factors associated with umbilical artery acidemia in term infants with low Apgar scores at 5 min,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 139, no. 2, pp. 146–150, 2008. View at Publisher · View at Google Scholar · View at Scopus
  13. E. M. Graham, K. A. Ruis, A. L. Hartman, F. J. Northington, and H. E. Fox, “A systematic review of the role of intrapartum hypoxia-ischemia in the causation of neonatal encephalopathy,” American Journal of Obstetrics & Gynecology, vol. 199, no. 6, pp. 587–595, 2008. View at Publisher · View at Google Scholar · View at Scopus
  14. A. Jensen, Y. Garnier, J. Middelanis, and R. Berger, “Perinatal brain damage—from pathophysiology to prevention,” European Journal of Obstetrics Gynecology and Reproductive Biology, vol. 110, pp. S70–S79, 2003. View at Publisher · View at Google Scholar · View at Scopus
  15. R. Hausmann, S. Seidl, and P. Betz, “Hypoxic changes in Purkinje cells of the human cerebellum,” International Journal of Legal Medicine, vol. 121, no. 3, pp. 175–183, 2007. View at Publisher · View at Google Scholar · View at Scopus
  16. J. Brillault, T. I. Lam, J. M. Rutkowsky, S. Foroutan, and M. E. O'Donnell, “Hypoxia effects on cell volume and ion uptake of cerebral microvascular endothelial cells,” The American Journal of Physiology—Cell Physiology, vol. 294, no. 1, pp. C88–C96, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. A. Fatemi, M. A. Wilson, and M. V. Johnston, “Hypoxic-ischemic encephalopathy in the term infant,” Clinics in Perinatology, vol. 36, no. 4, pp. 835–858, 2009. View at Publisher · View at Google Scholar
  18. P. J. Magistretti, L. Pellerin, D. L. Rothman, and R. G. Shulman, “Energy on demand,” Science, vol. 283, no. 5401, pp. 496–497, 1999. View at Publisher · View at Google Scholar · View at Scopus
  19. L. T. L. Sie, M. S. Van Der Knaap, J. Oosting, L. S. De Vries, H. N. Lafeber, and J. Valk, “MR patterns of hypoxic-ischemic brain damage after prenatal, perinatal or postnatal asphyxia,” Neuropediatrics, vol. 31, no. 3, pp. 128–136, 2000. View at Publisher · View at Google Scholar · View at Scopus
  20. M. V. Johnston, W. H. Trescher, A. Ishida, W. Nakajima, and A. Zipursky, “Neurobiology of hypoxic-ischemic injury in the developing brain,” Pediatric Research, vol. 49, no. 6, pp. 735–741, 2001. View at Publisher · View at Google Scholar · View at Scopus
  21. M. V. Johnston, W. Nakajima, and H. Hagberg, “Mechanisms of hypoxic neurodegeneration in the developing brain,” Neuroscientist, vol. 8, no. 3, pp. 212–220, 2002. View at Publisher · View at Google Scholar · View at Scopus
  22. D. W. Choi, “Calcium-mediated neurotoxicity: relationship to specific channel types and role in ischemic damage,” Trends in Neurosciences, vol. 11, no. 10, pp. 465–469, 1988. View at Publisher · View at Google Scholar · View at Scopus
  23. K. Biagas, “Hypoxic-ischemic brain injury: advancements in the understanding of mechanisms and potential avenues for therapy,” Current Opinion in Pediatrics, vol. 11, no. 3, pp. 223–228, 1999. View at Publisher · View at Google Scholar · View at Scopus
  24. D. M. Ferriero, “Neonatal brain injury,” The New England Journal of Medicine, vol. 351, no. 19, pp. 1985–1995, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. J. J. Volpe, “Neonatal encephalopathy: an inadequate term for hypoxic-ischemic encephalopathy,” Annals of Neurology, vol. 72, no. 2, pp. 156–166, 2012. View at Publisher · View at Google Scholar · View at Scopus
  26. T. Kristián and B. K. Siesjö, “Calcium-related damage in ischemia,” Life Sciences, vol. 59, no. 5-6, pp. 357–367, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. H. Hagberg, E. Gilland, N.-H. Diemer, and P. Andine, “Hypoxia-ischemia in the neonatal rat brain: histopathology after post-treatment with NMDA and Non-NMDA receptor antagonists,” Biology of the Neonate, vol. 66, no. 4, pp. 205–213, 1994. View at Publisher · View at Google Scholar · View at Scopus
  28. M. Hedtjärn, C. Mallard, and H. Hagberg, “Inflammatory gene profiling in the developing mouse brain after hypoxia-ischemia,” Journal of Cerebral Blood Flow and Metabolism, vol. 24, no. 12, pp. 1333–1351, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. M. Winerdal, M. E. Winerdal, J. Kinn, V. Urmaliya, O. Winqvist, and U. Ådén, “Long lasting local and systemic inflammation after cerebral hypoxic ischemia in Newborn Mice,” PLoS ONE, vol. 7, no. 5, Article ID e36422, 10 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. M. Hedtjärn, A.-L. Leverin, K. Eriksson, K. Blomgren, C. Mallard, and H. Hagberg, “Interleukin-18 involvement in hypoxic-ischemic brain injury,” The Journal of Neuroscience, vol. 22, no. 14, pp. 5910–5919, 2002. View at Google Scholar · View at Scopus
  31. U. Ådén, G. Favrais, F. Plaisant et al., “Systemic inflammation sensitizes the neonatal brain to excitotoxicity through a pro-/anti-inflammatory imbalance: key role of TNFα pathway and protection by etanercept,” Brain, Behavior, and Immunity, vol. 24, no. 5, pp. 747–758, 2010. View at Publisher · View at Google Scholar
  32. J. A. Wixey, H. E. Reinebrant, S. J. Spencer, and K. M. Buller, “Efficacy of post-insult minocycline administration to alter long-term hypoxia-ischemia-induced damage to the serotonergic system in the immature rat brain,” Neuroscience, vol. 182, pp. 184–192, 2011. View at Publisher · View at Google Scholar · View at Scopus
  33. J. E. Rice III, R. C. Vannucci, and J. B. Brierley, “The influence of immaturity on hypoxic-ischemic brain damage in the rat,” Annals of Neurology, vol. 9, no. 2, pp. 131–141, 1981. View at Publisher · View at Google Scholar · View at Scopus
  34. R. C. Vannucci, J. R. Connor, D. T. Mauger et al., “Rat model of perinatal hypoxic-ischemic brain damage,” Journal of Neuroscience Research, vol. 55, no. 2, pp. 158–163, 1999. View at Publisher · View at Google Scholar · View at Scopus
  35. Y. Deng, J. Lu, V. Sivakumar, E. A. Ling, and C. Kaur, “Amoeboid microglia in the periventricular white matter induce oligodendrocyte damage through expression of proinflammatory cytokines via MAP kinase signaling pathway in hypoxic neonatal rats,” Brain Pathology, vol. 18, no. 3, pp. 387–400, 2008. View at Publisher · View at Google Scholar · View at Scopus
  36. Y. Y. Deng, J. Lu, E.-A. Ling, and C. Kaur, “Microglia-derived macrophage colony stimulating factor promotes generation of proinflammatory cytokines by astrocytes in the periventricular white matter in the hypoxic neonatal brain,” Brain Pathology, vol. 20, no. 5, pp. 909–925, 2010. View at Publisher · View at Google Scholar · View at Scopus
  37. A. A. Baburamani, V. G. Supramaniam, H. Hagberg, and C. Mallard, “Microglia toxicity in preterm brain injury,” Reproductive Toxicology, vol. 48, pp. 106–112, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. L. Li, A. Lundkvist, D. Andersson et al., “Protective role of reactive astrocytes in brain ischemia,” Journal of Cerebral Blood Flow and Metabolism, vol. 28, no. 3, pp. 468–481, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. Z. Liu, Y. Li, Y. Cui et al., “Beneficial effects of gfap/vimentin reactive astrocytes for axonal remodeling and motor behavioral recovery in mice after stroke,” Glia, vol. 62, pp. 2022–2033, 2014. View at Publisher · View at Google Scholar · View at Scopus
  40. K. Järlestedt, C. I. Rousset, M. Faiz et al., “Attenuation of reactive gliosis does not affect infarct volume in neonatal hypoxic-ischemic brain injury in mice,” PLoS ONE, vol. 5, no. 4, Article ID e10397, 7 pages, 2010. View at Publisher · View at Google Scholar · View at Scopus
  41. T. S. U. Morken, E. Brekke, A. Haberg, M. Wideroe, A.-M. Brubakk, and U. Sonnewald, “Altered astrocyte-neuronal interactions after hypoxia-ischemia in the neonatal brain in female and male rats,” Stroke, vol. 45, no. 9, pp. 2777–2785, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. E. Sen and S. W. Levison, “Astrocytes and developmental white matter disorders,” Mental Retardation and Developmental Disabilities Research Reviews, vol. 12, no. 2, pp. 97–104, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. C. C. Leonardo, A. K. Eakin, J. M. Ajmo et al., “Delayed administration of a matrix metalloproteinase inhibitor limits progressive brain injury after hypoxia-ischemia in the neonatal rat,” Journal of Neuroinflammation, vol. 5, article 34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. M. Xiong, Y. Yang, G.-Q. Chen, and W.-H. Zhou, “Post-ischemic hypothermia for 24 h in P7 rats rescues hippocampal neuron: association with decreased astrocyte activation and inflammatory cytokine expression,” Brain Research Bulletin, vol. 79, no. 6, pp. 351–357, 2009. View at Publisher · View at Google Scholar · View at Scopus
  45. S. Hudome, C. Palmer, R. L. Roberts, D. Mauger, C. Housman, and J. Towfighi, “The role of neutrophils in the production of hypoxic-ischemic brain injury in the neonatal rat,” Pediatric Research, vol. 41, no. 5, pp. 607–616, 1997. View at Publisher · View at Google Scholar · View at Scopus
  46. E. Bona, A.-L. Andersson, K. Blomgren et al., “Chemokine and inflammatory cell response to hypoxia-ischemia in immature rats,” Pediatric Research, vol. 45, no. 4, part 1, pp. 500–509, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. C. Palmer, R. L. Roberts, and P. I. Young, “Timing of neutrophil depletion influences long-term neuroprotection in neonatal rat hypoxic-ischemic brain injury,” Pediatric Research, vol. 55, no. 4, pp. 549–556, 2004. View at Publisher · View at Google Scholar · View at Scopus
  48. F. J. Northington, D. M. Ferriero, D. L. Flock, and L. J. Martin, “Delayed neurodegeneration in neonatal rat thalamus after hypoxia-ischemia is apoptosis,” The Journal of Neuroscience, vol. 21, no. 6, pp. 1931–1938, 2001. View at Google Scholar · View at Scopus
  49. N. Benjelloun, S. Renolleau, A. Represa, Y. Ben-Ari, and C. Charriaut-Marlangue, “Inflammatory responses in the cerebral cortex after ischemia in the P7 neonatal rat,” Stroke, vol. 30, no. 9, pp. 1916–1924, 1999. View at Publisher · View at Google Scholar · View at Scopus
  50. J. Wang and Q. Lu, “Expression of T subsets and mIL-2R in peripheral blood of newborns with hypoxic ischemic encephalopathy,” World Journal of Pediatrics, vol. 4, no. 2, pp. 140–144, 2008. View at Publisher · View at Google Scholar
  51. E. Rocha-Ferreira and M. Hristova, “Antimicrobial peptides and complement in neonatal hypoxia-ischemia induced brain damage,” Frontiers in Immunology, vol. 6, article 56, 2015. View at Publisher · View at Google Scholar
  52. Y. Jin, A. J. Silverman, and S. J. Vannucci, “Mast cells are early responders after hypoxia-ischemia in immature rat brain,” Stroke, vol. 40, no. 9, pp. 3107–3112, 2009. View at Publisher · View at Google Scholar · View at Scopus
  53. G. S. Kendall, M. Hirstova, S. Horn et al., “TNF gene cluster deletion abolishes lipopolysaccharide-mediated sensitization of the neonatal brain to hypoxic ischemic insult,” Laboratory Investigation, vol. 91, no. 3, pp. 328–341, 2011. View at Publisher · View at Google Scholar · View at Scopus
  54. A. Kichev, C. I. Rousset, A. A. Baburamani et al., “Tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) signaling and cell death in the immature central nervous system after hypoxia-ischemia and inflammation,” The Journal of Biological Chemistry, vol. 289, no. 13, pp. 9430–9439, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. M. V. Johnston, W. H. Trescher, A. Ishida, W. Nakajima, and A. Zipursky, “Neurobiology of hypoxic-ischemic injury in the developing brain,” Pediatric Research, vol. 49, no. 6, pp. 735–741, 2001. View at Publisher · View at Google Scholar
  56. P. S. McQuillen, R. A. Sheldon, C. J. Shatz, and D. M. Ferriero, “Selective vulnerability of subplate neurons after early neonatal hypoxia-ischemia,” The Journal of Neuroscience, vol. 23, no. 8, pp. 3308–3315, 2003. View at Google Scholar · View at Scopus
  57. R. Schmidt-Kastner, “Genomic approach to selective vulnerability of the hippocampus in brain ischemia-hypoxia,” Neuroscience, vol. 309, pp. 259–279, 2015. View at Publisher · View at Google Scholar
  58. A. J. Barkovich, B. L. Hajnal, D. Vigneron et al., “Prediction of neuromotor outcome in perinatal asphyxia: evaluation of MR scoring systems,” American Journal of Neuroradiology, vol. 19, no. 1, pp. 143–149, 1998. View at Google Scholar · View at Scopus
  59. J. J. Volpe, “Perinatal brain injury: from pathogenesis to neuroprotection,” Mental Retardation and Developmental Disabilities Research Reviews, vol. 7, no. 1, pp. 56–64, 2001. View at Publisher · View at Google Scholar · View at Scopus
  60. L. J. Martin, A. Brambrink, R. C. Koehler, and R. J. Traystman, “Primary sensory and forebrain motor systems in the newborn brain are preferentially damaged by hypoxia-ischemia,” Journal of Comparative Neurology, vol. 377, no. 2, pp. 262–285, 1997. View at Publisher · View at Google Scholar · View at Scopus
  61. J. H. Menkes and J. Curran, “Clinical and MR correlates in children with extrapyramidal cerebral palsy,” American Journal of Neuroradiology, vol. 15, no. 3, pp. 451–457, 1994. View at Google Scholar · View at Scopus
  62. A. H. Hoon Jr., E. M. Reinhardt, R. I. Kelley et al., “Brain magnetic resonance imaging in suspected extrapyramidal cerebral palsy: observations in distinguishing genetic-metabolic from acquired causes,” Journal of Pediatrics, vol. 131, no. 2, pp. 240–245, 1997. View at Publisher · View at Google Scholar · View at Scopus
  63. R. P. Skoff, D. Bessert, J. D. E. Barks, and F. S. Silverstein, “Plasticity of neurons and glia following neonatal hypoxic-ischemic brain injury in rats,” Neurochemical Research, vol. 32, no. 2, pp. 331–342, 2007. View at Publisher · View at Google Scholar · View at Scopus
  64. R. Geddes, R. C. Vannucci, and S. J. Vannucci, “Delayed cerebral atrophy following moderate hypoxia-ischemia in the immature rat,” Developmental Neuroscience, vol. 23, no. 3, pp. 180–185, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. M. Blennow, M. Ingvar, H. Lagercrantz et al., “Early [18F]FDG positron emission tomography in infants with hypoxic-ischaemic encephalopathy shows hypermetabolism during the postasphyctic period,” Acta Paediatrica, vol. 84, no. 11, pp. 1289–1295, 1995. View at Publisher · View at Google Scholar · View at Scopus
  66. Y. Pu, Q.-F. Li, C.-M. Zeng et al., “Increased detectability of alpha brain glutamate/glutamine in neonatal hypoxic-ischemic encephalopathy,” American Journal of Neuroradiology, vol. 21, no. 1, pp. 203–212, 2000. View at Google Scholar · View at Scopus
  67. L. Sokoloff, “Energetics of functional activation in neural tissues,” Neurochemical Research, vol. 24, no. 2, pp. 321–329, 1999. View at Publisher · View at Google Scholar · View at Scopus
  68. N. R. Sibson, A. Dhankhar, G. F. Mason, D. L. Rothman, K. L. Behar, and R. G. Shulman, “Stoichiometric coupling of brain glucose metabolism and glutamatergic neuronal activity,” Proceedings of the National Academy of Sciences of the United States of America, vol. 95, no. 1, pp. 316–321, 1998. View at Publisher · View at Google Scholar · View at Scopus
  69. Z. Pfund, D. C. Chugani, C. Juhász et al., “Evidence for coupling between glucose metabolism and glutamate cycling using FDG PET and 1H magnetic resonance spectroscopy in patients with epilepsy,” Journal of Cerebral Blood Flow and Metabolism, vol. 20, no. 5, pp. 871–878, 2000. View at Google Scholar · View at Scopus
  70. G. E. Alexander and M. D. Crutcher, “Functional architecture of basal ganglia circuits: neural substrates of parallel processing,” Trends in Neurosciences, vol. 13, no. 7, pp. 266–271, 1990. View at Publisher · View at Google Scholar · View at Scopus
  71. M. V. Johnston and A. H. Hoon, “Possible mechanisms in infants for selective basal ganglia damage from asphyxia, kernicterus, or mitochondrial encephalopathies,” Journal of Child Neurology, vol. 15, no. 9, pp. 588–591, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. H. Hagberg, E. Thornberg, M. Blennow et al., “Excitatory amino acids in the cerebrospinal fluid of asphyxiated infants: relationship to hypoxic-ischemic encephalopathy,” Acta Paediatrica, vol. 82, no. 11, pp. 925–929, 1993. View at Publisher · View at Google Scholar · View at Scopus
  73. M. Dallas, H. E. Boycott, L. Atkinson et al., “Hypoxia suppresses glutamate transport in astrocytes,” The Journal of Neuroscience, vol. 27, no. 15, pp. 3946–3955, 2007. View at Publisher · View at Google Scholar · View at Scopus
  74. M. Murugan, E.-A. Ling, and C. Kaur, “Dysregulated glutamate uptake by astrocytes causes oligodendroglia death in hypoxic perventricular white matter damage,” Molecular and Cellular Neuroscience, vol. 56, pp. 342–354, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. P. K. Stys, “General mechanisms of axonal damage and its prevention,” Journal of the Neurological Sciences, vol. 233, no. 1-2, pp. 3–13, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. Y. Bakiri, N. B. Hamilton, R. Káradóttir, and D. Attwell, “Testing NMDA receptor block as a therapeutic strategy for reducing ischaemic damage to CNS white matter,” Glia, vol. 56, no. 2, pp. 233–240, 2008. View at Publisher · View at Google Scholar · View at Scopus
  77. R. Káradóttir, P. Cavelier, L. H. Bergersen, and D. Attwell, “NMDA receptors are expressed in oligodendrocytes and activated in ischaemia,” Nature, vol. 438, no. 7071, pp. 1162–1166, 2005. View at Publisher · View at Google Scholar · View at Scopus
  78. V. Gallo and B. Deneen, “Glial development: the crossroads of regeneration and repair in the CNS,” Neuron, vol. 83, no. 2, pp. 283–308, 2014. View at Publisher · View at Google Scholar · View at Scopus
  79. Z. Yang and S. W. Levison, “Hypoxia/ischemia expands the regenerative capacity of progenitors in the perinatal subventricular zone,” Neuroscience, vol. 139, no. 2, pp. 555–564, 2006. View at Publisher · View at Google Scholar · View at Scopus
  80. A. U. Zaidi, D. A. Bessert, J. E. Ong et al., “New oligodendrocytes are generated after neonatal hypoxic-ischemic brain injury in rodents,” Glia, vol. 46, no. 4, pp. 380–390, 2004. View at Publisher · View at Google Scholar · View at Scopus
  81. R. P. Skoff, M. S. Ghandour, and P. E. Knapp, “Postmitotic oligodendrocytes generated during postnatal cerebral development are derived from proliferation of immature oligodendrocytes,” Glia, vol. 12, no. 1, pp. 12–23, 1994. View at Publisher · View at Google Scholar · View at Scopus
  82. P. S. McQuillen, M. F. DeFreitas, G. Zada, and C. J. Shatz, “A novel role for p75NTR in subplate growth cone complexity and visual thalamocortical innervation,” Journal of Neuroscience, vol. 22, no. 9, pp. 3580–3593, 2002. View at Google Scholar · View at Scopus
  83. J. J. M. Chun, M. J. Makamura, and C. J. Shatz, “Transient cells of the developing mammalian telencephalon are peptide-immunoreactive neurons,” Nature, vol. 325, no. 6105, pp. 617–620, 1987. View at Publisher · View at Google Scholar · View at Scopus
  84. P. O. Kanold, “Subplate neurons: crucial regulators of cortical development and plasticity,” Frontiers in Neuroanatomy, vol. 3, article 16, 2009. View at Publisher · View at Google Scholar · View at Scopus
  85. S. W. Levison, R. P. Rothstein, M. J. Romanko, M. J. Snyder, R. L. Meyers, and S. J. Vannucci, “Hypoxia/ischemia depletes the rat perinatal subventricular zone of oligodendrocyte progenitors and neural stem cells,” Developmental Neuroscience, vol. 23, no. 3, pp. 234–247, 2001. View at Publisher · View at Google Scholar · View at Scopus
  86. G. Cioni, B. Fazzi, M. Coluccini, L. Bartalena, A. Boldrini, and J. van Hof-van Duin, “Cerebral visual impairment in preterm infants with periventricular leukomalacia,” Pediatric Neurology, vol. 17, no. 4, pp. 331–338, 1997. View at Publisher · View at Google Scholar · View at Scopus
  87. J. Penrice, A. Lorek, E. B. Cady et al., “Proton magnetic resonance spectroscopy of the brain during acute hypoxia-ischemia and delayed cerebral energy failure in the newborn piglet,” Pediatric Research, vol. 41, no. 6, pp. 795–802, 1997. View at Publisher · View at Google Scholar · View at Scopus
  88. P. L. Hope, E. B. Cady, P. S. Tofts et al., “Cerebral energy metabolism studied with phosphorus NMR spectroscopy in normal and birth-asphyxiated infants,” The Lancet, vol. 324, no. 8399, pp. 366–370, 1984. View at Publisher · View at Google Scholar · View at Scopus
  89. E. Gilland, M. Puka-Sundvall, L. Hillered, and H. Hagberg, “Mitochondrial function and energy metabolism after hypoxia-ischemia in the immature rat brain: involvement of NMDA-receptors,” Journal of Cerebral Blood Flow and Metabolism, vol. 18, no. 3, pp. 297–304, 1998. View at Google Scholar · View at Scopus
  90. R. C. Vannucci, J. Y. Yager, and S. J. Vannucci, “Cerebral glucose and energy utilization during the evolution of hypoxic-ischemic brain damage in the immature rat,” Journal of Cerebral Blood Flow and Metabolism, vol. 14, no. 2, pp. 279–288, 1994. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Puka-Sundvall, B. Gajkowska, M. Cholewinski, K. Blomgren, J. W. Lazarewicz, and H. Hagberg, “Subcellular distribution of calcium and ultrastructural changes after cerebral hypoxia-ischemia in immature rats,” Developmental Brain Research, vol. 125, no. 1-2, pp. 31–41, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. C. E. Williams, A. Gunn, and P. D. Gluckman, “Time course of intracellular edema and epileptiform activity following prenatal cerebral ischemia in sheep,” Stroke, vol. 22, no. 4, pp. 516–521, 1991. View at Publisher · View at Google Scholar · View at Scopus
  93. A. Lorek, Y. Takei, E. B. Cady et al., “Delayed (‘secondary’) cerebral energy failure after acute hypoxia-ischemia in the newborn piglet: continuous 48-hour studies by phosphorus magnetic resonance spectroscopy,” Pediatric Research, vol. 36, no. 6, pp. 699–706, 1994. View at Publisher · View at Google Scholar · View at Scopus
  94. R. M. Blumberg, E. B. Cady, J. S. Wigglesworth, J. E. McKenzie, and A. D. Edwards, “Relation between delayed impairment of cerebral energy metabolism and infarction following transient focal hypoxia-ischaemia in the developing brain,” Experimental Brain Research, vol. 113, no. 1, pp. 130–137, 1997. View at Publisher · View at Google Scholar · View at Scopus
  95. J. P. Kehrer, “The Haber-Weiss reaction and mechanisms of toxicity,” Toxicology, vol. 149, no. 1, pp. 43–50, 2000. View at Publisher · View at Google Scholar · View at Scopus
  96. R. J. Traystman, J. R. Kirsch, and R. C. Koehler, “Oxygen radical mechanisms of brain injury following ischemia and reperfusion,” Journal of Applied Physiology, vol. 71, no. 4, pp. 1185–1195, 1991. View at Google Scholar · View at Scopus
  97. K. J. Davies and A. L. Goldberg, “Oxygen radicals stimulate intracellular proteolysis and lipid peroxidation by independent mechanisms in erythrocytes,” The Journal of Biological Chemistry, vol. 262, no. 17, pp. 8220–8226, 1987. View at Google Scholar · View at Scopus
  98. B. Vasiljevic, S. Maglajlic-Djukic, M. Gojnic, and S. Stankovic, “The role of oxidative stress in perinatal hypoxic-ischemic brain injury,” Srpski Arhiv za Celokupno Lekarstvo, vol. 140, no. 1-2, pp. 35–41, 2012. View at Publisher · View at Google Scholar
  99. C. Palmer, J. Towfighi, R. L. Roberts, and D. F. Heitjan, “Allopurinol administered after inducing hypoxia-ischemia reduces brain injury in 7-day-old rats,” Pediatric Research, vol. 33, no. 4, part 1, pp. 405–411, 1993. View at Google Scholar · View at Scopus
  100. E. Millerot-Serrurot, N. Bertrand, C. Mossiat et al., “Temporal changes in free iron levels after brain ischemia. Relevance to the timing of iron chelation therapy in stroke,” Neurochemistry International, vol. 52, no. 8, pp. 1442–1448, 2008. View at Publisher · View at Google Scholar · View at Scopus
  101. T.-I. Peng and J. T. Greenamyre, “Privileged access to mitochondria of calcium influx through N-methyl-D-aspartate receptors,” Molecular Pharmacology, vol. 53, no. 6, pp. 974–980, 1998. View at Google Scholar · View at Scopus
  102. M. Puka-Sundvall, U. Hallin, C. Zhu et al., “NMDA blockade attenuates caspase-3 activation and DNA fragmentation after neonatal hypoxia-ischemia,” NeuroReport, vol. 11, no. 13, pp. 2833–2836, 2000. View at Publisher · View at Google Scholar · View at Scopus
  103. J. S. Beckman, “The double-edged role of nitric oxide in brain function and superoxide-mediated injury,” Journal of Developmental Physiology, vol. 15, no. 1, pp. 53–59, 1991. View at Google Scholar · View at Scopus
  104. A. Bal-Price and G. C. Brown, “Inflammatory neurodegeneration mediated by nitric oxide from activated glia-inhibiting neuronal respiration, causing glutamate release and excitotoxicity,” Journal of Neuroscience, vol. 21, no. 17, pp. 6480–6491, 2001. View at Google Scholar · View at Scopus
  105. C. I. Rousset, A. A. Baburamani, C. Thornton, and H. Hagberg, “Mitochondria and perinatal brain injury,” Journal of Maternal-Fetal and Neonatal Medicine, vol. 25, supplement 1, pp. 35–38, 2012. View at Publisher · View at Google Scholar · View at Scopus
  106. Y. Hamada, T. Hayakawa, H. Hattori, and H. Mikawa, “Inhibitor of nitric oxide synthesis reduces hypoxic-ischemic brain damage in the neonatal rat,” Pediatric Research, vol. 35, no. 1, pp. 10–14, 1994. View at Publisher · View at Google Scholar · View at Scopus
  107. D. M. Ferriero, D. M. Holtzman, S. M. Black, and R. A. Sheldon, “Neonatal mice lacking neuronal nitric oxide synthase are less vulnerable to hypoxic-ischemic injury,” Neurobiology of Disease, vol. 3, no. 1, pp. 64–71, 1996. View at Publisher · View at Google Scholar · View at Scopus
  108. E. R. W. van den Tweel, C. M. P. C. D. Peeters-Scholte, F. van Bel, C. J. Heijnen, and F. Groenendaal, “Inhibition of nNOS and iNOS following hypoxia-ischaemia improves long-term outcome but does not influence the inflammatory response in the neonatal rat brain,” Developmental Neuroscience, vol. 24, no. 5, pp. 389–395, 2002. View at Publisher · View at Google Scholar · View at Scopus
  109. K. Blomgren and H. Hagberg, “Free radicals, mitochondria, and hypoxia-ischemia in the developing brain,” Free Radical Biology and Medicine, vol. 40, no. 3, pp. 388–397, 2006. View at Publisher · View at Google Scholar · View at Scopus
  110. C. L. Robertson, S. Scafidi, M. C. McKenna, and G. Fiskum, “Mitochondrial mechanisms of cell death and neuroprotection in pediatric ischemic and traumatic brain injury,” Experimental Neurology, vol. 218, no. 2, pp. 371–380, 2009. View at Publisher · View at Google Scholar · View at Scopus
  111. H. Hagberg, C. Mallard, C. I. Rousset, and X. Wang, “Apoptotic mechanisms in the immature brain: involvement of mitochondria,” Journal of Child Neurology, vol. 24, no. 9, pp. 1141–1146, 2009. View at Publisher · View at Google Scholar · View at Scopus
  112. B. Han, Q. Wang, G. Cui, X. Shen, and Z. Zhu, “Post-treatment of Bax-inhibiting peptide reduces neuronal death and behavioral deficits following global cerebral ischemia,” Neurochemistry International, vol. 58, no. 2, pp. 224–233, 2011. View at Publisher · View at Google Scholar · View at Scopus
  113. X. Wang, W. Han, X. Du et al., “Neuroprotective effect of Bax-inhibiting peptide on neonatal brain injury,” Stroke, vol. 41, no. 9, pp. 2050–2055, 2010. View at Publisher · View at Google Scholar · View at Scopus
  114. K. Blomgren, C. Zhu, U. Hallin, and H. Hagberg, “Mitochondria and ischemic reperfusion damage in the adult and in the developing brain,” Biochemical and Biophysical Research Communications, vol. 304, no. 3, pp. 551–559, 2003. View at Publisher · View at Google Scholar · View at Scopus
  115. H. Hagberg, “Mitochondrial impairment in the developing brain after hypoxia-ischemia,” Journal of Bioenergetics and Biomembranes, vol. 36, no. 4, pp. 369–373, 2004. View at Publisher · View at Google Scholar · View at Scopus
  116. S. P. Cregan, V. L. Dawson, and R. S. Slack, “Role of AIF in caspase-dependent and caspase-independent cell death,” Oncogene, vol. 23, no. 16, pp. 2785–2796, 2004. View at Publisher · View at Google Scholar · View at Scopus
  117. A. Hoshino, S. Matoba, E. Iwai-Kanai et al., “P53-TIGAR axis attenuates mitophagy to exacerbate cardiac damage after ischemia,” Journal of Molecular and Cellular Cardiology, vol. 52, no. 1, pp. 175–184, 2012. View at Publisher · View at Google Scholar · View at Scopus
  118. W. Yin, A. P. Signore, M. Iwai, G. Cao, Y. Gao, and J. Chen, “Rapidly increased neuronal mitochondrial biogenesis after hypoxic-ischemic brain injury,” Stroke, vol. 39, no. 11, pp. 3057–3063, 2008. View at Publisher · View at Google Scholar · View at Scopus
  119. F. J. Northington, M. E. Zelaya, D. P. O'Riordan et al., “Failure to complete apoptosis following neonatal hypoxia-ischemia manifests as ‘continuum’ phenotype of cell death and occurs with multiple manifestations of mitochondrial dysfunction in rodent forebrain,” Neuroscience, vol. 149, no. 4, pp. 822–833, 2007. View at Publisher · View at Google Scholar · View at Scopus
  120. C. Zhu, X. Wang, F. Xu et al., “The influence of age on apoptotic and other mechanisms of cell death after cerebral hypoxia-ischemia,” Cell Death and Differentiation, vol. 12, no. 2, pp. 162–176, 2005. View at Publisher · View at Google Scholar · View at Scopus
  121. W. Nakajima, A. Ishida, M. S. Lange et al., “Apoptosis has a prolonged role in the neurodegeneration after hypoxic ischemia in the newborn rat,” Journal of Neuroscience, vol. 20, no. 21, pp. 7994–8004, 2000. View at Google Scholar · View at Scopus
  122. Y. Li, C. Powers, N. Jiang, and M. Chopp, “Intact, injured, necrotic and apoptotic cells after focal cerebral ischemia in the rat,” Journal of the Neurological Sciences, vol. 156, no. 2, pp. 119–132, 1998. View at Publisher · View at Google Scholar · View at Scopus
  123. Y. Du, K. R. Bales, R. C. Dodel et al., “Activation of a caspase 3-related cysteine protease is required for glutamate-mediated apoptosis of cultured cerebellar granule neurons,” Proceedings of the National Academy of Sciences of the United States of America, vol. 94, no. 21, pp. 11657–11662, 1997. View at Publisher · View at Google Scholar · View at Scopus
  124. J. B. Schulz, M. Weller, and M. A. Moskowitz, “Caspases as treatment targets in stroke and neurodegenerative diseases,” Annals of Neurology, vol. 45, no. 4, pp. 421–429, 1999. View at Publisher · View at Google Scholar · View at Scopus
  125. Y. Cheng, M. Deshmukh, A. D'Costa et al., “Caspase inhibitor affords neuroprotection with delayed administration in a rat model of neonatal hypoxic-ischemic brain injury,” The Journal of Clinical Investigation, vol. 101, no. 9, pp. 1992–1999, 1998. View at Publisher · View at Google Scholar · View at Scopus
  126. B. R. Hu, C. L. Liu, Y. Ouyang, K. Blomgren, and B. K. Siesjö, “Involvement of caspase-3 in cell death after hypoxia-ischemia declines during brain maturation,” Journal of Cerebral Blood Flow and Metabolism, vol. 20, no. 9, pp. 1294–1300, 2000. View at Publisher · View at Google Scholar · View at Scopus
  127. Y. Carlsson, X. Wang, L. Schwendimann et al., “Combined effect of hypothermia and caspase-2 gene deficiency on neonatal hypoxic-ischemic brain injury,” Pediatric Research, vol. 71, no. 5, pp. 566–572, 2012. View at Publisher · View at Google Scholar · View at Scopus
  128. X. Wang, Y. Carlsson, E. Basso et al., “Developmental shift of cyclophilin D contribution to hypoxic-ischemic brain injury,” Journal of Neuroscience, vol. 29, no. 8, pp. 2588–2596, 2009. View at Publisher · View at Google Scholar · View at Scopus
  129. K. Blomgren, A. Mcrae, A. Elmered et al., “The calpain proteolytic system in neonatal hypoxic-ischemia,” Annals of the New York Academy of Sciences, vol. 825, pp. 104–119, 1997. View at Publisher · View at Google Scholar · View at Scopus
  130. J. Towfighi, N. Zec, J. Yager, C. Housman, and R. C. Vannucci, “Temporal evolution of neuropathologic changes in an immature rat model of cerebral hypoxia: a light microscopic study,” Acta Neuropathologica, vol. 90, no. 4, pp. 375–386, 1995. View at Publisher · View at Google Scholar · View at Scopus
  131. F. J. Northington, D. M. Ferriero, E. M. Graham, R. J. Traystman, and L. J. Martin, “Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis,” Neurobiology of Disease, vol. 8, no. 2, pp. 207–219, 2001. View at Publisher · View at Google Scholar · View at Scopus
  132. C. Portera-Cailliau, D. L. Price, and L. J. Martin, “Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum,” Journal of Comparative Neurology, vol. 378, no. 1, pp. 70–87, 1997. View at Google Scholar · View at Scopus
  133. K. Blomgren, M. Leist, and L. Groc, “Pathological apoptosis in the developing brain,” Apoptosis, vol. 12, no. 5, pp. 993–1010, 2007. View at Publisher · View at Google Scholar · View at Scopus
  134. R. A. Sheldon, J. J. Hall, L. J. Noble, and D. M. Ferriero, “Delayed cell death in neonatal mouse hippocampus from hypoxia-ischemia is neither apoptotic nor necrotic,” Neuroscience Letters, vol. 304, no. 3, pp. 165–168, 2001. View at Publisher · View at Google Scholar · View at Scopus
  135. M. Leist, B. Single, A. F. Castoldi, S. Kühnle, and P. Nicotera, “Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis,” The Journal of Experimental Medicine, vol. 185, no. 8, pp. 1481–1486, 1997. View at Publisher · View at Google Scholar · View at Scopus
  136. R. A. Lockshin and Z. Zakeri, “Apoptosis, autophagy, and more,” International Journal of Biochemistry and Cell Biology, vol. 36, no. 12, pp. 2405–2419, 2004. View at Publisher · View at Google Scholar · View at Scopus
  137. C. He and D. J. Klionsky, “Regulation mechanisms and signaling pathways of autophagy,” Annual Review of Genetics, vol. 43, pp. 67–93, 2009. View at Publisher · View at Google Scholar · View at Scopus
  138. F. J. Northington, R. Chavez-Valdez, and L. J. Martin, “Neuronal cell death in neonatal hypoxia-ischemia,” Annals of Neurology, vol. 69, no. 5, pp. 743–758, 2011. View at Publisher · View at Google Scholar · View at Scopus
  139. W. Bursch, “The autophagosomal-lysosomal compartment in programmed cell death,” Cell Death & Differentiation, vol. 8, no. 6, pp. 569–581, 2001. View at Publisher · View at Google Scholar · View at Scopus
  140. C. Descloux, V. Ginet, P. G. H. Clarke, J. Puyal, and A. Truttmann, “Neuronal death after perinatal cerebral hypoxia-ischemia: focus on autophagy—mediated cell death,” International Journal of Developmental Neuroscience, vol. 45, pp. 75–85, 2015. View at Publisher · View at Google Scholar
  141. E. Ogier-Denis and P. Codogno, “Autophagy: a barrier or an adaptive response to cancer,” Biochimica et Biophysica Acta (BBA)—Reviews on Cancer, vol. 1603, no. 2, pp. 113–128, 2003. View at Publisher · View at Google Scholar · View at Scopus
  142. V. Ginet, J. Puyal, P. G. H. Clarke, and A. C. Truttmann, “Enhancement of autophagic flux after neonatal cerebral hypoxia-ischemia and its region-specific relationship to apoptotic mechanisms,” The American Journal of Pathology, vol. 175, no. 5, pp. 1962–1974, 2009. View at Publisher · View at Google Scholar · View at Scopus
  143. V. Ginet, M. P. Pittet, C. Rummel et al., “Dying neurons in thalamus of asphyxiated term newborns and rats are autophagic,” Annals of Neurology, vol. 76, no. 5, pp. 695–711, 2014. View at Publisher · View at Google Scholar · View at Scopus
  144. M. Koike, M. Shibata, M. Tadakoshi et al., “Inhibition of autophagy prevents hippocampal pyramidal neuron death after hypoxic-ischemic injury,” The American Journal of Pathology, vol. 172, no. 2, pp. 454–469, 2008. View at Publisher · View at Google Scholar · View at Scopus
  145. C. Xie, V. Ginet, Y. Sun et al., “Neuroprotection by selective neuronal deletion of Atg7 in neonatal brain injury,” Autophagy, vol. 12, no. 2, pp. 410–423, 2016. View at Publisher · View at Google Scholar
  146. J. Puyal, A. Vaslin, V. Mottier, and P. G. H. Clarke, “Postischemic treatment of neonatal cerebral ischemia should target autophagy,” Annals of Neurology, vol. 66, no. 3, pp. 378–389, 2009. View at Publisher · View at Google Scholar · View at Scopus
  147. S. Carloni, G. Buonocore, and W. Balduini, “Protective role of autophagy in neonatal hypoxia-ischemia induced brain injury,” Neurobiology of Disease, vol. 32, no. 3, pp. 329–339, 2008. View at Publisher · View at Google Scholar · View at Scopus
  148. S. R. Mayoral, G. Omar, and A. A. Penn, “Sex differences in a hypoxia model of preterm brain damage,” Pediatric Research, vol. 66, no. 3, pp. 248–253, 2009. View at Publisher · View at Google Scholar · View at Scopus
  149. M. R. Golomb, J. A. Zimmer, and B. P. Garg, “Age-related variation in the presentation of childhood stroke varies with inclusion criteria,” Acta Paediatrica, vol. 99, no. 1, pp. 6–7, 2010. View at Publisher · View at Google Scholar · View at Scopus
  150. M. R. Golomb, H. J. Fullerton, U. Nowak-Gottl, and G. Deveber, “Male predominance in childhood ischemic stroke: findings from the international pediatric stroke study,” Stroke, vol. 40, no. 1, pp. 52–57, 2009. View at Publisher · View at Google Scholar · View at Scopus
  151. M. D. Lauterbach, S. Raz, and C. J. Sander, “Neonatal hypoxic risk in preterm birth infants: the influence of sex and severity of respiratory distress on cognitive recovery,” Neuropsychology, vol. 15, no. 3, pp. 411–420, 2001. View at Publisher · View at Google Scholar · View at Scopus
  152. A. L. Smith, M. Alexander, T. S. Rosenkrantz, M. L. Sadek, and R. H. Fitch, “Sex differences in behavioral outcome following neonatal hypoxia ischemia: insights from a clinical meta-analysis and a rodent model of induced hypoxic ischemic brain injury,” Experimental Neurology, vol. 254, pp. 54–67, 2014. View at Publisher · View at Google Scholar · View at Scopus
  153. J. L. Peacock, L. Marston, N. Marlow, S. A. Calvert, and A. Greenough, “Neonatal and infant outcome in boys and girls born very prematurely,” Pediatric Research, vol. 71, no. 3, pp. 305–310, 2012. View at Publisher · View at Google Scholar · View at Scopus
  154. B. Manwani and L. D. McCullough, “Sexual dimorphism in ischemic stroke: lessons from the laboratory,” Women's Health, vol. 7, no. 3, pp. 319–339, 2011. View at Publisher · View at Google Scholar · View at Scopus
  155. J. T. Lang and L. D. McCullough, “Pathways to ischemic neuronal cell death: are sex differences relevant?” Journal of Translational Medicine, vol. 6, article 33, 2008. View at Publisher · View at Google Scholar · View at Scopus
  156. C. C. Giza and M. L. Prins, “Is being plastic fantastic? Mechanisms of altered plasticity after developmental traumatic brain injury,” Developmental Neuroscience, vol. 28, no. 4-5, pp. 364–379, 2006. View at Publisher · View at Google Scholar · View at Scopus
  157. W. T. Greenough, F. R. Volkmar, and J. M. Juraska, “Effects of rearing complexity on dendritic branching in frontolateral and temporal cortex of the rat,” Experimental Neurology, vol. 41, no. 2, pp. 371–378, 1973. View at Publisher · View at Google Scholar · View at Scopus
  158. B. Jacobs, M. Schall, and A. B. Scheibel, “A quantitative dendritic analysis of Wernicke's area in humans. II. Gender, hemispheric, and environmental factors,” Journal of Comparative Neurology, vol. 327, no. 1, pp. 97–111, 1993. View at Publisher · View at Google Scholar · View at Scopus
  159. M. R. Rosenzweig and E. L. Bennett, “Psychobiology of plasticity: effects of training and experience on brain and behavior,” Behavioural Brain Research, vol. 78, no. 1, pp. 57–65, 1996. View at Publisher · View at Google Scholar · View at Scopus
  160. M. V. Johnston, “Excitotoxicity in perinatal brain injury,” Brain Pathology, vol. 15, no. 3, pp. 234–240, 2005. View at Google Scholar · View at Scopus
  161. J. W. McDonald and M. V. Johnston, “Physiological and pathophysiological roles of excitatory amino acids during central nervous system development,” Brain Research Reviews, vol. 15, no. 1, pp. 41–70, 1990. View at Publisher · View at Google Scholar · View at Scopus
  162. E. Molnar and J. T. R. Isaac, “Developmental and activity dependent regulation of ionotropic glutamate receptors at synapses,” TheScientificWorldJOURNAL, vol. 2, pp. 27–47, 2002. View at Publisher · View at Google Scholar
  163. H. Monyer, N. Burnashev, D. J. Laurie, B. Sakmann, and P. H. Seeburg, “Developmental and regional expression in the rat brain and functional properties of four NMDA receptors,” Neuron, vol. 12, no. 3, pp. 529–540, 1994. View at Publisher · View at Google Scholar · View at Scopus
  164. J. W. McDonald, M. V. Johnston, and A. B. Young, “Differential ontogenic development of three receptors comprising the NMDA receptor/channel complex in the rat hippocampus,” Experimental Neurology, vol. 110, no. 3, pp. 237–247, 1990. View at Publisher · View at Google Scholar · View at Scopus
  165. M. C. Crair and R. C. Malenka, “A critical period for long-term potentiation at thalamocortical synapses,” Nature, vol. 375, no. 6529, pp. 325–328, 1995. View at Publisher · View at Google Scholar · View at Scopus
  166. P. H. Seeburg and J. Hartner, “Regulation of ion channel/neurotransmitter receptor function by RNA editing,” Current Opinion in Neurobiology, vol. 13, no. 3, pp. 279–283, 2003. View at Publisher · View at Google Scholar · View at Scopus
  167. M. V. Johnston, “Clinical disorders of brain plasticity,” Brain and Development, vol. 26, no. 2, pp. 73–80, 2004. View at Publisher · View at Google Scholar · View at Scopus
  168. A. Holtmaat, L. Wilbrecht, G. W. Knott, E. Welker, and K. Svoboda, “Experience-dependent and cell-type-specific spine growth in the neocortex,” Nature, vol. 441, no. 7096, pp. 979–983, 2006. View at Publisher · View at Google Scholar · View at Scopus
  169. E. Gould, “How widespread is adult neurogenesis in mammals?” Nature Reviews Neuroscience, vol. 8, no. 6, pp. 481–488, 2007. View at Publisher · View at Google Scholar · View at Scopus
  170. V. Donega, C. T. J. van Velthoven, C. H. Nijboer, A. Kavelaars, and C. J. Heijnen, “The endogenous regenerative capacity of the damaged newborn brain: boosting neurogenesis with mesenchymal stem cell treatment,” Journal of Cerebral Blood Flow and Metabolism, vol. 33, no. 5, pp. 625–634, 2013. View at Publisher · View at Google Scholar · View at Scopus
  171. J. Han, J. Pollak, T. Yang et al., “Delayed administration of a small molecule tropomyosin-related kinase B ligand promotes recovery after hypoxic-ischemic stroke,” Stroke, vol. 43, no. 7, pp. 1918–1924, 2012. View at Publisher · View at Google Scholar · View at Scopus
  172. M. Iwai, R. A. Stetler, J. Xing et al., “Enhanced oligodendrogenesis and recovery of neurological function by erythropoietin after neonatal hypoxic/ischemic brain injury,” Stroke, vol. 41, no. 5, pp. 1032–1037, 2010. View at Publisher · View at Google Scholar · View at Scopus
  173. L. Titomanlio, A. Kavelaars, J. Dalous et al., “Stem cell therapy for neonatal brain injury: perspectives and challenges,” Annals of Neurology, vol. 70, no. 5, pp. 698–712, 2011. View at Publisher · View at Google Scholar · View at Scopus
  174. V. Donega, C. H. Nijboer, G. van Tilborg, R. M. Dijkhuizen, A. Kavelaars, and C. J. Heijnen, “Intranasally administered mesenchymal stem cells promote a regenerative niche for repair of neonatal ischemic brain injury,” Experimental Neurology, vol. 261, pp. 53–64, 2014. View at Publisher · View at Google Scholar · View at Scopus
  175. V. Donega, C. H. Nijboer, C. T. van Velthoven et al., “Assessment of long-term safety and efficacy of intranasal mesenchymal stem cell treatment for neonatal brain injury in the mouse,” Pediatric Research, vol. 78, no. 5, pp. 520–526, 2015. View at Publisher · View at Google Scholar