Journal of Neural Transmission

, Volume 117, Issue 8, pp 1009–1017 | Cite as

Inflammation processes in perinatal brain damage

  • Vincent Degos
  • Géraldine Favrais
  • Angela M. Kaindl
  • Stéphane Peineau
  • Anne Marie Guerrot
  • Catherine Verney
  • Pierre Gressens
Movement Disorders-Review Article


Once viewed as an isolated, immune-privileged organ, the central nervous system has undergone a conceptual change. Neuroinflammation has moved into the focus of research work regarding pathomechanisms underlying perinatal brain damage. In this review, we provide an overview of current concepts regarding perinatal brain damage and the role of inflammation in the disease pathomechanism.


Neuroinflammation Perinatal brain damage Microglia Cytokines 



Our research work is supported by Inserm, Université Paris 7, PremUP, the Sixth Framework Program of the European Commission, the Fondation des Gueules Cassées, the Fondation Motrice, the ELA Foundation, the Fondation Grace de Monaco, the Institut pour la Recherche sur la Moelle épinière et l’Encéphale (IRME), the Medical Research Council, the Charité, the German Research Foundation (DFG), the German Federal Ministry of Education and Research, the Sonnenfeld Stiftung and the Sanitätsrat Dr.-Emil-Alexander-Huebner-und-Gemahlin-Stiftung.


  1. Adén U, Favrais G, Plaisant F, Winerdal M, Felderhoff-Mueser UJL, Lelievre V, Gressens P (2010) Systemic inflammation sensitizes the neonatal brain to excitotoxicity through a pro-/anti-inflammatory imbalance: key role of TNF-α pathway and protection by etanercept. Brain Behav Immun (in press)Google Scholar
  2. Anthony DC, Bolton SJ, Fearn S, Perry VH (1997) Age-related effects of interleukin-1 beta on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain 120(Pt 3):435–444CrossRefPubMedGoogle Scholar
  3. Anthony D, Dempster R, Fearn S, Clements J, Wells G, Perry VH, Walker K (1998) CXC chemokines generate age-related increases in neutrophil-mediated brain inflammation and blood-brain barrier breakdown. Curr Biol 8:923–926CrossRefPubMedGoogle Scholar
  4. Arvin KL, Han BH, Du Y, Lin SZ, Paul SM, Holtzman DM (2002) Minocycline markedly protects the neonatal brain against hypoxic-ischemic injury. Ann Neurol 52:54–61CrossRefPubMedGoogle Scholar
  5. Bartha AI, Foster-Barber A, Miller SP, Vigneron DB, Glidden DV, Barkovich AJ, Ferriero DM (2004) Neonatal encephalopathy: association of cytokines with MR spectroscopy and outcome. Pediatr Res 56:960–966CrossRefPubMedGoogle Scholar
  6. Baud O, Daire JL, Dalmaz Y, Fontaine RH, Krueger RC, Sebag G, Evrard P, Gressens P, Verney C (2004) Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol 14:1–10CrossRefPubMedGoogle Scholar
  7. Biran V, Cochois V, Karroubi A, Arrang JM, Charriaut-Marlangue C, Heron A (2008) Stroke induces histamine accumulation and mast cell degranulation in the neonatal rat brain. Brain Pathol 18:1–9CrossRefPubMedGoogle Scholar
  8. Dammann O, Leviton A (1997) Maternal intrauterine infection, cytokines, and brain damage in the preterm newborn. Pediatr Res 42:1–8CrossRefPubMedGoogle Scholar
  9. Dammann O, Leviton A (2007) Perinatal brain damage causation. Dev Neurosci 29:280–288CrossRefPubMedGoogle Scholar
  10. Dammann O, Kuban KC, Leviton A (2002) Perinatal infection, fetal inflammatory response, white matter damage, and cognitive limitations in children born preterm. Ment Retard Dev Disabil Res Rev 8:46–50CrossRefPubMedGoogle Scholar
  11. Debillon T, Gras-Leguen C, Verielle V, Winer N, Caillon J, Roze JC, Gressens P (2000) Intrauterine infection induces programmed cell death in rabbit periventricular white matter. Pediatr Res 47:736–742CrossRefPubMedGoogle Scholar
  12. Degos V, Loron G, Mantz J, Gressens P (2008) Neuroprotective strategies for the neonatal brain. Anesth Analg 106:1670–1680CrossRefPubMedGoogle Scholar
  13. Denker SP, Ji S, Dingman A, Lee SY, Derugin N, Wendland MF, Vexler ZS (2007) Macrophages are comprised of resident brain microglia not infiltrating peripheral monocytes acutely after neonatal stroke. J Neurochem 100:893–904CrossRefPubMedGoogle Scholar
  14. Derrick M, Luo NL, Bregman JC, Jilling T, Ji X, Fisher K, Gladson CL, Beardsley DJ, Murdoch G, Back SA, Tan S (2004) Preterm fetal hypoxia–ischemia causes hypertonia and motor deficits in the neonatal rabbit: a model for human cerebral palsy? J Neurosci 24:24–34CrossRefPubMedGoogle Scholar
  15. Dingman A, Lee SY, Derugin N, Wendland MF, Vexler ZS (2006) Aminoguanidine inhibits caspase-3 and calpain activation without affecting microglial activation following neonatal transient cerebral ischemia. J Neurochem 96:1467–1479CrossRefPubMedGoogle Scholar
  16. Dommergues MA, Patkai J, Renauld JC, Evrard P, Gressens P (2000) Proinflammatory cytokines and interleukin-9 exacerbate excitotoxic lesions of the newborn murine neopallium. Ann Neurol 47:54–63CrossRefPubMedGoogle Scholar
  17. Dommergues MA, Plaisant F, Verney C, Gressens P (2003) Early microglial activation following neonatal excitotoxic brain damage in mice: a potential target for neuroprotection. Neuroscience 121:619–628CrossRefPubMedGoogle Scholar
  18. Doverhag C, Keller M, Karlsson A, Hedtjarn M, Nilsson U, Kapeller E, Sarkozy G, Klimaschewski L, Humpel C, Hagberg H, Simbruner G, Gressens P, Savman K (2008) Pharmacological and genetic inhibition of NADPH oxidase does not reduce brain damage in different models of perinatal brain injury in newborn mice. Neurobiol Dis 31:133–144CrossRefPubMedGoogle Scholar
  19. Ek CJ, Habgood MD, Dziegielewska KM, Potter A, Saunders NR (2001) Permeability and route of entry for lipid-insoluble molecules across brain barriers in developing Monodelphis domestica. J Physiol 536(Pt 3):841–853CrossRefPubMedGoogle Scholar
  20. Ek CJ, Dziegielewska KM, Stolp H, Saunders NR (2006) Functional effectiveness of the blood-brain barrier to small water-soluble molecules in developing and adult opossum (Monodelphis domestica). J Comp Neurol 496(1):13–26CrossRefPubMedGoogle Scholar
  21. Eklind S, Mallard C, Leverin AL, Gilland E, Blomgren K, Mattsby-Baltzer I, Hagberg H (2001) Bacterial endotoxin sensitizes the immature brain to hypoxic-ischaemic injury. Eur J Neurosci 13:1101–1106CrossRefPubMedGoogle Scholar
  22. Eklind S, Mallard C, Arvidsson P, Hagberg H (2005) Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr Res 58:112–116CrossRefPubMedGoogle Scholar
  23. Engelhardt B (2003) Development of the blood-brain barrier. Cell Tissue Res 314:119–129CrossRefPubMedGoogle Scholar
  24. Faustino J, Liu B, Lee S, Derugin N, Wendland MF, Vexler ZS (2009) Blockade of endogenous cytokine-induced neutrophil chemoattractant protein 1 exacerbates injury after neonatal stroke Stroke meeting. San DiegoGoogle Scholar
  25. Favrais G, Schwendimann L, Gressens P, Lelievre V (2007) Cyclooxygenase-2 mediates the sensitizing effects of systemic IL-1-beta on excitotoxic brain lesions in newborn mice. Neurobiol Dis 25:496–505CrossRefPubMedGoogle Scholar
  26. Feldhaus B, Dietzel ID, Heumann R, Berger R (2004) Effects of interferon-gamma and tumor necrosis factor-alpha on survival and differentiation of oligodendrocyte progenitors. J Soc Gynecol Investig 11:89–96CrossRefPubMedGoogle Scholar
  27. Follett PL, Rosenberg PA, Volpe JJ, Jensen FE (2000) NBQX attenuates excitotoxic injury in developing white matter. J Neurosci 20:9235–9241PubMedGoogle Scholar
  28. Follett PL, Deng W, Dai W, Talos DM, Massillon LJ, Rosenberg PA, Volpe JJ, Jensen FE (2004) Glutamate receptor-mediated oligodendrocyte toxicity in periventricular leukomalacia: a protective role for topiramate. J Neurosci 24:4412–4420CrossRefPubMedGoogle Scholar
  29. Fontaine RH, Cases O, Lelievre V, Mesples B, Renauld JC, Loron G, Degos V, Dournaud P, Baud O, Gressens P (2008) IL-9/IL-9 receptor signaling selectively protects cortical neurons against developmental apoptosis. Cell Death Differ 15:1542–1552CrossRefPubMedGoogle Scholar
  30. Foster-Barber A, Ferriero DM (2002) Neonatal encephalopathy in the term infant: neuroimaging and inflammatory cytokines. Ment Retard Dev Disabil Res Rev 8:20–24CrossRefPubMedGoogle Scholar
  31. Fox C, Dingman A, Derugin N, Wendland MF, Manabat C, Ji S, Ferriero DM, Vexler ZS (2005) Minocycline confers early but transient protection in the immature brain following focal cerebral ischemia-reperfusion. J Cereb Blood Flow Metab 25:1138–1149CrossRefPubMedGoogle Scholar
  32. Galasso JM, Miller MJ, Cowell RM, Harrison JK, Warren JS, Silverstein FS (2000) Acute excitotoxic injury induces expression of monocyte chemoattractant protein-1 and its receptor, CCR2, in neonatal rat brain. Exp Neurol 165:295–305CrossRefPubMedGoogle Scholar
  33. Ghersi-Egea JF, Strazielle N, Murat A, Jouvet A, Buénerd A, Belin MF (2006) Brain protection at the blood-cerebrospinal fluid interface involves a glutathione-dependent metabolic barrier mechanism. J Cereb Blood Flow Metab 26(9):1165–1175PubMedGoogle Scholar
  34. Girard S, Kadhim H, Larouche A, Roy M, Gobeil F, Sebire G (2008) Pro-inflammatory disequilibrium of the IL-1 beta/IL-1ra ratio in an experimental model of perinatal brain damages induced by lipopolysaccharide and hypoxia–ischemia. Cytokine 43:54–62CrossRefPubMedGoogle Scholar
  35. Gressens P, Marret S, Hill JM, Brenneman DE, Gozes I, Fridkin M, Evrard P (1997) Vasoactive intestinal peptide prevents excitotoxic cell death in the murine developing brain. J Clin Invest 100:390–397CrossRefPubMedGoogle Scholar
  36. Gressens P, Rogido M, Paindaveine B, Sola A (2002) The impact of neonatal intensive care practices on the developing brain. J Pediatr 140:646–653CrossRefPubMedGoogle Scholar
  37. Grether JK, Nelson KB (1997) Maternal infection and cerebral palsy in infants of normal birth weight. JAMA 278:207–211CrossRefPubMedGoogle Scholar
  38. Hagberg H, Mallard C (2005) Effect of inflammation on central nervous system development and vulnerability. Curr Opin Neurol 18:117–123CrossRefPubMedGoogle Scholar
  39. Hagberg H, Gilland E, Bona E, Hanson LA, Hahin-Zoric M, Blennow M, Holst M, McRae A, Soder O (1996) Enhanced expression of interleukin (IL)-1 and IL-6 messenger RNA and bioactive protein after hypoxia–ischemia in neonatal rats. Pediatr Res 40:603–609CrossRefPubMedGoogle Scholar
  40. Hagberg H, Peebles D, Mallard C (2002) Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment Retard Dev Disabil Res Rev 8:30–38CrossRefPubMedGoogle Scholar
  41. Harding DR, Dhamrait S, Whitelaw A, Humphries SE, Marlow N, Montgomery HE (2004) Does interleukin-6 genotype influence cerebral injury or developmental progress after preterm birth? Pediatrics 114:941–947CrossRefPubMedGoogle Scholar
  42. Haynes RL, Folkerth RD, Keefe RJ, Sung I, Swzeda LI, Rosenberg PA, Volpe JJ, Kinney HC (2003) Nitrosative and oxidative injury to premyelinating oligodendrocytes in periventricular leukomalacia. J Neuropathol Exp Neurol 62:441–450PubMedGoogle Scholar
  43. Hedtjarn M, Leverin AL, Eriksson K, Blomgren K, Mallard C, Hagberg H (2002) Interleukin-18 involvement in hypoxic-ischemic brain injury. J Neurosci 22:5910–5919PubMedGoogle Scholar
  44. Hedtjarn M, Mallard C, Iwakura Y, Hagberg H (2005) Combined deficiency of IL-1beta18, but not IL-1alphabeta, reduces susceptibility to hypoxia–ischemia in the immature brain. Dev Neurosci 27:143–148CrossRefPubMedGoogle Scholar
  45. Himmelmann K, Hagberg G, Beckung E, Hagberg B, Uvebrant P (2005) The changing panorama of cerebral palsy in Sweden. IX. Prevalence and origin in the birth-year period 1995–1998. Acta Paediatr 94:287–294PubMedGoogle Scholar
  46. Inder T, Mocatta T, Darlow B, Spencer C, Volpe JJ, Winterbourn C (2002) Elevated free radical products in the cerebrospinal fluid of VLBW infants with cerebral white matter injury. Pediatr Res 52:213–218PubMedGoogle Scholar
  47. Ivacko JA, Sun R, Silverstein FS (1996) Hypoxic-ischemic brain injury induces an acute microglial reaction in perinatal rats. Pediatr Res 39:39–47CrossRefPubMedGoogle Scholar
  48. Jin Y, Silverman AJ, Vannucci SJ (2007) Mast cell stabilization limits hypoxic-ischemic brain damage in the immature rat. Dev Neurosci 29:373–384CrossRefPubMedGoogle Scholar
  49. Johnson DL, Getson P, Shaer C, O’Donnell R (1987) Intraventricular hemorrhage in the newborn beagle puppy. A limited model of intraventricular hemorrhage in the premature infant. Pediatr Neurosci 13:78–83CrossRefPubMedGoogle Scholar
  50. Kirton A, deVeber G (2009) Advances in perinatal ischemic stroke. Pediatr Neurol 40:205–214CrossRefPubMedGoogle Scholar
  51. Kniesel U, Risau W, Wolburg H (1996) Development of blood-brain barrier tight junctions in the rat cortex. Brain Res Dev Brain Res 96:229–240CrossRefPubMedGoogle Scholar
  52. Laudenbach V, Calo G, Guerrini R, Lamboley G, Benoist JF, Evrard P, Gressens P (2001) Nociceptin/orphanin FQ exacerbates excitotoxic white-matter lesions in the murine neonatal brain. J Clin Invest 107:457–466CrossRefPubMedGoogle Scholar
  53. Leonardo CC, Eakin AK, Ajmo JM, Collier LA, Pennypacker KR, Strongin AY, Gottschall PE (2008) Delayed administration of a matrix metalloproteinase inhibitor limits progressive brain injury after hypoxia–ischemia in the neonatal rat. J Neuroinflammation 5:34CrossRefPubMedGoogle Scholar
  54. Lim HB, Smith M (2007) Systemic complications after head injury: a clinical review. Anaesthesia 62:474–482CrossRefPubMedGoogle Scholar
  55. Loeliger M, Watson CS, Reynolds JD, Penning DH, Harding R, Bocking AD, Rees SM (2003) Extracellular glutamate levels and neuropathology in cerebral white matter following repeated umbilical cord occlusion in the near term fetal sheep. Neuroscience 116:705–714CrossRefPubMedGoogle Scholar
  56. Lu J, Goh SJ, Tng PY, Deng YY, Ling EA, Moochhala S (2009) Systemic inflammatory response following acute traumatic brain injury. Front Biosci 14:3795–3813CrossRefPubMedGoogle Scholar
  57. Malaeb S, Dammann O (2009) Fetal inflammatory response and brain injury in the preterm newborn. J Child Neurol 24:1119–1126CrossRefPubMedGoogle Scholar
  58. Mallard C, Welin AK, Peebles D, Hagberg H, Kjellmer I (2003) White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem Res 28:215–223CrossRefPubMedGoogle Scholar
  59. McColl BW, Allan SM, Rothwell NJ (2009) Systemic infection, inflammation and acute ischemic stroke. Neuroscience 158:1049–1061CrossRefPubMedGoogle Scholar
  60. McRae A, Gilland E, Bona E, Hagberg H (1995) Microglia activation after neonatal hypoxic-ischemia. Brain Res Dev Brain Res 84:245–252CrossRefPubMedGoogle Scholar
  61. Mesples B, Plaisant F, Gressens P (2003) Effects of interleukin-10 on neonatal excitotoxic brain lesions in mice. Brain Res Dev Brain Res 141:25–32CrossRefPubMedGoogle Scholar
  62. Mesples B, Plaisant F, Fontaine RH, Gressens P (2005) Pathophysiology of neonatal brain lesions: lessons from animal models of excitotoxicity. Acta Paediatr 94:185–190CrossRefPubMedGoogle Scholar
  63. Miller RJ, Tran PB (2005) Chemokinetics. Neuron 47:621–623CrossRefPubMedGoogle Scholar
  64. Monier A, Evrard P, Gressens P, Verney C (2006) Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J Comp Neurol 499:565–582CrossRefPubMedGoogle Scholar
  65. Monier A, Adle-Biassette H, Delezoide AL, Evrard P, Gressens P, Verney C (2007) Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex. J Neuropathol Exp Neurol 66:372–382CrossRefPubMedGoogle Scholar
  66. Nelson KB, Chang T (2008) Is cerebral palsy preventable? Curr Opin Neurol 21:129–135CrossRefPubMedGoogle Scholar
  67. Nelson KB, Grether JK (1999) Causes of cerebral palsy. Curr Opin Pediatr 11:487–491CrossRefPubMedGoogle Scholar
  68. Nelson KB, Willoughby RE (2000) Infection, inflammation and the risk of cerebral palsy. Curr Opin Neurol 13:133–139CrossRefPubMedGoogle Scholar
  69. Nijboer CH, Kavelaars A, Vroon A, Groenendaal F, van Bel F, Heijnen CJ (2008) Low endogenous G-protein-coupled receptor kinase 2 sensitizes the immature brain to hypoxia–ischemia-induced gray and white matter damage. J Neurosci 28:3324–3332CrossRefPubMedGoogle Scholar
  70. Normann E, Lacaze-Masmonteil T, Eaton F, Schwendimann L, Gressens P, Thebaud B (2009) A novel mouse model of ureaplasma-induced perinatal inflammation: effects on lung and brain injury. Pediatr Res 65:430–436CrossRefPubMedGoogle Scholar
  71. Olivier P, Baud O, Evrard P, Gressens P, Verney C (2005) Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol 64:998–1006CrossRefPubMedGoogle Scholar
  72. Pang Y, Campbell L, Zheng B, Fan L, Cai Z, Rhodes P (2010) Lipopolysaccharide-activated microglia induce death of oligodendrocyte progenitor cells and impede their development. Neuroscience 166(2):464–475CrossRefPubMedGoogle Scholar
  73. Patkai J, Mesples B, Dommergues MA, Fromont G, Thornton EM, Renauld JC, Evrard P, Gressens P (2001) Deleterious effects of IL-9-activated mast cells and neuroprotection by antihistamine drugs in the developing mouse brain. Pediatr Res 50:222–230CrossRefPubMedGoogle Scholar
  74. Plaisant F, Dommergues MA, Spedding M, Cecchelli R, Brillault J, Kato G, Munoz C, Gressens P (2003) Neuroprotective properties of tianeptine: interactions with cytokines. Neuropharmacology 44:801–809CrossRefPubMedGoogle Scholar
  75. Rezaie P, Male D (1999) Colonisation of the developing human brain and spinal cord by microglia: a review. Microsc Res Tech 45:359–382CrossRefPubMedGoogle Scholar
  76. Rezaie P, Patel K, Male DK (1999) Microglia in the human fetal spinal cord—patterns of distribution, morphology and phenotype. Brain Res Dev Brain Res 115:71–81CrossRefPubMedGoogle Scholar
  77. Robertson CM, Watt MJ, Yasui Y (2007) Changes in the prevalence of cerebral palsy for children born very prematurely within a population-based program over 30 years. JAMA 297:2733–2740CrossRefPubMedGoogle Scholar
  78. Rousset CI, Chalon S, Cantagrel S, Bodard S, Andres C, Gressens P, Saliba E (2006) Maternal exposure to LPS induces hypomyelination in the internal capsule and programmed cell death in the deep gray matter in newborn rats. Pediatr Res 59:428–433CrossRefPubMedGoogle Scholar
  79. Strazielle N, Ghersi-Egea JF (2000) Choroid plexus in the central nervous system: biology and physiopathology. J Neuropathol Exp Neurol 59(7):561–574PubMedGoogle Scholar
  80. Streit WJ, Kreutzberg GW (1988) Response of endogenous glial cells to motor neuron degeneration induced by toxic ricin. J Comp Neurol 268:248–263CrossRefPubMedGoogle Scholar
  81. Svedin P, Hagberg H, Savman K, Zhu C, Mallard C (2007) Matrix metalloproteinase-9 gene knock-out protects the immature brain after cerebral hypoxia–ischemia. J Neurosci 27:1511–1518CrossRefPubMedGoogle Scholar
  82. Tahraoui SL, Marret S, Bodenant C, Leroux P, Dommergues MA, Evrard P, Gressens P (2001) Central role of microglia in neonatal excitotoxic lesions of the murine periventricular white matter. Brain Pathol 11:56–71CrossRefPubMedGoogle Scholar
  83. Tikka T, Fiebich BL, Goldsteins G, Keinanen R, Koistinaho J (2001) Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia. J Neurosci 21:2580–2588PubMedGoogle Scholar
  84. van den Tweel ER, Nijboer C, Kavelaars A, Heijnen CJ, Groenendaal F, van Bel F (2005) Expression of nitric oxide synthase isoforms and nitrotyrosine formation after hypoxia–ischemia in the neonatal rat brain. J Neuroimmunol 167:64–71CrossRefPubMedGoogle Scholar
  85. Vela JM, Molina-Holgado E, Arevalo-Martin A, Almazan G, Guaza C (2002) Interleukin-1 regulates proliferation and differentiation of oligodendrocyte progenitor cells. Mol Cell Neurosci 20:489–502CrossRefPubMedGoogle Scholar
  86. Vincer MJ, Allen AC, Joseph KS, Stinson DA, Scott H, Wood E (2006) Increasing prevalence of cerebral palsy among very preterm infants: a population-based study. Pediatrics 118:e1621–e1626CrossRefPubMedGoogle Scholar
  87. Volpe JJ (2001) Neurobiology of periventricular leukomalacia in the premature infant. Pediatr Res 50:553–562CrossRefPubMedGoogle Scholar
  88. Volpe JJ (2009) The encephalopathy of prematurity-brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 16:167–178CrossRefPubMedGoogle Scholar
  89. Wilson-Costello D, Friedman H, Minich N, Fanaroff AA, Hack M (2005) Improved survival rates with increased neurodevelopmental disability for extremely low birth weight infants in the 1990s. Pediatrics 115:997–1003CrossRefPubMedGoogle Scholar
  90. Wilson-Costello D, Friedman H, Minich N, Siner B, Taylor G, Schluchter M, Hack M (2007) Improved neurodevelopmental outcomes for extremely low birth weight infants in 2000–2002. Pediatrics 119:37–45CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2010

Authors and Affiliations

  • Vincent Degos
    • 1
    • 2
    • 3
  • Géraldine Favrais
    • 1
    • 2
    • 3
    • 4
  • Angela M. Kaindl
    • 1
    • 2
    • 3
    • 5
    • 6
  • Stéphane Peineau
    • 1
    • 2
    • 3
    • 7
  • Anne Marie Guerrot
    • 1
    • 2
    • 3
  • Catherine Verney
    • 1
    • 2
    • 3
  • Pierre Gressens
    • 1
    • 2
    • 3
    • 8
  1. 1.Hôpital Robert DebréInserm, U676ParisFrance
  2. 2.Faculté de Médecine Denis-DiderotUniversité Paris 7ParisFrance
  3. 3.PremUPParisFrance
  4. 4.Réanimation Pédiatrique et Néonatologie, Hôpital Clocheville, CHRU ToursUniversité François RabelaisToursFrance
  5. 5.Pediatric NeurologyCharité, Universitätsmedizin BerlinBerlinGermany
  6. 6.Institute of Cell Biology and Neurobiology, Center for AnatomyCharité, Universitätsmedizin BerlinBerlinGermany
  7. 7.MRC Centre for Synaptic Plasticity, Department of Anatomy, School of Medical, SciencesUniversity WalkBristolUK
  8. 8.Institute for Reproductive and Developmental BiologyImperial CollegeLondonUK

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