Jump to ContentJump to Main Navigation
Show Summary Details
More options …

Reviews in the Neurosciences

Editor-in-Chief: Huston, Joseph P.

Editorial Board: Topic, Bianca / Adeli, Hojjat / Buzsaki, Gyorgy / Crawley, Jacqueline / Crow, Tim / Gold, Paul / Holsboer, Florian / Korth, Carsten / Lubec, Gert / McEwen, Bruce / Pan, Weihong / Pletnikov, Mikhail / Robbins, Trevor / Schnitzler, Alfons / Stevens, Charles / Steward, Oswald / Trojanowski, John

8 Issues per year


IMPACT FACTOR 2017: 2.590
5-year IMPACT FACTOR: 3.078

CiteScore 2017: 2.81

SCImago Journal Rank (SJR) 2017: 0.980
Source Normalized Impact per Paper (SNIP) 2017: 0.804

Online
ISSN
2191-0200
See all formats and pricing
More options …
Ahead of print

Issues

The optimal choices of animal models of white matter injury

Yan Zeng
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Huiqing Wang
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Li Zhang
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Jun Tang
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Jing Shi
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Dongqiong Xiao
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Yi Qu
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, Chengdu 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
/ Dezhi Mu
  • Corresponding author
  • Department of Pediatrics, West China Second University Hospital, Sichuan University, No. 20, section 3, Renmin South Road, Chengdu, Sichuan 610041, China
  • Key Laboratory of Obstetric and Gynecologic and Pediatric Diseases and Birth Defects, Ministry of Education, Sichuan University, Chengdu 610041, China, Telephone: +86-28-85503226, Fax: +86-28-85559065
  • Email
  • Other articles by this author:
  • De Gruyter OnlineGoogle Scholar
Published Online: 2018-10-31 | DOI: https://doi.org/10.1515/revneuro-2018-0044

Abstract

White matter injury, the most common neurological injury in preterm infants, is a major cause of chronic neurological morbidity, including cerebral palsy. Although there has been great progress in the study of the mechanism of white matter injury in newborn infants, its pathogenesis is not entirely clear, and further treatment approaches are required. Animal models are the basis of study in pathogenesis, treatment, and prognosis of white matter injury in preterm infants. Various species have been used to establish white matter injury models, including rodents, rabbits, sheep, and non-human primates. Small animal models allow cost-effective investigation of molecular and cellular mechanisms, while large animal models are particularly attractive for pathophysiological and clinical-translational studies. This review focuses on the features of commonly used white matter injury animal models, including their modelling methods, advantages, and limitations, and addresses some clinically relevant animal models that allow reproduction of the insults associated with clinical conditions that contribute to white matter injury in human infants.

Keywords: advantages; animal model; histological changes; limitations; white matter injury

References

  • Albertsson, A.-M., Bi, D., Duan, L., Zhang, X., Leavenworth, J.W., Qiao, L., and Hagberg, H. (2014). The immune response after hypoxia-ischemia in a mouse model of preterm brain injury. J. Neuroinflamm. 11, 153.Google Scholar

  • Albertsson, A.-M. and Wang, X. (2014). A mouse model of preterm brain injury after hypoxia-ischemia. Bio-protocol. 5, e1526.Google Scholar

  • Back, S.A. (2017). White matter injury in the preterm infant: pathology and mechanisms. Acta Neuropathol. 134, 331–349.Google Scholar

  • Back, S.A. and Miller, S.P. (2014). Brain injury in premature neonates: a primary cerebral dysmaturation disorder? Ann. Neurol. 75, 469–486.Google Scholar

  • Back, S.A. and Rosenberg, P.A. (2014). Pathophysiology of glia in perinatal white matter injury. Glia 62, 1790–1815.Google Scholar

  • Back, S.A., Han, B.H., Luo, N.L., Chricton, C.A., Xanthoudakis, S., Tam, J., and Holtzman, D.M. (2002). Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J. Neurosci. 22, 455–463.Google Scholar

  • Back, S.A., Riddle, A., and Hohimer, A.R. (2015). The sheep as a model of brain injury in the premature infant. In: Animal Models of Neurodevelopmental Disorders (New York, NY: Humana Press), pp. 107–128.Google Scholar

  • Ballabh, P. (2010). Intraventricular hemorrhage in premature infants: mechanism of disease. Pediatr. Res. 67, 1–8.Google Scholar

  • Barlow, R. (1969). The foetal sheep: morphogenesis of the nervous system and histochemical aspects of myelination. J. Comp. Neurol. 135, 249–261.Google Scholar

  • Barrett, R.D., Bennet, L., Naylor, A., George, S.A., Dean, J.M., and Gunn, A.J. (2012). Effect of cerebral hypothermia and asphyxia on the subventricular zone and white matter tracts in preterm fetal sheep. Brain Res. 1469, 35–42.Google Scholar

  • Baud, O., Daire, J.L., Dalmaz, Y., Fontaine, R.H., Krueger, R.C., Sebag, G., and Verney, C. (2004). Gestational hypoxia induces white matter damage in neonatal rats: a new model of periventricular leukomalacia. Brain Pathol. 14, 1–10.Google Scholar

  • Bell, M.J. and Hallenbeck, J.M. (2002). Effects of intrauterine inflammation on developing rat brain. J. Neurosci. Res. 70, 570–579.Google Scholar

  • Bernhard, C., Kolmodin, G., and Meyerson, B. (1967). On the prenatal development of function and structure in the somesthetic cortex of the sheep. Prog. Brain. Res. 26, 60–77.Google Scholar

  • Blencowe, H., Cousens, S., Chou, D., Oestergaard, M., Say, L., Moller, A.B., and Born Too Soon Preterm Birth Action Group. (2013). Born too soon: the global epidemiology of 15 million preterm births. Reprod. Health 10 (Suppl. 1), S2.Google Scholar

  • Brambrink, A.M., Back, S.A., Riddle, A., Gong, X., Moravec, M.D., Dissen, G.A., and Olney, J.W. (2012). Isoflurane-induced apoptosis of oligodendrocytes in the neonatal primate brain. Ann. Neurol. 72, 525–535.Google Scholar

  • Buser, J.R., Segovia, K.N., Dean, J.M., Nelson, K., Beardsley, D., Gong, X., and Riddle, A. (2010). Timing of appearance of late oligodendrocyte progenitors coincides with enhanced susceptibility of preterm rabbit cerebral white matter to hypoxia-ischemia. J. Cereb. Blood Flow Metab. 30, 1053–1065.Google Scholar

  • Cai, Z., Pan, Z.-L., Pang, Y., Evans, O.B., and Rhodes, P.G. (2000). Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration. Pediatr. Res. 47, 64–72.Google Scholar

  • Cai, Z., Pang, Y., Lin, S., and Rhodes, P.G. (2003). Differential roles of tumor necrosis factor-α and interleukin-1β in lipopolysaccharide-induced brain injury in the neonatal rat. Brain Res. 975, 37–47.Google Scholar

  • Chau, V., Poskitt, K.J., McFadden, D.E., Bowen-Roberts, T., Synnes, A., Brant, R., and Miller, S.P. (2009). Effect of chorioamnionitis on brain development and injury in premature newborns. Ann. Neurol. 66, 155–164.Google Scholar

  • Choi, E.-K., Park, D., Kim, T.K., Lee, S.H., Bae, D.-K., Yang, G., and Lee, W.R. (2011). Animal models of periventricular leukomalacia. Lab. Anim. Res. 27, 77–84.Google Scholar

  • Coleman, K., Robertson, N.D., Dissen, G.A., Neuringer, M.D., Martin, L.D., Carlson, V.C.C., and Brambrink, A.M. (2017). Isoflurane anesthesia has long-term consequences on motor and behavioral development in infant rhesus macaques. Anesthesiology 126, 74–84.Google Scholar

  • Cook, C., Gluckman, P., Johnston, B., and Williams, C. (1987a). The development of the somatosensory evoked potential in the unanaesthetized fetal sheep. J. Dev. Physiol. 9, 441–455.Google Scholar

  • Cook, C., Williams, C., and Gluckman, P. (1987b). Brainstem auditory evoked potentials in the fetal sheep, in utero. J. Dev. Physiol. 9, 429–439.Google Scholar

  • Cooley, K. and Vanderwolf, C. (2004). The Sheep Brain-A Photographic Series (London, ON, Canada: AJ Kirby Co).Google Scholar

  • Creeley, C., Dikranian, K., Dissen, G., Martin, L., Olney, J., and Brambrink, A. (2013). Propofol-induced apoptosis of neurones and oligodendrocytes in fetal and neonatal rhesus macaque brain. Br. J. Anaesth. 110, i29–i38.Google Scholar

  • Creeley, C.E., Dikranian, K.T., Dissen, G.A., Back, S.A., Olney, J.W., and Brambrink, A.M. (2014). Isoflurane-induced apoptosis of neurons and oligodendrocytes in the fetal rhesus macaque brain. Anesthesiology 120, 626–638.Google Scholar

  • de Waal, K.A., Evans, N., Osborn, D.A., and Kluckow, M. (2007). Cardiorespiratory effects of changes in end expiratory pressure in ventilated newborns. Arch. Dis. Child Fetal Neonatal. Ed. 92, F444–F448.Google Scholar

  • Dean, J.M., Moravec, M.D., Grafe, M., Abend, N., Ren, J., Gong, X., and Back, S.A. (2011a). Strain-specific differences in perinatal rodent oligodendrocyte lineage progression and its correlation with human. Dev. Neurosci. 33, 251–260.Google Scholar

  • Dean, J.M., Van De Looij, Y., Sizonenko, S.V., Lodygensky, G.A., Lazeyras, F., Bolouri, H., and Mallard, C. (2011b). Delayed cortical impairment following lipopolysaccharide exposure in preterm fetal sheep. Ann. Neurol. 70, 846–856.Google Scholar

  • Del Toro, J., Louis, P.T., and Goddard-Finegold, J. (1991). Cerebrovascular regulation and neonatal brain injury. Pediatr. Neurol. 7, 3–12.Google Scholar

  • Delcour, M., Russier, M., Amin, M., Baud, O., Paban, V., Barbe, M.F., and Coq, J.-O. (2012). Impact of prenatal ischemia on behavior, cognitive abilities and neuroanatomy in adult rats with white matter damage. Behav. Brain Res. 232, 233–244.Google Scholar

  • Dizon, M.L., Maa, T., and Kessler, J.A. (2011). The bone morphogenetic protein antagonist noggin protects white matter after perinatal hypoxia–ischemia. Neurobiol. Dis. 42, 318–326.Google Scholar

  • Doyle, L.W. (2012). Antenatal magnesium sulfate and neuroprotection. Curr. Opin. Pediatr. 24, 154–159.Google Scholar

  • Drobyshevsky, A., Jiang, R., Lin, L., Derrick, M., Luo, K., Back, S.A., and Tan, S. (2014). Unmyelinated axon loss with postnatal hypertonia after fetal hypoxia. Ann. Neurol. 75, 533–541.Google Scholar

  • Eklind, S., Mallard, C., Leverin, A.L., Gilland, E., Blomgren, K., Mattsby-Baltzer, I., and Hagberg, H. (2001). Bacterial endotoxin sensitizes the immature brain to hypoxic–ischaemic injury. Eur. J. Neurosci. 13, 1101–1106.Google Scholar

  • Eklind, S., Mallard, C., Arvidsson, P., and Hagberg, H. (2005). Lipopolysaccharide induces both a primary and a secondary phase of sensitization in the developing rat brain. Pediatr. Res. 58, 112–116.Google Scholar

  • Fan, L.W., Lin, S., Pang, Y., Lei, M., Zhang, F., Rhodes, P.G., and Cai, Z. (2005). Hypoxia-ischemia induced neurological dysfunction and brain injury in the neonatal rat. Behav. Brain Res. 165, 80–90.Google Scholar

  • Favrais, G., Van De Looij, Y., Fleiss, B., Ramanantsoa, N., Bonnin, P., Stoltenburg-Didinger, G., and Gallego, J. (2011). Systemic inflammation disrupts the developmental program of white matter. Ann. Neurol. 70, 550–565.Google Scholar

  • Group, E., Fellman, V., Hellstrom-Westas, L., Norman, M., Westgren, M., Kallen, K., and Wennergren, M. (2009). One-year survival of extremely preterm infants after active perinatal care in Sweden. J. Am. Med. Assoc. 301, 2225–2233.Google Scholar

  • Fowlie, P.W. and Davis, P.G. (2003). Prophylactic indomethacin for preterm infants: a systematic review and meta-analysis. Arch. Dis. Child Fetal Neonatal Ed. 88, F464–466.Google Scholar

  • Fujihara, M., Muroi, M., Tanamoto, K., Suzuki, T., Azuma, H., and Ikeda, H. (2003). Molecular mechanisms of macrophage activation and deactivation by lipopolysaccharide: roles of the receptor complex. Pharmacol. Ther. 100, 171–194.Google Scholar

  • Gerstner, B., DeSilva, T.M., Genz, K., Armstrong, A., Brehmer, F., Neve, R.L., and Rosenberg, P.A. (2008). Hyperoxia causes maturation-dependent cell death in the developing white matter. J. Neurosci. 28, 1236–1245.Google Scholar

  • Girard, S., Kadhim, H., Beaudet, N., Sarret, P., and Sebire, G. (2009). Developmental motor deficits induced by combined fetal exposure to lipopolysaccharide and early neonatal hypoxia/ischemia: a novel animal model for cerebral palsy in very premature infants. Neurosci. 158, 673–682.Google Scholar

  • Girard, S., Tremblay, L., Lepage, M., and Sebire, G. (2010). IL-1 receptor antagonist protects against placental and neurodevelopmental defects induced by maternal inflammation. J. Immunol. 184, 3997–4005.Google Scholar

  • Gluckman, P. and Parsons, Y. (1983). Stereotaxic method and atlas for the ovine fetal forebrain. J. Dev. Physiol. 5, 101–128.Google Scholar

  • Granholm, A.C., Zaman, V., Godbee, J., Smith, M., Ramadan, R., Umphlet, C., and Boger, H.A. (2011). Prenatal LPS increases inflammation in the substantia nigra of Gdnf heterozygous mice. Brain Pathol. 21, 330–348.Google Scholar

  • Gressens, P., Marret, S., and Evrard, P. (1996). Developmental spectrum of the excitotoxic cascade induced by ibotenate: a model of hypoxic insults in fetuses and neonates. Neuropathol. Appl. Neurobiol. 22, 498–502.Google Scholar

  • Gressens, P., Schwendimann, L., Husson, I., Sarkozy, G., Mocaer, E., Vamecq, J., and Spedding, M. (2008). Agomelatine, a melatonin receptor agonist with 5-HT(2C) receptor antagonist properties, protects the developing murine white matter against excitotoxicity. Eur. J. Pharmacol. 588, 58–63.Google Scholar

  • Griffith, J.L., Shimony, J.S., Cousins, S.A., Rees, S.E., McCurnin, D.C., Inder, T.E., and Neil, J.J. (2012). MR imaging correlates of white-matter pathology in a preterm baboon model. Pediatr. Res. 71, 185–191.Google Scholar

  • Grow, J.L., Liu, Y.Q., and Barks, J.D. (2003). Can lateralizing sensorimotor deficits be identified after neonatal cerebral hypoxia-ischemia in rats? Dev. Neurosci. 25, 394–402.Google Scholar

  • Gunn, A.J. and Bennet, L. (2009). Fetal hypoxia insults and patterns of brain injury: insights from animal models. Clin. Perinatol. 36, 579–593.Google Scholar

  • Guo, F., Ma, J., McCauley, E., Bannerman, P., and Pleasure, D. (2009). Early postnatal proteolipid promoter-expressing progenitors produce multilineage cells in vivo. J. Neurosci. 29, 7256–7270.Google Scholar

  • Hagberg, H., Peebles, D., and Mallard, C. (2002). Models of white matter injury: comparison of infectious, hypoxic-ischemic, and excitotoxic insults. Ment. Retard. Dev. Disabil. Res. Rev. 8, 30–38.Google Scholar

  • Hagberg, H., Mallard, C., Ferriero, D.M., Vannucci, S.J., Levison, S.W., Vexler, Z.S., and Gressens, P. (2015). The role of inflammation in perinatal brain injury. Nat. Rev. Neurol. 11, 192–208.Google Scholar

  • Hagen, M.W., Riddle, A., McClendon, E., Gong, X., Shaver, D., Srivastava, T., and Gunn, A.J. (2014). Role of recurrent hypoxia-ischemia in preterm white matter injury severity. PLoS One 9, e112800.Google Scholar

  • Herzog, M., Cerar, L.K., Sršen, T.P., Verdenik, I., and Lučovnik, M. (2015). Impact of risk factors other than prematurity on periventricular leukomalacia. A population-based matched case control study. Eur. J. Obstet. Gynecol. Reprod. Biol. 187, 57–59.Google Scholar

  • Honeycutt, A.A., Grosse, S.D., Dunlap, L.J., Schendel, D.E., Chen, H., Brann, E., and al Homsi, G. (2003). Economic costs of mental retardation, cerebral palsy, hearing loss, and vision impairment. In: Using Survey Data to Study Disability: Results from the National Health Survey on Disability (Emerald Group Publishing Ltd.), pp. 207–228.Google Scholar

  • Huang, Z., Liu, J., Cheung, P.-Y., and Chen, C. (2009). Long-term cognitive impairment and myelination deficiency in a rat model of perinatal hypoxic-ischemic brain injury. Brain Res. 1301, 100–109.Google Scholar

  • Huang, L., Zhao, F., Qu, Y., Zhang, L., Wang, Y., and Mu, D. (2017). Animal models of hypoxic-ischemic encephalopathy: optimal choices for the best outcomes. Rev. Neurosci. 28, 31–43.Google Scholar

  • Ikeda, T., Mishima, K., Aoo, N., Egashira, N., Iwasaki, K., Fujiwara, M., and Ikenoue, T. (2004). Combination treatment of neonatal rats with hypoxia-ischemia and endotoxin induces long-lasting memory and learning impairment that is associated with extended cerebral damage. Am. J. Obstet. Gynecol. 191, 2132–2141.Google Scholar

  • Inder, T., Neil, J., Yoder, B., and Rees, S. (2004). Non-human primate models of neonatal brain injury. Semin. Perinatol. 28, 396–404.Google Scholar

  • Inder, T., Neil, J., Kroenke, C., Dieni, S., Yoder, B., and Rees, S. (2005). Investigation of cerebral development and injury in the prematurely born primate by magnetic resonance imaging and histopathology. Dev. Neurosci. 27, 100–111.Google Scholar

  • Jansen, E.M. and Low, W.C. (1996). Quantitative analysis of contralateral hemisphere hypertrophy and sensorimotor performance in adult rats following unilateral neonatal ischemic-hypoxic brain injury. Brain Res. 708, 93–99.Google Scholar

  • Juul, S. (2012). Neuroprotective role of erythropoietin in neonates. J. Matern. Fetal Neonatal Med. 25 (Suppl. 4), 105–107.Google Scholar

  • Kannan, S., Saadani-Makki, F., Muzik, O., Chakraborty, P., Mangner, T.J., Janisse, J., and Chugani, D.C. (2007). Microglial activation in perinatal rabbit brain induced by intrauterine inflammation: detection with 11C-(R)-PK11195 and small-animal PET. J. Nucl. Med. 48, 946–954.Google Scholar

  • Kuypers, E., Jellema, R.K., Ophelders, D.R., Dudink, J., Nikiforou, M., Wolfs, T.G., and Kemp, M.W. (2013). Effects of intra-amniotic lipopolysaccharide and maternal betamethasone on brain inflammation in fetal sheep. PLoS One 8, e81644.Google Scholar

  • Lam, J.S., Anderson, E.M., and Hao, Y. (2014). LPS quantitation procedures. Methods Mol. Biol. 1149, 375–402.Google Scholar

  • Lan, W.-C.J., Priestley, M., Mayoral, S.R., Tian, L., Shamloo, M., and Penn, A.A. (2011). Sex-specific cognitive deficits and regional brain volume loss in mice exposed to chronic, sublethal hypoxia. Pediatr. Res. 70, 15–20.Google Scholar

  • Leuchter, R.H., Gui, L., Poncet, A., Hagmann, C., Lodygensky, G.A., Martin, E., and Huppi, P.S. (2014). Association between early administration of high-dose erythropoietin in preterm infants and brain MRI abnormality at term-equivalent age. J. Am. Med. Assoc. 312, 817–824.Google Scholar

  • Lin, H.-Y., Huang, C.-C., and Chang, K.-F. (2009). Lipopolysaccharide preconditioning reduces neuroinflammation against hypoxic ischemia and provides long-term outcome of neuroprotection in neonatal rat. Pediatr. Res. 66, 254–259.Google Scholar

  • Lin, W.-Y., Chang, Y.-C., Ho, C.-J., and Huang, C.-C. (2013). Ischemic preconditioning reduces neurovascular damage after hypoxia-ischemia via the cellular inhibitor of apoptosis 1 in neonatal brain. Stroke 44, 162–169.Google Scholar

  • Loeliger, M., Inder, T.E., Dalitz, P.A., Cain, S., Camm, E.J., Yoder, B., and Rees, S.M. (2009). Developmental and neuropathological consequences of ductal ligation in the preterm baboon. Pediatr. Res. 65, 209–214.Google Scholar

  • Makinodan, M., Tatsumi, K., Manabe, T., Yamauchi, T., Makinodan, E., Matsuyoshi, H., and Wanaka, A. (2008). Maternal immune activation in mice delays myelination and axonal development in the hippocampus of the offspring. J. Neurosci. Res. 86, 2190–2200.Google Scholar

  • Mallard, C., Welin, A.-K., Peebles, D., Hagberg, H., and Kjellmer, I. (2003). White matter injury following systemic endotoxemia or asphyxia in the fetal sheep. Neurochem. Res. 28, 215–223.Google Scholar

  • Marret, S., Mukendi, R., Gadisseux, J.F., Gressens, P., and Evrard, P. (1995). Effect of ibotenate on brain development: an excitotoxic mouse model of microgyria and posthypoxic-like lesions. J. Neuropathol. Exp. Neurol. 54, 358–370.Google Scholar

  • Matsuda, T., Okuyama, K., Cho, K., Hoshi, N., Matsumoto, Y., Kobayashi, Y., and Fujimoto, S. (1999). Induction of antenatal periventricular leukomalacia by hemorrhagic hypotension in the chronically instrumented fetal sheep. Am. J. Obstet. Gynecol. 181, 725–730.Google Scholar

  • McClure, M.M., Riddle, A., Manese, M., Luo, N.L., Rorvik, D.A., Kelly, K.A., and Roberts, C.T. (2008). 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, 995–1008.Google Scholar

  • Meyer, U., Feldon, J., and Fatemi, S.H. (2009). In-vivo rodent models for the experimental investigation of prenatal immune activation effects in neurodevelopmental brain disorders. Neurosci. Biobehav. Rev. 33, 1061–1079.Google Scholar

  • Meyer, U. and Feldon, J. (2012). To poly(I:C) or not to poly(I:C): advancing preclinical schizophrenia research through the use of prenatal immune activation models. Neuropharmacol. 62, 1308–1321.Google Scholar

  • Miyamoto, N., Maki, T., Shindo, A., Liang, A.C., Maeda, M., Egawa, N., and Ihara, M. (2015). Astrocytes promote oligodendrogenesis after white matter damage via brain-derived neurotrophic factor. J. Neurosci. 35, 14002–14008.Google Scholar

  • Nijboer, C.H., Kavelaars, A., van Bel, F., Heijnen, C.J., and Groenendaal, F. (2007). Gender-dependent pathways of hypoxia-ischemia-induced cell death and neuroprotection in the immature P3 rat. Dev. Neurosci. 29, 385–392.Google Scholar

  • Noguchi, K., Johnson, S., Dissen, G., Martin, L., Manzella, F., Schenning, K., and Brambrink, A. (2017). Isoflurane exposure for three hours triggers apoptotic cell death in neonatal macaque brain. Br. J. Anaesth. 119, 524–531.Google Scholar

  • Ohls, R.K., Kamath-Rayne, B.D., Christensen, R.D., Wiedmeier, S.E., Rosenberg, A., Fuller, J., and Lowe, J.R. (2014). Cognitive outcomes of preterm infants randomized to darbepoetin, erythropoietin, or placebo. Pediatr. 133, 1023–1030.Google Scholar

  • Pang, Y., Cai, Z., and Rhodes, P.G. (2000). Effects of lipopolysaccharide on oligodendrocyte progenitor cells are mediated by astrocytes and microglia. J. Neurosci. Res. 62, 510–520.Google Scholar

  • Pansiot, J., Pham, H., Dalous, J., Chevenne, D., Colella, M., Schwendimann, L., and Schang, A.-L. (2016). Glial response to 17β-estradiol in neonatal rats with excitotoxic brain injury. Exp. Neurol. 282, 56–65.Google Scholar

  • Penning, D.H., Grafe, M.R., Hammond, R., Matsuda, Y., Patrick, J., and Richardson, B. (1994). Neuropathology of the near-term and midgestation ovine fetal brain after sustained in utero hypoxemia. Am. J. Obstet. Gynecol. 170, 1425–1432.Google Scholar

  • Polglase, G.R., Hooper, S.B., Gill, A.W., Allison, B.J., McLean, C.J., Nitsos, I., and Kluckow, M. (2009). Cardiovascular and pulmonary consequences of airway recruitment in preterm lambs. J. Appl. Physiol. 106, 1347–1355.Google Scholar

  • Polglase, G.R., Miller, S.L., Barton, S.K., Baburamani, A.A., Wong, F.Y., Aridas, J.D., and Kluckow, M. (2012). Initiation of resuscitation with high tidal volumes causes cerebral hemodynamic disturbance, brain inflammation and injury in preterm lambs. PLoS One 7, e39535.Google Scholar

  • Raper, J., Alvarado, M.C., Murphy, K.L., and Baxter, M.G. (2015). Multiple anesthetic exposure in infant monkeys alters emotional reactivity to an acute stressor. Anesthesiology 123, 1084–1092.Google Scholar

  • Rees, S.M., Camm, E.J., Loeliger, M., Cain, S., Dieni, S., McCurnin, D., and Inder, T.E. (2007). Inhaled nitric oxide: effects on cerebral growth and injury in a baboon model of premature delivery. Pediatr. Res. 61, 552–558.Google Scholar

  • Rees, S., Hale, N., De Matteo, R., Cardamone, L., Tolcos, M., Loeliger, M., and Greenwood, D. (2010). Erythropoietin is neuroprotective in a preterm ovine model of endotoxin-induced brain injury. J. Neuropathol. Exp. Neurol. 69, 306–319.Google Scholar

  • Rice, J.E., Vannucci, R.C., and Brierley, J.B. (1981). The influence of immaturity on hypoxic-ischemic brain damage in the rat. Ann. Neurol. 9, 131–141.Google Scholar

  • Richetto, J., Calabrese, F., Meyer, U., and Riva, M.A. (2013). Prenatal versus postnatal maternal factors in the development of infection-induced working memory impairments in mice. Brain Behav. Immun. 33, 190–200.Google Scholar

  • Riddle, A., Luo, N.L., Manese, M., Beardsley, D.J., Green, L., Rorvik, D.A., and Hohimer, A.R. (2006). Spatial heterogeneity in oligodendrocyte lineage maturation and not cerebral blood flow predicts fetal ovine periventricular white matter injury. J. Neurosci. 26, 3045–3055.Google Scholar

  • Riddle, A., Dean, J., Buser, J.R., Gong, X., Maire, J., Chen, K., and Kroenke, C.D. (2011). Histopathological correlates of magnetic resonance imaging–defined chronic perinatal white matter injury. Ann. Neurol. 70, 493–507.Google Scholar

  • Rousset, C.I., Chalon, S., Cantagrel, S., Bodard, S., Andres, C., Gressens, P., and 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, 428–433.Google Scholar

  • Schenning, K.J., Noguchi, K.K., Martin, L.D., Manzella, F.M., Cabrera, O.H., Dissen, G.A., and Brambrink, A.M. (2017). Isoflurane exposure leads to apoptosis of neurons and oligodendrocytes in 20-and 40-day old rhesus macaques. Neurotoxicol. Teratol. 60, 63–68.Google Scholar

  • Schmitz, T., Ritter, J., Mueller, S., Felderhoff-Mueser, U., Chew, L.J., and Gallo, V. (2011). Cellular changes underlying hyperoxia-induced delay of white matter development. J. Neurosci. 31, 4327–4344.Google Scholar

  • Sfaello, I., Daire, J.-L., Husson, I., Kosofsky, B., Sebag, G., and Gressens, P. (2005). Patterns of excitotoxin-induced brain lesions in the newborn rabbit: a neuropathological and MRI correlation. Dev. Neurosci. 27, 160–168.Google Scholar

  • Shah, D.K., Doyle, L.W., Anderson, P.J., Bear, M., Daley, A.J., Hunt, R.W., and Inder, T.E. (2008). Adverse neurodevelopment in preterm infants with postnatal sepsis or necrotizing enterocolitis is mediated by white matter abnormalities on magnetic resonance imaging at term. J. Pediatr. 153, 170–175, 175 el.Google Scholar

  • Sheldon, R.A., Sedik, C., and Ferriero, D.M. (1998). Strain-related brain injury in neonatal mice subjected to hypoxia-ischemia. Brain Res. 810, 114–122.Google Scholar

  • Shindo, A., Liang, A.C., Maki, T., Miyamoto, N., Tomimoto, H., Lo, E.H., and Arai, K. (2016). Subcortical ischemic vascular disease: roles of oligodendrocyte function in experimental models of subcortical white-matter injury. J. Cereb. Blood. Flow Metab. 36, 187–198.Google Scholar

  • Sørensen, A., Pedersen, M., Tietze, A., Ottosen, L., Duus, L., and Uldbjerg, N. (2009). BOLD MRI in sheep fetuses: a non-invasive method for measuring changes in tissue oxygenation. Ultrasound Obstet. Gynecol. 34, 687–692.Google Scholar

  • Stetler, R.A., Leak, R.K., Gan, Y., Li, P., Zhang, F., Hu, X., and Gao, Y. (2014). Preconditioning provides neuroprotection in models of CNS disease: paradigms and clinical significance. Prog. Neurobiol. 114, 58–83.Google Scholar

  • Tan, S., Drobyshevsky, A., Jilling, T., Ji, X., Ullman, L.M., Englof, I., and Derrick, M. (2005). Model of cerebral palsy in the perinatal rabbit. J. Child Neurol. 20, 972–979.Google Scholar

  • van den Heuij, L.G., Mathai, S., Davidson, J.O., Lear, C.A., Booth, L.C., Fraser, M., and Bennet, L. (2014). Synergistic white matter protection with acute-on-chronic endotoxin and subsequent asphyxia in preterm fetal sheep. J. Neuroinflamm. 11, 89.Google Scholar

  • Vannucci, S.J. and Hagberg, H. (2004). Hypoxia-ischemia in the immature brain. J. Exp. Biol. 207, 3149–3154.Google Scholar

  • Vannucci, R.C. and Vannucci, S.J. (2005). Perinatal hypoxic-ischemic brain damage: evolution of an animal model. Dev. Neurosci. 27, 81–86.Google Scholar

  • Vannucci, R.C., Lyons, D.T., and Vasta, F. (1988). Regional cerebral blood flow during hypoxia-ischemia in immature rats. Stroke 19, 245–250.Google Scholar

  • Volpe, J.J. (2008). Neurology of the Newborn (5th ed.) (Philadelphia, USA: Saunders/Elsevier).Google Scholar

  • Vose, L.R., Vinukonda, G., Jo, S., Miry, O., Diamond, D., Korumilli, R., and Ballabh, P. (2013). Treatment with thyroxine restores myelination and clinical recovery after intraventricular hemorrhage. J. Neurosci. 33, 17232–17246.Google Scholar

  • Vottier, G., Pham, H., Pansiot, J., Biran, V., Gressens, P., Charriaut-Marlangue, C., and Baud, O. (2011). Deleterious effect of hyperoxia at birth on white matter damage in the newborn rat. Dev. Neurosci. 33, 261–269.Google Scholar

  • Wang, X., Rousset, C.I., Hagberg, H., and Mallard, C. (2006). Lipopolysaccharide-induced inflammation and perinatal brain injury. Semin. Fetal Neonatal Med. 11, 343–53.Google Scholar

  • Wang, L.-W., Chang, Y.-C., Lin, C.-Y., Hong, J.-S., and Huang, C.-C. (2010). Low-dose lipopolysaccharide selectively sensitizes hypoxic ischemia-induced white matter injury in the immature brain. Pediatr. Res. 68, 41–47.Google Scholar

  • Wang, C., Luan, Z., Yang, Y., Wang, Z., Wang, Q., Lu, Y., and Du, Q. (2015). High purity of human oligodendrocyte progenitor cells obtained from neural stem cells: suitable for clinical application. J. Neurosci. Methods 240, 61–66.Google Scholar

  • Workman, A.D., Charvet, C.J., Clancy, B., Darlington, R.B., and Finlay, B.L. (2013). Modeling transformations of neurodevelopmental sequences across mammalian species. J. Neurosci. 33, 7368–7383.Google Scholar

  • Yang, L., Sameshima, H., Ikeda, T., and Ikenoue, T. (2004). Lipopolysaccharide administration enhances hypoxic-ischemic brain damage in newborn rats. J. Obstet. Gynaecol. Res. 30, 142–147.Google Scholar

  • Yawno, T., Mahen, M., Li, J., Fahey, M.C., Jenkin, G., and Miller, S.L. (2017). The beneficial effects of melatonin administration following hypoxia-ischemia in preterm fetal sheep. Front Cell Neurosci. 11, 296.Google Scholar

  • Yuan, T.M., Yu, H.M., Gu, W.Z., and Li, J.P. (2005). White matter damage and chemokine induction in developing rat brain after intrauterine infection. J. Perinat. Med. 33, 415–422.Google Scholar

  • Zhu, X., Bergles, D.E., and Nishiyama, A. (2008). NG2 cells generate both oligodendrocytes and gray matter astrocytes. Development 135, 145–157.Google Scholar

About the article

aYan Zeng and Huiqing Wang: These authors contributed equally to this article.


Received: 2018-05-01

Accepted: 2018-06-16

Published Online: 2018-10-31


Funding Source: National Natural Science Foundation of China

Award identifier / Grant number: 81330016

Award identifier / Grant number: 81630038

Award identifier / Grant number: 81330524

Award identifier / Grant number: 81771634

This work was supported by the National Science Foundation of China (Funder Id: 10.13039/501100001809, No. 81330016, 81630038, 81330524, 81771634), the National Key R&D Program of China (2017YFA0104200), grants from Ministry of Education of China (IRT0935), grants from the Science and Technology Bureau of Sichuan Province (2016TD0002), and a grant of the Clinical Discipline Program (Neonatology) from the Ministry of Health of China (1311200003303).


Citation Information: Reviews in the Neurosciences, 20180044, ISSN (Online) 2191-0200, ISSN (Print) 0334-1763, DOI: https://doi.org/10.1515/revneuro-2018-0044.

Export Citation

©2018 Walter de Gruyter GmbH, Berlin/Boston.Get Permission

Comments (0)

Please log in or register to comment.
Log in