Prenatal Ischemia Deteriorates White Matter, Brain Organization, and Function: Implications for Prematurity and Cerebral Palsy

Overview

Journal Dev Med Child Neurol

Date 2016 Mar 31

PMID 27027601

Citations 28

Authors

Jacques-Olivier Coq

Maxime Delcour

Vicky S Massicotte

Olivier Baud

Mary F Barbe

Affiliations

Soon will be listed here.

Abstract

Cerebral palsy (CP) describes a group of neurodevelopmental disorders of posture and movement that are frequently associated with sensory, behavioral, and cognitive impairments. The clinical picture of CP has changed with improved neonatal care over the past few decades, resulting in higher survival rates of infants born very preterm. Children born preterm seem particularly vulnerable to perinatal hypoxia-ischemia insults at birth. Animal models of CP are crucial for elucidating underlying mechanisms and for development of strategies of neuroprotection and remediation. Most animal models of CP are based on hypoxia-ischemia around the time of birth. In this review, we focus on alterations of brain organization and functions, especially sensorimotor changes, induced by prenatal ischemia in rodents and rabbits, and relate these alterations to neurodevelopmental disorders found in preterm children. We also discuss recent literature that addresses the relationship between neural and myelin plasticity, as well as possible contributions of white matter injury to the emergence of brain dysfunctions induced by prenatal ischemia.

Citing Articles

Constraint-Induced Movement Therapy (CIMT) and Neural Precursor Cell (NPC) Transplantation Synergistically Promote Anatomical and Functional Recovery in a Hypoxic-Ischemic Mouse Model.

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Neuroprotective Effect of Clemastine Improved Oligodendrocyte Proliferation through the MAPK/ERK Pathway in a Neonatal Hypoxia Ischemia Rat Model.

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No Impact of Enteral Nutrition on Fecal Short-Chain Fatty Acids in Children with Cerebral Palsy.

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Evaluation of Pain Prevalence in Children Who Experienced Perinatal Hypoxia-Ischemia Events: Characteristics and Associations With Sociodemographic Factors.

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References

Wittenberg G . Motor mapping in cerebral palsy. Dev Med Child Neurol. 2009; 51 Suppl 4:134-9. DOI: 10.1111/j.1469-8749.2009.03426.x. View

Olivier P, Baud O, Bouslama M, Evrard P, Gressens P, Verney C . Moderate growth restriction: deleterious and protective effects on white matter damage. Neurobiol Dis. 2007; 26(1):253-63. DOI: 10.1016/j.nbd.2007.01.001. View

Zhuravin I, Dubrovskaya N, Tumanova N . Postnatal physiological development of rats after acute prenatal hypoxia. Neurosci Behav Physiol. 2004; 34(8):809-16. DOI: 10.1023/b:neab.0000038132.08219.31. View

Elitt C, Rosenberg P . The challenge of understanding cerebral white matter injury in the premature infant. Neuroscience. 2014; 276:216-38. PMC: 4146717. DOI: 10.1016/j.neuroscience.2014.04.038. View

Xerri C, Bourgeon S, Coq J . Perceptual context-dependent remodeling of the forepaw map in the SI cortex of rats trained on tactile discrimination. Behav Brain Res. 2005; 162(2):207-21. DOI: 10.1016/j.bbr.2005.03.003. View

Marret S, Vanhulle C, Laquerriere A . Pathophysiology of cerebral palsy. Handb Clin Neurol. 2013; 111:169-76. DOI: 10.1016/B978-0-444-52891-9.00016-6. View

McKenzie I, Ohayon D, Li H, de Faria J, Emery B, Tohyama K . Motor skill learning requires active central myelination. Science. 2014; 346(6207):318-22. PMC: 6324726. DOI: 10.1126/science.1254960. View

Johnston M, Ferriero D, Vannucci S, Hagberg H . Models of cerebral palsy: which ones are best?. J Child Neurol. 2006; 20(12):984-7. DOI: 10.1177/08830738050200121001. View

Pitcher J, Schneider L, Burns N, Drysdale J, Higgins R, Ridding M . Reduced corticomotor excitability and motor skills development in children born preterm. J Physiol. 2012; 590(22):5827-44. PMC: 3528994. DOI: 10.1113/jphysiol.2012.239269. View

10.

Delcour M, Russier M, Xin D, Massicotte V, Barbe M, Coq J . Mild musculoskeletal and locomotor alterations in adult rats with white matter injury following prenatal ischemia. Int J Dev Neurosci. 2011; 29(6):593-607. DOI: 10.1016/j.ijdevneu.2011.02.010. View

11.

Zaehle T, Herrmann C . Neural synchrony and white matter variations in the human brain--relation between evoked γ frequency and corpus callosum morphology. Int J Psychophysiol. 2010; 79(1):49-54. DOI: 10.1016/j.ijpsycho.2010.06.029. View

12.

Lubsen J, Vohr B, Myers E, Hampson M, Lacadie C, Schneider K . Microstructural and functional connectivity in the developing preterm brain. Semin Perinatol. 2011; 35(1):34-43. PMC: 3063450. DOI: 10.1053/j.semperi.2010.10.006. View

13.

Wingert J, Burton H, Sinclair R, Brunstrom J, Damiano D . Joint-position sense and kinesthesia in cerebral palsy. Arch Phys Med Rehabil. 2009; 90(3):447-53. PMC: 2651562. DOI: 10.1016/j.apmr.2008.08.217. View

14.

Volpe J, Kinney H, Jensen F, Rosenberg P . The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci. 2011; 29(4):423-40. PMC: 3099053. DOI: 10.1016/j.ijdevneu.2011.02.012. View

15.

Suppiej A, Cappellari A, Franzoi M, Traverso A, Ermani M, Zanardo V . Bilateral loss of cortical somatosensory evoked potential at birth predicts cerebral palsy in term and near-term newborns. Early Hum Dev. 2010; 86(2):93-8. DOI: 10.1016/j.earlhumdev.2010.01.024. View

16.

Olivier P, Baud O, Evrard P, Gressens P, Verney C . Prenatal ischemia and white matter damage in rats. J Neuropathol Exp Neurol. 2005; 64(11):998-1006. DOI: 10.1097/01.jnen.0000187052.81889.57. View

17.

Duerden E, Taylor M, Miller S . Brain development in infants born preterm: looking beyond injury. Semin Pediatr Neurol. 2013; 20(2):65-74. DOI: 10.1016/j.spen.2013.06.007. View

18.

Nitsos I, Rees S . The effects of intrauterine growth retardation on the development of neuroglia in fetal guinea pigs. An immunohistochemical and an ultrastructural study. Int J Dev Neurosci. 1990; 8(3):233-44. DOI: 10.1016/0736-5748(90)90029-2. View

19.

Basilious A, Yager J, Fehlings M . Neurological outcomes of animal models of uterine artery ligation and relevance to human intrauterine growth restriction: a systematic review. Dev Med Child Neurol. 2014; 57(5):420-30. PMC: 4406147. DOI: 10.1111/dmcn.12599. View

20.

Sampaio-Baptista C, Khrapitchev A, Foxley S, Schlagheck T, Scholz J, Jbabdi S . Motor skill learning induces changes in white matter microstructure and myelination. J Neurosci. 2013; 33(50):19499-503. PMC: 3858622. DOI: 10.1523/JNEUROSCI.3048-13.2013. View