Disorganization of Oligodendrocyte Development in the Layer II/III of the Sensorimotor Cortex Causes Motor Coordination Dysfunction in a Model of White Matter Injury in Neonatal Rats

Overview

Journal Neurochem Res

Specialties Chemistry
Neurology

Date 2017 Aug 2

PMID 28762105

Citations 5

Authors

Yoshitomo Ueda

Sachiyo Misumi

Mina Suzuki

Shino Ogawa

Ruriko Nishigaki

Akimasa Ishida

Cha-Gyun Jung

Hideki Hida

Affiliations

Soon will be listed here.

Abstract

We previously established neonatal white matter injury (WMI) model rat that is made by right common carotid artery dissection at postnatal day 3, followed by 6% hypoxia for 60 min. This model has fewer oligodendrocyte progenitor cells and reduced myelin basic protein (MBP) positive areas in the sensorimotor cortex, but shows no apparent neuronal loss. However, how motor deficits are induced in this model is unclear. To elucidate the relationship between myelination disturbance and concomitant motor deficits, we first performed motor function tests (gait analysis, grip test, horizontal ladder test) and then analyzed myelination patterns in the sensorimotor cortex using transmission electron microscopy (TEM) and Contactin associated protein 1 (Caspr) staining in the neonatal WMI rats in adulthood. Behavioral tests revealed imbalanced motor coordination in this model. Motor deficit scores were higher in the neonatal WMI model, while hindlimb ladder stepping scores and forelimb grasping force were comparable to controls. Prolonged forelimb swing times and decreased hindlimb paw angles on the injured side were revealed by gait analysis. TEM revealed no change in myelinated axon number and the area g-ratio in the layer II/III of the cortex. Electromyographical durations and latencies in the gluteus maximus in response to electrical stimulation of the brain area were unchanged in the model. Caspr staining revealed fewer positive dots in layers II/III of the WMI cortex, indicating fewer and/or longer myelin sheath. These data suggest that disorganization of oligodendrocyte development in layers II/III of the sensorimotor cortex relates to imbalanced motor coordination in the neonatal WMI model rat.

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References

Wang X, Zhu C, Qiu L, Hagberg H, Sandberg M, Blomgren K . Activation of ERK1/2 after neonatal rat cerebral hypoxia-ischaemia. J Neurochem. 2003; 86(2):351-62. DOI: 10.1046/j.1471-4159.2003.01838.x. View

Rees S, Inder T . Fetal and neonatal origins of altered brain development. Early Hum Dev. 2005; 81(9):753-61. DOI: 10.1016/j.earlhumdev.2005.07.004. View

Costeloe K, Hennessy E, Haider S, Stacey F, Marlow N, Draper E . Short term outcomes after extreme preterm birth in England: comparison of two birth cohorts in 1995 and 2006 (the EPICure studies). BMJ. 2012; 345:e7976. PMC: 3514472. DOI: 10.1136/bmj.e7976. View

Ueda Y, Masuda T, Ishida A, Misumi S, Shimizu Y, Jung C . Enhanced electrical responsiveness in the cerebral cortex with oral melatonin administration after a small hemorrhage near the internal capsule in rats. J Neurosci Res. 2014; 92(11):1499-508. DOI: 10.1002/jnr.23434. View

Metz G, Whishaw I . Cortical and subcortical lesions impair skilled walking in the ladder rung walking test: a new task to evaluate fore- and hindlimb stepping, placing, and co-ordination. J Neurosci Methods. 2002; 115(2):169-79. DOI: 10.1016/s0165-0270(02)00012-2. View

Huang Z, Liu J, Cheung P, Chen C . Long-term cognitive impairment and myelination deficiency in a rat model of perinatal hypoxic-ischemic brain injury. Brain Res. 2009; 1301:100-9. DOI: 10.1016/j.brainres.2009.09.006. View

Mizuno K, Hida H, Masuda T, Nishino H, Togari H . Pretreatment with low doses of erythropoietin ameliorates brain damage in periventricular leukomalacia by targeting late oligodendrocyte progenitors: a rat model. Neonatology. 2008; 94(4):255-66. DOI: 10.1159/000151644. View

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

Stadlin A, James A, Fiscus R, Wong Y, Rogers M, Haines C . Development of a postnatal 3-day-old rat model of mild hypoxic-ischemic brain injury. Brain Res. 2003; 993(1-2):101-10. DOI: 10.1016/j.brainres.2003.08.058. View

10.

Liu Y, Silverstein F, Skoff R, Barks J . Hypoxic-ischemic oligodendroglial injury in neonatal rat brain. Pediatr Res. 2002; 51(1):25-33. DOI: 10.1203/00006450-200201000-00007. View

11.

Sizonenko S, Kiss J, Inder T, Gluckman P, Williams C . Distinctive neuropathologic alterations in the deep layers of the parietal cortex after moderate ischemic-hypoxic injury in the P3 immature rat brain. Pediatr Res. 2005; 57(6):865-72. DOI: 10.1203/01.PDR.0000157673.36848.67. View

12.

Inder T, Anderson N, Spencer C, Wells S, Volpe J . White matter injury in the premature infant: a comparison between serial cranial sonographic and MR findings at term. AJNR Am J Neuroradiol. 2003; 24(5):805-9. PMC: 7975772. View

13.

Buser J, Segovia K, Dean J, Nelson K, Beardsley D, Gong X . 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. 2010; 30(5):1053-65. PMC: 2915781. DOI: 10.1038/jcbfm.2009.286. View

14.

Drury P, Davidson J, Bennet L, Booth L, Tan S, Fraser M . Partial neural protection with prophylactic low-dose melatonin after asphyxia in preterm fetal sheep. J Cereb Blood Flow Metab. 2013; 34(1):126-35. PMC: 3887352. DOI: 10.1038/jcbfm.2013.174. View

15.

Robertson N, Faulkner S, Fleiss B, Bainbridge A, Andorka C, Price D . Melatonin augments hypothermic neuroprotection in a perinatal asphyxia model. Brain. 2012; 136(Pt 1):90-105. DOI: 10.1093/brain/aws285. View

16.

Volpe J . Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol. 2008; 8(1):110-24. PMC: 2707149. DOI: 10.1016/S1474-4422(08)70294-1. View

17.

Misumi S, Ueda Y, Nishigaki R, Suzuki M, Ishida A, Jung C . Dysfunction in Motor Coordination in Neonatal White Matter Injury Model Without Apparent Neuron Loss. Cell Transplant. 2015; 25(7):1381-93. DOI: 10.3727/096368915X689893. View

18.

Galtrey C, Fawcett J . Characterization of tests of functional recovery after median and ulnar nerve injury and repair in the rat forelimb. J Peripher Nerv Syst. 2007; 12(1):11-27. DOI: 10.1111/j.1529-8027.2007.00113.x. View

19.

Ness J, Romanko M, Rothstein R, Wood T, Levison S . Perinatal hypoxia-ischemia induces apoptotic and excitotoxic death of periventricular white matter oligodendrocyte progenitors. Dev Neurosci. 2001; 23(3):203-8. DOI: 10.1159/000046144. View

20.

Hamrick S, Miller S, Leonard C, Glidden D, Goldstein R, Ramaswamy V . Trends in severe brain injury and neurodevelopmental outcome in premature newborn infants: the role of cystic periventricular leukomalacia. J Pediatr. 2004; 145(5):593-9. DOI: 10.1016/j.jpeds.2004.05.042. View