The relationship between ventricular dilatation, neuropathological and neurobehavioural changes in hydrocephalic rats

Springer Science and Business Media LLC - Tập 9 - Trang 1-10 - 2012
Funmilayo Eniola Olopade1, Matthew Temitayo Shokunbi1,2, Anna-Leena Sirén3
1Department of Anatomy, College of Medicine, University of Ibadan, Ibadan, Nigeria
2Department of Neurological Surgery, College of Medicine, University of Ibadan, Ibadan, Nigeria
3Department of Neurosurgery, University of Wuerzburg, Wuerzburg, Germany

Tóm tắt

The motor and cognitive deficits observed in hydrocephalus are thought to be due to axonal damage within the periventricular white matter. This study was carried out to investigate the relationship between ventricular size, cellular changes in brain, and neurobehavioural deficits in rats with experimental hydrocephalus. Hydrocephalus was induced in three-week old rats by intracisternal injection of kaolin. Behavioural and motor function were tested four weeks after hydrocephalus induction and correlated to ventricular enlargement which was classified into mild, moderate or severe. Gross brain morphology, routine histology and immunohistochemistry for oligodendrocytes (CNPase), microglia (Iba-1) and astrocytes (GFAP) were performed to assess the cellular changes. Decreases in open field activity and forelimb grip strength in hydrocephalus correlated with the degree of ventriculomegaly. Learning in Morris water maze was significantly impaired in hydrocephalic rats. Gradual stretching of the ependymal layer, thinning of the corpus callosum, extracellular oedema and reduced cortical thickness were observed as the degree of ventriculomegaly increased. A gradual loss of oligodendrocytes in the corpus callosum and cerebral cortex was most marked in the severely-hydrocephalic brains, whereas the widespread astrogliosis especially in the subependymal layer was most marked in the brains with mild hydrocephalus. Retraction of microglial processes and increase in Iba-1 immunoreactivity in the white matter was associated ventriculomegaly. In hydrocephalic rats, oligodendrocyte loss, microglia activation, astrogliosis in cortical areas and thinning of the corpus callosum were associated with ventriculomegaly. The degree of ventriculomegaly correlated with motor and cognitive deficits.

Tài liệu tham khảo

Persson EK, Hagberg G, Uvebrant P: Hydrocephalus prevalence and outcome in a population-based cohort of children born in 1989–1998. Acta Paediat. 2005, 94: 726-732. 10.1080/08035250510027336. Del Bigio MR, Kanfer JN, Zhang YW: Myelination delay in the cerebral white matter of immature rats with kaolin-induced hydrocephalus is reversible. J Neuropath Exp Neurol. 1997, 56: 1053-1066. 10.1097/00005072-199709000-00010. Mello NK: Behavioural toxicology: a developing discipline. Fed Proc. 1975, 34: 1832-1834. Lorber J: Hydrocephalus in fruhen kindersalter. Hydrocephalus in fruhen kindersalter. Edited by: Stuttgart VD. 1983, Enke, Enke, 2-14. Feuillet L, Dufour H, Pelletier J: Brain of a white-collar worker. Lancet. 2007, 370 (9583): 262-10.1016/S0140-6736(07)61127-1. Jackson PH, Lorber J: Brain and ventricular volume in hydrocephalus. Z Kinderchir. 1984, 39 (Suppl 2): 91-93. Del Bigio MR, Wilson MJ, Enno T: Chronic hydrocephalus in rats and humans: white matter loss and behavior changes. Ann Neurol. 2003, 53: 337-346. 10.1002/ana.10453. Garcia GB, Quiroga AD, Sturtz N, Martinez AI, Biancardi ME: Morphological alterations of central nervous system (CNS) myelin in vanadium (V)-exposed adult rats. Drug Chem Toxicol. 2004, 27: 281-293. 10.1081/DCT-120037747. Tamashiro KLK, Wakayama T, Blanchard RJ, Blanchard C, Yanagimachi R: Postnatal growth and behavioral development of mice cloned from adult cumulus cells. Biol Reprod. 2000, 63: 328-334. 10.1095/biolreprod63.1.328. Van Dam V, Lenders G, De Deyn PP: Effect of Morris water maze diameter on visual-spatial learning in different mouse strains. Neurobiol Learn Mem. 2006, 85: 164-172. 10.1016/j.nlm.2005.09.006. D’Hooge R, De Deyn PP: Applications of the Morris water maze in the study of learning and memory. Brain Res Rev. 2001, 36: 60-90. 10.1016/S0165-0173(01)00067-4. Jones HC, Rivera KM, Harris NG: Learning deficits in congenitally hydrocephalic rats and prevention by early shunt treatment. Child's Nerv Syst. 1995, 11: 655-660. 10.1007/BF00300725. Khan OH, Enno TL, Del Bigio MR: Brain damage in neonatal rats following kaolin induction of hydrocephalus. Exp Neurol. 2006, 200: 311-320. 10.1016/j.expneurol.2006.02.113. Oi S, Yamada H, Sato O, Matsumoto S: Experimental models of congenital hydrocephalus and comparable clinical problems in the fetal and neonatal periods. Child’s Nerv Syst. 1996, 12: 292-302. 10.1007/BF00301016. Warf BC: Hydrocephalus in Uganda: the predominance of infectious origin and primary management with endoscopic third ventriculostomy. J Neurosurg. 2005, 102 (Suppl): 1-15. 10.3171/jns.2005.102.s_supplement.0001. Del Bigio MR: Future directions for therapy of childhood hydrocephalus: A view from the laboratory. Ped Neurosurg. 2001, 34: 172-181. 10.1159/000056016. Del Bigio MR, Crook CR, Buist R: Magnetic resonance imaging and behavioural analysis of immature rats with kaolin-induced hydrocephalus: pre- and post shunting observations. Exp Neurol. 1997, 148: 256-264. 10.1006/exnr.1997.6644. Del Bigio MR: Neuropathological changes caused by hydrocephalus. Acta Neuropathol. 1993, 85: 573-585. 10.1007/BF00334666. Morris RG, Garrud P, Rawlins JN, O’Keefe J: Place navigation impaired in rats with hippocampal lesions. Nature. 1984, 297: 681-683. Fukushima NK, Yokouchi K, Kawagishi K, Ren G, Higashiyama F, Moriizumi T: Proliferating cell populations in experimentally-induced hydrocephalus in developing rats. J Clin Neurosci. 2003, 10: 334-337. 10.1016/S0967-5868(03)00019-5. Del Bigio MR, Zhang YW: Cell death, axonal damage and cell birth in the immature rat brain following induction of hydrocephalus. Exp Neurol. 1998, 154: 157-169. 10.1006/exnr.1998.6922. Fawcett JW, Asher RA: The glial scar and central nervous system repair. Brain Res Bull. 1999, 49: 377-391. 10.1016/S0361-9230(99)00072-6. McAllister JP, Chovan P: Neonatal hydrocephalus: mechanisms and consequences. Neurosurg Clin N Am. 1998, 1998 (9): 73-93. Beems T, Simons KS, Van Geel WJ, De Reus HP, Vos PE, Verbeek MM: Serum- and CSF- concentrations of brain specific proteins in hydrocephalus. Acta Neurochir (Wien). 2003, 145: 37-43. 10.1007/s00701-002-1019-1. Fitch MT, Silver J: CNS injury, glial scars and inflammation: inhibitory extracellular matrices and regeneration failure. Exp Neurol. 2007, 209: 294-301. Miller JM, McAllister JP: Reduction of astrogliosis and microgliosis by CSF shunting in experimental hydrocephalus. Cerebrospinal Fluid Res. 2007, 4: 5-10.1186/1743-8454-4-5. Deren KE, Packer M, Forsyth J, Brett Milash B, Abdullah OM, Hsu EW, McAllister JP: Reactive astrocytosis, microgliosis and inflammation in rats with neonatal hydrocephalus. Exp Neurol. 2010, 226: 110-119. 10.1016/j.expneurol.2010.08.010. Mori F, Tanji K, Yoshida Y, Wakabayashi K: Thalamic retrograde degeneration in the congenitally hydrocephalic rat is attributable to apoptotic cell death. Neuropathol. 2002, 22: 186-193. 10.1046/j.1440-1789.2002.00445.x. Mc Allister JP, Maugans TA, Shah MV, Truex RC: Neuronal effects of experimentally induced hydrocephalus in newborn rats. J Neurosurg. 1985, 63: 776-783. 10.3171/jns.1985.63.5.0776. Shim I, Ha Y, Chung JY, Lee H, Yang KH, Chang JW: Association of learning and memory impairments with changes in the septohippocampal cholinergic system in rats with kaolin-induced hydrocephalus. Neurosurgery. 2003, 53: 416-425. 10.1227/01.NEU.0000073989.07810.D8. Tashiro Y, Chakrabortty S, Drake JM, Hattori T: Functional injury of cholinergic, GABAergic and dopaminergic systems in the basal ganglia of adult rat with kaolin-induced hydrocephalus. Brain Res. 1996, 770: 45-52.