Spectrum of short- and long-term brain pathology and long-term behavioral deficits in male repeated hypoxic rats closely resembling human extreme prematurity

Journal of Neuroscience

Volumn 33, Issue 29, 2013, Pages 11863-11877

  Oorschot, Dorothy E ^a,b   Voss, Logan ^a,b   Covey, Matthew V ^a,b   Goddard, Liping ^a,b   Huang, William ^a,b   Birchall, Penny ^a,b   Bilkey, David K ^b   Kohe, Sarah E ^a,b  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

[No Author keywords available]

Indexed keywords

MYELIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ATTENTION DEFICIT DISORDER; BODY WEIGHT; BRAIN ATROPHY; BRAIN CORTEX; BRAIN WEIGHT; CONTROLLED STUDY; CORPUS STRIATUM; HISTOLOGY; HYPOXIA; IMMUNOHISTOCHEMISTRY; MALE; NONHUMAN; OLIGODENDROGLIA; PREMATURITY; PRIORITY JOURNAL; PUP (RODENT); RAT; STEREOMETRY; TRANSMISSION ELECTRON MICROSCOPY; WHITE MATTER;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; ASTROCYTES; BEHAVIOR, ANIMAL; BRAIN; MALE; MAZE LEARNING; MYELIN SHEATH; NERVE FIBERS, MYELINATED; NEURONS; OLIGODENDROGLIA; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84880441407     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0342-12.2013     Document Type: Article

References (52)

1. Arnsten AF (2009) Toward a new understanding of attention-deficit hyperactivity disorder pathophysiology: an important role for prefrontal cortex dysfunction. CNS Drugs 23 [Suppl 1]:33-41. CrossRef Medline
2. Back SA, Han BH, Luo NL, Chricton CA, Xanthoudakis S, Tam J, Arvin KL, Holtzman DM (2002) Selective vulnerability of late oligodendrocyte progenitors to hypoxia-ischemia. J Neurosci 22:455-463. Medline
3. Back SA, Riddle A, McClure MM (2007) Birth maturation-dependent vulnerability of perinatal white matter in premature birth. Stroke 38:724-730. CrossRef Medline
4. Baddeley AJ, Gundersen HJ, Cruz-Orive LM (1986) Estimation of surface area from vertical sections. J Microsc 142:259-276. CrossRef Medline
5. Balasubramaniam J, Del Bigio MR (2006) Animal models of germinal matrix hemorrhage. J Child Neurol 21:365-371. CrossRef Medline
6. Billiards SS, Haynes RL, Folkerth RD, Borenstein NS, Trachtenberg FL, Rowitch DH, Ligon KL, Volpe JJ, Kinney HC (2008) Myelin abnormalities without oligodendrocyte loss in periventricular leukomalacia. Brain Pathol 18:153-163. CrossRef Medline
7. Braendgaard H, Evans SM, Howard CV, Gundersen HJ (1990) The total number of neurons in the human neocortex unbiasedly estimated using optical disectors. J Microsc 157:285-304. CrossRef Medline
8. Brake WG, Sullivan RM, Gratton A (2000) Perinatal distress leads to lateralized medial prefrontal cortical dopamine hypofunction in adult rats. J Neurosci 20:5538-5543. Medline
9. Castellanos FX, Lee PP, Sharp W, Jeffries NO, Greenstein DK, Clasen LS, Blumenthal JD, James RS, Ebens CL, Walter JM, Zijdenbos A, Evans AC, Giedd JN, Rapoport JL (2002) Developmental trajectories of brain volume abnormalities in children and adolescents with attention-deficit/ hyperactivity disorder. JAMA 288:1740-1748. CrossRef Medline
10. Chapados I, Cheung PY (2008) Not all models are created equal: animal models to study hypoxic-ischemic encephalopathy of the newborn. Neonatology 94:300-303. CrossRef Medline
11. Dorph-Petersen KA, Pierri JN, Sun Z, Sampson AR, Lewis DA (2004) Stereological analysis of the mediodorsal thalamic nucleus in schizophrenia: volume, neuron number, and cell types. J Comp Neurol 472:449-462. CrossRef Medline
12. Golden JA, Gilles FH, Rudelli R, Leviton A (1997) Frequency of neuropathological abnormalities in very low birth weight infants. J Neuropath Exp Neurol 56:472-478. CrossRef Medline
13. Gundersen HJ (1977) Notes on the estimation of numerical density of arbitrary profiles: the edge effect. J Microsc 111:219-223. CrossRef
14. Gundersen HJ, Bagger P, Bendtsen TF, Evans SM, Korbo L, Marcussen N, Møller A, Nielsen K, Nyengaard JR, Pakkenberg B, Sorenson FB, Vesterby A, West MJ (1988) The new stereological tools: disector, fractionator, nucleator and point sampled intercepts and their use in pathological research and diagnosis. APMIS 96:857-881. CrossRef Medline
15. Gundersen HJ, Jensen EB, Kiêu K, Nielsen J (1999) The efficiency of systematic sampling in stereology-reconsidered. J Microsc 193:199-211. CrossRef Medline
16. Hack M, Schluchter M, Cartar L, Rahman M, Cuttler L, Borawski E (2003) Growth of very low birth weight infants to age 20 years. Pediatrics 112: e30-e38. CrossRef Medline
17. Hagberg H, Bona E, Gilland E, Puka-Sundvall M (1997) Hypoxia-ischaemia model in the 7-day-old rat: possibilities and shortcomings. Acta Paediatr [Suppl] 422:85-88.
18. Halsey CL, Collin MF, Anderson CL (1996) Extremely low-birth-weight children and their peers. A comparison of school-age outcomes. Arch Pediatr Adolesc Med 150:790-794. CrossRef Medline
19. 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 62:441-450. Medline
20. Hobbs CE, Oorschot DE (2008) Neonatal rat hypoxia-ischemia: long-term rescue of striatal neurons and motor skills by combined antioxidanthypothermia treatment. Brain Pathol 18:443-454. CrossRef Medline
21. Johnson S (2007) Cognitive and behavioural outcomes following very preterm birth. Semin Fetal Neonatal Med 12:363-373. CrossRef Medline
22. Larsen M, Bjarkam CR, Østergaard K, West MJ, Sørensen JC (2004) The anatomy of the porcine subthalamic nucleus evaluated with immunohistochemistry and design-based stereology. Anat Embryol (Berl) 208:239-247. CrossRef Medline
23. Levison SW, Rothstein RP, Romanko MJ, Snyder MJ, Meyers RL, Vannucci SJ (2001) Hypoxia/ischemia depletes the rat perinatal subventricular zone of oligodendrocyte progenitors and neural stem cells. Dev Neurosci 23: 234-247. CrossRef Medline
24. Liu P, Bilkey DK (1999) The effect of excitotoxic lesions centered on the perirhinal cortex in two versions of the radial arm maze task. Behav Neurosci 113:672-682. CrossRef Medline
25. Liu P, Bilkey DK (2001) The effect of excitotoxic lesions centered on the hippocampus or perirhinal cortex in object recognition and spatial memory tasks. Behav Neurosci 115:94-111. CrossRef Medline
26. LouHC (1996) Etiology and pathogenesis of ADHD: significance of prematurity and perinatal hypoxic-haemodynamic encephalopathy. Acta Paediatrica 85:1266-1271. CrossRef Medline
27. Matoba N, Yu Y, Mestan K, Pearson C, Ortiz K, Porta N, Thorsen P, Skogstrand K, Hougaard DM, Zuckerman B, Wang X (2009) Differential patterns of 27 cord blood immune biomarkers across gestational age. Pediatrics 123:1320-1328. CrossRef Medline
28. Ment LR, Hirtz D, Hüppi PS (2009) Imaging biomarkers of outcome in the developing preterm brain. Lancet Neurol 8:1042-1055. CrossRef Medline
29. Michel RP, Cruz-Orive LM (1988) Application of the Cavalieri principle and vertical sections method to the lung: estimation of volume and pleural surface area. J Microsc 150:117-136. CrossRef Medline
30. Mikati MA, Zeinieh MP, Kurdi RM, Harb SA, El Hokayem JA, Daderian RH, Shamseddine A, Obeid M, Bitar FF, El Sabban M (2005) Long-term effects of acute and of chronic hypoxia on behavior and on hippocampal histology in the developing brain. Brain Res Dev Brain Res 157:98-102. CrossRef Medline
31. Northam GB, Liégeois F, Chong WK, Wyatt JS, Baldeweg T (2011) Total brain white matter is a major determinant of IQ in adolescents born preterm. Ann Neurol 69:702-711. CrossRef Medline
32. Oorschot DE (1994) Are you using neuronal densities, synaptic densities or neurochemical densities as your definitive data? There is a better way to go. Prog Neurobiol 44:233-247. CrossRef Medline
33. Oorschot DE (1996) The total number of neurons in the neostriatal, pallidal, subthalamic and substantia nigral nuclei of the rat basal ganglia: a stereological study using the Cavalieri and optical disector methods. J Comp Neurol 366:580-599. CrossRef Medline
34. Oorschot DE, Tunstall MJ, Wickens JR (2002) Local connectivity between striatal spiny projection neurons: a re-evaluation. In: The basal ganglia VII (Nicholson L, Faull RLM, eds), pp 421-434. New York: Plenum.
35. Oorschot DE, Voss L, Covey MV, Bilkey DK, Saunders SE (2007) ADHDlike hyperactivity, with no attention deficit, in adult rats after repeated hypoxia during the equivalent of extreme prematurity. J Neurosci Methods 166:315-322. CrossRef Medline
36. Partadiredja G, Miller R, Oorschot DE (2003) The number, size, and type of axons in rat subcortical white matter on left and right sides: a stereological, ultrastructural study. J Neurocytol 32:1165-1179. CrossRef Medline
37. Paul CM, Magda G, Abel S (2009) Spatial memory: theoretical basis and comparative review on experimental methods in rodents. Behav Brain Res 203:151-164. CrossRef Medline
38. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, Ed 4. San Diego: Academic.
39. Paxinos G, Watson C (2007) The rat brain in stereotaxic coordinates, Ed 6. Amsterdam: Academic.
40. Poets CF, Stebbens VA, Richard D, Southall DP (1995) Prolonged episodes of hypoxemia in preterm infants undetectable by cardiorespiratory monitors. Pediatrics 95:860-863. Medline
41. Sahin B, Aslan H, Unal B, Canan S, Bilgic S, Kaplan S, Tumkaya L (2001) Brain volumes of the lamb, rat and bird do not show hemispheric asymmetry: a stereological study. Image Anal Stereol 20:9-13. CrossRef
42. Scafidi J, Fagel DM, Ment LR, Vaccarino FM (2009) Modeling premature brain injury and recovery. Int J Dev Neurosci 27:863-871. CrossRef Medline
43. Silbereis JC, Huang EJ, Back SA, Rowitch DH (2010) Towards improved animal models of neonatal white matter injury associated with cerebral palsy. Dis Model Mech 3:678-688. CrossRef Medline
44. Slomianka L, West MJ (2005) Estimators of the precision of stereological estimates: an example based on the CA1 pyramidal cell layer of rats. Neuroscience 136:757-767. CrossRef Medline
45. Tandrup T (1993) A method for unbiased and efficient estimation of number and mean volume of specified neuronal subtypes in rat dorsal root ganglion. J Comp Neurol 329:269-276. CrossRef Medline
46. Tao JD, Barnette AR, Griffith JL, Neil JJ, Inder TE (2012) Histopathologic correlation with diffusion tensor imaging after chronic hypoxia in the immature ferret. Pediatr Res 71:192-198. CrossRef Medline
47. Taylor HG, Minich N, Bangert B, Filipek PA, Hack M (2004) Long-term neuropsychological outcomes of very low birth weight: associations with early risks for periventricular brain insults. J Int Neuropsychol Soc 10: 987-1004. Medline
48. Tos P, Ronchi G, Nicolino S, Audisio C, Raimondo S, Fornaro M, Battiston B, Graziani A, Perroteau I, Geuna S (2008) Employment of the mouse median nerve model for the experimental assessment of peripheral nerve regeneration. J Neurosci Methods 169:119-127. CrossRef Medline
49. Vederhus BJ, Markestad T, Eide GE, Graue M, Halvorsen T (2010) Health related quality of life after extremely preterm birth: a matched controlled cohort study. Health Qual Life Outcomes 8:53. CrossRef Medline
50. Volpe JJ (2009) Brain injury in premature infants: a complex amalgam of destructive and developmental disturbances. Lancet Neurol 8:110-124. CrossRef Medline
51. Volpe JJ, Kinney HC, Jensen FE, Rosenberg PA (2011) The developing oligodendrocyte: key cellular target in brain injury in the premature infant. Int J Dev Neurosci 29:423-440. CrossRef Medline
52. West MJ, Gundersen HJ (1990) Unbiased stereological estimation of the number of neurons in the human hippocampus. J Comp Neurol 296:1-22. CrossRef Medline