Functional integration of new neurons into hippocampal networks and poststroke comorbidities following neonatal stroke in mice

Epilepsy and Behavior

Volumn 18, Issue 4, 2010, Pages 344-357

  Kadam, S D ^a,b   Smith Hicks, C L ^b   Smith, D R ^c   Worley, P F ^b   Comi, A M ^a,b  

^a KENNEDY KRIEGER INSTITUTE   (United States)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

Arc; Behavioral comorbidities; Epilepsy; Hyperactivity; Lateralized circling; Neonatal stroke; Open field test; Timm stain

Indexed keywords

ACTIVITY REGULATED CYTOSKELETON ASSOCIATED PROTEIN; BROXURIDINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN ISCHEMIA; CAROTID ARTERY LIGATION; CIRCLING BEHAVIOR; COGNITIVE DEFECT; CONTROLLED STUDY; DISEASE SEVERITY; EPILEPSY; FEMALE; HIPPOCAMPUS; HYPERACTIVITY; MALE; MOUSE; NEONATAL STROKE; NERVE CELL; NEWBORN; NONHUMAN; SEIZURE; STROKE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; BROMODEOXYURIDINE; CELL DIFFERENTIATION; CYTOSKELETAL PROTEINS; DISEASE MODELS, ANIMAL; EPILEPSY; EXPLORATORY BEHAVIOR; FUNCTIONAL LATERALITY; HIPPOCAMPUS; MAZE LEARNING; MICE; NERVE TISSUE PROTEINS; NEUROGENESIS; NEURONS; STROKE; TIME FACTORS; VIDEO RECORDING;

EID: 77955582751     PISSN: 15255050     EISSN: 15255069     Source Type: Journal    
DOI: 10.1016/j.yebeh.2010.05.006     Document Type: Article

References (54)

1. Lynch J.K., Hirtz D.G., DeVeber G., Nelson K.B. Report of the National Institute of Neurological Disorders and Stroke Workshop on Perinatal and Childhood Stroke. Pediatrics 2002, 109:116-123.
2. Ben-Ari Y., Holmes G.L. Effects of seizures on developmental processes in the immature brain. Lancet Neurol 2006, 5:1055-1063.
3. Hartel C., Schilling S., Sperner J., Thyen U. The clinical outcomes of neonatal and childhood stroke: review of the literature and implications for future research. Eur J Neurol 2004, 11:431-438.
4. Anderson V., Jacobs R., Spencer-Smith M., et al. Does early age at brain insult predict worse outcome? Neuropsychological implications. J Pediatr Psychol 2009, [Electronic publication 7 December 2009].
5. Ho S.S., Kuzniecky R.I., Gilliam F., Faught E., Bebin M., Morawetz R. Congenital porencephaly: MR features and relationship to hippocampal sclerosis. AJNR Am J Neuroradiol 1998, 19:135-141.
6. Ho S.S., Kuzniecky R.I., Gilliam F., Faught E., Bebin M., Morawetz R. Congenital porencephaly and hippocampal sclerosis: clinical features and epileptic spectrum. Neurology 1997, 49:1382-1388.
7. Burneo J.G., Faught E., Knowlton R.C., et al. Temporal lobectomy in congenital porencephaly associated with hippocampal sclerosis. Arch Neurol 2003, 60:830-834.
8. Bartley J., Soltau T., Wimborne H., et al. BrdU-positive cells in the neonatal mouse hippocampus following hypoxic-ischemic brain injury. BMC Neurosci 2005, 6:15.
9. Chang Y.C., Tzeng S.F., Yu L., et al. Early-life fluoxetine exposure reduced functional deficits after hypoxic-ischemia brain injury in rat pups. Neurobiol Dis 2006, 24:101-113.
10. Kadam S.D., Mulholland J.D., McDonald J.W., Comi A.M. Neurogenesis and neuronal commitment following ischemia in a new mouse model for neonatal stroke. Brain Res 2008, 1208:35-45.
11. Kadam S.D., Mulholland J.D., McDonald J.W., Comi A.M. Poststroke subgranular and rostral subventricular zone proliferation in a mouse model of neonatal stroke. J Neurosci Res 2009, 87:2653-2666.
12. Altman J., Bayer S.A. Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 1990, 301:365-381.
13. Vaccarino F.M., Ment L.R. Injury and repair in developing brain. Arch Dis Child Fetal Neonatal Ed 2004, 89:F190-F192.
14. Anderson V., Spencer-Smith M., Leventer R., et al. Childhood brain insult: can age at insult help us predict outcome?. Brain 2009, 132:45-56.
15. Ramirez-Amaya V., Vazdarjanova A., Mikhael D., Rosi S., Worley P.F., Barnes C.A. Spatial exploration-induced Arc mRNA and protein expression: evidence for selective, network-specific reactivation. J Neurosci 2005, 25:1761-1768.
16. Ramirez-Amaya V., Marrone D.F., Gage F.H., Worley P.F., Barnes C.A. Integration of new neurons into functional neural networks. J Neurosci 2006, 26:12237-12241.
17. Temple M.D., Worley P.F., Steward O. Visualizing changes in circuit activity resulting from denervation and reinnervation using immediate early gene expression. J Neurosci 2003, 23:2779-2788.
18. Steward O. Reorganization of neuronal connections following CNS trauma: principles and experimental paradigms. J Neurotrauma 1989, 6:99-152.
19. Volpe J.J., Pasternak J.F. Parasagittal cerebral injury in neonatal hypoxic-ischemic encephalopathy: clinical and neuroradiologic features. J Pediatr 1977, 91:472-476.
20. Volpe J.J. Neurology of the newborn. Major Probl Clin Pediatr 2001, 22:1-648.
21. Kadam S.D., Mulholland J.D., Smith D.R., Johnston M.V., Comi A.M. Chronic brain injury and behavioral impairments in a mouse model of term neonatal strokes. Behav Brain Res 2009, 197:77-83.
22. Morrison R.S., Wenzel H.J., Kinoshita Y., Robbins C.A., Donehower L.A., Schwartzkroin P.A. Loss of the p53 tumor suppressor gene protects neurons from kainate-induced cell death. J Neurosci 1996, 16:1337-1345.
23. Ben Ari Y. Limbic seizure and brain damage produced by kainic acid: mechanisms and relevance to human temporal lobe epilepsy. Neuroscience 1985, 14:375-403.
24. Paxinos G., Franklin K.M. The mouse brain in stereotaxic coordinates 2001, Academic Press, San Diego. 2nd ed.
25. Babb T.L., Kupfer W.R., Pretorius J.K., Crandall P.H., Levesque M.F. Synaptic reorganization by mossy fibers in human epileptic fascia dentata. Neuroscience 1991, 42:351-363.
26. Racine R.J. Modification of seizure activity by electrical stimulation: II. Motor seizure. Electroencephalogr Clin Neurophysiol 1972, 32:281-294.
27. Hellier J.L., Dudek F.E. Spontaneous motor seizures of rats with kainate-induced epilepsy: effect of time of day and activity state. Epilepsy Res 1999, 35:47-57.
28. Kadam S.D., Dudek F.E. Neuropathogical features of a rat model for perinatal hypoxic-ischemic encephalopathy with associated epilepsy. J Comp Neurol 2007, 505:716-737.
29. Gorter J.A., van Vliet E.A., Aronica E., da Silva F.H.L. Progression of spontaneous seizures after status epilepticus is associated with mossy fibre sprouting and extensive bilateral loss of hilar parvalbumin and somatostatin-immunoreactive neurons. Eur J Neurosci 2001, 13:657-669.
30. Zhang X., Cui S.S., Wallace A.E., et al. Relations between brain pathology and temporal lobe epilepsy. J Neurosci 2002, 22:6052-6061.
31. Parent J.M., Yu T.W., Leibowitz R.T., Geschwind D.H., Sloviter R.S., Lowenstein D.H. Dentate granule cell neurogenesis is increased by seizures and contributes to aberrant network reorganization in the adult rat hippocampus. J Neurosci 1997, 17:3727-3738.
32. Guzowski J.F., Lyford G.L., Stevenson G.D., et al. Inhibition of activity-dependent Arc protein expression in the rat hippocampus impairs the maintenance of long-term potentiation and the consolidation of long-term memory. J Neurosci 2000, 20:3993-4001.
33. Pinaud R., Penner M.R., Robertson H.A., Currie R.W. Upregulation of the immediate early gene Arc in the brains of rats exposed to environmental enrichment: implications for molecular plasticity. Mol Brain Res 2001, 91:50-56.
34. Johnston M.V. Clinical disorders of brain plasticity. Brain Dev 2004, 26:73-80.
35. Sadato N., Yamada H., Okada T., et al. Age-dependent plasticity in the superior temporal sulcus in deaf humans: a functional MRI study. BMC Neurosci 2004, 5:56.
36. Ten V.S., Wu E.X., Tang H., et al. Late measures of brain injury after neonatal hypoxia-ischemia in mice. Stroke 2004, 35:2183-2188.
37. Johnston M.V., Ishida A., Ishida W.N., Matsushita H.B., Nishimura A., Tsuji M. Plasticity and injury in the developing brain. Brain Dev 2009, 31:1-10.
38. Loscher W. Abnormal circling behavior in rat mutants and its relevance to model specific brain dysfunctions. Neurosci Biobehav Rev 2010, 34:31-49.
39. Anderson M.J., Barnes G.W., Briggs J.F., et al. Effects of ontogeny on performance of rats in a novel object-recognition task. Psychol Rep 2004, 94:437-443.
40. Chapillon P., Roullet P. Use of proximal and distal cues in place navigation by mice changes during ontogeny. Dev Psychobiol 1996, 29:529-545.
41. Rossier J., Schenk F. Olfactory and/or visual cues for spatial navigation through ontogeny: olfactory cues enable the use of visual cues. Behav Neurosci 2003, 117:412-425.
42. Demers E.J., McPherson R.J., Juul S.E. Erythropoietin protects dopaminergic neurons and improves neurobehavioral outcomes in juvenile rats after neonatal hypoxia-ischemia. Pediatr Res 2005, 58:297-301.
43. Lyford G.L., Yamagata K., Kaufmann W.E., et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14:433-445.
44. Steward O., Worley P.F. A cellular mechanism for targeting newly synthesized mRNAs to synaptic sites on dendrites. Proc Natl Acad Sci USA 2001, 98:7062-7068.
45. Rodriguez J.J., Davies H.A., Errington M.L., Verkhratsky A., Bliss T.V., Stewart M.G. ARG3.1/ARC expression in hippocampal dentate gyrus astrocytes: ultrastructural evidence and co-localization with glial fibrillary acidic protein. J Cell Mol Med 2008, 12:671-678.
46. Lindemann S., Lessenich A., Ebert U., Loscher W. Spontaneous paroxysmal circling behavior in the ci2 rat mutant: epilepsy with rotational seizures or hyperkinetic movement disorder?. Exp Neurol 2001, 172:437-445.
47. Akiyama K., Ishikawa M., Saito A. mRNA expression of activity-regulated cytoskeleton-associated protein (arc) in the amygdala-kindled rats. Brain Res 2008, 1189:236-246.
48. Max J.E., Mathews K., Manes F.F., et al. Attention deficit hyperactivity disorder and neurocognitive correlates after childhood stroke. J Int Neuropsychol Soc 2003, 9:815-829.
49. Williams C.M., El Mohsen M.A., Vauzour D., et al. Blueberry-induced changes in spatial working memory correlate with changes in hippocampal CREB phosphorylation and brain-derived neurotrophic factor (BDNF) levels. Free Rad Biol Med 2008, 45:295-305.
50. Huang F., Chotiner J.K., Steward O. Actin polymerization and ERK phosphorylation are required for Arc/Arg3.1 mRNA targeting to activated synaptic sites on dendrites. J Neurosci 2007, 27:9054-9067.
51. Marrone D.F., Schaner M.J., McNaughton B.L., Worley P.F., Barnes C.A. Immediate-early gene expression at rest recapitulates recent experience. J Neurosci 2008, 28:1030-1033.
52. Miyashita T., Kubik S., Lewandowski G., Guzowski J.F. Networks of neurons, networks of genes: an integrated view of memory consolidation. Neurobiol Learn Mem 2008, 89:269-284.
53. Johnston M.V. Plasticity in the developing brain: implications for rehabilitation. Dev Disabil Res Rev 2009, 15:94-101.
54. Snyder J.S., Choe J.S., Clifford M.A., et al. Adult-born hippocampal neurons are more numerous, faster maturing, and more involved in behavior in rats than in mice. J Neurosci 2009, 29:14484-14495.