Reproductive experience facilitates recovery from kainic acid-induced neural insult in female Long-Evans rats

Brain Research

Volumn 1454, Issue , 2012, Pages 80-89

  Franssen, R Adam ^b   Rzucidlo, Amanda M ^a   Franssen, Catherine L ^a   Hampton, J Ezekiel ^a   Benkovic Jr , Stanley A ^c   Bardi, Massimo ^e   Kinsley, Craig H ^d   Lambert, Kelly G ^a  

^a RANDOLPH MACON COLLEGE   (United States)

^b LONGWOOD UNIVERSITY   (United States)

^c Neuroscience Associates Inc   (United States)

^d UNIVERSITY OF RICHMOND   (United States)

^e MARSHALL UNIVERSITY   (United States)

Author keywords

Gliosis; Maternal behavior; Memory; Neurotoxicity; Traumatic brain injury

Indexed keywords

GLIAL FIBRILLARY ACIDIC PROTEIN; KAINIC ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; COGNITION; CONTROLLED STUDY; FEMALE; GLIOSIS; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MATERNAL BEHAVIOR; MEMORY; MULTIPARA; NERVE CELL DEGENERATION; NERVE CELL PLASTICITY; NEUROPROTECTION; NEUROPSYCHOLOGICAL TEST; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT; REPRODUCTION; SCORING SYSTEM; SEIZURE THRESHOLD; TASK PERFORMANCE;

ANIMALS; BRAIN; FEMALE; KAINIC ACID; MAZE LEARNING; MEMORY; NEURONS; RATS; RATS, LONG-EVANS; RECOVERY OF FUNCTION; SEXUAL BEHAVIOR, ANIMAL;

ANIMALIA; RATTUS;

EID: 84860240937     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2012.03.028     Document Type: Article

References (51)

1. I. Azcoitia, M.A. Arevalo, A.F. De Nicola, and L.M. Garcia-Segura Neuroprotective actions of estradiol revisited Trends Endocrinol. Metab. 119 2011 1084 1096
2. I. Azcoitia, M. Santos-Galindo, M.A. Arevalo, and L.M. Garcia-Segura Role of astroglia in the neuroplastic and neuroprotective actions of estradiol Eur. J. Neurosci. 32 2010 1995 2002
3. C.K. Barha, T. Ishrat, J.R. Epp, L.A. Galea, and D.G. Stein Progesterone treatment normalizes the levels of cell proliferation and cell death in the dentate gyrus of the hippocampus after traumatic brain injury Exp. Neurol. 231 2011 72 81
4. G.R. Barker, F. Bird, V. Alexander, and E.C. Warburton Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex J. Neurosci. 27 2007 2948 2957 (Pubitemid 46438982)
5. G. Barreto, M. Santos-Galindo, Y. Diz-Chaves, O. Pernía, P. Carrero, I. Azcoitia, and L.M. Garcia-Segura Selective estrogen receptor modulators decrease reactive astrogliosis in the injured brain: effects of aging and prolonged depletion of ovarian hormones Endocrinology 150 2009 5010 5015
6. E. Baulieu, and M. Schumacher Progesterone as a neuroactive neurosteroid, with special reference to the effect of progesterone on myelination Steroids 65 2000 605 612
7. S.A. Benkovic, J.P. O'Callaghan, and D.B. Miller Sensitive indicators of injury reveal hippocampal damage in C57BL/6J mice treated with kainic acid in the absence of tonic-clonic seizures Brain Res. 1034 2004 59 76 (Pubitemid 39307088)
8. G.J. Bouma, and J.P. Muizelaar Cerebral blood flow, cerebral blood volume, and cerebrovascular reactivity after severe head injury Neurotrauma 1 1992 S333 S348
9. V. Cabrera, D. Cantu, E. Ramos, A. Vanoye-Carlo, M. Cerbon, and T. Morales Lactation is a natural model of hippocampus neuroprotection against excitotoxicity Neurosci. Lett. 461 2009 136 139
10. J.C. Carroll, E.R. Rosario, L. Chang, F.Z. Stanczyk, S. Oddo, F.M. LaFerla, and C.J. Pike Progesterone and estrogen regulate Alzheimer-like neuropathy in female 3xTg-AD mice J. Neurosci. 27 2007 13357 13365 (Pubitemid 350220504)
11. Y. Chen, and R.A. Swanson Astrocytes and brain injury J. Cereb. Blood Flow Metab. 23 2003 137 149 (Pubitemid 36188452)
12. C.L. Franssen, M. Bardi, E.A. Shea, J.E. Hampton, R.A. Franssen, C.H. Kinsley, and K.G. Lambert Fatherhood alters behavioural and neural responsiveness in a spatial task J. Neuroendocrinol. 23 2011 1177 1187
13. J.D. Gatewood, M.D. Morgan, M. Eaton, I.M. McNamara, L.F. Stevens, A.H. Macbeth, E.A. Meyer, L.M. Lomas, F.J. Kozub, K.G. Lambert, and C.H. Kinsley Motherhood mitigates aging-related decrements in learning and memory and positively affects brain aging in the rat Brain Res. Bull. 66 2005 91 98 (Pubitemid 40854080)
14. T.A. Genarelli, and D.I. Graham Neuropathology J.M. Silver, T.W. McAllister, S.C. Yudofsky, Textbook of Traumatic Brain Injury 2005 American Psychiatric Publishing, Inc. Washington DC 27 50
15. C.L. Gibson, D. Constantin, M.J. Prior, P.M. Bath, and S.P. Murphy Progesterone suppresses the inflammatory response and nitric oxide synthase-2 expression following cerebral ischemia Exp. Neurol. 193 2005 522 530 (Pubitemid 40616199)
16. C. Guerra-Araiza, M.A. Cerbon, S. Morimoto, and I. Camacho-Arroyo Progesterone receptor isoforms expression pattern in the rat brain during the estrous cycle Life Sci. 66 2000 1743 1752 (Pubitemid 30185577)
17. C. Guerra-Araiza, A. Reyna-Neyra, A.M. Salazar, M.A. Cerbon, S. Morimoto, and I. Camacho-Arroyo Progesterone receptor isoforms expression in the prepubertal and adult male rat brain Brain Res. Bull. 54 2001 13 17 (Pubitemid 32156912)
18. C. Guerra-Araiza, O. Villamar-Cruz, A. Gonzalez-Arenas, R. Chavira, and I. Camacho-Arroyo Changes in progesterone receptor isoforms content in the rat brain during the oestrous cycle and after oestradiol and progesterone treatments J. Neuroendocrinol. 15 2003 984 990 (Pubitemid 37193016)
19. J. He, C.O. Evans, S.W. Hoffman, N.M. Oyesiku, and D.G. Stein Progesterone and allopregnanolone reduce inflammatory cytokines after traumatic brain injury Exp. Neurol. 189 2004 404 412 (Pubitemid 39221832)
20. G.D. Hilton, L.L. Bambrick, S.M. Thompson, and M.M. McCarthy Estradiol modulation of kainic acid-induced calcium elevation in neonatal hippocampal neurons Endocrinology 147 2006 1246 1255 (Pubitemid 43244357)
21. R.W. Irwin, J. Yao, R.T. Hamilton, E. Cadenas, R.D. Brinton, and J. Nilson Progesterone and estrogen regulate oxidative metabolism in brain mitochondria Endocrinology 149 2008 3167 3175 (Pubitemid 351724522)
22. J.P. Kesslak, and F.H. Gage Recovery of spatial alternation deficits following selective hippocampal destruction with kainic acid Behav. Neurosci. 100 1986 280 283 (Pubitemid 16142536)
23. C.H. Kinsley, and K.G. Lambert The maternal brain Sci. Am. 294 2006 72 79 (Pubitemid 43051575)
24. C.H. Kinsley, L. Madonia, G.W. Gifford, K. Tureski, G.R. Griffin, C. Lowry, J. Williams, J. Collins, H. McLearie, and K.G. Lambert Motherhood improves learning and memory: neural activity in rats is enhanced by pregnancy and the demands of rearing offspring Nature 402 1999 137 138
25. C.H. Kinsley, R. Trainer, G. Stafisso-Sandoz, P. Quadros, L. Keyser-Marcus, C. Hearon, N. Wightman, M.D. Morgan, F.J. Kozub, and K.G. Lambert Motherhood and pregnancy hormones modify concentrations of hippocampal neuronal dendritic spines Horm. Behav. 49 2006 131 142 (Pubitemid 43152485)
26. C.H. Kinsley, M. Bardi, K. Karelina, B. Rima, L. Christon, J. Friedenberg, and G. Griffin Motherhood induces and maintains behavioral and neural plasticity across the lifespan in the rat Arch. Sex. Behav. 37 2008 43 56
27. C.H. Kinsley, and K.G. Lambert Reproduction-induced neuroplasticity: natural behavioral and neuronal alterations associated with the production and care of offspring J. Neuroendocrinol. 20 2008 515 525 (Pubitemid 351437037)
28. M. Krajewska, Z. You, J. Rong, C. Kress, X. Huang, J. Yang, T. Kyoda, R. Leyva, S. Banares, Y. Hu, C.H. Sze, M.J. Whalen, L. Salmena, R. Hakem, B.P. Head, J.C. Reed, and S. Krajewski Neuronal deletion of caspace 8 protects against brain injury in mouse models of controlled cortical impact and kainic acid-induced excitotoxicity PLoS One 6 2011 e24341
29. K.G. Lambert, A.E. Berry, G. Griffins, E. Amory-Meyers, G.L. Madonia-Lomas, and C.H. Kinsley Pup exposure differentially enhances foraging ability in primiparous and nulliparous rats Physiol. Behav. 13 2005 799 806 (Pubitemid 40693444)
30. K.G. Lambert, and C.H. Kinsley The Neuroeconomics of Motherhood: Costs and Benefits of Maternal Investment R. Bridges, The Parental Brain 2008 Elsevier New York
31. G. Love, N. Torrey, I. McNamara, M. Morgan, M. Banks, N.W. Hester, E.R. Glasper, A.C. DeVries, C.H. Kinsley, and K.G. Lambert Maternal experience produces long-lasting behavioral modification in the rat Behav. Neuro. 119 2005 1084 1096 (Pubitemid 41377259)
32. T.K. McIntosh Neurochemical sequelae of traumatic brain injury: therapeutic implications Cerebrovasc. Brain Metab. Rev. 6 1994 109 162 (Pubitemid 2086237)
33. T. Morales Recent findings on neuroprotection against excitotoxicity in the hippocampus of female rats J. Neuroendocrinol. 23 2011 994 1001
34. J.V. Nadler, B.W. Perry, C. Gentry, and C.W. Cotman Intraventricular kainic acid preferentially destroys hippocampal pyramid cells Nature 271 1978 676 677 (Pubitemid 8278952)
35. J. Nilsen, and R.D. Brinton Impact of progestins on estrogen-induced neuroprotection: synergy by progesterone and 19-norprogesterone and antagonism by medroxyprogesterone acetate Endocrinology 143 2002 205 212 (Pubitemid 34056421)
36. J. Nilsen, and R.D. Brinton Divergent impact of progesterone and medroxyprogesterone acetate (Provera) on nuclear mitogen-activated protein kinase activity signaling Proc. Natl. Acad. Sci. U. S. A. 100 2003 10506 10511 (Pubitemid 37071908)
37. J.W. Olney, T. Fuller, and T. DeGubareff Acute dendrotoxic changes in the hippocampus of kainate treated rats Brain Res. 176 1979 91 100 (Pubitemid 9250993)
38. N. Otani, H. Nawashiro, S. Fukui, O. Hidetoshi, A. Ohsumi, T. Toyooka, K. Shima, H. Gomi, and M. Brenner Enhanced hippocampal neurodegeneration after traumatic or kainate excitotoxicity in GFAP-null mice J. Clin. Neurosci. 13 2006 934 938 (Pubitemid 44666419)
39. S. Panter, and A. Faden Biochemical changes and secondary injury from stroke and trauma R.R. Young, P.J. Delwade, Principles and Practice of Restorative Neurology 1992 Butterworths New York 32 52
40. G. Paxinos, and C. Watson The Rat Brain in Stereotaxic Coordinates Second Edition 1986 Academic Press New York
41. R.J. Racine Modification of seizure activity by electrical stimulation. II. Motor seizure Electroencephalogr. Clin. Neurophysiol. 32 1972 281 294
42. J.L. Ridet, S.K. Malhotra, A. Privat, and F.H. Gage Reactive astrocytes: cellular and molecular cues to biological function Trends Neurosci. 20 1997 570 577 (Pubitemid 27508969)
43. R.L. Roof, R. Duvdevani, and D.G. Stein Gender influences outcome of brain injury: progesterone plays a protective role Brain Res. 607 1993 333 336 (Pubitemid 23104985)
44. N. Salmaso, N. Popeski, L.A. Peronace, and B. Woodside Differential effects of reproductive and hormonal state on basic fibroblast growth factor and glial fibrillary acid protein immunoreactivity in the hypothalamus and cingulate cortex of female rats Neuroscience 134 2005 1431 1440 (Pubitemid 41207390)
45. L.C. Schmued, and K.J. Hopkins Fluoro-Jade B: a high affinity fluorescent marker for the localization of neuronal degeneration Brain Res. 874 2000 123 130
46. M. Schumacher, R. Guennoun, D.G. Stein, and A.F. De Nicola Progesterone: therapeutic opportunities for neuroprotection and myelin repair Pharmacol. Ther. 116 2007 77 106 (Pubitemid 47398920)
47. G. Sperk, H. Lassmann, H. Baran, S.J. Kish, F. Seitelberger, and O. Hornykiewicz Kainic acid induced seizures: neurochemical and histopathological changes Neuroscience 10 1983 1301 1315 (Pubitemid 14178574)
48. M. Sofroniew Reactive astrocytesin neural repair and protection Neuroscientist 11 2005 400 407 (Pubitemid 41339226)
49. D.G. Stein Progesterone exerts neuroprotective effects after brain injury Brain Res. Rev. 57 2008 387 397
50. A. Vanoye-Carlo, T. Morales, E. Ramos, A. Mendoza-Rodríguez, and M. Cerbón Neuroprotective effects of lactation against kainic acid treatment in the dorsal hippocampus of the rat Horm. Behav. 53 2008 112 123
51. R.M. Warner Applied Statistics 2007 Sage Los Angeles, CA