Hyper-excitability and epilepsy generated by chronic early-life stress

Neurobiology of Stress

Volumn 2, Issue , 2015, Pages 10-19

  Dubé, Céline M ^a   Molet, Jenny ^a   Singh Taylor, Akanksha ^a   Ivy, Autumn ^a   Maras, Pamela M ^a   Baram, Tallie Z ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Amygdala; Corticotropin releasing hormone; Epilepsy; Infantile spasms; Seizures; Stress

Indexed keywords

CORTICOTROPIN RELEASING FACTOR;

ADOLESCENT; AGE SPECIFIC SEIZURE; AMYGDALOID NUCLEUS; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CENTRAL NUCLEUS (AMYGDALA); CHRONIC STRESS; COMPLEX PARTIAL SEIZURE; CONTROLLED STUDY; DISEASE COURSE; EARLY LIFE STRESS; ELECTRODE IMPLANTATION; ELECTROENCEPHALOGRAM; EPILEPSY; FEMALE; HIPPOCAMPUS; HISTOCHEMISTRY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; INFANTILE SPASM; MALE; NERVE CELL EXCITABILITY; NONHUMAN; PARIETAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA ISOLATION; SEIZURE; SPIKE; TELEMETRY;

EID: 84925612452     PISSN: None     EISSN: 23522895     Source Type: Journal    
DOI: 10.1016/j.ynstr.2015.03.001     Document Type: Article

References (84)

1. Aldenhoff J.B., Gruol D.L., Rivier J., Vale W., Siggins G.R. Corticotropin releasing factor decreases postburst hyperpolarizations and excites hippocampal neurons. Science 1983, 221:875-877.
2. Avishai-Eliner S., Gilles E.E., Eghbal-Ahmadi Y., Bar-El Y., Baram T.Z. Altered regulation of gene and protein expression of hypothalamic-pituitary-adrenal axis components in an immature rat model of chronic stress. J.Neuroendocrinol. 2001, 13:799-807.
3. Avishai-Eliner S., Brunson K.L., Sandman C.A., Baram T.Z. Stressed-out, or in (utero)?. Trends Neurosci. 2002, 25:518-524.
4. Bale T.L., Baram T.Z., Brown A.S., Goldstein J.M., Insel T.R., McCarthy M.M., et al. Early life programming and neurodevelopmental disorders. Biol. Psychiatry 2010, 68:314-319.
5. Baram T.Z. Pathophysiology of massive infantile spasms: perspective on the putative role of the brain adrenal axis. Ann. Neurol. 1993, 33:231-236.
6. Baram T.Z. The brain, seizures and epilepsy throughout life: understanding a moving target. Epilepsy Curr. 2012, 12:7-12.
7. Baram T.Z., Hatalski C.G. Neuropeptide-mediated excitability: a key triggering mechanism for seizure generation in the developing brain. Trends Neurosci. 1998, 21:471-476.
8. Baram T.Z., Mitchell W.G., Snead O.C., Horton E.J., Saito M. Brain-adrenal axis hormones are altered in the CSF of infants with massive infantile spasms. Neurology 1992, 42:1171-1175.
9. Baram T.Z., Hirsch E., Snead O.C., Schultz L. Corticotropin-releasing hormone-induced seizures in infant rats originate in the amygdala. Ann. Neurol. 1992, 31:488-494.
10. Baram T.Z., Mitchell W.G., Tournay A., Snead O.C., Hanson R.A., Horton E.J. High-dose corticotropin (ACTH) versus prednisone for infantile spasms: a prospective, randomized, blinded study. Pediatrics 1996, 97:375-379.
11. Baram T.Z., Gerth A., Schultz L. Febrile seizures: an appropriate-aged model suitable for long-term studies. Brain Res. Dev. Brain Res. 1997, 98:265-270.
12. Baram T.Z., Davis E.P., Obenaus A., Sandman C.A., Small S.L., Solodkin A., et al. Fragmentation and unpredictability of early-life experience in mental disorders. Am. J. Psychiatry 2012, 169:907-915.
13. Ben-Ari Y., Tremblay E., Berger M., Nitecka L. Kainic acid seizure syndrome and binding sites in developing rats. Brain Res. 1984, 316:284-288.
14. Berg A.T., Langfitt J.T., Testa F.M., Levy S.R., DiMario F., Westerveld M., et al. Global cognitive function in children with epilepsy: a community-based study. Epilepsia 2008, 49:608-614.
15. Brunson K.L., Khan N., Eghbal-Ahmadi M., Baram T.Z. Corticotropin (ACTH) acts directly on amygdala neurons to down-regulate corticotropin-releasing hormone gene expression. Ann. Neurol. 2001, 49:304-312.
16. Brunson K.L., Avishai-Eliner S., Hatalski C.G., Baram T.Z. Neurobiology of the stress response early in life: evolution of a concept and the role of corticotropin releasing hormone. Mol. Psychiatry 2001, 6:647-656.
17. Brunson K.L., Kramár E., Lin B., Chen Y., Colgin L.L., Yanagihara T.K., et al. Mechanisms of late-onset cognitive decline after early-life stress. J.Neurosci. 2005, 25:9328-9338.
18. Camfield C., Camfield P., Smith B., Gordon K., Dooley J. Biologic factors as predictors of social outcome of epilepsy in intellectually normal children: a population-based study. J.Pediatr. 1993, 22:869-873.
19. Chachua T., Yum M.S., Velíšková J., Velíšek L. Validation of the rat model of cryptogenic infantile spasms. Epilepsia 2011, 52:1666-1677.
20. Chen Y., Bender R.A., Frotscher M., Baram T.Z. Novel and transient populations of corticotropin-releasing hormone-expressing neurons in developing hippocampus suggest unique functional roles: a quantitative spatiotemporal analysis. J.Neurosci. 2001, 21:7171-7181.
21. Chen Y., Fenoglio K.A., Dubé C.M., Grigoriadis D.E., Baram T.Z. Cellular and molecular mechanisms of hippocampal activation by acute stress are age-dependent. Mol. Psychiatry 2006, 11:992-1002.
22. Choy M., Dubé C.M., Patterson K., Barnes S.R., Maras P., Blood A.B., et al. Anovel, noninvasive, predictive epilepsy biomarker with clinical potential. J.Neurosci. 2014, 34:8672-8684.
23. Cormack F., Cross J.H., Isaacs E., Harkness W., Wright I., Vargha-Khadem F., et al. The development of intellectual abilities in pediatric temporal lobe epilepsy. Epilepsia 2007, 48:201-204.
24. Cortez M.A., Shen L., Wu Y., Aleem I.S., Trepanier C.H., Sadeghnia H.R., et al. Infantile spasms and Down syndrome: a new animal model. Pediatr. Res. 2009, 65:499-503.
25. Danzer S.C. Depression, stress, epilepsy and adult neurogenesis. Exp. Neurol. 2012, 233:22-32.
26. Dedeurwaerdere S., Friedman A., Fabene P.F., Mazarati A., Murashima Y.L., Vezzani A., Baram T.Z. Finding a better drug for epilepsy: antiinflammatory targets. Epilepsia 2012, 53:1113-1118.
27. Desgent S., Duss S., Sanon N.T., Lema P., Lévesque M., Hébert D., et al. Early-life stress is associated with gender-based vulnerability to epileptogenesis in rat pups. PLoS One 2012, 7:e42622.
28. Dubé C.M., Richichi C., Bender R.A., Chung G., Litt B., Baram T.Z. Temporal lobe epilepsy after experimental prolonged febrile seizures: prospective analysis. Brain 2006, 129:911-922.
29. Dubé C.M., Zhou J.L., Hamamura M., Zhao Q., Ring A., Abrahams J., et al. Cognitive dysfunction after experimental febrile seizures. Exp. Neurol. 2009, 215:167-177.
30. Dubé C.M., Ravizza T., Hamamura M., Zha Q., Keebaugh A., Fok K., et al. Epileptogenesis provoked by prolonged experimental febrile seizures: mechanisms and biomarkers. J.Neurosci. 2010, 30:7484-7494.
31. Dulac O., Milh M., Holmes G.L. Brain maturation and epilepsy. Handb. Clin. Neurol. 2013, 111:441-446.
32. Edwards H.E., Dortok D., Tam J., Won D., Burnham W.M. Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats. Horm. Behav. 2002, 42:437-447.
33. Frucht M.M., Quigg M., Schwaner C., Fountain N.B. Distribution of seizure precipitants among epilepsy syndromes. Epilepsia 2000, 41:1534-1539.
34. Gaitatzis A., Johnson A.L., Chadwick D.W., Shorvon S.D., Sander J.W. Life expectancy in people with newly diagnosed epilepsy. Brain 2004, 127:2427-2432.
35. Galvan C., Hrachovy R.A., Smith K.L., Swann J.W. Blockade of neuronal activity during hippocampal development produces a chronic focal epilepsy in the rat. J.Neurosci. 2000, 20:2904-2916.
36. Gilles E.E., Schultz L., Baram T.Z. Abnormal corticosterone regulation in an immature rat model of continuous chronic stress. Pediatr. Neurol. 1996, 15:114-119.
37. Hatalski C.G., Baram T.Z. Stress-induced transcriptional regulation in the developing rat brain involves increased cyclic adenosine 3',5'-monophosphate-regulatory element binding activity. Mol. Endocrinol. 1997, 11:2016-2024.
38. Hatalski C.G., Guirguis C., Baram T.Z. Corticotropin releasing factor mRNA expression in the hypothalamic paraventricular nucleus and the central nucleus of the amygdala is modulated by repeated acute stress in the immature rat. J.Neuroendocrinol. 1998, 10:663-669.
39. Haut S.R., Hall C.B., Masur J., Lipton R.B. Seizure occurrence: precipitants and prediction. Neurology 2007, 69:1905-1910.
40. Heaney D.C., MacDonald B.K., Everitt A., Stevenson S., Leonardi G.S., Wilkinson P., et al. Socioeconomic variation in incidence of epilepsy: prospective community based study in south east England. BMJ 2002, 325:1013-1016.
41. Hesdorffer D.C., Tian H., Anand K., Hauser W.A., Ludvigsson P., Olafsson E., et al. Socioeconomic status is a risk factor for epilepsy in Icelandic adults but not in children. Epilepsia 2005, 46:1297-1303.
42. Hollrigel G.S., Chen K., Baram T.Z., Soltesz I. The pro-convulsant actions of corticotropin-releasing hormone in the hippocampus of infant rats. Neuroscience 1998, 84:71-79.
43. Holmes G.L., Ben-Ari Y. Seizures in the developing brain: perhaps not so benign after all. Neuron 1998, 21:1231-1234.
44. Holmes G.L., Khazipov R., Ben-Ari Y. Seizure-induced damage in the developing human: relevance of experimental models. Prog. Brain Res. 2002, 135:321-334.
45. Hrachovy R.A., Frost J.D., Kellaway P., Zion T.E. Double-blind study of ACTH vs prednisone therapy in infantile spasms. J.Pediatr. 1983, 103:641-645.
46. Huang L.T. Early-life stress impacts the developing hippocampus and primes seizure occurrence: cellular, molecular, and epigenetic mechanisms. Front. Mol. Neurosci. 2014, 7:8.
47. Ivy A.S., Brunson K.L., Sandman C., Baram T.Z. Dysfunctional nurturing behavior in rat dams with limited access to nesting material: a clinically relevant model for early-life stress. Neuroscience 2008, 154:1132-1142.
48. Ivy A.S., Rex C.S., Chen Y., Dubé C., Maras P.M., Grigoriadis D.E., et al. Hippocampal dysfunction and cognitive impairments provoked by chronic early-life stress involve excessive activation of CRH receptors. J.Neurosci. 2010, 30:13005-13015.
49. Joëls M. Stress, the hippocampus, and epilepsy. Epilepsia 2009, 50:586-597.
50. Joëls M., Baram T.Z. The neuro-symphony of stress. Nat. Rev. Neurosci. 2009, 10:459-466.
51. Kumar G., Jones N.C., Morris M.J., Rees S., O'Brien T.J., Salzberg M.R. Early life stress enhancement of limbic epileptogenesis in adult rats: mechanistic insights. PLoS One 2011, 6:e24033.
52. Lee C.L., Frost J.D., Swann J.W., Hrachovy R.A. Anew animal model of infantile spasms with unprovoked persistent seizures. Epilepsia 2008, 49:298-307.
53. Li J., Vestergaard M., Obel C., Precht D.H., Christensen J., Lu M., et al. Prenatal stress and epilepsy in later life: a nationwide follow-up study in Denmark. Epilepsy Res. 2008, 81:52-57.
54. Lynch M., Sayin U., Bownds J., Janumpalli S., Sutula T. Long-term consequences of early postnatal seizures on hippocampal learning and plasticity. Eur. J. Neurosci. 2000, 12:2252-2264.
55. Mackay M.T., Weiss S.K., Adams-Webber T., Ashwal S., Stephens D., Ballaban-Gill K., et al. Practice parameter: medical treatment of infantile spasms: report of the American Academy of Neurology and the Child Neurology society. Neurology 2004, 62:1668-1681.
56. Mares P., Velísek L. N-methyl-D-aspartate (NMDA)-induced seizures in developing rats. Brain Res. Dev. Brain Res. 1992, 65:185-189.
57. Marsh E., Fulp C., Gomez E., Nasrallah I., Minarcik J., Sudi J., et al. Targeted loss of Arx results in a developmental epilepsy mouse model and recapitulates the human phenotype in heterozygous females. Brain 2009, 132:1563-1576.
58. McEwen B.S. Physiology and neurobiology of stress and adaptation: central role of the brain. Physiol. Rev. 2007, 87:873-904.
59. Molet J., Maras P.M., Ivy A.S., Baram T.Z. Mechanisms of Enduring Cognitive/Memory Vulnerability Provoked by Chronic Early-life Stress 2013, Society for Neuroscience conference abstract.
60. Molet J., Maras P.M., Avishai-Eliner S., Baram T.Z. Naturalistic rodent models of chronic early-life stress. Dev. Psychobiol. 2014, 56:1675-1688.
61. Nairismägi J., Gröhn O.H., Kettunen M.I., Nissinen J., Kauppinen R.A., Pitkänen A. Progression of brain damage after status epilepticus and its association with epileptogenesis: a quantitative MRI study in a rat model of temporal lobe epilepsy. Epilepsia 2004, 45:1024-1034.
62. Nakken K.O., Solaas M.H., Kjeldsen M.J., Friis M.L., Pellock J.M., Corey L.A. Which seizure-precipitating factors do patients with epilepsy most frequently report?. Epilepsy Behav. 2005, 6:85-89.
63. Neugebauer R., Paik M., Hauser W.A., Nadel E., Leppik I., Susser M. Stressful life events and seizure frequency in patients with epilepsy. Epilepsia 1994, 35:336-343.
64. Nordli D.R. Infantile seizures and epilepsy syndromes. Epilepsia 2002, 43:11-16.
65. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 1998, Academic Press, San Diego. fourth ed.
66. Price M.G., Yoo J.W., Burgess D.L., Deng F., Hrachovy R.A., Frost J.D., et al. Atriplet repeat expansion genetic mouse model of infantile spasms syndrome, Arx(GCG)10+7, with interneuronopathy, spasms in infancy, persistent seizures, and adult cognitive and behavioral impairment. J.Neurosci. 2009, 29:8752-8763.
67. Racine R.J. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr. Neurophysiol. Clin. 1972, 32:281-294.
68. Roozendaal B., Brunson K.L., Holloway B.L., McGaugh J.L., Baram T.Z. Involvement of stress-released corticotropin-releasing hormone in the basolateral amygdala in regulating memory consolidation. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:13908-13913.
69. Sadaghiani M.M., Saboory E. Prenatal stress potentiates pilocarpine-induced epileptic behaviors in infant rats both time and sex dependently. Epilepsy Behav. 2010, 18:166-170.
70. Salzberg M., Kumar G., Supit L., Jones N.C., Morris M.J., Rees S., et al. Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia 2007, 48:2079-2085.
71. Scantlebury M.H., Galanopoulou A.S., Chudomelova L., Raffo E., Betancourth D., Moshé S.L. Amodel of symptomatic infantile spasms syndrome. Neurobiol. Dis. 2010, 37:604-612.
72. Schridde U., Strauss U., Brauer A.U., van Luijtelaar G. Environmental manipulations early in development alter seizure activity, Ih and HCN1 protein expression later in life. Eur. J. Neurosci. 2006, 23:3346-3358.
73. Shamansky S.L., Glaser G.H. Socioeconomic characteristics of childhood seizure disorders in the New Haven area: an epidemiologic study. Epilepsia 1979, 20:457-474.
74. Snead O.C. How does ACTH work against infantile spasms? Bedside to bench. Ann. Neurol. 2001, 49:288-289.
75. Snead O.C., Benton J.W., Hosey L.C., Swann J.W., Spink D., Martin D., et al. Treatment of infantile spasms with high-dose ACTH: efficacy and plasma levels of ACTH and cortisol. Neurology 1989, 39:1027-1031.
76. Spector S., Cull C., Goldstein L.H. Seizure precipitants and perceived self-control of seizures in adults with poorly-controlled epilepsy. Epilepsy Res. 2000, 38:207-216.
77. Stafstrom C.E., Holmes G.L. Infantile spasms: criteria for an animal model. Int. Rev. Neurobiol. 2002, 49:391-411.
78. Stafstrom C.E., Arnason B.G., Baram T.Z., Catania A., Cortez M.A., Glauser T.A., et al. Treatment of infantile spasms: emerging insights from clinical and basic science perspectives. J.Child Neurol. 2011, 26:1411-1421.
79. Staley K.J., White A., Dudek F.E. Interictal spikes: harbingers or causes of epilepsy?. Neurosci. Lett. 2011, 497:247-250.
80. Tekgul H., Polat M., Tosun A., Serdaroglu G., Kutukculer N., Gokben S. Cerebrospinal fluid interleukin-6 levels in patients with West syndrome. Brain Dev. 2006, 28:19-23.
81. Temkin N.R., Davis G.R. Stress as a risk factor for seizures among adults with epilepsy. Epilepsia 1984, 25:450-456.
82. van Campen J.S., Jansen F.E., Steinbusch L.C., Joëls M., Braun K.P. Stress sensitivity of childhood epilepsy is related to experienced negative life events. Epilepsia 2012, 53:1554-1562.
83. Velísek L., Jehle K., Asche S., Velísková J. Model of infantile spasms induced by N-methyl-D-aspartic acid in prenatally impaired brain. Ann. Neurol. 2007, 61:109-119.
84. Wang W., Dow K.E., Fraser D.D. Elevated corticotropin releasing hormone/corticotropin releasing hormone-R1 expression in postmortem brain obtained from children with generalized epilepsy. Ann. Neurol. 2001, 50:404-409.