Stress during first pregnancy increases seizure threshold in adult male offspring

Document Type: Original Article

Authors

1 Azad Islamic University-Damghan Branch, Damghan, Iran

2 School of Biology, Damghan University, Damghan, Iran 3 Institute of Biological Sciences, Damghan University, Damghan, Iran

Abstract

 




Objective(s):
Stress induces many homeostatic aberrations which are followed by lifelong allostatic responses. Epilepsy is developed or influenced by different environmental factors, i.e. prenatal stress which makes many contradictory developmental changes in seizure threshold and intensity. We investigated the potential seizure response of the rat offspring to prenatal stress; the stress which was applied to their mothers.
 
Materials and Methods:
 
Nine day heterogeneous sequential stress (HSS) model was used before and during the first and before the second pregnancy. The kindling was induced using 13 IP injections of pentylenetetrazol (PTZ) every 48 hr to adult male Wistar rat's offspring.
 
Results:
The results of the present study demonstrated that, before pregnancy stress decreased the rate of kindling (P<0.05) in the offspring, while stress which was applied during pregnancy completely prevented kindling (P <0.001). Further, their convulsive latency was increased and tonic clonic seizure duration was decreased. In contrast, previous pregnancy and between pregnancies stress could not change kindling process. Although maternal separation stress did not change kindling development, it could increase convulsive intensities by elongating the duration of seizures (P<0.05) and reducing convulsion latency (P
<0.05).
 
Conclusion:
It is concluded that stress detrimental effects could be prevented by stress which was applied around first pregnancy; however this beneficial effect is weakened by before second pregnancy stress.

Keywords


1. Blumcke I, Beck H, Lie AA, Wiestler OD. Molecular neuropathology of human mesial temporal lobe epilepsy. Epilepsy Res 1999; 36:205-223.

2. Pitkanen A, Lukasiuk K. Molecular and cellular basis of epileptogenesis in symptomatic epilepsy. Epilepsy Behav 2009; 14:16-25.

3. Goddard GV. Development of epileptic seizures through brain stimulation at low intensity. Nature 1967; 214:1020-1021.

4. Salmani ME, Fathollahi Y, Mirnajafizadeh J, Semnanian S. Epileptogenic insult alters endogenous adenosine control on long-term changes in synaptic strength by theta pattern stimulation in hippocampus area CA1. Synapse 2011; 65:189-197.

5. Corda MG, Giorgi O, Longoni B, Orlandi M, Biggio G. Decrease in the function of the gamma-aminobutyric acid-coupled chloride channel produced by the repeated administration of pentylenetetrazol to rats. J Neurochem 1990; 55:1216-1221.

6. Sgado P, Dunleavy M, Genovesi S, Provenzano G, Bozzi Y. The role of GABAergic system in neurodevelopmental disorders: a focus on autism and epilepsy. Int J Physiol Pathophysiol Pharmacol 2011; 3:223-235.

7. Gatto CL, Broadie K. Genetic controls balancing excitatory and inhibitory synaptogenesis in neurodevelopmental disorder models. Front Synaptic Neurosci 2010; 2:4.

8. Joels M, Baram TZ. The neuro-symphony of stress. Nat Rev Neurosci 2009; 10:459-466.

9. Weinstock M. The potential influence of maternal stress hormones on development and mental health of the offspring. Brain Behav Immun 2005; 19:296-308.

10. Edwards HE, Dortok D, Tam J, Won D, Burnham WM. Prenatal stress alters seizure thresholds and the development of kindled seizures in infant and adult rats. Horm Behav 2002; 42:437-447.

11. Takahashi LK, Turner JG, Kalin NH. Prolonged stress-induced elevation in plasma corticosterone during pregnancy in the rat: implications for prenatal stress studies. Psychoneuroendocrinology 1998; 23:571-581.

12. Mastorakos G, Ilias I. Maternal and fetal hypothalamic-pituitary-adrenal axes during pregnancy and postpartum. Ann N Y Acad Sci 2003; 997:136-149.

13. Henry C, Kabbaj M, Simon H, Le Moal M, Maccari S. Prenatal stress increases the hypothalamo-pituitary-adrenal axis response in young and adult rats. J Neuroendocrinol 1994 ; 6:341-345.

14. Maccari S, Morley-Fletcher S. Effects of prenatal restraint stress on the hypothalamus-pituitary-adrenal axis and related behavioural and neurobiological alterations. Psychoneuroendocrino-

logy 2007; 32:S10-5.

15. Bock J, Murmu MS, Biala Y, Weinstock M, Braun K. Prenatal stress and neonatal handling induce sex-specific changes in dendritic complexity and dendritic spine density in hippocampal subregions of prepubertal rats. Neuroscience 2011; 193:34-43.

16. Li J, Vestergaard M, Obel C, Precht DH, 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.

17. Li J, Olsen J, Obel C, Christensen J, Precht DH, Vestergaard M. Prenatal stress and risk of febrile seizures in children: a nationwide longitudinal study in Denmark. J Autism Dev Disord 2009; 39:1047-1052.

18. Seckl JR, Holmes MC. Mechanisms of disease: glucocorticoids, their placental metabolism and fetal 'programming' of adult pathophysiology. Nat Clin Pract Endocrinol Metab 2007; 3:479-488.

19. Van den Bergh BR, Mulder EJ, Mennes M, Glover V. Antenatal maternal anxiety and stress and the neurobehavioural development of the fetus and child: links and possible mechanisms. A review. Neurosci Biobehav Rev 2005; 29:237-258.

20. Lemaire V, Koehl M, Le Moal M, Abrous DN. Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc Natl Acad Sci U S A 2000; 97:11032-11037.

21. Green MK, Rani CS, Joshi A, Soto-Pina AE, Martinez PA, Frazer A,

et al. Prenatal stress induces Prenatal stress increases seizure susceptibility Pajand et al

Iran J Basic Med Sci, Vol. 17, No. 1, 2014 40

long term stress vulnerability, compromising stress response systems in the brain and impairing extinction of conditioned fear after adult stress. Neuroscience 2011; 192:438-451.

22. Espinosa-Oliva AM, de Pablos RM, Villaran RF, Arguelles S, Venero JL, Machado A,

et al. Stress is critical for LPS-induced activation of microglia and damage in the rat hippocampus. Neurobiol Aging 2011; 32:85-102.

23. Racine R, Okujava V, Chipashvili S. Modification of seizure activity by electrical stimulation. 3. Mechanisms. Electroencephalogr Clin Neurophysiol 1972; 32:295-299.

24. Salmani ME, Mirnajafizadeh J, Fathollahi Y. Offsetting of aberrations associated with seizure proneness in rat hippocampus area CA1 by theta pulse stimulation-induced activity pattern. Neuroscience 2007; 149:518-526.

25. Santos JG Jr, Do Monte FH, Russi M, Agustine PE, Lanziotti VM. Proconvulsant effects of high doses of venlafaxine in pentylenetetrazole-convulsive rats. Braz J Med Biol Res 2002 ; 35:469-472.

26. Hashemi P, Ebrahimi L, Saboory E, Roshan-Milani S. Effect of restraint stress during gestation on pentylenetetrazol induced epileptic behaviors in rat offspring. Iran J Basic Med Sci 2013; 16:979-984.

27. Harai T, Inoue R, Fujita Y, Tanaka A, Horio M, Hashimoto K,

et al. Decreased susceptibility to seizures induced by pentylenetetrazole in serine racemase knockout mice. Epilepsy Res 2012; 102:180-187.

28. Rakhade SN, Fitzgerald EF, Klein PM, Zhou C, Sun H, Huganir RL,

et al. Glutamate receptor 1 phosphorylation at serine 831 and 845 modulates seizure susceptibility and hippocampal hyperexcitability after early life seizures. J Neurosci 2012; 32:17800-17812.

29. Krugers HJ, Lucassen PJ, Karst H, Joels M. Chronic stress effects on hippocampal structure and synaptic function: relevance for depression and normalization by anti-glucocorticoid treatment. Front Synaptic Neurosci 2010; 2:24.

30. Reddy DS, Rogawski MA. Stress-induced deoxycorticosterone-derived neurosteroids modulate GABA(A) receptor function and seizure susceptibility. J Neurosci 2002; 22:3795-3805.

31. Reddy DS. Physiological role of adrenal deoxycorticosterone-derived neuroactive steroids in stress-sensitive conditions. Neuroscience 2006; 138:911-920.

32. Salzberg M, Kumar G, Supit L, Jones NC, Morris MJ, Rees S,

et al. Early postnatal stress confers enduring vulnerability to limbic epileptogenesis. Epilepsia 2007; 48:2079-2085.

33. Brunton PJ, Russell JA. The expectant brain: adapting for motherhood. Nat Rev Neurosci 2008; 9:11-25.

34. Besedovsky HO, del Rey A, Klusman I, Furukawa H, Monge Arditi G, Kabiersch A. Cytokines as modulators of the hypothalamus-pituitary-adrenal axis. J Steroid Biochem Mol Biol 1991; 40:613-618.

35. Kohman RA, Tarr AJ, Day CE, McLinden KA, Boehm GW. Influence of prenatal stress on behavioral, endocrine, and cytokine responses to adulthood bacterial endotoxin exposure. Behav Brain Res 2008; 193:257-268.

36. Brunton PJ, Russell JA. Attenuated hypothalamo-pituitary-adrenal axis responses to immune challenge during pregnancy: the neurosteroid opioid connection. J Physiol 2008; 586:369-375.

37.Liang LP, Waldbaum S, Rowley S, Huang TT, Day BJ, Patel M. Mitochondrial oxidative stress and epilepsy in SOD2 deficient mice: Attenuation by a lipophilic metalloporphyrin. Neurobiol Dis 2012; 45:1068-1076.

38. Waldbaum S, Patel M. Mitochondria, oxidative stress, and temporal lobe epilepsy. Epilepsy Res 2010; 88:23-45.

39. Koehl M, Lemaire V, Le Moal M, Abrous DN. Age-dependent effect of prenatal stress on hippocampal cell proliferation in female rats. Eur J Neurosci 2009; 29:635-640.

40. Meijer A. Child psychiatric sequelae of maternal war stress. Acta Psychiatr Scand 1985 ; 72:505-511.