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Sport Sciences for Health

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24.07.2018 | Original Article

Positive effect of moderate-intensity aerobic activity on pentylenetetrazol-induced epileptic behaviors in pregnant mice and cognitive performance in adult male offspring

verfasst von: Ayoob Sabaghi, Ali Heyrani, Amir Kiani, Namdar Yousofvand

Erschienen in: Sport Sciences for Health | Ausgabe 1/2019

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Abstract

Purpose

Epilepsy is one of the common neurological disorders. It has been reported that physical activity can be a complementary therapy to treat seizures. Therefore, the present study was designed to investigate the effect of aerobic training on pentylenetetrazol (PTZ)-induced seizure in pregnant mice.

Methods

The kindled female mice were divided into eight groups including (1) pregnant mice (PC) treated with PTZ without physical training (PT), (2) PC treated with PTZ with aerobic training (AT), (3) PC treated with normal saline (NS), (4) PC without any injection in pregnancy, (5) non-PC treated with PTZ without PT, (6) non-PC treated with PTZ with AT, (7) non-PC treated with NS and (8) non-PC without any injection. The seizure activity was measured for half an hour after PTZ injection and anxiety activity was assessed 2 h after PTZ injection. Also, at postnatal day 94, cognitive performance at male offspring of the groups was evaluated.

Results

The results showed that aerobic training reduced seizure severity and restored seizure-induced anxiety in pregnant and non-pregnant mice to control levels. It was also observed that aerobic activity during pregnancy would restore the cognitive function of the offspring in pregnant mice treated with PTZ to the male offspring’s level in control group.

Conclusion

Generally, the results of this study showed that moderate-intensity AT is an appropriate treatment strategy for reducing the severity of seizure, seizure-induced anxiety and also prevents cognitive impairment due to seizure induction during pregnancy in the male offspring.

Fisher RS, Acevedo C, Arzimanoglou A, Bogacz A, Cross JH, Elger CE et al (2014) ILAE official report: a practical clinical definition of epilepsy. Epilepsia 55(4):475–482PubMed

Ablah E, Hesdorfferr DC, Liuc Y et al (2014) Prevalence of epilepsy in rural Kansas. Epilepsy Res 108(4):792–801PubMed

Cossa AC, Lima DC, do Vale TG, de Alencar Rocha AK, da Graça Naffah-Mazzacoratti M, da Silva Fernandes MJ et al (2016) Maternal seizures can affect the brain developing of offspring. Metab Brain Dis 31:891PubMed

Pourmotabbed A, Nedaei SE, Cheraghi M, Moradian S, Touhidi A, Aeinfar M, Seyfi Z, Pourmotabbed T (2011) Effect of prenatal pentylenetetrazol-induced kindling on learning and memory of male offspring. Neuroscience 172:205–211PubMed

Leal-Campanario R, Alarcon-Martinez L, Rieiro H, Martinez-Conde S, Alarcon-Martinez T, Zhao X et al (2017) Abnormal capillary vasodynamics contribute to ictal neurodegeneration in epilepsy. Sci Rep 7:43276PubMedPubMedCentral

Li Y, Gonzalez P, Zhang L (2012) Fetal stress and programming of hypoxic/ischemic-sensitive phenotype in the neonatal brain: mechanisms and possible interventions. Prog Neurobiol 98(2):145–165PubMedPubMedCentral

Beltramini GC, Cendes F, Yasuda CL (2015) The effects of antiepileptic drugs on cognitive functional magnetic resonance imaging. Quant Imaging Med Surg 5(2):238–246PubMedPubMedCentral

Mattson RH, Gidal BE (2004) Fractures, epilepsy, and antiepileptic drugs. Epilepsy Behav 5(Suppl 2):S36–S40 (review) PubMed

Meador K, Reynolds MW, Crean S, Fahrbach K, Probst C (2008) Pregnancy outcomes in women with epilepsy: a systematic review and meta-analysis of published pregnancy registries and cohorts. Epilepsy 81(1):1–13

10.

Tomson T, Battino D, Bonizzoni E, Craig J, Lindhout D, Sabers A et al (2011) EURAP study group. Dose-dependent risk of malformations with antiepileptic drugs: an analysis of data from the EURAP epilepsy and pregnancy registry. Lancet Neurol 10:609–617PubMed

11.

Bromley R, Weston J, Adab N, Greenhalgh J, Sanniti A, McKay AJ et al (2014) Treatment for epilepsy in pregnancy: neurodevelopmental outcomes in the child. Cochrane Database Syst Rev 30(10):CD010236

12.

Nakken KO, Loyning A, Loyning T, Gløersen G, Larsson PG (1997) Does physical exercise influence the occurrence of epileptiform EEG discharges in children? Epilepsia 38:279–284PubMed

13.

McAuley JW, Long L, Heise J, Kirby T, Buckworth J, Pitt C, Lehman KJ, Moore JL, Reeves AL (2001) A prospective evaluation of the effects of a 12-week outpatient exercise program on clinical and behavioral outcomes in patients with epilepsy. Epilepsy Behav 2:592–600PubMed

14.

Arida RM, de Jesus VA, Cavalheiro EA (1998) Effect of physical exercise on kindling development. Epilepsy Res 30:127–132PubMed

15.

Arida RM, Scorza FA, dos Santos NF, Peres CA, Cavalheiro EA (1999) Effect of physical exercise on seizure occurrence in a model of temporal lobe epilepsy in rats. Epilepsy Res 37:45–52PubMed

16.

Arida RM, Sanabria ER, Silva AC, Faria LC, Scorza FA, Cavalheiro EA (2004) Physical training reverts hippocampal electrophysiological changes in rats submitted to the pilocarpine model of epilepsy. Physiol Behav 83:165–171PubMed

17.

Arida RM, Scorza CA, Scorza FA, Cavalheiro M EA (2007) Gomes da Silva S, da Grac¸a Naffah-azzacoratti. Effects of different types of physical exercise on the staining of parvalbumin-positive neurons in the hippocampal formation of rats with epilepsy. Prog Neuropsychopharmacol Biol Psychiatry 31:814–822PubMed

18.

Zhang B, Zhang JW, Wang WP, Dong RF, Tian S, Zhang C (2017) Effect of lamotrigine on epilepsy-induced cognitive impairment and hippocampal neuronal apoptosis in pentylenetetrazole-kindled animal model. Synapse 71:e21945

19.

Rajabzadeh A, Bideskan AE, Fazel A, Sankian M, Rafatpanah H, Haghir H (2012) The effect of PTZ-induced epileptic seizures on hippocampal expression of PSA-NCAM in offspring born to kindled rats. J BiomedSci 31 19:56

20.

Becker A, Grecksch G, Ruthrich HL, Pohle W, Marx B, Matthies H (1992) Kindling and its consequences on learning in rats. BehavNeuralBiol 57:37–43

21.

Zybura-Broda K, Amborska R, AmbrozekLatecka M, Wilemska J, Bogusz A, Bucko J et al (2016) Epigenetics of epileptogenesis-evoked upregulation of matrix metalloproteinase-9 in hippocampus. PLoS ONE 11(8):e0159745PubMedPubMedCentral

22.

Gomes FG, Gomes Da Silva S, Cavalheiro EA, Arida RM (2014) Beneficial influence of physical exercise following status epilepticus in the immature brain of rats. Neuroscience 22:274:69–81

23.

Salari AA, Fatehi-Gharehlar L, Motayagheni N, Homberg JR (2016) Fluoxetine normalizes the effects of prenatal maternal stress on depression- and anxiety-like behaviors in mouse dams and male offspring. Behav Brain Res 311:354–367

24.

Gomes da Silva S, de Almeida AA, Fernandes J, Lopim GM, Cabral FR, Scerni DA, et al (2016) Maternal exercise during pregnancy increases BDNF levels and cell numbers in the hippocampal formation but not in the cerebral cortex of adult rat offspring. PLoSOne 15:e0147200

25.

Wang N, Liu Y, Ma Y, Wen D (2017) High-intensity interval versus moderate-intensity continuous training: superior metabolic benefits in diet-induced obesity mice. Life Sci 191:122–131PubMed

26.

Henriques I, Lopes-Pacheco M, Padilha GA, Marques PS, Magalhães RF, Antunes MA et al (2016) Moderate aerobic training improves cardiorespiratory parameters in elastase-induced emphysema. Front Physiol 7:329PubMedPubMedCentral

27.

Sharma RK, Singh T, Mishra A, Goel RK (2017) Relative safety of different antidepressants for treatment of depression in chronic epileptic animals associated with depression. J Epilepsy Res 7(1):25–32PubMedPubMedCentral

28.

Kameda SR, Fukushiro DF, Trombin TF, Procópio-Souza R, Patti CL, Hollais AW et al (2011) Adolescent mice are more vulnerable than adults to single injection-induced behavioral sensitization to amphetamine. Pharmacol Biochem Behav 98(2):320–324PubMed

29.

Ngoupaye GT, Yassi FB, Bahane DAN, Bum EN (2017) Combined corticosterone treatment and chronic restraint stress lead to depression associated with early cognitive deficits in mice. Metab Brain Dis 33(2):421–431PubMed

30.

Rabbani M, Hajhashemi V, Mesripour A (2009) Increase in brain corticosterone concentration and recognition memory impairment following morphine withdrawal in mice. Stress 12(5):451–456PubMed

31.

Campos DV, Lopim GM, de Almeida VS, Amado D, Arida RM (2016) Effects of different physical exercise programs on susceptibility to pilocarpine-induced seizures in female rats. Epilepsy Behav 64:262–267

32.

Chen JX, Zhao X, Yue GX, Wang ZF (2007) Influence of acute and chronic treadmill exercise on rat plasma lactate and brain NPY, L-ENK, DYN A1–13. Cell Mol Neurobiol 27:1–10PubMed

33.

Gall C, Lauterborn J, Bundman M, Murray K, Isackson P (1991) Seizures and the regulation of neurotrophic factor and neuropeptide gene expression in brain. Epilepsy Res Suppl 4:225–245PubMed

34.

Chaouloff F (1989) Physical exercise and brain monoamines: a review. Acta Physiol Scand 137:1–13PubMed

35.

Westerberg V, Lewis J, Corcoran ME (1984) Depletion of noradrenaline fails to affect kindling seizures. Exp Neurol 84:237–240PubMed

36.

Arida RM, Cavalheiro EA, Silva AC, Scorza FA (2008) Physical activity and epilepsy: proven and predicted benefits. Sports Med 38:607–615PubMed

37.

Sloviter RS, Sollas AL, Barbaro NM, Laxer KD (1991) Calcium-binding protein (calbindin-D28K) and parvalbumin immunocytochemistry in the normal and epileptic human hippocampus. J Comp Neurol 308:381–396PubMed

38.

Henry JF, Sherwin BB (2012) Hormones and cognitive functioning during late pregnancy and postpartum: a longitudinal study. Behav Neurosci 126(1):73–85PubMed

39.

Tauboll E, Sveberg L, Svalheim S (2015) Interactions between hormones and epilepsy. Seizure 28:3–11PubMed

40.

Moezi L, Hassanipour M, Zaeri M, Ghorbani H, Shafaroodi H (2015) The influence of ovariectomy on anti-convulsant effect of pioglitazone in mice. Pathophysiology 3:159–163

41.

Battino D, Tomson T, Bonizzoni E, Craig J, Lindhout D, Sabers A et al (2013) Seizure control and treatment changes in pregnancy: observations from the EURAP epilepsy pregnancy registry. Epilepsia 54:1621–1627PubMed

42.

Reisinger T, Newman M, Loring D, Pennell P, Meador K (2013) Antiepileptic drug clearance and seizure frequency during pregnancy in women with epilepsy. Epilepsy Behav 29:13–18PubMedPubMedCentral

43.

Kwon O-Y, Park S-P (2014) Depression and anxiety in people with epilepsy. J Clin Neurol 10(3):175–188PubMedPubMedCentral

44.

Mohler H (2006) GABAA receptors in central nervous system disease: anxiety, epilepsy, and insomnia. J Recept Signal Transduct Res 26:731–740PubMed

45.

Ekonomou A, Smith AL, Angelatou F (2001) Changes in AMPA receptor binding and subunit messenger RNA expression in hippocampus and cortex in the pentylenetetrazole-induced ‘kindling’ model of epilepsy. Brain Res Mol Brain Res 95(1–2):27–35PubMed

46.

Tran L, Lasher B, Young K, Keele N (2013) Depletion of serotonin in the basolateral amygdala elevates glutamate receptors and facilitates fear-potentiated startle. Transl Psychiatry 3(9):e298PubMedPubMedCentral

47.

Frantz AL, Regner GG, Pflüger P, Coelho VR, da Silva LL, Viau CM et al (2017) Manual acupuncture improves parameters associated with oxidative stress and inflammation in PTZ-induced kindling in mice. Neurosci Lett 20:661:33–40

48.

Salim S (2014) Oxidative stress and psychological disorders. Curr Neuropharmacol 12(2):140–147PubMedPubMedCentral

49.

Dao AT, Zagaar MA, Salim S, Eriksen JL, Alkadhi KA (2014) Regular exercise prevents non-cognitive disturbances in a rat model of Alzheimer’s disease. Int J Neuropsychoph 17:593–602

50.

Lalanza JF, Sanchez-Roige S, Gagliano H, Fuentes S, Bayod S, Camins A et al (2012) Physiological and behavioural consequences of long-term moderate treadmill exercise. Psychoneuroendocrinology 37:1745–1754PubMed

51.

Anderson E, Shivakumar G (2013) Effects of exercise and physical activity on anxiety. Front Psychiatry 4:27PubMedPubMedCentral

52.

Ghodrati-Jaldbakhan S, Ahmadalipour A, Rashidy-Pour A, Vafaei AA, Miladi-Gorji H, Alizadeh M (2017) Low- and high-intensity treadmill exercise attenuates chronic morphine-induced anxiogenesis and memory impairment but not reductions in hippocampal BDNF in female rats. Brain Res 15:20–28

53.

Munehiro T, Kitaoka K, Ueda Y, Maruhashi Y, Tsuchiya H (2012) Establishment of an animal model for delayed-onset muscle soreness after high-intensity eccentric exercise and its application for investigating the efficacy of low-load eccentric training. J Orthop Sci 17(3):244–252PubMed

54.

Vieira JM, Carvalho FB, Gutierres JM, Soares MS, Oliveira PS, Rubin MA, Morsch et al (2017) Caffeine prevents high-intensity exercise-induced increase in enzymatic antioxidant and Na⁺–K⁺–ATPase activities and reduction of anxiolytic like-behaviour in rats. Redox Rep 22(6):493–500PubMedPubMedCentral

55.

Rosa EF, Takahashi S, Aboulafia J, Nouailhetas VL, Oliveira MG (2007) Oxidative stress induced by intense and exhaustive exercise impairs murine cognitive function. J Neurophysiol 98(3):1820–1826PubMed

56.

Pal S, Chaki B, Chattopadhyay S, Bandyopadhyay A (2018) High-intensity exercise induced oxidative stress and skeletal muscle damage in postpubertal boys and girls: a comparative study. J Strength Cond Res 32(4):1045–1052PubMed

57.

Ho Y-H, Lin Y-T, Wu C-WJ, Chao Y-M, Chang AYW, Chan JY H (2015) Peripheral inflammation increases seizure susceptibility via the induction of neuroinflammation and oxidative stress in the hippocampus. J Biomed Sci 22(1):46PubMedPubMedCentral

58.

Ashrafi MR, Shams S, Nouri M, Mohseni M, Shabanian R, Yekaninejad MS et al (2007) A probable causative factor for an old problem: selenium and glutathione peroxidase appear to play important roles in epilepsy pathogenesis. Epilepsia 48:1750–1755PubMed

59.

Arida RM, Scorza FA, Terra VC, Scorza CA, de Almeida AC, Cavalheiro EA (2009) Physical exercise in epilepsy: what kind of stressor is it? Epilepsy Behav 16:381–387PubMed

60.

Brown DA, Johnson MS, Armstrong CJ, Lynch JM, Caruso NM, Ehlers LB, et al (2007) Short-term treadmill running in the rat: what kind of stressor is it? J Appl Physiol 103(6):1979–1985PubMed

61.

Tolmacheva EA, Oitzl MS, van Luijtelaar G (2012) Stress, glucocorticoids and absences in a genetic epilepsy model. Horm Behav 61:706–710PubMed

62.

Sachs BD, Ni JR, Caron MG (2014) Sex differences in response to chronic mild stress and congenital serotonin deficiency. Sychoneuroendocrinology 40:123–129

63.

Hodes GE, Kana V, Menard C, Merad M, Russo SJ (2015) Neuroimmune mechanisms of depression. Nat Neurosci 18:1386–1393PubMedPubMedCentral

64.

Russo SJ, Nestler EJ (2013) The brain reward circuitry in mood disorders. Nat Rev Neurosci 14:609–625PubMed

65.

Brancato A, Bregman D, Ahn HF, Pfau ML, Menard C, Cannizzaro C et al (2017) Sub-chronic variable stress induces sex-specific effects on glutamatergic synapses in the nucleus accumbens. Neuroscience 14(350):180–189

66.

Neumann ID, Johnstone HA, Hatzinger M, Liebsch G, Shipston M, Russell JA et al (1998) Attenuated neuroendocrine responses to emotional and physical stressors in pregnant rats involve adenohypophysial changes. J Physiol 508(Pt 1):289–300PubMedPubMedCentral

67.

Boersma GJ, Lee RS, Cordner ZA, Ewald ER, Purcell RH, Moghadam AA, Tamashiro KL (2014) Prenatal stress decreases Bdnf expression and increases methylation of Bdnf exon IV in rats. Epigenetics 9(3):437–447PubMed

68.

Akhavan MM, Emami-Abarghoie M, Safari M, Sadighi-Moghaddam B, Vafaei AA, Bandegi AR, Rashidy-Pour A (2008) Serotonergic and noradrenergic lesions suppress the enhancing effect of maternal exercise during pregnancy on learning and memory in rat pups. Neuroscience 151(4):1173–1183PubMed

69.

Kim H, Lee SH, Kim SS, Yoo JH, Kim CJ (2007) The influence of maternal treadmill running during pregnancy on short-term memory and hippocampal cell survival in rat pups. Int J Dev Neurosci 25(4):243–249PubMed

70.

Bick-Sander A, Steiner B, Wolf SA, Babu H, Kempermann G (2006) Running in pregnancy transiently increases postnatal hippocampal neurogenesis in the offspring. Proc Natl Acad Sci USA 7(10):3852–3857 103(

Titel: Positive effect of moderate-intensity aerobic activity on pentylenetetrazol-induced epileptic behaviors in pregnant mice and cognitive performance in adult male offspring
verfasst von: Ayoob Sabaghi
Ali Heyrani
Amir Kiani
Namdar Yousofvand
Publikationsdatum: 24.07.2018
Verlag: Springer Milan
Erschienen in: Sport Sciences for Health / Ausgabe 1/2019
Print ISSN: 1824-7490
Elektronische ISSN: 1825-1234
DOI: https://doi.org/10.1007/s11332-018-0485-7

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Positive effect of moderate-intensity aerobic activity on pentylenetetrazol-induced epileptic behaviors in pregnant mice and cognitive performance in adult male offspring

Abstract

Purpose

Methods

Results

Conclusion

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