@2024 Afarand., IRAN
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(2):79-87
ISSN: 2252-0805 The Horizon of Medical Sciences 2018;24(2):79-87
Anxiolytic Effect of Lithium Chloride in Model of PTZ-Induced Seizure
ARTICLE INFO
Article Type
Original ResearchAuthors
Edalatmanesh MA (*)Yazdani M (1)
Davoodi A (2)
Rafiei S (3)
(*) Department of Biology, College of Sciences, Shiraz Branch, Islamic Azad University, Shiraz, Iran
(1) Department of Biology, College of Sciences, Shiraz Branch, Islamic Azad University, Shiraz, Iran
(2) Department of Psychology, College of Humanities, Islamic Azad University, Shiraz Branch , Shiraz, Iran
(3) Department of Exercise Physiology, Kish International Campus, Tehran University, Kish, Iran
Correspondence
Article History
Received: October 28, 2017Accepted: May 2, 2018
ePublished: May 16, 2018
BRIEF TEXT
Epilepsy is a known brain disorder characterized by frequent and unplanned interruptions of normal brain function, called epileptic seizures [1].
... [2, 3]. Glutamate and γ-aminobutyric acid (GABA) are two neurotransmitters that have been studied extensively in relation to seizure induced by chemical kindling. Both of these systems play an important role in the epilepsy and the resulted seizure [4]. The inhibition of GABA is an important factor in the pathogenesis of anxiety [5, 6]. Pentylenetetrazol (PTZ) can induce a seizure by blocking GABA receptors and it also induces anxiety symptoms by inducing a limbic epilepsy model [7]. .... [8-15]. Lithium not only acts as a moderator, but also has anti-depressant and anti-anxiety effects [17]. ... [18-20].
This study evaluated the anxiolytic effect of administration of lithium chloride (LiCl) in penthylentetrazole (PTZ)-induced seizure in rat model.
The present research was an experimental study.
This experimental study was performed on 50 male Sprague Dawley male rats between June and September in 2016.
This experimental study was performed on 50 male Sprague Dawley male rats weighted 200±20 gr.
During the study period, the animals were kept at standard temperature (25±2°C) and relative humidity (50±5%) and the 12-h light/darkness (6 am-6 pm). All experiments were performed according to the Standards for Laboratory Animal and supervised by the Ethics Committee of Islamic Azad University, Shiraz Branch (Ethics code: 95-2034-8324). Animals were randomly divided into 5 groups (10 rats per group), including control, Sham (PTZ+Saline), three experimental groups (PTZ+Li20, PTZ+Li40 and PTZ+Li80). Control group did not receive any treatment. The PTZ+Saline group received normal saline as a lithium solvent for 14 days following the five stages of PTZ-induced seizure. This group was used to evaluate the effects of PTZ on anxiety level. Three treatment groups received lithium chloride (Sigma-Aldrich, USA) by daily intraperitoneal injection (20, 40 and 80 mg/kg) for 14 days. PTZ (Sigma-Aldrich, USA) was used to induce seizure. PTZ (40 mg/kg) was injected intraperitoneally for 5 consecutive days (animals were weighed before each injection). Thirty minutes after each PTZ injection, the rats were examined for seizure. Seizures were examined using the Racine's scale [21-23]. Behavioral experiments The elevated plus maze test It is used to measure anxiety-like behaviors in rodents [24]. Open field test It is used to measure exploratory, search and anxiety behaviors [25]. Measurement of hippocampal BDNF levels After behavioral tests, animals with a lethal dose of chloroform were anesthetized. Immediately the animal head was separated and the brain completely removed from the skull and placed on the ice. Rats’ hippocampus was carefully removed from the rest of the brain under a stereoscope. After washing with saline and Tris buffer (Sigma-Aldrich, Germany), it was homogenized at 5,000 rpm for 5 min using Homogenizer (IKA, Germany). The homogenized solution was centrifuged by a refrigerated centrifuge machine (Hermle, Germany). To prevent degradation of enzymes and proteins, all experiments were carried out at 4 C (refrigerated centrifuge) and Phenylmethylsulfonyl fluoride (0.5 μm) was used as a protease inhibitor (Sigma-Aldrich, Germany) [26]. One-way analysis of variance and Tukey's post hoc tests by SPSS 22 were used to determine significant differences in the anxiety and behavioral indices among the groups.
The elevated plus maze test The mean spent time in the closed arm in the PTZ+Saline group showed a significant difference with the control group (p<0.0001; Figure 1). On the other hand, there was a significant difference in three groups treated with lithium chloride (p<0.001 for all three groups). Comparison of the lithium chloride treated groups with PTZ+Saline group showed a significant difference between PTZ+Li20 and PTZ+Saline group (Figure 1, p<0.05). No significant difference was observed between the other treatment groups with lithium chloride and PTZ+Saline group. These results showed that lithium treatment in PTZ groups only at a minimum dose (PTZ+Li20) has could reduce anxiety levels. Open field test Number of squares crossed: The results showed a significant difference between the control group and the PTZ+Saline group (p<0.0001; Table 1). This difference indicated an increase in anxiety in the PTZ group compared with the control group. Also, there was a significant difference between the control group and lithium chloride treated groups (40 and 80 mg) (p<0.05 and p<0.001, respectively; Table 1). On the other hand, the results showed a significant difference between PTZ+Saline and PTZ+Li20 groups (p<0.0001). Also, there was a significant difference between PTZ+Li40 and PTZ+Li80 groups with PTZ+Li20 group (p<0.001; Table 1). In fact, the results showed that treatment with lithium at a minimum dose reduced anxiety levels following PTZ-induced seizure. Number of central squares entries: The mean number of central squares entries in the open field test showed a significant difference between the control and PTZ+Saline groups (p<0.0001; Table 1). This difference indicates a decrease in the exploratory behaviors and an increase in anxiety levels in the PTZ groups compared with the control group. This study also showed a significant difference between the control and the PTZ+Li80 groups (p<0.01; Table 1). On the other hand, there was a significant difference between PTZ+Saline group and lithium treated groups (PTZ+Li20, PTZ+Li40 and PTZ+Li80) (p<0.0001, p<0.001 and p<0.05, respectively; Figure 3). This difference indicates increased exploratory behaviors in lithium chloride treated groups, especially at the minimum dose in comparison to the PTZ + Saline group. Climbing on the wall: The results showed a significant difference between the control and the PTZ+Saline groups (p<0.001). Also, there was a significant difference between the control group and the PTZ+Li40 and PTZ+Li80 groups (p<0.001; Table 1). The results of this study showed a significant difference between PTZ+Saline group and PTZ+Li20 group (p<0.001). Moreover, there was a significant difference between PTZ+Li40 and PTZ+Li80 groups with PTZ+Li20 group (p<0.001; Table 1). Exploratory behaviors in the PTZ treated group reduced and treatment with 20 mg/kg of body weight of rats significantly increased exploratory behaviors. Number of fecal boli: The number of fecal boli left was used as an index for anxiety between the control and PTZ+Saline groups and the results of one-way ANOVA showed a significant difference between two groups (p<0.0001; Figure 5), which indicates an increased level of anxiety in the PTZ rats compared with the control group. Also, there was a significant difference between control and PTZ+Li40 and PTZ+Li80 groups (p<0.01). In addition, a significant difference was found between PTZ+Saline and PTZ+Li20 and PTZ+Li40 groups (p<0.0001 and p<0.001, respectively; Table 1). It can be concluded that treatment with lithium chloride could reduce the level of anxiety. On the other hand, there was a significant difference between PTZ+Li40 and PTZ+Li80 groups with PTZ+Li20 group (p<0.01; Table 1). Measurement of hippocampal BDNF levels PTZ-induced seizures significantly reduced the hippocampal level of BDNF in comparison to the control group (p<0.0001; Figure 2). Meanwhile, lithium chloride treatment significantly increased the level of BDNF in the experimental groups compared with the PTZ+Saline group.
... [27-40]. PTZ causes anxiety disorder in the animal model of seizure, and treatment with lithium chloride can reduce the level of anxiety in this model. Other researchers also found that PTZ-induced Kindling seizures cause anxiety symptoms [41-42]. Also, the anti-anxiety effect of lithium has been observed in previous studies [16, 17]. The present study showed that, following PTZ-induced seizures, the level of BDNF in the rat hippocampus was decreased, which can cause behavioral disorders, including anxiety. On the other hand, administration of lithium chloride could significantly increase BDNF levels in treated groups, which indicates the beneficial effects of this element. Lithium administration increases the expression of BDNF in rodent brain, especially in the limbicular and frontal cortex. Studies have also shown that for neurotrophic effects of lithium in cortical neurons BDNF expression is needed [43]. ... [44-46].
It is suggested that the expression of BDNF receptors and depression-like behaviors be investigated in this model.
Anxiolytic-like effects of lithium may improve the symptoms of anxiety in PTZ-induced seizure.
The efforts of Research Director of Islamic Azad University of Shiraz for the essential facilities to perform this study are appreciated.
None declared.
None declared.
This study was partially supported by the research deputy of Islamic Azad University, Shiraz branch as a research project.
TABLES and CHARTS
Show attach fileCITIATION LINKS
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[2]Naseer MI, Shupeng L, Kim MO. Maternal epileptic seizure induced by pentylenetetrazol: apoptotic neurodegeneration and decreased GABAB1 receptor expression in prenatal rat brain. Mol Brain. 2009;2:20:660-701.
[3]Zamponi GW, Lory P, Perez-Reyes E. Role of voltage-gated calcium channels in epilepsy. Pflugers Arch. 2010;460(2):395-403
[4]Hui Yin Y, Ahmad N, Makmor-Bakry M. Pathogenesis of epilepsy: Challenges in animal models. Iran J Basic Med Sci. 2013;16(11):1119-32
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[6]Neumeister A, Bain E, Nugent AC, Carson RE, Bonne O, Luckenbaugh DA, et al. Reduced serotonin type 1A receptor binding in panic disorder. J Neurosci. 2004;24(3):589-91
[7]Jung ME, Lal H, Gatch MB. The discriminative stimulus effects of pentylenetetrazol as a model of anxiety: Recent developments. Neurosci Biobehav Rev. 2002;26(4):429-39.
[8]Lei P, Ayton S, Bush AI, Adlard PA. GSK-3 in neurodegenerative diseases. Int J Alzheimers Dis. 2011;2011:189246
[9]Tso CY, Chiu KH, Cheung KW. Ceramic insert dislodgment after revision ceramic-on-ceramic total hip arthroplasty. J Arthroplasty. 2010;25(4):660.e5-7.
[10]Quiroz JA, Machado-Vieira R, Zarate CA Jr, Manji HK. Novel insights into lithium's mechanism of action: Neurotrophic and neuroprotective effects. Neuropsychobiology. 2010;62(1):50-60.
[11]Chiu CT, Chuang DM. Neuroprotective action of lithium in disorders of the central nervous system. Zhong Nan Da Xue Bao Yi Xue Ban. 2011;36(6):461-76.
[12]Su H, Zhang W, Guo J, Guo A, Yuan Q, Wu W. Lithium enhances the neuronal differentiation of neural progenitor cells in vitro and after transplantation into the avulsed ventral horn of adult rats through the secretion of brain-derived neurotrophic factor. J Neurochem. 2009;108(6):1385-98.
[13]Wada A. Lithium and neuropsychiatric therapeutics: Neuroplasticity via glycogen synthase kinase-3β, β-catenin, and neurotrophin cascades. J Pharmacol Sci. 2009;110(1):14-28.
[14]Lapmanee S, Charoenphandhu J, Teerapornpuntakit J, Krishnamra N, Charoenphandhu N. Agomelatine, venlafaxine, and running exercise effectively prevent anxiety- and depression-like behaviors and memory impairment in restraint stressed rats. PLoS One. 2017;12(11):e0187671.
[15]Mendez-David I, Guilloux JP, Papp M, Tritschler L, Mocaer E, Gardier AM, et al. S 47445 produces antidepressant- and anxiolytic-like effects through neurogenesis dependent and independent mechanisms. Front Pharmacol. 2017;8:462.
[16]An Y, Inoue T, Kitaichi Y, Chen C, Nakagawa S, Wang C, et al. Combined treatment with subchronic lithium and acute intracerebral mirtazapine microinjection into the median raphe nucleus exerted an anxiolytic-like effect synergistically. Eur J Pharmacol. 2016;783:112-6.
[17]Motaghinejad M, Seyedjavadein Z, Motevalian M, Asadi M. The neuroprotective effect of lithium against high dose methylphenidate: Possible role of BDNF. Neurotoxicology. 2016;56:40-54.
[18]Nikoui V, Javadi-Paydar M, Salehi M, Behestani S, Dehpour AR. Protective effects of lithium on sumatriptan-induced memory impairment in mice. Acta Med Iran. 2016;54(4):226-32.
[19]Smagin DA, Kudryavtseva NN. Anxiogenic and anxiolytic effects of lithium chloride under preventive and therapeutic treatments of male mice with repeated experience of aggression. Zh Vyssh Nerv Deiat Im I P Pavlova. 2014;64(6):646-59. [Russian]
[20]Youngs RM, Chu MS, Meloni EG, Naydenov A, Carlezon WA Jr, Konradi C. Lithium administration to preadolescent rats causes long-lasting increases in anxiety-like behavior and has molecular consequences. J Neurosci. 2006;26(22):6031-9
[21]Roohbakhsh A, Esmaeili H, Asami Z, Arab Baniasad F, Shamsizadeh A, Rezvani ME. Effect of Anethum graveolens hydroalcoholic extract on pentylenetetrazole-induced paroxysm. Horizon Med Sci. 2013;19(1):41-5. [Persian]
[22]Seghatoleslam M, Alipour F, Shafieian R, Hassanzadeh Z, Edalatmanesh MA, Sadeghnia HR, et al. The effects of Nigella sativa on neural damage after pentylenetetrazole induced seizures in rats. J Tradit Complement Med. 2016;6(3):262-8.
[23]Vafaee F, Hosseini M, Hassanzadeh Z, Edalatmanesh MA, Sadeghnia HR, Seghatoleslam M, et al. The Effects of Nigella Sativa Hydro-alcoholic Extract on Memory and Brain Tissues Oxidative Damage after Repeated Seizures in Rats. Iran J Pharm Res. 2015;14(2):547-57.
[24]Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007;2(2):322-8.
[25]Murray CL, Obiang P, Bannerman D, Cunningham C. Endogenous IL-1 in Cognitive Function and Anxiety: A Study in IL-1RI−/− Mice. PLoS One. 2013;8(10):e78385.
[26]Kalynchuk LE. Long-term amygdala kindling in rats as a model for the study of interictal emotionality in temporal lobe epilepsy. Neurosci Biobehav Rev. 2000;24(7):691-704.
[27]Milman A, Rosenberg A, Weizman R, Pick CG. Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J Neurotrauma. 2005;22(9):1003-10.
[28]Mazarati AM, Pineda E, Shin D, Tio D, Taylor AN, Sankar R. Comorbidity between epilepsy and depression: Role of hippocampal interleukin-1beta. Neurobiol Dis. 2010;37(2):461-7.
[29]Jones NC, Cardamone L, Williams JP, Salzberg MR, Myers D, O’Brien TJ. Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J Neurotrauma. 2008;25(11):1367-74.
[30]Detour J, Schroeder H, Desor D, Nehlig A. A 5-month period of epilepsy impairs spatial memory, decreases anxiety, but spares object recognition in the lithium-pilocarpine model in adult rats. Epilepsia. 2005;46(4):499-508.
[31]Kemppainen EJ, Nissinen J, Pitkänen A. Fear conditioning is impaired in systemic kainic acid and amygdala-stimulation models of epilepsy. Epilepsia. 2006;47(5):820-9.
[32]Jessberger S, Nakashima K, Clemenson GD Jr, Mejia E, Mathews E, Ure K, et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci. 2007;27(22):5967-75.
[33]Chauvière L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C. Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci. 2009;29(17):5402-10.
[34]Kastenberger I, Lutsch C, Herzog H, Schwarzer Ch. Influence of sex and genetic background on anxiety-related and stress-induced behavior of prodynorphin deficient mice. PLoS One. 2012;7(3):e34251.
[35]Leach G, Adidharma W, Yan L. Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). Plos One. 2013;8(2):e57115.
[36]Godlevsky LS, Muratova TN, Kresyun NV, van Luijtelaar G, Coenen AM. Anxiolytic and antidepressive effects of electric stimulation of the paleocerebellar cortex in pentylenetetrazol kindled rats. Acta Neurobiol Exp (Wars). 2014;74(4):456-64.
[37]Zárraga-Galindo N, Vergara-Aragón P, Rosales-Meléndez S, Ibarra-Guerrero P, Domínguez-Marrufo LE, Oviedo-García RE, et al. Effects of bee products on pentylenetetrazole-induced seizures in the rat. Proc West Pharmacol Soc. 2011;54:33-40.
[38]Liu ZH, Chuang DM, Smith CB. Lithium ameliorates phenotypic deficits in a mouse model of fragile X syndrome. Int J Neuropsychopharmacol. 2011;14(5):618-30.
[39]Yan XB, Hou HL, Wu LM, Liu J, Zhou JN. Lithium regulates hippocampal neurogenesis by ERK pathway and facilitates recovery of spatial learning and memory in rats after transient global cerebral ischemia. Neuropharmacology. 2007;53(4):487-95.
[40]Chen X, Sun W, Pan Y, Yang Q, Cao K, Zhang J, et al. Lithium ameliorates open-field and elevated plus maze behaviors, and brain phospho-glycogen synthase kinase 3-beta expression in fragile X syndrome model mice. Neurosciences (Riyadh). 2013;18(4):356-62.
[41]Hoeller AA, de Carvalho CR, Franco PLC, Formolo DA, Imthon AK, Dos Santos HR, et al. Behavioral and neurochemical consequences of pentylenetetrazol-induced kindling in young and middle-aged rats. Pharmaceuticals (Basel). 2017;10(3).
[42]Kordi Jaz E, Moghimi A, Fereidoni M, Asadi S, Shamsizadeh A, Roohbakhsh A. SB-334867, an orexin receptor 1 antagonist, decreased seizure and anxiety in pentylenetetrazol-kindled rats. Fundam Clin Pharmacol. 2017;31(2):201-7.
[43]Hashimoto R, Takei N, Shimazu K, Christ L, Lu B, Chuang DM. Lithium induces brain-derived neurotrophic factor and activates TrkB in rodent cortical neurons: An essential step for neuroprotection against glutamate excitotoxicity. Neuropharmacology. 2002;43(7):1173-9.
[44]Zhen JL, Chang YN, Qu ZZ, Fu T, Liu JQ, Wang WP. Luteolin rescues pentylenetetrazole-induced cognitive impairment in epileptic rats by reducing oxidative stress and activating PKA/CREB/BDNF signaling. Epilepsy Behav. 2016;57(Pt A):177-84.
[45]Moghadas M, Edalatmanesh MA, Hosseini M. Effect of Lithium Chloride on Serum Levels of BDNF, TNF-α, and Wet Weight of Brain in an Animal Model of Depression. Shefaye Khatam. 2014;2(4):9-19.
[46]Liu ZH, Chuang DM, Beebe Smith C. Lithium ameliorates phenotypic deficits in a mouse model of fragile X syndrome. Int J Neuropsychopharmacol. 2011;14(5):618-30.
[2]Naseer MI, Shupeng L, Kim MO. Maternal epileptic seizure induced by pentylenetetrazol: apoptotic neurodegeneration and decreased GABAB1 receptor expression in prenatal rat brain. Mol Brain. 2009;2:20:660-701.
[3]Zamponi GW, Lory P, Perez-Reyes E. Role of voltage-gated calcium channels in epilepsy. Pflugers Arch. 2010;460(2):395-403
[4]Hui Yin Y, Ahmad N, Makmor-Bakry M. Pathogenesis of epilepsy: Challenges in animal models. Iran J Basic Med Sci. 2013;16(11):1119-32
[5]- Mula M, Pini S, Cassano GB. The role of anticonvulsant drugs in anxiety disorders: A critical review of the evidence. J Clin Psychopharmacol .2007;27(3):263-72
[6]Neumeister A, Bain E, Nugent AC, Carson RE, Bonne O, Luckenbaugh DA, et al. Reduced serotonin type 1A receptor binding in panic disorder. J Neurosci. 2004;24(3):589-91
[7]Jung ME, Lal H, Gatch MB. The discriminative stimulus effects of pentylenetetrazol as a model of anxiety: Recent developments. Neurosci Biobehav Rev. 2002;26(4):429-39.
[8]Lei P, Ayton S, Bush AI, Adlard PA. GSK-3 in neurodegenerative diseases. Int J Alzheimers Dis. 2011;2011:189246
[9]Tso CY, Chiu KH, Cheung KW. Ceramic insert dislodgment after revision ceramic-on-ceramic total hip arthroplasty. J Arthroplasty. 2010;25(4):660.e5-7.
[10]Quiroz JA, Machado-Vieira R, Zarate CA Jr, Manji HK. Novel insights into lithium's mechanism of action: Neurotrophic and neuroprotective effects. Neuropsychobiology. 2010;62(1):50-60.
[11]Chiu CT, Chuang DM. Neuroprotective action of lithium in disorders of the central nervous system. Zhong Nan Da Xue Bao Yi Xue Ban. 2011;36(6):461-76.
[12]Su H, Zhang W, Guo J, Guo A, Yuan Q, Wu W. Lithium enhances the neuronal differentiation of neural progenitor cells in vitro and after transplantation into the avulsed ventral horn of adult rats through the secretion of brain-derived neurotrophic factor. J Neurochem. 2009;108(6):1385-98.
[13]Wada A. Lithium and neuropsychiatric therapeutics: Neuroplasticity via glycogen synthase kinase-3β, β-catenin, and neurotrophin cascades. J Pharmacol Sci. 2009;110(1):14-28.
[14]Lapmanee S, Charoenphandhu J, Teerapornpuntakit J, Krishnamra N, Charoenphandhu N. Agomelatine, venlafaxine, and running exercise effectively prevent anxiety- and depression-like behaviors and memory impairment in restraint stressed rats. PLoS One. 2017;12(11):e0187671.
[15]Mendez-David I, Guilloux JP, Papp M, Tritschler L, Mocaer E, Gardier AM, et al. S 47445 produces antidepressant- and anxiolytic-like effects through neurogenesis dependent and independent mechanisms. Front Pharmacol. 2017;8:462.
[16]An Y, Inoue T, Kitaichi Y, Chen C, Nakagawa S, Wang C, et al. Combined treatment with subchronic lithium and acute intracerebral mirtazapine microinjection into the median raphe nucleus exerted an anxiolytic-like effect synergistically. Eur J Pharmacol. 2016;783:112-6.
[17]Motaghinejad M, Seyedjavadein Z, Motevalian M, Asadi M. The neuroprotective effect of lithium against high dose methylphenidate: Possible role of BDNF. Neurotoxicology. 2016;56:40-54.
[18]Nikoui V, Javadi-Paydar M, Salehi M, Behestani S, Dehpour AR. Protective effects of lithium on sumatriptan-induced memory impairment in mice. Acta Med Iran. 2016;54(4):226-32.
[19]Smagin DA, Kudryavtseva NN. Anxiogenic and anxiolytic effects of lithium chloride under preventive and therapeutic treatments of male mice with repeated experience of aggression. Zh Vyssh Nerv Deiat Im I P Pavlova. 2014;64(6):646-59. [Russian]
[20]Youngs RM, Chu MS, Meloni EG, Naydenov A, Carlezon WA Jr, Konradi C. Lithium administration to preadolescent rats causes long-lasting increases in anxiety-like behavior and has molecular consequences. J Neurosci. 2006;26(22):6031-9
[21]Roohbakhsh A, Esmaeili H, Asami Z, Arab Baniasad F, Shamsizadeh A, Rezvani ME. Effect of Anethum graveolens hydroalcoholic extract on pentylenetetrazole-induced paroxysm. Horizon Med Sci. 2013;19(1):41-5. [Persian]
[22]Seghatoleslam M, Alipour F, Shafieian R, Hassanzadeh Z, Edalatmanesh MA, Sadeghnia HR, et al. The effects of Nigella sativa on neural damage after pentylenetetrazole induced seizures in rats. J Tradit Complement Med. 2016;6(3):262-8.
[23]Vafaee F, Hosseini M, Hassanzadeh Z, Edalatmanesh MA, Sadeghnia HR, Seghatoleslam M, et al. The Effects of Nigella Sativa Hydro-alcoholic Extract on Memory and Brain Tissues Oxidative Damage after Repeated Seizures in Rats. Iran J Pharm Res. 2015;14(2):547-57.
[24]Walf AA, Frye CA. The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat Protoc. 2007;2(2):322-8.
[25]Murray CL, Obiang P, Bannerman D, Cunningham C. Endogenous IL-1 in Cognitive Function and Anxiety: A Study in IL-1RI−/− Mice. PLoS One. 2013;8(10):e78385.
[26]Kalynchuk LE. Long-term amygdala kindling in rats as a model for the study of interictal emotionality in temporal lobe epilepsy. Neurosci Biobehav Rev. 2000;24(7):691-704.
[27]Milman A, Rosenberg A, Weizman R, Pick CG. Mild traumatic brain injury induces persistent cognitive deficits and behavioral disturbances in mice. J Neurotrauma. 2005;22(9):1003-10.
[28]Mazarati AM, Pineda E, Shin D, Tio D, Taylor AN, Sankar R. Comorbidity between epilepsy and depression: Role of hippocampal interleukin-1beta. Neurobiol Dis. 2010;37(2):461-7.
[29]Jones NC, Cardamone L, Williams JP, Salzberg MR, Myers D, O’Brien TJ. Experimental traumatic brain injury induces a pervasive hyperanxious phenotype in rats. J Neurotrauma. 2008;25(11):1367-74.
[30]Detour J, Schroeder H, Desor D, Nehlig A. A 5-month period of epilepsy impairs spatial memory, decreases anxiety, but spares object recognition in the lithium-pilocarpine model in adult rats. Epilepsia. 2005;46(4):499-508.
[31]Kemppainen EJ, Nissinen J, Pitkänen A. Fear conditioning is impaired in systemic kainic acid and amygdala-stimulation models of epilepsy. Epilepsia. 2006;47(5):820-9.
[32]Jessberger S, Nakashima K, Clemenson GD Jr, Mejia E, Mathews E, Ure K, et al. Epigenetic modulation of seizure-induced neurogenesis and cognitive decline. J Neurosci. 2007;27(22):5967-75.
[33]Chauvière L, Rafrafi N, Thinus-Blanc C, Bartolomei F, Esclapez M, Bernard C. Early deficits in spatial memory and theta rhythm in experimental temporal lobe epilepsy. J Neurosci. 2009;29(17):5402-10.
[34]Kastenberger I, Lutsch C, Herzog H, Schwarzer Ch. Influence of sex and genetic background on anxiety-related and stress-induced behavior of prodynorphin deficient mice. PLoS One. 2012;7(3):e34251.
[35]Leach G, Adidharma W, Yan L. Depression-like responses induced by daytime light deficiency in the diurnal grass rat (Arvicanthis niloticus). Plos One. 2013;8(2):e57115.
[36]Godlevsky LS, Muratova TN, Kresyun NV, van Luijtelaar G, Coenen AM. Anxiolytic and antidepressive effects of electric stimulation of the paleocerebellar cortex in pentylenetetrazol kindled rats. Acta Neurobiol Exp (Wars). 2014;74(4):456-64.
[37]Zárraga-Galindo N, Vergara-Aragón P, Rosales-Meléndez S, Ibarra-Guerrero P, Domínguez-Marrufo LE, Oviedo-García RE, et al. Effects of bee products on pentylenetetrazole-induced seizures in the rat. Proc West Pharmacol Soc. 2011;54:33-40.
[38]Liu ZH, Chuang DM, Smith CB. Lithium ameliorates phenotypic deficits in a mouse model of fragile X syndrome. Int J Neuropsychopharmacol. 2011;14(5):618-30.
[39]Yan XB, Hou HL, Wu LM, Liu J, Zhou JN. Lithium regulates hippocampal neurogenesis by ERK pathway and facilitates recovery of spatial learning and memory in rats after transient global cerebral ischemia. Neuropharmacology. 2007;53(4):487-95.
[40]Chen X, Sun W, Pan Y, Yang Q, Cao K, Zhang J, et al. Lithium ameliorates open-field and elevated plus maze behaviors, and brain phospho-glycogen synthase kinase 3-beta expression in fragile X syndrome model mice. Neurosciences (Riyadh). 2013;18(4):356-62.
[41]Hoeller AA, de Carvalho CR, Franco PLC, Formolo DA, Imthon AK, Dos Santos HR, et al. Behavioral and neurochemical consequences of pentylenetetrazol-induced kindling in young and middle-aged rats. Pharmaceuticals (Basel). 2017;10(3).
[42]Kordi Jaz E, Moghimi A, Fereidoni M, Asadi S, Shamsizadeh A, Roohbakhsh A. SB-334867, an orexin receptor 1 antagonist, decreased seizure and anxiety in pentylenetetrazol-kindled rats. Fundam Clin Pharmacol. 2017;31(2):201-7.
[43]Hashimoto R, Takei N, Shimazu K, Christ L, Lu B, Chuang DM. Lithium induces brain-derived neurotrophic factor and activates TrkB in rodent cortical neurons: An essential step for neuroprotection against glutamate excitotoxicity. Neuropharmacology. 2002;43(7):1173-9.
[44]Zhen JL, Chang YN, Qu ZZ, Fu T, Liu JQ, Wang WP. Luteolin rescues pentylenetetrazole-induced cognitive impairment in epileptic rats by reducing oxidative stress and activating PKA/CREB/BDNF signaling. Epilepsy Behav. 2016;57(Pt A):177-84.
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