Skip to main content
Log in

Differences in vulnerability to nicotine-induced kindling between female and male periadolescent rats

  • Original Investigation
  • Published:
Psychopharmacology Aims and scope Submit manuscript

Abstract

Rationale

It has recently been reported that chronic nicotine administration at subconvulsive doses causes seizures, a phenomenon referred to as kindling. Evidence points to the involvement of oxidative stress in pharmacological and electrical kindling, sex is known to influence the brain’s response to nicotine.

Objectives

This study investigated the sex differences in vulnerability to nicotine-induced kindling and the involvement of oxidative stress in this phenomenon.

Methods

Male and female periadolescent Wistar rats received repeated injections of a subconvulsive dose of nicotine (hemisulfate salt; 2 mg/kg, i.p.) every weekday for up to 25 days. To better understand the influence of oxidative stress in nicotine kindling, the antioxidant vitamin E (200 and 400 mg/kg, p.o.) was administered prior to nicotine administration. The levels of gluthatione (GSH), superoxide dismutase (SOD) activity, and lipid peroxidation were determined in the hippocampus (HC), prefrontal cortex (PFC), and striatum.

Results

Female animals developed kindling more rapidly than male rats. In female rats, kindling was associated with decreases in antioxidant defenses, including GSH levels in the HC and striatum and SOD activity in the PFC and striatum, and increased lipid peroxidation in all brain areas studied. By contrast, male kindled animals presented only with a decrease in the GSH in the HC. Vitamin E prevented the occurrence of kindled seizures by 80 % and 75 % in male and female rats, respectively.

Conclusion

These novel findings indicate that female periadolescent rats develop nicotine-kindled seizures earlier than their male counterparts. Differences in the oxidative balance may be involved in this mechanism.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Adams JD, Wang B (1994) Vitamin E uptake into the brain and 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine toxicity. J Cereb Blood Flow Metab 14:362–363

    Article  CAS  PubMed  Google Scholar 

  • Agarwal NB, Jain S, Agarwal NK, Mediratta PK, Sharma KK (2011) Modulation of pentylenetetrazole-induced kindling and oxidative stress by curcumin in mice. Phytomedicine 18:756–759

    Article  CAS  PubMed  Google Scholar 

  • Alkondon M, Pereira EFR, Almeida LEF, Randall WR, Albuquerque EX (2000) Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus. Neuropharmacology 39:2726–2739

    Article  CAS  PubMed  Google Scholar 

  • Andersen SL, Rutstein M, Benzo JM, Hostetter JC, Teicher MH (1997) Sex differences in dopamine receptor overproduction and elimination. Neuroreport 8:1495–1498

    Article  CAS  PubMed  Google Scholar 

  • Andersen SL, Thompson AT, Rutstein M, Hostetter JC, Teicher MH (2000) Dopamine receptor pruning in prefrontal cortex during the periadolescent period in rats. Synapse 37:167–169

    Article  CAS  PubMed  Google Scholar 

  • Andersen SL, Thompson AP, Krenzel E, Teicher MH (2002) Pubertal changes in gonadal hormones do not underlie adolescent dopamine receptor overproduction. Psychoneuroendocrinology 27:683–691

    Article  CAS  PubMed  Google Scholar 

  • Bastlund JF, Berry D, Watson WP (2005) Pharmacological and histological characterisation of nicotine-kindled seizures in mice. Neuropharmacology 48:975–983

    Article  CAS  PubMed  Google Scholar 

  • Becker JB, Robinson TE, Lorenz KA (1982) Sex differences and estrous cycle variations in amphetamine-elicited rotational behavior. Eur J Pharmacol 80:65–72

    Article  CAS  PubMed  Google Scholar 

  • Bell IR, Rossi J, Gilbert ME, Kobal G, Morrow LA, Newlin DB, Sorg BA, Wood RW (1997) Testing the neural sensitization and kindling hypothesis for illness from low levels of environmental chemicals. Environ Health Perspect 105:539–547

    CAS  PubMed  Google Scholar 

  • Bob P, Glaslova K, Susta M, Jasova D, Raboch J (2006) Traumatic dissociation, epileptic-like phenomena, and schizophrenia. Neuroendocrinol Lett 27:321–326

    PubMed  Google Scholar 

  • Booze RM, Welch MA, Wood ML, Billings KA, Apple SR, Mactutus CF (1999) Behavioral sensitization following repeated intravenous nicotine administration: gender differences and gonadal hormones. Pharmacol Biochem Behav 64:827–839

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Buchmann AF, Blomeyer D, Jennen-Steinmetz C, Schmidt MH, Esser G, Banaschewski T, Laucht M (2011) Early smoking onset may promise initial pleasurable sensations and later addiction. Addict Biol. doi:10.1111/j.1369-1600.2011.00377.x

  • Burton GW, Traber MG (1990) Vitamin E: antioxidant activity, biokinetics, and bioavailability. Annu Rev Nutr 10:357–382

    Article  CAS  PubMed  Google Scholar 

  • Castle L, Perkins MJ (1986) Inhibition-kinetics of chain-breaking phenolic antioxidants in SDS micelles — evidence that intermicellar diffusion rates may be rate-limiting for hydrophobic inhibitors such as alpha-tocopherol. J Am Chem Soc 108:6381–6382

    Article  CAS  Google Scholar 

  • Champtiaux N, Gotti C, Cordero-Erausquin M, David DJ, Przybylski C, Lena C, Clementi F, Moretti M, Rossi FM, Le Novere N, McIntosh JM, Gardier AM, Changeux JP (2003) Subunit composition of functional nicotinic receptors in dopaminergic neurons investigated with knock-out mice. J Neurosci 23:7820–7829

    CAS  PubMed  Google Scholar 

  • Chen TY, Zhang D, Dragomir A, Akay Y, Akay M (2011) The effects of nicotine exposure and PFC transection on the time-frequency distribution of VTA DA neurons' firing activities. Med Biol Eng Comput 49:605–612

    Article  PubMed  Google Scholar 

  • Clarke PB, Kumar R (1983) The effects of nicotine on locomotor activity in non-tolerant and tolerant rats. Br J Pharmacol 78:329–337

    Article  CAS  PubMed  Google Scholar 

  • Collins SL, Wade D, Ledon J, Izenwasser S (2004) Neurochemical alterations produced by daily nicotine exposure in periadolescent vs. adult male rats. Eur J Pharmacol 502:75–85

    Article  CAS  PubMed  Google Scholar 

  • Damaj MI, Glassco W, Dukat M, Martin BR (1999) Pharmacological characterization of nicotine-induced seizures in mice. J Pharmacol Exp Ther 291:1284–1291

    CAS  PubMed  Google Scholar 

  • Delfino RJ, Jamner LD, Whalen CK (2001) Temporal analysis of the relationship of smoking behavior and urges to mood states in men versus women. Nicotine Tob Res 3:235–248

    Article  CAS  PubMed  Google Scholar 

  • Doura MB, Gold AB, Keller AB, Perry DC (2008) Adult and periadolescent rats differ in expression of nicotinic cholinergic receptor subtypes and in the response of these subtypes to chronic nicotine exposure. Brain Res 1215:40–52

    Article  CAS  PubMed  Google Scholar 

  • Dringen R, Hirrlinger J (2003) Glutathione pathways in the brain. Biol Chem 384:505–516

    Article  CAS  PubMed  Google Scholar 

  • Duchen MR (2000) Mitochondria and calcium: from cell signalling to cell death. J Physiol Lond 529:57–68

    Article  CAS  PubMed  Google Scholar 

  • Edwards HE, Burnham WM, MacLusky NJ (1999) Testosterone and its metabolites affect afterdischarge thresholds and the development of amygdala kindled seizures. Brain Res 838:151–157

    Article  CAS  PubMed  Google Scholar 

  • El-Abhar Hanan S, El Gawad Hanan MA (2003) Modulation of cortical nitric oxide synthase, glutamate, and redox state by nifedipine and taurine in PTZ-kindled mice. Epilepsia 44:276–281

    Article  CAS  PubMed  Google Scholar 

  • Erakovic V, Zupan G, Varljen J, Simonic A (2003) Pentylenetetrazol-induced seizures and kindling: changes in free fatty acids, superoxide dismutase, and glutathione peroxidase activity. Neurochem Int 42:173–178

    Article  CAS  PubMed  Google Scholar 

  • Frantseva MV, Velazquez JLP, Tsoraklidis G, Mendonca AJ, Adamchik Y, Mills LR, Carlen PL, Burnham MW (2000) Oxidative stress is involved in seizure-induced neurodegeneration in the kindling model of epilepsy. Neuroscience 97:431–435

    Article  CAS  PubMed  Google Scholar 

  • Freitas RM, Vasconcelos SMM, Souza FCF, Viana GSB, Fonteles MMF (2005) Oxidative stress in the hippocampus after pilocarpine-induced status epilepticus in Wistar rats. FEBS J 272:1307–1312

    Article  CAS  PubMed  Google Scholar 

  • Frye CA, Reed TA (1998) Androgenic neurosteroids: anti-seizure effects in an animal model of epilepsy. Psychoneuroendocrinology 23:385–399

    Article  CAS  PubMed  Google Scholar 

  • Gluck MR, Jayatilleke E, Shaw S, Rowan AJ, Haroutunian V (2000) CNS oxidative stress associated with the kainic acid rodent model of experimental epilepsy. Epilepsy Res 39:63–71

    Article  CAS  PubMed  Google Scholar 

  • Goddard GV (1969) Analysis of avoidance conditioning following cholinergic stimulation of amygdala in rats. J Comp Physiol Psychol 68:1–18

    Article  CAS  PubMed  Google Scholar 

  • Grunberg NE, Winders SE, Wewers ME (1991) Gender differences in tobacco use. Health Psychol 10:143–153

    Article  CAS  PubMed  Google Scholar 

  • Grunberg NE, Berger SS, Starosciak A (2011) Tobacco use: Psychology, neurobiology, and clinical implications. In: Baum A, Revenson T, Singer JE (eds) Handbook of health psychology. Psychology Press, New York

    Google Scholar 

  • Gumustekin K, Altinkaynak K, Timur H, Taysi S, Oztasan N, Polat MF, Akcay F, Suleyman H, Dane S, Gul M (2003) Vitamin E but not Hippophea rhamnoides L. prevented nicotine-induced oxidative stress in rat brain. Hum Exp Toxicol 22:425–431

    CAS  PubMed  Google Scholar 

  • Gusakov I, Sharonov B, Oparina T, Kambarova D (1995) Effect of superoxide dismutase on convulsive seizures in rat models of epilepsy. Bull Exp Biol Med 120:665–667

    Article  Google Scholar 

  • Hamed SA, Abdellah MM, El-Melegy N (2004) Blood levels of trace elements, electrolytes, and oxidative stress/antioxidant systems in epileptic patients. J Pharmacol Sci 96:465–473

    Article  CAS  PubMed  Google Scholar 

  • Harrod SB, Mactutus CF, Bennett K, Hasselrot U, Wu G, Welch M, Booze RM (2004) Sex differences and repeated intravenous nicotine: behavioral sensitization and dopamine receptors. Pharmacol Biochem Behav 78:581–592

    Article  CAS  PubMed  Google Scholar 

  • Huong NT, Matsumoto K, Watanabe H (1998) The antistress effect of majonoside-R2, a major saponin component of Vietnamese ginseng: neuronal mechanisms of action. Methods Find Exp Clin Pharmacol 20:65–76

    Article  CAS  PubMed  Google Scholar 

  • Ilhan A, Aladag MA, Kocer A, Boluk A, Gurel A, Armutcu F (2005) Erdosteine ameliorates PTZ-induced oxidative stress in mice seizure model. Brain Res Bull 65:495–499

    Article  CAS  PubMed  Google Scholar 

  • Ishige K, Schubert D, Sagara Y (2001) Flavonoids protect neuronal cells from oxidative stress by three distinct mechanisms. Free Radic Biol Med 30:433–446

    Article  CAS  PubMed  Google Scholar 

  • Itzhak Y (1996) Attenuation of cocaine kindling by 7-nitroindazole, an inhibitor of brain nitric oxide synthase. Neuropharmacology 35:1065–1073

    Article  CAS  PubMed  Google Scholar 

  • Janáky R, Dohovics R, Saransaari P, Oja S (2007) Modulation of [3H] dopamine release by glutathione in mouse striatal slices. Neurochem Res 32:1357–1364

    Article  PubMed  Google Scholar 

  • Kovacic P, Cooksy A (2005) Iminium metabolite mechanism for nicotine toxicity and addiction: oxidative stress and electron transfer. Med Hypotheses 64:104–111

    Article  CAS  PubMed  Google Scholar 

  • Kumar P, Kale RK, McLean P, Baquer NZ (2011) Protective effects of 17 beta estradiol on altered age related neuronal parameters in female rat brain. Neurosci Lett 502:56–60

    Article  CAS  PubMed  Google Scholar 

  • Levin ED, Rezvani AH, Montoya D, Rose JE, Swartzwelder HS (2003) Adolescent-onset nicotine self-administration modeled in female rats. Psychopharmacology (Berl) 169:141–149

    Article  CAS  Google Scholar 

  • Levin ED, Slade S, Wells C, Cauley M, Petro A, Vendittelli A, Johnson M, Williams P, Horton K, Rezvani AH (2011) Threshold of adulthood for the onset of nicotine self-administration in male and female rats. Behav Brain Res 225:473–481

    Article  CAS  PubMed  Google Scholar 

  • Lin YT, Han YX, Xu JJ, Cao LL, Gao J, Xie NC, Zhao XH, Jiang H, Chi ZF (2010) Mitochondrial DNA damage and the involvement of antioxidant defense and repair system in hippocampi of rats with chronic seizures. Cell Mol Neurobiol 30:947–954

    Article  CAS  PubMed  Google Scholar 

  • McClernon FJ, Hiott FB, Westman EC, Rose JE, Levin ED (2006) Transdermal nicotine attenuates depression symptoms in nonsmokers: a double-blind, placebo-controlled trial. Psychopharmacology 189:125–133

    Article  CAS  PubMed  Google Scholar 

  • Meredith M (1998) Vomeronasal, olfactory, hormonal convergence in the brain. Cooperation or coincidence? Ann N Y Acad Sci 855:349–361

    Article  CAS  PubMed  Google Scholar 

  • Minozzi S, Amato L, Davoli M, Farrell M, Lima R, Pani PP, Silva DM, Soares B, Vecchi S (2008) Anticonvulsants for cocaine dependence. Cochrane Database Syst Rev 35:CD:006754

  • Mula M, Marotta AE, Monaco F (2010) Epilepsy and bipolar disorders. Expert Rev Neurother 10:13–23

    Article  PubMed  Google Scholar 

  • Nordberg A (1993) In-vivo detection of neurotransmitter changes in alzheimers disease. In: Nitsch RM et al (eds) Alzheimers disease: amyloid precusor proteins, signal transduction, and neuronal transplantation, vol 695. New York Acad Sciences, New York, pp 27–33

    Google Scholar 

  • Okamoto M, Kita T, Okuda H, Nakashima T (1992) Tolerance to the convulsions induced by daily nicotine treatment in rats. Jpn J Pharmacol 59:449–455

    Article  CAS  PubMed  Google Scholar 

  • Olfert ED, Cross BM, McWilliam AA (1993) Guide to the care and use of experimental animals. Canadian Council on Animal Care, Ontario Canada

    Google Scholar 

  • Ortiz GG, Sanchez-Ruiz MY, Tan DX, Reiter RJ, Benitez-King G, Beas-Zarate C (2001) Melatonin, vitamin E, and estrogen reduce damage induced by kainic acid in the hippocampus: potassium-stimulated GABA release. J Pineal Res 31:62–67

    Article  CAS  PubMed  Google Scholar 

  • Pappert EJ, Tangney CC, Goetz CG, Ling ZD, Lipton JW, Stebbins GT, Carvey PM (1996) Alpha-tocopherol in the ventricular cerebrospinal fluid of Parkinson's disease patients: dose-response study and correlations with plasma levels. Neurology 47:1037–1042

    Article  CAS  PubMed  Google Scholar 

  • Parameshwaran K, Buabeid MA, Karuppagounder SS, Uthayathas S, Thiruchelvam K, Shonesy B, Dityatev A, Escobar MC, Dhanasekaran M, Suppiramaniam V (2012) Developmental nicotine exposure induced alterations in behavior and glutamate receptor function in hippocampus. Cell Mol Life Sci 69:829–841

    Google Scholar 

  • Pauly JR (2008) Gender differences in tobacco smoking dynamics and the neuropharmacological actions of nicotine. Front Biosci 13:505–516

    Article  CAS  PubMed  Google Scholar 

  • Perkins KA (1999) Nicotine discrimination in men and women. Pharmacol Biochem Behav 64:295–299

    Article  CAS  PubMed  Google Scholar 

  • Pontieri FE, Tanda G, Orzi F, Di Chiara G (1996) Effects of nicotine on the nucleus accumbens and similarity to those of addictive drugs. Nature 382:255–257

    Article  CAS  PubMed  Google Scholar 

  • Post RM (2004) Neurobiology of seizures and behavioral abnormalities. Epilepsia 45:5–14

    Article  CAS  PubMed  Google Scholar 

  • Post RM (2007) Kindling and sensitization as models for affective episode recurrence, cyclicity, and tolerance phenomena. Neurosci Biobehav Rev 31:858–873

    Article  PubMed  Google Scholar 

  • Post RM, Weiss SRB (1992) Endogenous biochemical-abnormalities in affective-illness—therapeutic versus pathogenic. Biol Psychiatry 32:469–484

    Article  CAS  PubMed  Google Scholar 

  • Post RM, Weiss SRB, Smith M, Li H, McCann U (1997) Kindling versus quenching — implications for the evolution and treatment of posttraumatic stress disorder. In: Yehuda R, McFarlane AC (eds) Psychobiology of posttraumatic stress disorder, vol 821. New York Academy of Sciences, New York, pp 285–295

    Google Scholar 

  • Racine RJ, Gartner JG, Burnham WM (1972) Epileptiform activity and neural plasticity in limbic structures. Brain Res 47:262–268

    Article  CAS  PubMed  Google Scholar 

  • Rasheed N, Ahmad A, Al-Sheeha M, Alghasham A, Palit G (2011) Neuroprotective and anti-stress effect of A68930 in acute and chronic unpredictable stress model in rats. Neurosci Lett 504:151–155

    Article  CAS  PubMed  Google Scholar 

  • Rauca C, Wiswedel I, Zerbe R, Keilhoff G, Krug M (2004) The role of superoxide dismutase and alpha-tocopherol in the development of seizures and kindling induced by pentylenetetrazol — influence of the radical scavenger alpha-phenyl-N-tert-butyl nitrone. Brain Res 1009:203–212

    Article  CAS  PubMed  Google Scholar 

  • Reddy DS, Jian K (2010) The testosterone-derived neurosteroid androstanediol is a positive allosteric modulator of GABAA receptors. J Pharmacol Exp Ther 334:1031–1041

    Article  CAS  PubMed  Google Scholar 

  • Reichert VC, Seltzer V, Efferen LS, Kohn N (2009) Women and tobacco dependence. Obstet Gynecol Clin North Am 36:877–890, xi

    Article  PubMed  Google Scholar 

  • Riljak V, Milotova M, Jandova K, Pokorny J, Langmeier M (2007) Morphological changes in the hippocampus following nicotine and kainic acid administration. Physiol Res 56:641–649

    CAS  PubMed  Google Scholar 

  • Rosse RB, Mastropaolo J, Novitzki MR, Deutsch SI (1990) Depot testosterone attenuates the anticonvulsant effect of flurazepam in mice. Psychoneuroendocrinology 15:83–85

    Article  CAS  PubMed  Google Scholar 

  • Rubboli F, Court JA, Sala C, Morris C, Perry E, Clementi F (1994) Distribution of neuronal nicotinic receptor subunits in human brain. Neurochem Int 25:69–71

    Article  CAS  PubMed  Google Scholar 

  • Sashindranath M, McLean KJ, Trounce IA, Cotton RGH, Cook MJ (2010) Early hippocampal oxidative stress is a direct consequence of seizures in the rapid electrical amygdala kindling model. Epilepsy Res 90:285–294

    Article  CAS  PubMed  Google Scholar 

  • Sechi G, Rosati G, Deiana GA, Petruzzi V, Deriu F, Correddu P, De Riu PL (1997) Co-variation of free amino acids in brain interstitial fluid during pentylenetetrazole-induced convulsive status epilepticus. Brain Res 764:230–236

    Article  CAS  PubMed  Google Scholar 

  • Sedlak J, Hanus L (1982) Changes of glutathione and protein bound SH-groups concentration in rat adrenals under acute and repeated stress. Endocrinol Exp 16:103–109

    CAS  PubMed  Google Scholar 

  • Sejima H, Ito M, Kishi K, Tsuda H, Shiraishi H (1997) Regional excitatory and inhibitory amino acid concentrations in pentylenetetrazol kindling and kindled rat brain. Brain Dev 19:171–175

    Article  CAS  PubMed  Google Scholar 

  • Shandra AA, Mazarati AM, Godlevsky LS, Vastyanov RS (1996) Chemical kindling: implications for antiepileptic drugs — sensitive and resistant epilepsy models. Epilepsia 37:269–274

    Article  CAS  PubMed  Google Scholar 

  • Shin EJ, Jeong JH, Chung YH, Kim WK, Ko KH, Bach JH, Hong JS, Yoneda Y, Kim HC (2011) Role of oxidative stress in epileptic seizures. Neurochem Int 59:122–137

    Article  CAS  PubMed  Google Scholar 

  • Silverstein B, Feld S, Kozlowski LT (1980) The availability of low-nicotine cigarettes as a cause of cigarette-smoking among teenage females. J Health Soc Behav 21:383–388

    Article  CAS  PubMed  Google Scholar 

  • Singh R, Pathak DN (1990) Lipid-peroxidation and glutathione-peroxidase, glutathione-reductase, seperoxide-dismutase, catalase and glucose-6-phosphate-dehydrogenase activities in FeCl3-induced epileptogenic foci in the rat brain. Epilepsia 31:15–26

    Article  CAS  PubMed  Google Scholar 

  • Sleven H, Gibbs JE, Heales S, Thom M, Cock HR (2006) Depletion of reduced glutathione precedes inactivation of mitochondrial enzymes following limbic status epilepticus in the rat hippocampus. Neurochem Int 48:75–82

    Article  CAS  PubMed  Google Scholar 

  • Slotkin TA, Cousins MM, Seidler FJ (2004) Administration of nicotine to adolescent rats evokes regionally selective upregulation of CNS alpha 7 nicotinic acetylcholine receptors. Brain Res 1030:159–163

    Article  CAS  PubMed  Google Scholar 

  • Smith RF (2003) Animal models of periadolescent substance abuse. Neurotoxicol Teratol 25:291–301

    Article  CAS  PubMed  Google Scholar 

  • Sood N, Sahai AK, Medhi B, Chakrabarti A (2008) Dose-finding study with nicotine as a proconvulsant agent in PTZ-induced seizure model in mice. J Biomed Sci 15:755–765

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Colburn NH, Oberley LW (1993) Decreased expression of manganese superoxide dismutase mRNA and protein after immortalization and transformation of mouse liver cells. Oncol Res 5:127–132

    CAS  PubMed  Google Scholar 

  • Tchekalarova J, Sotiriou E, Angelatou F (2004) Down-regulation of dopamine D1 and D2 receptors in the basal ganglia of PTZ kindling model of epilepsy: effects of angiotensin IV. Brain Res 1024:159–166

    Article  CAS  PubMed  Google Scholar 

  • Tizabi Y, Hauser SR, Tyler KY, Getachew B, Madani R, Sharma Y, Manaye KF (2010) Effects of nicotine on depressive-like behavior and hippocampal volume of female WKY rats. Prog Neuropsychopharmacol Biol Psychiatry 34:62–69

    Article  CAS  PubMed  Google Scholar 

  • Trauth JA, Seidler FJ, Slotkin TA (2000) Persistent and delayed behavioral changes after nicotine treatment in adolescent rats. Brain Res 880:167–172

    Article  CAS  PubMed  Google Scholar 

  • USHHS (1988) The health consequences of smoking: nicotine addiction: a report of the Surgeon General: Center for Health Promotion and Education. Office on Smoking and Health

  • Waldbaum S, Liang LP, Patel M (2010) Persistent impairment of mitochondrial and tissue redox status during lithium-pilocarpine-induced epileptogenesis. J Neurochem 115:1172–1182

    Article  CAS  PubMed  Google Scholar 

  • Walker QD, Rooney MB, Wightman RM, Kuhn CM (2000) Dopamine release and uptake are greater in female than male rat striatum as measured by fast cyclic voltammetry. Neuroscience 95:1061–1070

    Article  CAS  PubMed  Google Scholar 

  • Wallace TL, Porter RH (2011) Targeting the nicotinic alpha7 acetylcholine receptor to enhance cognition in disease. Biochem Pharmacol 82:891–903

    Article  CAS  PubMed  Google Scholar 

  • Wang X-J, Zhang S, Yan Z-Q, Zhao Y-X, Zhou H-Y, Wang Y, Lu G-Q, Zhang J-D (2011) Impaired CD200–CD200R-mediated microglia silencing enhances midbrain dopaminergic neurodegeneration: roles of aging, superoxide, NADPH oxidase, and p38 MAPK. Free Radic Biol Med 50:1094–1106

    Article  CAS  PubMed  Google Scholar 

  • Wonnacott S, Soliakov L, Wilkie G, Redfern P, Marshall D (1996) Presynaptic nicotinic acetylcholine receptors in the brain. Drug Dev Res 38:149–159

    Article  CAS  Google Scholar 

  • Yang JL, Tadokoro T, Keijzers G, Mattson MP, Bohr VA (2010) Neurons efficiently repair glutamate-induced oxidative DNA damage by a process involving CREB-mediated up-regulation of apurinic endonuclease 1. J Biol Chem 285:28191–28199

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

Prof. Macêdo received a grant from the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq), Brazil, to support this research. Drs. Gomes and Oliveira are supported by doctoral scholarships from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Brazil. We thank Dr. James R. Pauly, University of Kentucky, for helpful input, Dr. Francisco Vagnaldo F. Jamacaru for valuable assistance with the statistical analysis and American Journal Experts for English editing service.

Disclosures

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Danielle S. Macêdo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gomes, P.X.L., de Oliveira, G.V., de Araújo, F.Y.R. et al. Differences in vulnerability to nicotine-induced kindling between female and male periadolescent rats. Psychopharmacology 225, 115–126 (2013). https://doi.org/10.1007/s00213-012-2799-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00213-012-2799-5

Keywords

Navigation