Effects of Maternal Separation on Nicotine-Induced Conditioned Place Preference and Later Spatial Learning and Memory Function in Adolescent Male Rats

Fatemeh Delavari, Vahid Sheibani, Khadijeh Esmaeilpour, Saeid Esmaeili-Mahani, Nouzar Nakhaee

Abstract


Background: Disturbances in maternal care have been associated with increased risk for drug abuse later in life. However, there has been little investigation of the effects of maternal separation (MS), a model of early life stress, on nicotine dependence, specifically during adolescence. In the present study, we aimed to investigate the effect of MS on nicotine-conditioned place preference (CPP) in adolescent male rats. We also examined the impact of nicotine on spatial learning and memory impairments induced by MS.

Methods: Rat pups were exposed to daily MS for 15 (MS15) or 180 (MS180) minutes during the first 2 weeks of life or reared under normal animal facility rearing (AFR) conditions. In postnatal day (PND) 28-34, they were conditioned with nicotine [0.6 mg/kg, subcutaneously (SC)] or saline and tested for preference over a period of 6 conditioning trials. Morris water maze (MWM) testing was performed to assess spatial cognitive function.

Findings: The MS procedure used in our study failed to affect nicotine reward as measured by CPP in the adolescent male rats. Notably, significant spatial learning deficit was seen in the MS180 rats compared to those in the AFR and MS15 groups and nicotine administration modified the MS-induced learning defect in adolescent male rats.

Conclusion: In conclusion, although MS revealed no influence on the sensitivity to the nicotine's reinforcing effects in adolescent male rats, the simultaneous effect of MS on learning performance may be altered by nicotine intake.


Keywords


Separation; Nicotine; Spatial learning; Spatial memory; Rats

Full Text:

PDF

References


Nishi M, Horii-Hayashi N, Sasagawa T, Matsunaga W. Effects of early life stress on brain activity: Implications from maternal separation model in rodents. Gen Comp Endocrinol 2013; 181: 306-9.

Meaney MJ. Maternal care, gene expression, and the transmission of individual differences in stress reactivity across generations. Annu Rev Neurosci 2001; 24: 1161-92.

Ladd CO, Huot RL, Thrivikraman KV, Nemeroff CB, Meaney MJ, Plotsky PM. Long-term behavioral and neuroendocrine adaptations to adverse early experience. Prog Brain Res 2000; 122: 81-103.

Li M, Xue X, Shao S, Shao F, Wang W. Cognitive, emotional and neurochemical effects of repeated maternal separation in adolescent rats. Brain Res 2013; 1518: 82-90.

Hall FS, Wilkinson LS, Humby T, Robbins TW. Maternal deprivation of neonatal rats produces enduring changes in dopamine function. Synapse 1999; 32(1): 37-43.

Gordon HW. Early environmental stress and biological vulnerability to drug abuse. Psychoneuroendocrinology 2002; 27(1-2): 115-26.

Sinha R. How does stress increase risk of drug abuse and relapse? Psychopharmacology (Berl) 2001; 158(4): 343-59.

Delavari F, Sheibani V, Esmaeili-Mahani S, Nakhaee N. Maternal separation and the risk of drug abuse in later life. Addict Health 2016; 8(2): 107-14.

Spear LP. The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 2000; 24(4): 417-63.

Cohen A, George O. Animal models of nicotine exposure: Relevance to second-hand smoking, electronic cigarette use, and compulsive smoking. Front Psychiatry 2013; 4: 41.

Rezvani AH, Levin ED. Cognitive effects of nicotine. Biol Psychiatry 2001; 49(3): 258-67.

Andersen SL, Lyss PJ, Dumont NL, Teicher MH. Enduring neurochemical effects of early maternal separation on limbic structures. Ann N Y Acad Sci 1999; 877: 756-9.

Weiss IC, Domeney AM, Heidbreder CA, Moreau JL, Feldon J. Early social isolation, but not maternal separation, affects behavioral sensitization to amphetamine in male and female adult rats. Pharmacol Biochem Behav 2001; 70(2-3): 397-409.

Watterson E, Daniels CW, Watterson LR, Mazur GJ, Brackney RJ, Olive MF, et al. Nicotine-induced place conditioning and locomotor activity in an adolescent animal model of attention deficit/hyperactivity disorder (ADHD). Behav Brain Res 2015; 291: 184-8.

Vastola BJ, Douglas LA, Varlinskaya EI, Spear LP. Nicotine-induced conditioned place preference in adolescent and adult rats. Physiol Behav 2002; 77(1): 107-14.

Hashemizadeh S, Sardari M, Rezayof A. Basolateral amygdala CB1 cannabinoid receptors mediate nicotine-induced place preference. Prog Neuropsychopharmacol Biol Psychiatry 2014; 51: 65-71.

Hajali V, Sheibani V, Esmaeili-Mahani S, Shabani M. Female rats are more susceptible to the deleterious effects of paradoxical sleep deprivation on cognitive performance. Behav Brain Res 2012; 228(2): 311-8.

Crews F, He J, Hodge C. Adolescent cortical development: A critical period of vulnerability for addiction. Pharmacol Biochem Behav 2007; 86(2): 189-99.

Adriani W, Chiarotti F, Laviola G. Elevated novelty seeking and peculiar d-amphetamine sensitization in periadolescent mice compared with adult mice. Behav Neurosci 1998; 112(5): 1152-66.

Martini M, Valverde O. A single episode of maternal deprivation impairs the motivation for cocaine in adolescent mice. Psychopharmacology (Berl) 2012; 219(1): 149-58.

Ruedi-Bettschen D, Pedersen EM, Feldon J, Pryce CR. Early deprivation under specific conditions leads to reduced interest in reward in adulthood in Wistar rats. Behav Brain Res 2005; 156(2): 297-310.

Lehmann J, Pryce CR, Bettschen D, Feldon J. The maternal separation paradigm and adult emotionality and cognition in male and female Wistar rats. Pharmacol Biochem Behav 1999; 64(4): 705-15.

Oitzl MS, Workel JO, Fluttert M, Frosch F, De Kloet ER. Maternal deprivation affects behaviour from youth to senescence: Amplification of individual differences in spatial learning and memory in senescent Brown Norway rats. Eur J Neurosci 2000; 12(10): 3771-80.

Garner B, Wood SJ, Pantelis C, van den Buuse M. Early maternal deprivation reduces prepulse inhibition and impairs spatial learning ability in adulthood: No further effect of post-pubertal chronic corticosterone treatment. Behav Brain Res 2007; 176(2): 323-32.

Roceri M, Hendriks W, Racagni G, Ellenbroek BA, Riva MA. Early maternal deprivation reduces the expression of BDNF and NMDA receptor subunits in rat hippocampus. Mol Psychiatry 2002; 7(6): 609-16.

Aisa B, Elizalde N, Tordera R, Lasheras B, Del Rio J, Ramirez MJ. Effects of neonatal stress on markers of synaptic plasticity in the hippocampus: implications for spatial memory. Hippocampus 2009; 19(12): 1222-31.

Hui JJ, Zhang ZJ, Liu SS, Xi GJ, Zhang XR, Teng GJ, et al. Hippocampal neurochemistry is involved in the behavioural effects of neonatal maternal separation and their reversal by post-weaning environmental enrichment: A magnetic resonance study. Behav Brain Res 2011; 217(1): 122-7.

Levin ED, Torry D. Acute and chronic nicotine effects on working memory in aged rats. Psychopharmacology (Berl) 1996; 123(1): 88-97.

Brioni JD, Arneric SP. Nicotinic receptor agonists facilitate retention of avoidance training: Participation of dopaminergic mechanisms. Behav Neural Biol 1993; 59(1): 57-62.

Yamada K, Furukawa S, Iwasaki T, Ichitani Y. Nicotine improves AF64A-induced spatial memory deficits in Morris water maze in rats. Neurosci Lett 2010; 469(1): 88-92.

Socci DJ, Sanberg PR, Arendash GW. Nicotine enhances Morris water maze performance of young and aged rats. Neurobiol Aging 1995; 16(5): 857-60.

Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA. Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 1996; 383(6602): 713-6.

Hamid S, Dawe GS, Gray JA, Stephenson JD. Nicotine induces long-lasting potentiation in the dentate gyrus of nicotine-primed rats. Neurosci Res 1997; 29(1): 81-5.




DOI: http://dx.doi.org/10.22122/ahj.v8i4.436

Refbacks

  • There are currently no refbacks.