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Effects of acute stress on acquisition of nicotine conditioned place preference in adolescent rats: a role for corticotropin-releasing factor 1 receptors

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Abstract

Rationale

Studies indicate that adolescence is a time of increased sensitivity to the rewarding effects of nicotine, and that stress is associated with an increased risk for smoking initiation in this age group. It is possible that stress leads to increased nicotine use in adolescence by augmenting its rewarding properties. Corticotropin-releasing factor type 1 receptors (CRF-R1) mediate physiological and behavioral stress responses. They may also mediate stress-induced potentiation of activity in multiple neural substrates implicated in nicotine reward.

Objectives

The aim of the present study was to determine the effect of acute stressor exposure on single trial nicotine conditioned place preference (CPP) in adolescent male rats using a biased CPP procedure and the role of CRF-R1 in this effect.

Results

A single episode of intermittent footshock administered 24 h before the start of place conditioning dose-dependently facilitated acquisition of CPP to nicotine (0.2, 0.4, and 0.6 mg/kg). Pretreatment with CP-154,526 (20 mg/kg), a selective CRF-R1 antagonist, 30 min before footshock exposure significantly attenuated the effect of prior stress to facilitate nicotine CPP acquisition. CP-154,526 pretreatment had no effect in animals conditioned with a nicotine dose that produced CPP under non-stress conditions, suggesting a specific role for CRF-R1 following stress.

Conclusions

Taken together, the results suggest that during adolescence, nicotine reward is enhanced by recent stressor exposure in a manner that involves signaling at CRF-R1. Information from studies such as this may be used to inform efforts to prevent and treat adolescent nicotine dependence.

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References

  • Anstrom KK, Woodward DJ (2005) Restraint increases dopaminergic burst firing in awake rats. Neuropsychopharmacology 30:1832–1840

    Article  PubMed  CAS  Google Scholar 

  • Bakshi VP, Smith-Roe S, Newman SM, Grigoriadis DE, Kalin NH (2002) Reduction of stress-induced behavior by antagonism of corticotropin-releasing hormone 2 (CRH2) receptors in lateral septum or CRH1 receptors in amygdala. J Neurosci 22:2926–2935

    PubMed  CAS  Google Scholar 

  • Balfour DJ, Khullar AK, Longden A (1975) Effects of nicotine on plasma corticosterone and brain amines in stressed and unstressed rats. Pharmacol Biochem Behav 3:179–184

    Article  PubMed  CAS  Google Scholar 

  • Behan DP, De Souza EB, Lowry PJ, Potter E, Sawchenko P, Vale WW (1995) Corticotropin releasing factor (CRF) binding protein: a novel regulator of CRF and related peptides. Front Neuroendocrinol 16(4):362–382

    Article  PubMed  CAS  Google Scholar 

  • Belluzzi JD, Lee AG, Oliff HS, Leslie FM (2004) Age-dependent effects of nicotine on locomotor activity and conditioned place preference in rats. Psychopharmacology 174:389–395

    Article  PubMed  CAS  Google Scholar 

  • Blank T, Nijholt I, Eckart K, Spiess J (2002) Priming of long-term potentiation in mouse hippocampus by corticotropin-releasing factor and acute stress: implications for hippocampus-dependent learning. J Neurosci 22:3788–3794

    PubMed  CAS  Google Scholar 

  • Brielmaier JM, McDonald CG, Smith RF (2007) Immediate and long-term behavioral effects of a single nicotine injection in adolescent and adult rats. Neurotoxicol Teratol 29:74–80

    Article  PubMed  CAS  Google Scholar 

  • Brielmaier JM, McDonald CG, Smith RF (2008) Nicotine place preference in a biased conditioned place preference design. Pharmacol Biochem Behav 89:94–100

    Article  PubMed  CAS  Google Scholar 

  • Bruijnzeel AW, Prado M, Isaac S (2009) Corticotropin-releasing factor-1 receptor activation mediates nicotine withdrawal-induced deficit in brain reward function and stress-induced relapse. Biol Psychiatry 66:110–117

    Article  PubMed  CAS  Google Scholar 

  • Buczek Y, Lê AD, Wang A, Stewart J, Shaham Y (1999) Stress reinstates nicotine seeking but not sucrose solution seeking in rats. Psychopharmacology 144:183–188

    Article  PubMed  CAS  Google Scholar 

  • Capriles N, Cancela LM (1999) Effect of acute and chronic stress restraint on amphetamine-associated place preference: involvement of dopamine D(1) and D(2) receptors. Eur J Pharmacol 386(2–3):127–134

    Article  PubMed  CAS  Google Scholar 

  • Centers for Disease Control and Prevention. National Health Interview Survey, 2008. Available at http://www.cdc.gov/nchs/nhis.htm. Accessed 14 June 2010

  • Chalmers DT, Lovenberg TW, Grigoriadis DE, Behan DP, De Souza EB (1996) Corticotrophin-releasing factor receptors: from molecular biology to drug design. Trends Pharmacol Sci 17:166–172

    Article  PubMed  CAS  Google Scholar 

  • Cheeta S, Irvine EE, Tucci S, Sandhu J, File SE (2001) In adolescence, female rats are more sensitive to the anxiolytic effect of nicotine than are male rats. Neuropsychopharmacology 25:601–607

    Article  PubMed  CAS  Google Scholar 

  • Cordero MI, Venero C, Kruyt ND, Sandi C (2003) Prior exposure to a single stress session facilitates subsequent contextual fear conditioning in rats. Evidence for a role of corticosterone. Horm Behav 44:338–345

    Article  PubMed  CAS  Google Scholar 

  • Dai Z, Kang L, Wang L, Ma L (2006) Different roles of dopamine receptor subtypes in footshock stress-induced enhancement of morphine conditioned place preference. Neurosci Lett 409:52–56

    Article  PubMed  CAS  Google Scholar 

  • Deak T, Nguyen KT, Ehrlich AL, Watkins LR, Spencer RL, Maier SF, Licinio J, Wong ML, Chrousos GP, Webster E, Gold PW (1999) The impact of the nonpeptide corticotropin-releasing hormone antagonist antalarmin on behavioral and endocrine responses to stress. Endocrinology 140:79–86

    Article  PubMed  CAS  Google Scholar 

  • Der-Avakian A, Will MJ, Bland ST, Deak T, Nguyen KT, Schmid MJ, Spencer RL, Watkins LR, Maier SF (2005) Surgical and pharmacological suppression of glucocorticoids prevents the enhancement of morphine conditioned place preference by uncontrollable stress in rats. Psychopharmacology 179:409–417

    Article  PubMed  CAS  Google Scholar 

  • Der-Avakian A, Bland ST, Schimd MJ, Watkins L, Spencer RL, Maier SF (2006) The role of glucocorticoids in the uncontrollable stress-induced potentiation of nucleus accumbens shell dopamine and conditioned place preference responses to morphine. Psychoneuroendocrinology 31:653–663

    Article  PubMed  CAS  Google Scholar 

  • Der-Avakian A, Bland ST, Rozeske RR, Tamblyn JP, Hutchinson MR, Watkins L, Maier SF (2007) The effects of a single exposure to uncontrollable stress on the subsequent conditioned place preference responses to oxycodone, cocaine, and ethanol in rats. Psychopharmacology 191:909–917

    Article  PubMed  CAS  Google Scholar 

  • Deroche V, Piazza PV, Deminière JM, Le Moal M, Simon H (1993) Rats orally self-administer corticosterone. Brain Res 622(1–2):315–320

    Google Scholar 

  • Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85:5274–5278

    Article  PubMed  Google Scholar 

  • DiFranza JR, Savageau JA, Fletcher K, Pbert L, O'Loughlin J, McNeill AD, Ockene JK, Friedman K, Hazelton J, Wood C, Dussault G, Wellman RJ (2007) Susceptibility to nicotine dependence: the Development and Assessment of Nicotine Dependence in Youth 2 study. Pediatrics 120:e974–e983

    Article  PubMed  Google Scholar 

  • File SE, Kenny PJ, Ouagazzal AM (1998) Bimodal modulation by nicotine of anxiety in the social interaction test: role of the dorsal hippocampus. Behav Neurosci 112(6):1423–1429

    Article  PubMed  CAS  Google Scholar 

  • Goldman L, Winget C, Hollingshead GW, Levine S (1973) Postweaning development of negative feedback in the pituitary-adrenal system of the rat. Neuroendocrinology 12:199–211

    Article  PubMed  CAS  Google Scholar 

  • Grakalic I, Schindler CW, Baumann MH, Rice KC, Riley AL (2006) Effects of stress modulation on morphine-induced conditioned place preferences and plasma corticosterone levels in Fischer, Lewis, and Sprague–Dawley rat strains. Psychopharmacology 189:277–286

    Article  PubMed  CAS  Google Scholar 

  • Hikichi T, Akiyoshi J, Yamamoto Y, Tsutsumi T, Isogawa K, Nagayama H (2000) Suppression of conditioned fear by administration of CRF receptor antagonist CP-154,526. Pharmacopsychiatry 33:189–193

    Article  PubMed  CAS  Google Scholar 

  • Imperato A, Angelucci L, Casolini P, Zocchi A, Puglisi-Allegra S (1992) Repeated stressful experiences differently affect limbic dopamine release during and following stress. Brain Res 577:194–199

    Article  PubMed  CAS  Google Scholar 

  • Irvine EE, Cheeta S, File SE (1999) Time-course of changes in the social interaction test of anxiety following acute and chronic administration of nicotine. Behav Pharmacol 10:691–697

    Article  PubMed  CAS  Google Scholar 

  • Kalivas PW, Duffy P (1995) Selective activation of dopamine transmission in the shell of the nucleus accumbens by stress. Brain Res 675:325–328

    Article  PubMed  CAS  Google Scholar 

  • Kandel DB, Chen K (2000) Extent of smoking and nicotine dependence in the United States: 1991–1993. Nicotine Tob Res 2:263–274

    Article  PubMed  CAS  Google Scholar 

  • Kandel DB, Hu MC, Griesler PC, Schaffran C (2007) On the development of nicotine dependence in adolescence. Drug Alcohol Depend 91:26–39

    Article  PubMed  CAS  Google Scholar 

  • Kant GJ, Mougey EH, Pennington LL, Meyerhoff JL (1983) Graded footshock stress elevates pituitary cyclic AMP and plasma beta-endorphin, beta-LPH corticosterone and prolactin. Life Sci 33:2657–2663

    Article  PubMed  CAS  Google Scholar 

  • Keller C, Bruelisauer A, Lemaire M, Enz A (2002) Brain pharmacokinetics of a nonpeptidic corticotropin-releasing factor receptor antagonist. Drug Metab Dispos 30:173–176

    Article  PubMed  CAS  Google Scholar 

  • Koob GF, Heinrichs SC (1999) A role for corticotropin releasing factor and urocortin in behavioral responses to stressors. Brain Res 848:141–152

    Article  PubMed  CAS  Google Scholar 

  • Koval JJ, Pederson LL, Mills CA, McGrady GA, Carvajal SC (2000) Models of the relationship of stress, depression, and other psychosocial factors to smoking behavior: a comparison of a cohort of students in grades 6 and 8. Prev Med 30:463–477

    Article  PubMed  CAS  Google Scholar 

  • Kreibich AS, Briand L, Cleck JN, Ecke L, Rice KC, Blendy JA (2009) Stress-induced potentiation of cocaine reward: a role for CRF R1 and CREB. Neuropsychopharmacology 34:2609–2617

    Article  PubMed  CAS  Google Scholar 

  • Laviolette SR, Lauzon NM, Bishop SF, Sun N, Tan H (2008) Dopamine signaling through D1-like versus D2-like receptors in the nucleus accumbens core versus shell differentially modulates nicotine reward sensitivity. J Neurosci 28:8025–8033

    Article  PubMed  CAS  Google Scholar 

  • Leão RM, Cruz FC, Planeta CS (2009) Exposure to acute restraint stress reinstates nicotine-induced place preference in rats. Behav Pharmacol 20:109–113

    Article  PubMed  Google Scholar 

  • Matsuzawa S, Suzuki T, Misawa M (1998a) Conditioned fear stress induces ethanol-associated place preference in rats. Eur J Pharmacol 341:127–130

    Article  PubMed  CAS  Google Scholar 

  • Matsuzawa S, Suzuki T, Misawa M, Nagase H (1998b) Involvement of mu- and delta-opioid receptors in the ethanol-associated place preference in rats exposed to foot shock stress. Brain Res 803:169–177

    Article  PubMed  CAS  Google Scholar 

  • McKenzie M, Olsson CA, Jorm AF, Romaniuk H, Patton GC (2010) Association of adolescent symptoms of depression and anxiety with daily smoking and nicotine dependence in young adulthood: findings from a 10-year longitudinal study. Addiction 105:1652–1659

    Article  PubMed  Google Scholar 

  • Merchenthaler I, Vigh S, Petrusz P, Schally AV (1982) Immunocytochemical localization of corticotropin-releasing factor (CRF) in the rat brain. Am J Anat 165:385–396

    Article  PubMed  CAS  Google Scholar 

  • National Center for Health Statistics (2004) Health, United States, 2004. National Center for Health Statistics, Hyattsville

    Google Scholar 

  • National Research Council (1996) Guide for the care and use of laboratory animals. National Academy Press, Washington, D.C.

  • Niehaus JL, Murali M, Kauer JA (2010) Drugs of abuse and stress impair LTP at inhibitory synapses in the ventral tegmental area. Eur J Neurosci 32:108–117

    Article  PubMed  Google Scholar 

  • Peciña S, Schulkin J, Berridge KC (2006) Nucleus accumbens corticotropin-releasing factor increases cue-triggered motivation for sucrose reward: paradoxical positive incentive effects in stress? BMC Biol 4:8

    Google Scholar 

  • Piazza PV, Deroche V, Deminière JM, Maccari S, Le Moal M, Simon H (1993) Corticosterone in the range of stress-induced levels possesses reinforcing properties: implications for sensation-seeking behaviors. Proc Natl Acad Sci USA 90(24):11738–11742

    Google Scholar 

  • Potter E, Sutton S, Donaldson C, Chen R, Perrin M, Lewis K, Sawchenko PE, Vale W (1994) Distribution of corticotropin-releasing factor receptor mRNA expression in the rat brain and pituitary. Proc Natl Acad Sci USA 91:8777–8781

    Article  PubMed  CAS  Google Scholar 

  • Puglisi-Allegra S, Imperato A, Angelucci L, Cabib S (1991) Acute stress induces time-dependent responses in dopamine mesolimbic system. Brain Res 554:217–222

    Article  PubMed  CAS  Google Scholar 

  • Radulovic J, Rühmann A, Liepold T, Spiess J (1999) Modulation of learning and anxiety by corticotropin-releasing factor (CRF) and stress: differential roles of CRF receptors 1 and 2. J Neurosci 19:5016–5025

    PubMed  CAS  Google Scholar 

  • Rao U, Hammen CL, London ED, Poland RE (2009) Contribution of hypothalamic-pituitary-adrenal activity and environmental stress to vulnerability for smoking in adolescents. Neuropsychopharmacology 34:2721–2732

    Article  PubMed  Google Scholar 

  • Rodaros D, Caruana DA, Amir S, Stewart J (2007) Corticotropin-releasing factor projections from limbic forebrain and paraventricular nucleus of the hypothalamus to the region of the ventral tegmental area. Neuroscience 150:8–13

    Article  PubMed  CAS  Google Scholar 

  • Rodríguez Manzanares PA, Isoardi NA, Carrer HF, Molina VA (2005) Previous stress facilitates fear memory, attenuates GABAergic inhibition, and increases synaptic plasticity in the rat basolateral amygdala. J Neurosci 25:8725–8734

    Article  PubMed  Google Scholar 

  • Romeo RD, Lee SJ, Chhua N, McPherson CR, McEwen BS (2004a) Testosterone cannot activate an adult-like stress response in prepubertal male rats. Neuroendocrinology 79:125–132

    Article  PubMed  CAS  Google Scholar 

  • Romeo RD, Lee SJ, McEwen BS (2004b) Differential stress reactivity in intact and ovariectomized prepubertal and adult female rats. Neuroendocrinology 80(6):387–393

    Article  PubMed  CAS  Google Scholar 

  • Saal D, Dong Y, Bonci A, Malenka RC (2003) Drugs of abuse and stress trigger a common synaptic adaptation in dopamine neurons. Neuron 37:577–582

    Article  PubMed  CAS  Google Scholar 

  • Sandi C, Pinelo-Nava MT (2007) Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast 2007:78970

    Article  PubMed  Google Scholar 

  • Sauvage M, Steckler T (2001) Detection of corticotropin-releasing hormone receptor 1 immunoreactivity in cholinergic, dopaminergic and noradrenergic neurons of the murine basal forebrain and brainstem nuclei—potential implication for arousal and attention. Neuroscience 104:643–652

    Article  PubMed  CAS  Google Scholar 

  • Sawchenko PE, Imaki T, Potter E, Kovacs K, Imaki J, Vale W (1993) The functional neuroanatomy of corticotropin-releasing factor. Ciba Found Symp 172:5–21, discussion 21–29

    PubMed  CAS  Google Scholar 

  • Schulz DW, Mansbach RS, Sprouse J, Braselton JP, Collins J, Corman M, Dunaiskis A, Faraci S, Schmidt AW, Seeger T, Seymour P, Tingley FD 3rd, Winston EN, Chen YL, Heym J (1996) CP-154,526: a potent and selective nonpeptide antagonist of corticotropin releasing factor receptors. Proc Natl Acad Sci USA 93(19):10477–10482

    Article  PubMed  CAS  Google Scholar 

  • Sellings LH, Baharnouri G, McQuade LE, Clarke PB (2008) Rewarding and aversive effects of nicotine are segregated within the nucleus accumbens. Eur J Neurosci 28:342–352

    Article  PubMed  Google Scholar 

  • Shors TJ (2004) Learning during stressful times. Learn Mem 11:137–144

    Article  PubMed  Google Scholar 

  • Shram MJ, Lê AD (2010) Adolescent male Wistar rats are more responsive than adult rats to the conditioned rewarding effects of intravenously administered nicotine in the place conditioning procedure. Behav Brain Res 206:240–244

    Article  PubMed  CAS  Google Scholar 

  • Smagin GN, Heinrichs SC, Dunn AJ (2001) The role of CRH in behavioral responses to stress. Peptides 22:713–724

    Article  PubMed  CAS  Google Scholar 

  • Smith SM, Vale WW (2006) The role of the hypothalamic-pituitary-adrenal axis in neuroendocrine responses to stress. Dialogues Clin Neurosci 8:383–395

    PubMed  Google Scholar 

  • Spear LP (2000) The adolescent brain and age-related behavioral manifestations. Neurosci Biobehav Rev 24:417–463

    Article  PubMed  CAS  Google Scholar 

  • Spina L, Fenu S, Longoni R, Rivas E, Di Chiara G (2006) Nicotine-conditioned single-trial place preference: selective role of nucleus accumbens shell dopamine D1 receptors in acquisition. Psychopharmacology 184:447–455

    Article  PubMed  CAS  Google Scholar 

  • Stam R, Bruijnzeel AW, Wiegant VM (2000) Long-lasting stress sensitisation. Eur J Pharmacol 405:217–224

    Article  PubMed  CAS  Google Scholar 

  • Stone EA, Quartermain D (1997) Greater behavioral effects of stress in immature as compared to mature male mice. Physiol Behav 63:143–145

    Article  PubMed  CAS  Google Scholar 

  • Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165–186

    Article  PubMed  CAS  Google Scholar 

  • Thiel KJ, Sanabria F, Neisewander JL (2009) Synergistic interaction between nicotine and social rewards in adolescent male rats. Psychopharmacology 204(3):391–402

    Article  PubMed  CAS  Google Scholar 

  • Torres OV, Tejeda HA, Natividad LA, O'Dell LE (2008) Enhanced vulnerability to the rewarding effects of nicotine during the adolescent period of development. Pharmacol Biochem Behav 90(4):658–663

    Article  PubMed  CAS  Google Scholar 

  • Van Dijken HH, Van der Heyden JA, Mos J, Tilders FJ (1992a) Inescapable footshocks induce progressive and long-lasting behavioural changes in male rats. Physiol Behav 51:787–794

    Article  PubMed  Google Scholar 

  • Van Dijken HH, Mos J, van der Heyden JA, Tilders FJ (1992b) Characterization of stress-induced long-term behavioural changes in rats: evidence in favor of anxiety. Physiol Behav 52:945–951

    Article  PubMed  Google Scholar 

  • Van Pett K, Viau V, Bittencourt JC, Chan RK, Li HY, Arias C, Prins GS, Perrin M, Vale W, Sawchenko PE (2000) Distribution of mRNAs encoding CRF receptors in brain and pituitary of rat and mouse. J Comp Neurol 428:191–212

    Article  PubMed  Google Scholar 

  • Vazquez DM, Akil H (1993) Pituitary-adrenal response to ether vapor in the weanling animal: characterization of the inhibitory effect of glucocorticoids on adrenocorticotropin secretion. Pediatr Res 34:646–653

    PubMed  CAS  Google Scholar 

  • Wanat MJ, Hopf FW, Stuber GD, Phillips PE, Bonci A (2008) Corticotropin-releasing factor increases mouse ventral tegmental area dopamine neuron firing through a protein kinase C-dependent enhancement of Ih. J Physiol 586:2157–2170

    Article  PubMed  CAS  Google Scholar 

  • Wang B, Shaham Y, Zitzman D, Azari S, Wise RA, You ZB (2005) Cocaine experience establishes control of midbrain glutamate and dopamine by corticotropin-releasing factor: a role in stress-induced relapse to drug seeking. J Neurosci 25:5389–5396

    Article  PubMed  CAS  Google Scholar 

  • Will MJ, Watkins LR, Maier SF (1998) Uncontrollable stress potentiates morphine's rewarding properties. Pharmacol Biochem Behav 60:655–664

    Article  PubMed  CAS  Google Scholar 

  • Wise RA (2002) Brain reward circuitry: insights from unsensed incentives. Neuron 36(2):229–240

    Google Scholar 

  • Zislis G, Desai TV, Prado M, Shah HP, Bruijnzeel AW (2007) Effects of the CRF receptor antagonist D-Phe CRF(12–41) and the alpha2-adrenergic receptor agonist clonidine on stress-induced reinstatement of nicotine-seeking behavior in rats. Neuropharmacology 53:958–966

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Department of Psychology, George Mason University, Fairfax, VA, 22030, USA

    Jennifer Brielmaier, Craig G. McDonald & Robert F. Smith

  2. Laboratory of Behavioral Neuroscience, Intramural Research Program, National Institute of Mental Health, Porter Neuroscience Research Center Building 35 Room 1 C909, MSC 3730, Bethesda, MD, 20892, USA

    Jennifer Brielmaier

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  1. Jennifer Brielmaier
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  2. Craig G. McDonald
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  3. Robert F. Smith
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Correspondence to Jennifer Brielmaier.

Additional information

This research was supported by a grant from the Virginia Foundation for Healthy Youth to R.F. Smith and a grant from the American Psychological Association to J. Brielmaier. CP-154,526 was generously donated by Pfizer. The authors certify that they have no actual or potential conflicts of interest in relation to this article, nor do they have a financial relationship with either of the organizations that sponsored the research. The authors have full control of all primary data and agree to allow the journal to review the data if requested. The authors thank Drs. Theodore Dumas and Katherine McKnight for their valuable advice.

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Brielmaier, J., McDonald, C.G. & Smith, R.F. Effects of acute stress on acquisition of nicotine conditioned place preference in adolescent rats: a role for corticotropin-releasing factor 1 receptors. Psychopharmacology 219, 73–82 (2012). https://doi.org/10.1007/s00213-011-2378-1

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