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The role of conditioning history and reinforcer strength in the reinforcement enhancing effects of nicotine in rats

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Abstract

Rationale

Nicotine (NIC) administration can increase behaviors that result in delivery of non-drug reinforcers (e.g., salient sensory stimuli). However, little is known about the circumstances under which NIC increases these behaviors.

Objective

The present studies sought to extend the reinforcement enhancing effects of NIC to sucrose rewards for which intensity could be systematically manipulated.

Method

In Experiment 1, rats were trained to respond for sucrose (30% w/v) on a progressive ratio (PR) schedule of reinforcement and were pretreated with NIC (0.4 mg/kg free-base) or physiological saline (SAL). The intensity of the sucrose reward was manipulated over subsequent testing sessions (0–60% w/v). Similar procedures were used in Experiment 2; however, each subject received only one sucrose concentration (0–20%) to control for conditioning history. In Experiment 3, a fixed ratio 3 (FR3) schedule of reinforcement was used to investigate putative activating effects of NIC. Experiment 4 investigated whether NIC pretreatment would reduce sucrose intake in limited-access drinks.

Results

In Experiment 1, NIC increased the motivation to obtain all sucrose concentrations, including water. However, when conditioning history was controlled (Experiment 2) the reinforcement enhancing effects of NIC were systematically related to the strength of the reinforcer. In Experiment 3, NIC neither increased nor decreased responding for sucrose. In Experiment 4, NIC reduced sucrose intake, but only at concentrations that resulted in peak drink volumes (5–20%).

Conclusion

The results suggest that the reinforcement enhancing effects of NIC depend on conditioning history and do not appear to be the result of simple behavioral activation.

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References

  • Arregui-Aguirre A, Claro-Izaguirre F, Goni-Garrido MJ, Zarate-Oleaga JA, Morgado-Bernal I (1987) Effects of acute nicotine and ethanol on medial prefrontal cortex self-stimulation in rats. Pharmacol Biochem Behav 27:15–20

    Article  PubMed  CAS  Google Scholar 

  • Avena NM, Bocarsly ME, Rada P, Kim A, Hoebel BG (2008a) After daily bingeing on a sucrose solution, food deprivation induces anxiety and accumbens dopamine/acetylcholine imbalance. Physiol Behav 94:309–315

    Article  PubMed  CAS  Google Scholar 

  • Avena NM, Rada P, Hoebel BG (2008b) Underweight rats have enhanced dopamine release and blunted acetylcholine response in the nucleus accumbens while bingeing on sucrose. Neuroscience 156:865–871

    Article  PubMed  CAS  Google Scholar 

  • Balfour DJ, Wright AE, Benwell ME, Birrell CE (2000) The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence. Behav Brain Res 113:73–83

    Article  PubMed  CAS  Google Scholar 

  • Bauco P, Wise RA (1994) Potentiation of lateral hypothalamic and midline mesencephalic brain stimulation reinforcement by nicotine: examination of repeated treatment. J Pharmacol Exp Ther 271:294–301

    PubMed  CAS  Google Scholar 

  • Blackburn JR, Phillips AG, Fibiger HC (1987) Dopamine and preparatory behavior: I. Effects of pimozide. Behav Neurosci 101:352–360

    Article  PubMed  CAS  Google Scholar 

  • Blackburn JR, Phillips AG, Fibiger HC (1989a) Dopamine and preparatory behavior: III. Effects of metoclopramide and thioridazine. Behav Neurosci 103:903–906

    Article  PubMed  CAS  Google Scholar 

  • Blackburn JR, Phillips AG, Jakubovic A, Fibiger HC (1989b) Dopamine and preparatory behavior: II. A neurochemical analysis. Behav Neurosci 103:15–23

    Article  PubMed  CAS  Google Scholar 

  • Caggiula AR, Donny EC, Palmatier MI, Liu X, Chaudhri N, Sved AF (2009) The role of nicotine in smoking: a dual-reinforcement model. Nebr Symp Motiv 55:91–109

    PubMed  Google Scholar 

  • Caggiula AR, Epstein LH, Antelman SM, Saylor SS, Perkins KA, Knopf S, Stiller R (1991) Conditioned tolerance to the anorectic and corticosterone-elevating effects of nicotine. Pharmacol Biochem Behav 40:53–59

    Article  PubMed  CAS  Google Scholar 

  • Chaudhri N, Caggiula AR, Donny EC, Booth S, Gharib M, Craven L, Palmatier MI, Liu X, Sved AF (2006a) Operant responding for conditioned and unconditioned reinforcers in rats is differentially enhanced by the primary reinforcing and reinforcement-enhancing effects of nicotine. Psychopharmacology (Berl) 189:27–36

    Article  CAS  Google Scholar 

  • Chaudhri N, Caggiula AR, Donny EC, Booth S, Gharib M, Craven L, Palmatier MI, Liu X, Sved AF (2007) Self-administered and noncontingent nicotine enhance reinforced operant responding in rats: impact of nicotine dose and reinforcement schedule. Psychopharmacology (Berl) 190:353–362

    Article  CAS  Google Scholar 

  • Chaudhri N, Caggiula AR, Donny EC, Palmatier MI, Liu X, Sved AF (2006b) Complex interactions between nicotine and nonpharmacological stimuli reveal multiple roles for nicotine in reinforcement. Psychopharmacology 184:353–366

    Article  PubMed  CAS  Google Scholar 

  • Corrigall WA, Coen KM, Adamson KL (1994) Self-administered nicotine activates the mesolimbic dopamine system through the ventral tegmental area. Brain Res 653:278–284

    Article  PubMed  CAS  Google Scholar 

  • Corrigall WA, Coen KM, Adamson KL, Chow BL, Zhang J (2000) Response of nicotine self-administration in the rat to manipulations of mu-opioid and gamma-aminobutyric acid receptors in the ventral tegmental area. Psychopharmacology (Berl) 149:107–114

    Article  CAS  Google Scholar 

  • Donny EC, Chaudhri N, Caggiula AR, Evans-Martin FF, Booth S, Gharib MA, Clements LA, Sved AF (2003) Operant responding for a visual reinforcer in rats is enhanced by noncontingent nicotine: implications for nicotine self-administration and reinforcement. Psychopharmacology 169:68–76

    Article  PubMed  CAS  Google Scholar 

  • Frenk H, Dar R (2004) Reward potentiation or behavioral activation? A comment on Donny et al. Psychopharmacology 171:472–473

    Article  PubMed  CAS  Google Scholar 

  • Grimm JW, Harkness JH, Ratliff C, Barnes J, North K, Collins S (2011) Effects of systemic or nucleus accumbens-directed dopamine D1 receptor antagonism on sucrose seeking in rats. Psychopharmacology (Berl)

  • Harrison AA, Gasparini F, Markou A (2002) Nicotine potentiation of brain stimulation reward reversed by DH beta E and SCH 23390, but not by eticlopride, LY 314582 or MPEP in rats. Psychopharmacology 160:56–66

    Article  PubMed  CAS  Google Scholar 

  • Hodos W (1961) Progressive ratio as a measure of reward strength. Science 134:943–944

    Article  PubMed  CAS  Google Scholar 

  • Kenny PJ, Chartoff E, Roberto M, Carlezon WA Jr, Markou A (2009) NMDA receptors regulate nicotine-enhanced brain reward function and intravenous nicotine self-administration: role of the ventral tegmental area and central nucleus of the amygdala. Neuropsychopharmacology 34:266–281

    Article  PubMed  CAS  Google Scholar 

  • Konorski J (1967) Integrative activity of the brain; an interdisciplinary approach. University of Chicago Press, University of Chicago Press

  • Liu X, Palmatier MI, Caggiula AR, Donny EC, Booth S, Gharib M, Craven L, Sved AF (2007) Cholinergic substrates of the reinforcement enhancing effects of nicotine. Psychopharmacology Submitted

  • Olausson P, Jentsch JD, Taylor JR (2003) Repeated nicotine exposure enhances reward-related learning in the rat. Neuropsychopharmacology 28:1264–1271

    Article  PubMed  CAS  Google Scholar 

  • Olausson P, Jentsch JD, Taylor JR (2004a) Nicotine enhances responding with conditioned reinforcement. Psychopharmacology 171:173–178

    Article  PubMed  CAS  Google Scholar 

  • Olausson P, Jentsch JD, Taylor JR (2004b) Repeated nicotine exposure enhances responding with conditioned reinforcement. Psychopharmacology 173:98–104

    Article  PubMed  CAS  Google Scholar 

  • Palmatier MI, Coddington SB, Liu X, Donny EC, Caggiula AR, Sved AF (2008) The motivation to obtain nicotine-conditioned reinforcers depends on nicotine dose. Neuropharmacology

  • Palmatier MI, Evans-Martin FF, Hoffman A, Caggiula AR, Chaudhri N, Donny EC, Liu X, Booth S, Gharib M, Craven L, Sved AF (2006) Dissociating the primary reinforcing and reinforcement-enhancing effects of nicotine using a rat self-administration paradigm with concurrently available drug and environmental reinforcers. Psychopharmacology (Berl) 184:391–400

    Article  CAS  Google Scholar 

  • Palmatier MI, Levin ME, Mays KL, Donny EC, Caggiula AR, Sved AF (2009) Bupropion and nicotine enhance responding for nondrug reinforcers via dissociable pharmacological mechanisms in rats. Psychopharmacology (Berl) 207:381–390

    Article  CAS  Google Scholar 

  • Palmatier MI, Liu X, Caggiula AR, Donny EC, Sved AF (2007a) The role of nicotinic acetylcholine receptors in the primary reinforcing and reinforcement-enhancing effects of nicotine. Neuropsychopharmacology 32:1098–1108

    Article  PubMed  CAS  Google Scholar 

  • Palmatier MI, Liu X, Matteson GL, Donny EC, Caggiula AR, Sved AF (2007b) Conditioned reinforcement in rats established with self-administered nicotine and enhanced by noncontingent nicotine. Psychopharmacology 195:235–243

    Article  PubMed  CAS  Google Scholar 

  • Palmatier MI, Matteson GL, Black JJ, Liu X, Caggiula AR, Craven L, Donny EC, Sved AF (2007c) The reinforcement enhancing effects of nicotine depend on the incentive value of non-drug reinforcers and increase with repeated drug injections. Drug Alcohol Depend

  • Parker LA, Doucet K (1995) The effects of nicotine and nicotine withdrawal on taste reactivity. Pharmacol Biochem Behav 52:125–129

    Article  PubMed  CAS  Google Scholar 

  • Paterson NE, Balfour DJ, Markou A (2008) Chronic bupropion differentially alters the reinforcing, reward-enhancing and conditioned motivational properties of nicotine in rats. Nicotine Tob Res 10:995–1008

    Article  PubMed  CAS  Google Scholar 

  • Perkins KA, Epstein LH, Grobe J, Fonte C (1994) Tobacco abstinence, smoking cues, and the reinforcing value of smoking. Pharmacol Biochem Behav 47:107–112

    Article  PubMed  CAS  Google Scholar 

  • Rauhut AS, Fenton L, Bardo MT (2010) Renewal of sucrose-seeking behavior in rats: role of D(2) dopamine receptors. Pharmacol Biochem Behav 96:354–362

    Article  PubMed  CAS  Google Scholar 

  • Reilly S (1999) Reinforcement value of gustatory stimuli determined by progressive ratio performance. Pharmacol Biochem Behav 63:301–311

    Article  PubMed  CAS  Google Scholar 

  • Reilly S, Trifunovic R (1999) Progressive ratio performance in rats with gustatory thalamus lesions. Behav Neurosci 113:1008–1019

    Article  PubMed  CAS  Google Scholar 

  • Richardson NR, Roberts DC (1996) Progressive ratio schedules in drug self-administration studies in rats: a method to evaluate reinforcing efficacy. J Neurosci Meth 66:1–11

    Article  CAS  Google Scholar 

  • Robinson TE, Berridge KC (1993) The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 18:247–291

    Article  PubMed  CAS  Google Scholar 

  • Robinson TE, Flagel SB (2009) Dissociating the predictive and incentive motivational properties of reward-related cues through the study of individual differences. Biol Psychiatr 65:869–873

    Article  Google Scholar 

  • Rose JE (2006) Nicotine and nonnicotine factors in cigarette addiction. Psychopharmacology 184:274–285

    Article  PubMed  CAS  Google Scholar 

  • Rose JE, Behm FM, Westman EC, Bates JE, Salley A (2003) Pharmacologic and sensorimotor components of satiation in cigarette smoking. Pharmacol Biochem Behav 76:243–250

    Article  PubMed  CAS  Google Scholar 

  • Sclafani A, Ackroff K (2003) Reinforcement value of sucrose measured by progressive ratio operant licking in the rat. Physiol Behav 79:663–670

    Article  PubMed  CAS  Google Scholar 

  • Uslaner JM, Acerbo MJ, Jones SA, Robinson TE (2006) The attribution of incentive salience to a stimulus that signals an intravenous injection of cocaine. Behav Brain Res 169:320–324

    Article  PubMed  CAS  Google Scholar 

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Correspondence to Matthew I. Palmatier.

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All experiments followed the “Principles of laboratory animal care” (NIH #85-23, revised 1985) and were approved by the Kansas State University Institutional Animal Care and Use Committee (Assurance # A3609-01). This research was supported by NIH grant DA-24801. We thank Scott Jones and Ashley Sheppard for their comments on a previous version of the manuscript.

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Palmatier, M.I., O’Brien, L.C. & Hall, M.J. The role of conditioning history and reinforcer strength in the reinforcement enhancing effects of nicotine in rats. Psychopharmacology 219, 1119–1131 (2012). https://doi.org/10.1007/s00213-011-2439-5

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  • DOI: https://doi.org/10.1007/s00213-011-2439-5

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