Repeated nicotine exposure during adolescence alters reward-related learning in male and female rats

Behavioural Brain Research

Volumn 261, Issue , 2014, Pages 171-176

  Quick, Stacey L ^a   Olausson, Peter ^a   Addy, Nii A ^a   Taylor, Jane R ^a  

^a YALE UNIVERSITY   (United States)

Author keywords

Conditioned reinforcement; Nicotine; Pavlovian approach; Reward learning; Sex differences

Indexed keywords

NICOTINE;

ADOLESCENT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APPETITE; ARTICLE; BEHAVIOR CHANGE; BRAIN FUNCTION; CONTROLLED STUDY; DRUG SEEKING BEHAVIOR; FEMALE; FUNCTIONAL ASSESSMENT; LEARNING; LOCOMOTION; MALE; MENTAL TASK; MOUSE; NONHUMAN; PRIORITY JOURNAL; REINFORCEMENT; REWARD; SEX DIFFERENCE; SMOKING; STIMULUS RESPONSE; TASK PERFORMANCE; TOBACCO DEPENDENCE;

CONDITIONED REINFORCEMENT; NICOTINE; PAVLOVIAN APPROACH; REWARD LEARNING; SEX DIFFERENCES;

ANALYSIS OF VARIANCE; ANIMALS; ANIMALS, NEWBORN; CONDITIONING, CLASSICAL; CONDITIONING, OPERANT; FEMALE; MALE; MOTOR ACTIVITY; NICOTINE; NICOTINIC AGONISTS; RATS; RATS, SPRAGUE-DAWLEY; REWARD; SEX CHARACTERISTICS; TIME FACTORS;

EID: 84891701332     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.12.001     Document Type: Article

References (64)

1. Torregrossa M.M., Corlett P.R., Taylor J.R. Aberrant learning and memory in addiction. Neurobiol Learn Mem 2011, 96:609-623.
2. Tiffany S.T., Carter B.L. Is craving the source of compulsive drug use?. J Psychopharmacol (Oxford, England) 1998, 12:23-30.
3. Caggiula A.R., Donny E.C., White A.R., Chaudhri N., Booth S., Gharib M.A., Hoffman A., Perkins K.A., Sved A.F. Cue dependency of nicotine self-administration and smoking. Pharmacol Biochem Behav 2001, 70:515-530.
4. Mucha R.F., Geier A., Pauli P. Modulation of craving by cues having differential overlap with pharmacological effect: evidence for cue approach in smokers and social drinkers. Psychopharmacology (Berl) 1999, 147:306-313.
5. Dols M., Willems B., van den Hout M., Bittoun R. Smokers can learn to influence their urge to smoke. Addictive Behav 2000, 25:103-108.
6. Brody A.L., Mandelkern M.A., London E.D., Childress A.R., Lee G.S., Bota R.G., Ho M.L., Saxena S., Baxter L.R., Madsen D., Jarvik M.E. Brain metabolic changes during cigarette craving. Arch Gen Psychiatry 2002, 59:1162-1172.
7. Due D.L., Huettel S.A., Hall W.G., Rubin D.C. Activation in mesolimbic and visuospatial neural circuits elicited by smoking cues: evidence from functional magnetic resonance imaging. Am J Psychiatry 2002, 159:954-960.
8. Donny E.C., Caggiula A.R., Weaver M.T., Levin M.E., Sved A.F. The reinforcement-enhancing effects of nicotine: implications for the relationship between smoking, eating and weight. Physiol Behav 2011, 104:143-148.
9. Grimm J.W., Hope B.T., Wise R.A., Shaham Y. Neuroadaptation. Incubation of cocaine craving after withdrawal. Nature 2001, 412:141-142.
10. See R.E. Neural substrates of conditioned-cued relapse to drug-seeking behavior. Pharmacol Biochem Behav 2002, 71:517-529.
11. Feltenstein M.W., Ghee S.M., See R.E. Nicotine self-administration and reinstatement of nicotine-seeking in male and female rats. Drug Alcohol Depend 2012, 121:240-246.
12. Everitt B.J., Parkinson J.A., Olmstead M.C., Arroyo M., Robledo P., Robbins T.W. Associative processes in addiction and reward. The role of amygdala-ventral striatal subsystems. Ann NY Acad Sci 1999, 877:412-438.
13. Cardinal R.N., Parkinson J.A., Hall J., Everitt B.J. Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 2002, 26:321-352.
14. Hutchison K.E., Rutter M.C., Niaura R., Swift R.M., Pickworth W.B., Sobik L. Olanzapine attenuates cue-elicited craving for tobacco. Psychopharmacology 2004, 175:407-413.
15. Harmer C.J., Phillips G.D. Enhanced appetitive conditioning following repeated pretreatment with d-amphetamine. Behav Pharmacol 1998, 9:299-308.
16. Taylor J.R., Jentsch J.D. Repeated intermittent administration of psychomotor stimulant drugs alters the acquisition of Pavlovian approach behavior in rats: differential effects of cocaine, d-amphetamine and 3,4- methylenedioxymethamphetamine (Ecstasy). Biol Psychiatry 2001, 50:137-143.
17. Olausson P., Jentsch J.D., Taylor J.R. Repeated nicotine exposure enhances reward-related learning in the rat. Neuropsychopharmacology 2003, 28:1264-1271.
18. Olausson P., Jentsch J.D., Taylor J.R. Nicotine enhances responding with conditioned reinforcement. Psychopharmacology (Berl) 2004, 171:173-178.
19. Robinson T.E., Berridge K.C. The neural basis of drug craving: an incentive-sensitization theory of addiction. Brain Res Brain Res Rev 1993, 18:247-291.
20. Jentsch J.D., Taylor J.R. Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Psychopharmacology (Berl) 1999, 146:373-390.
21. Berke J.D., Hyman S.E. Addiction, dopamine, and the molecular mechanisms of memory. Neuron 2000, 25:515-532.
22. Robinson T.E., Berridge K.C. The psychology and neurobiology of addiction: an incentive-sensitization view. Addiction 2000, 95(Suppl 2):S91-S117.
23. Everitt B.J., Dickinson A., Robbins T.W. The neuropsychological basis of addictive behaviour. Brain Res Brain Res Rev 2001, 36:129-138.
24. Balfour D.J., Wright A.E., Benwell M.E., Birrell C.E. The putative role of extra-synaptic mesolimbic dopamine in the neurobiology of nicotine dependence. Behav Brain Res 2000, 113:73-83.
25. Olausson P., Jentsch J.D., Taylor J.R. Repeated nicotine exposure enhances responding with conditioned reinforcement. Psychopharmacology (Berl) 2004.
26. Robbins T.W. Reward enhancement by psychomotor stimulant drugs [proceedings]. Neuropharmacology 1977, 16:529-530.
27. Taylor J.R., Robbins T.W. Enhanced behavioural control by conditioned reinforcers following microinjections of d-amphetamine into the nucleus accumbens. Psychopharmacology (Berl) 1984, 84:405-412.
28. Taylor J.R., Horger B.A. Enhanced responding for conditioned reward produced by intra-accumbens amphetamine is potentiated after cocaine sensitization. Psychopharmacology (Berl) 1999, 142:31-40.
29. Barrett S.T., Odum A.L. The effects of repeated exposure on the reward-enhancing effects of nicotine. Behav Pharmacol 2011, 22:283-290.
30. Heishman S.J., Lee D.C., Taylor R.C., Singleton E.G. Prolonged duration of craving, mood, and autonomic responses elicited by cues and imagery in smokers: Effects of tobacco deprivation and sex. Exp Clin Psychopharmacol 2010, 18:245-256.
31. McClernon F.J., Kozink R.V., Rose J.E. Individual differences in nicotine dependence, withdrawal symptoms, and sex predict transient fMRI-BOLD responses to smoking cues. Neuropsychopharmacology 2008, 33:2148-2157.
32. Chaudhri N., Caggiula A.R., Donny E.C., Booth S., Gharib M.A., Craven L.A., Allen S.S., Sved A.F., Perkins K.A. Sex differences in the contribution of nicotine and nonpharmacological stimuli to nicotine self-administration in rats. Psychopharmacology (Berl) 2005, 180:258-266.
33. Patton G.C., Carlin J.B., Coffey C., Wolfe R., Hibbert M., Bowes G. Depression, anxiety, and smoking initiation: a prospective study over 3 years. Am J Public Health 1998, 88:1518-1522.
34. Chambers R.A., Taylor J.R., Potenza M.N. Developmental neurocircuitry of motivation in adolescence: a critical period of addiction vulnerability. Am J Psychiatry 2003, 160:1041-1052.
35. Shingo A.S., Yonezawa M., Sakurai K., Kito S. Nicotine inhibits estrogen response element binding in the rat brain. J Neural Transm 2000, 107:1491-1495.
36. Luine V.N. Sex steroids and cognitive function. JNeuroendocrinol 2008, 20:866-872.
37. Quinn J.J., Hitchcott P.K., Umeda E.A., Arnold A.P., Taylor J.R. Sex chromosome complement regulates habit formation. Nat Neurosci 2007, 10:1398-1400.
38. Barker J.M., Torregrossa M.M., Arnold A.P., Taylor J.R. Dissociation of genetic and hormonal influences on sex differences in alcoholism-related behaviors. J Neurosci 2010, 30:9140-9144.
39. Dagher A., Bleicher C., Aston J.A., Gunn R.N., Clarke P.B., Cumming P. Reduced dopamine D1 receptor binding in the ventral striatum of cigarette smokers. Synapse 2001, 42:48-53.
40. David S.P., Munafo M.R., Johansen-Berg H., Smith S.M., Rogers R.D., Matthews P.M., Walton R.T. Ventral striatum/nucleus accumbens activation to smoking-related pictorial cues in smokers and nonsmokers: a functional magnetic resonance imaging study. Biol Psychiatry 2005, 58:488-494.
41. McBride D., Barrett S.P., Kelly J.T., Aw A., Dagher A. Effects of expectancy and abstinence on the neural response to smoking cues in cigarette smokers: an fMRI study. Neuropsychopharmacology 2006, 31:2728-2738.
42. Rose E.J., Ross T.J., Salmeron B.J., Lee M., Shakleya D.M., Huestis M., Stein E.A. Chronic exposure to nicotine is associated with reduced reward-related activity in the striatum but not the midbrain. Biol Psychiatry 2012, 71:206-213.
43. Hitchcott P.K., Phillips G.D. Double dissociation of the behavioural effects of R(+) 7-OH-DPAT infusions in the central and basolateral amygdala nuclei upon Pavlovian and instrumental conditioned appetitive behaviours. Psychopharmacology (Berl) 1998, 140:458-469.
44. Parkinson J.A., Olmstead M.C., Burns L.H., Robbins T.W., Everitt B.J. Dissociation in effects of lesions of the nucleus accumbens core and shell on appetitive pavlovian approach behavior and the potentiation of conditioned reinforcement and locomotor activity by d-amphetamine. J Neurosci 1999, 19:2401-2411.
45. Phillips G.D., Harmer C.J., Hitchcott P.K. Blockade of sensitisation-induced facilitation of appetitive conditioning by post-session intra-amygdala nafadotride. Behav Brain Res 2002, 134:249-257.
46. Harmer C.J., Phillips G.D. Enhanced conditioned inhibition following repeated pretreatment with d-amphetamine. Psychopharmacology (Berl) 1999, 142:120-131.
47. Jentsch J.D., Olausson P., Nestler E.J., Taylor J.R. Stimulation of protein kinase a activity in the rat amygdala enhances reward-related learning. Biol Psychiatry 2002, 52:111-118.
48. Tzavara E.T., Monory K., Hanoune J., Nomikos G.G. Nicotine withdrawal syndrome: behavioural distress and selective up-regulation of the cyclic AMP pathway in the amygdala. Eur J Neurosci 2002, 16:149-153.
49. Brunzell D.H., Chang J.R., Schneider B., Olausson P., Taylor J.R., Picciotto M.R. beta2-Subunit-containing nicotinic acetylcholine receptors are involved in nicotine-induced increases in conditioned reinforcement but not progressive ratio responding for food in C57BL/6 mice. Psychopharmacology (Berl) 2006, 184:328-338.
50. Lof E., Olausson P., deBejczy A., Stomberg R., McIntosh J.M., Taylor J.R., Soderpalm B. Nicotinic acetylcholine receptors in the ventral tegmental area mediate the dopamine activating and reinforcing properties of ethanol cues. Psychopharmacology (Berl) 2007, 195:333-343.
51. Lof E., Olausson P., Stomberg R., Taylor J.R., Soderpalm B. Nicotinic acetylcholine receptors are required for the conditioned reinforcing properties of sucrose-associated cues. Psychopharmacology (Berl) 2010, 212:321-328.
52. Taylor J.R., Robbins T.W. 6-Hydroxydopamine lesions of the nucleus accumbens, but not of the caudate nucleus, attenuate enhanced responding with reward-related stimuli produced by intra-accumbens d-amphetamine. Psychopharmacology (Berl) 1986, 90:390-397.
53. Cador M., Robbins T.W., Everitt B.J. Involvement of the amygdala in stimulus-reward associations: interaction with the ventral striatum. Neuroscience 1989, 30:77-86.
54. Robbins T.W., Cador M., Taylor J.R., Everitt B.J. Limbic-striatal interactions in reward-related processes. Neurosci Biobehav Rev 1989, 13:155-162.
55. Cador M., Taylor J.R., Robbins T.W. Potentiation of the effects of reward-related stimuli by dopaminergic-dependent mechanisms in the nucleus accumbens. Psychopharmacology (Berl) 1991, 104:377-385.
56. Saladin M.E., Gray K.M., Carpenter M.J., LaRowe S.D., DeSantis S.M., Upadhyaya H.P. Gender differences in craving and cue reactivity to smoking and negative affect/stress cues. Am J Addict 2012, 21:210-220.
57. Levin E.D., McClernon F.J., Rezvani A.H. Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology (Berl) 2006, 184:523-539.
58. Everitt B.J., Robbins T.W. Neural systems of reinforcement for drug addiction: from actions to habits to compulsion. Nat Neurosci 2005, 8:1481-1489.
59. Everitt B.J., Belin D., Economidou D., Pelloux Y., Dalley J.W., Robbins T.W. Review. Neural mechanisms underlying the vulnerability to develop compulsive drug-seeking habits and addiction. Philos Trans Roy Soc 2008, 363:3125-3135.
60. Flagel S.B., Akil H., Robinson T.E. Individual differences in the attribution of incentive salience to reward-related cues: implications for addiction. Neuropharmacology 2009, 1(56 Suppl):139-148.
61. Taylor J.R., Olausson P., Quinn J.J., Torregrossa M.M. Targeting extinction and reconsolidation mechanisms to combat the impact of drug cues on addiction. Neuropharmacology 2009, 56(Suppl 1):186-195.
62. Mucha R.F., Geier A., Stuhlinger M., Mundle G. Appetitve effects of drug cues modelled by pictures of the intake ritual: generality of cue-modulated startle examined with inpatient alcoholics. Psychopharmacology (Berl) 2000, 151:428-432.
63. Rose J.E., Behm F.M. Extinguishing the rewarding value of smoke cues: pharmacological and behavioral treatments. Nicotine Tob Res 2004, 6:523-532.
64. Franklin T., Wang Z., Suh J.J., Hazan R., Cruz J., Li Y., Goldman M., Detre J.A., O'Brien C.P., Childress A.R. Effects of varenicline on smoking cue-triggered neural and craving responses. Arch Gen Psychiatry 2011, 68:516-526.