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Associative processes in addiction relapse models: A review of their Pavlovian and instrumental mechanisms, history, and terminology


Associative processes in addiction relapse models: A review of their Pavlovian and instrumental mechanisms, history, and terminology

Lay, Belinda Po Pyn ORCID: https://orcid.org/0000-0003-0522-9480 and Khoo, Shaun Yon-Seng ORCID: https://orcid.org/0000-0002-0972-3788 (2021) Associative processes in addiction relapse models: A review of their Pavlovian and instrumental mechanisms, history, and terminology. Neuroanatomy and Behaviour, 3 (1). e18. ISSN 2652-1768

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Official URL: https://doi.org/10.35430/nab.2021.e18


Animal models of relapse to drug-seeking have borrowed heavily from associative learning approaches. In studies of relapse-like behaviour, animals learn to self-administer drugs then receive a period of extinction during which they learn to inhibit the operant response. Several triggers can produce a recovery of responding which form the basis of a variety of models. These include the passage of time (spontaneous recovery), drug availability (rapid reacquisition), extinction of an alternative response (resurgence), context change (renewal), drug priming, stress, and cues (reinstatement). In most cases, the behavioural processes driving extinction and recovery in operant drug self-administration studies are similar to those in the Pavlovian and behavioural literature, such as context effects. However, reinstatement in addiction studies have several differences with Pavlovian reinstatement, which have emerged over several decades, in experimental procedures, associative mechanisms, and terminology. Interestingly, in cue-induced reinstatement, drug-paired cues that are present during acquisition are omitted during lever extinction. The unextinguished drug-paired cue may limit the model’s translational relevance to cue exposure therapy and renders its underlying associative mechanisms ambiguous. We review major behavioural theories that explain recovery phenomena, with a particular focus on cue-induced reinstatement because it is a widely used model in addiction. We argue that cue-induced reinstatement may be explained by a combination of behavioural processes, including reacquisition of conditioned reinforcement and Pavlovian to Instrumental Transfer. While there are important differences between addiction studies and the behavioural literature in terminology and procedures, it is clear that understanding associative learning processes is essential for studying relapse.

Divisions:Concordia University > Research Units > Centre for Studies in Behavioural Neurobiology
Item Type:Article
Authors:Lay, Belinda Po Pyn and Khoo, Shaun Yon-Seng
Journal or Publication:Neuroanatomy and Behaviour
Date:23 February 2021
  • Fonds de Recherche du Québec - Santé
Digital Object Identifier (DOI):10.35430/nab.2021.e18
Keywords:Addiction, Reinstatement, Cues, Extinction, Conditioned reinforcement,Pavlovian to Instrumental Transfer
ID Code:988008
Deposited On:16 Mar 2021 21:34
Last Modified:16 Mar 2021 21:34


1. Hoffman DC. The use of place conditioning in studying the neuropharmacology of drug reinforcement. Brain Research Bulletin. 1989;23(4–5):373-87. doi: 10.1016/0361-9230(89)90224-4.
2. Weeks JR. Experimental morphine addiction: Method for automatic intravenous injections in unrestrained rats. Science. 1962;138(3537):143-4. doi: 10.1126/science.138.3537.143.
3. Konova AB, Goldstein RZ. The emerging neuroscience of appetitive and drug cue extinction in humans. Psychopharmacology. 2019;236(1):407-14. doi: 10.1007/s00213-018-5098-y.
4. Pavlov I. Conditional reflexes: An investigation of the physiological activity of the cerebral cortex. New York: Dover Publications; 1927.
5. Byrne SP, Haber P, Baillie A, Giannopolous V, Morley K. Cue exposure therapy for alcohol use disorders: What can be learned from exposure therapy for anxiety disorders? Substance Use & Misuse. 2019;54(12):2053-63. doi: 10.1080/10826084.2019.1618328.
6. Segawa T, Baudry T, Bourla A, Blanc J-V, Peretti C-S, Mouchabac S, et al. Virtual reality (VR) in assessment and treatment of addictive disorders: A systematic review. Frontiers in Neuroscience. 2020;13(1409). doi: 10.3389/fnins.2019.01409.
7. Conklin CA, Tiffany ST. Applying extinction research and theory to cue-exposure addiction treatments. Addiction. 2002;97(2):155-67. doi: 10.1046/j.1360-0443.2002.00014.x.
8. Marissen MAE, Franken IHA, Blanken P, van den Brink W, Hendriks VM. Cue exposure therapy for the treatment of opiate addiction: Results of a randomized controlled clinical trial. Psychotherapy and Psychosomatics. 2007;76(2):97-105. doi: 10.1159/000097968.
9. Torregrossa MM, Taylor JR. Learning to forget: manipulating extinction and reconsolidation processes to treat addiction. Psychopharmacology. 2013;226(4):659-72. doi: 10.1007/s00213-012-2750-9.
10. Havermans RC, Jansen ATM. Increasing the efficacy of cue exposure treatment in preventing relapse of addictive behavior. Addictive Behaviors. 2003;28(5):989-94. doi: 10.1016/S0306-4603(01)00289-1.
11. Maren S. Fear of the unexpected: Hippocampus mediates novelty-induced return of extinguished fear in rats. Neurobiology of Learning and Memory. 2014;108:88-95. doi: 10.1016/j.nlm.2013.06.004.
12. Kehoe EJ, Macrae M. Savings in animal learning: Implications for relapse and maintenance after therapy. Behavior Therapy. 1997;28(1):141-55. doi: 10.1016/S0005-7894(97)80039-1.
13. Rescorla RA. Retraining of extinguished Pavlovian stimuli. Journal of Experimental Psychology: Animal Behavior Processes. 2001;27(2):115-24. doi: 10.1037/0097-7403.27.2.115.
14. Bouton ME, Winterbauer NE, Todd TP. Relapse processes after the extinction of instrumental learning: Renewal, resurgence, and reacquisition. Behavioural Processes. 2012;90(1):130-41. doi: 10.1016/j.beproc.2012.03.004.
15. Rescorla RA. Spontaneous recovery after Pavlovian conditioning with multiple outcomes. Animal Learning & Behavior. 1997;25(1):99-107. doi: 10.3758/BF03199028.
16. Leung HT, Westbrook FR. Spontaneous recovery of extinguished fear responses deepens their extinction: A role for error-correction mechanisms. Journal of Experimental Psychology: Animal Behavior Processes. 2008;34(4):461-74. doi: 10.1037/0097-7403.34.4.461.
17. Bouton ME. Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biological Psychiatry. 2002;52(10):976-86. doi: 10.1016/S0006-3223(02)01546-9.
18. Epstein R, Skinner BF. Resurgence of responding after the cessation of response-independent reinforcement. Proceedings of the National Academy of Sciences. 1980;77(10):6251-3. doi: 10.1073/pnas.77.10.6251.
19. Maren S, Phan KL, Liberzon I. The contextual brain: implications for fear conditioning, extinction and psychopathology. Nature Reviews Neuroscience. 2013;14(6):417-28. doi: 10.1038/nrn3492.
20. Goode TD, Maren S. Animal models of fear relapse. ILAR Journal. 2014;55(2):246-58. doi: 10.1093/ilar/ilu008.
21. Bouton ME, Bolles RC. Contextual control of the extinction of conditioned fear. Learning and Motivation. 1979;10(4):445-66. doi: 10.1016/0023-9690(79)90057-2.
22. Rescorla RA, Heth CD. Reinstatement of fear to an extinguished conditioned stimulus. Journal of Experimental Psychology: Animal Behavior Processes. 1975;1(1):88-96. doi: 10.1037/0097-7403.1.1.88.
23. Kalivas PW, McFarland K. Brain circuitry and the reinstatement of cocaine-seeking behavior. Psychopharmacology. 2003;168(1):44-56. doi: 10.1007/s00213-003-1393-2.
24. McFarland K, Kalivas PW. The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. The Journal of Neuroscience. 2001;21(21):8655-63. doi: 10.1523/JNEUROSCI.21-21-08655.2001.
25. Crombag HS, Grimm JW, Shaham Y. Effect of dopamine receptor antagonists on renewal of cocaine seeking by reexposure to drug-associated contextual cues. Neuropsychopharmacology. 2002;27(6):1006-15. doi: 10.1016/S0893-133X(02)00356-1.
26. Peters J, De Vries TJ. Pavlovian conditioned approach, extinction, and spontaneous recovery to an audiovisual cue paired with an intravenous heroin infusion. Psychopharmacology. 2014;231(2):447-53. doi: 10.1007/s00213-013-3258-7.
27. McConnell BL, Miller RR. Associative accounts of recovery-from-extinction effects. Learning and Motivation. 2014;46:1-15. doi: 10.1016/j.lmot.2014.01.003.
28. Bouton ME, Maren S, McNally GP. Behavioral and neurobiological mechanisms of Pavlovian and instrumental extinction learning. Physiological Reviews. 2020. doi: 10.1152/physrev.00016.2020.
29. Ellson DG. Quantitative studies of the interaction of simple habits. I. Recovery from specific and generalized effects of extinction. Journal of Experimental Psychology. 1938;23(4):339–58. doi: 10.1037/h0056285.
30. Youtz REP. Reinforcement, extinction, and spontaneous recovery in a non-Pavlovian reaction. Journal of Experimental Psychology. 1938;22(4):305-18. doi: 10.1037/h0056358.
31. Skinner BF. The behavior of organisms. New York: Appleton-Century-Crofts; 1938.
32. Rescorla RA. Spontaneous recovery. Learning & Memory. 2004;11(5):501-9. doi: 10.1101/lm.77504.
33. Di Ciano P, Everitt BJ. Reinstatement and spontaneous recovery of cocaine-seeking following extinction and different durations of withdrawal. Behavioural Pharmacology. 2002;13(5). doi: 10.1097/00008877-200209000-00013.
34. Peters J, Vallone J, Laurendi K, Kalivas PW. Opposing roles for the ventral prefrontal cortex and the basolateral amygdala on the spontaneous recovery of cocaine-seeking in rats. Psychopharmacology. 2008;197(2):319-26. doi: 10.1007/s00213-007-1034-2.
35. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, et al. Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: II. Adult exposure. Alcoholism: Clinical and Experimental Research. 2002;26(11):1642-52. doi: 10.1111/j.1530-0277.2002.tb02466.x.
36. Rodd-Henricks ZA, Bell RL, Kuc KA, Murphy JM, McBride WJ, Lumeng L, et al. Effects of ethanol exposure on subsequent acquisition and extinction of ethanol self-administration and expression of alcohol-seeking behavior in adult alcohol-preferring (P) rats: I. Periadolescent exposure. Alcoholism: Clinical and Experimental Research. 2002;26(11):1632-41. doi: 10.1111/j.1530-0277.2002.tb02465.x.
37. Hauser SR, Wilden JA, Deehan Jr GA, McBride WJ, Rodd ZA. Cocaine influences alcohol-seeking behavior and relapse drinking in alcohol-preferring (P) rats. Alcoholism: Clinical and Experimental Research. 2014;38(10):2678-86. doi: 10.1111/acer.12540.
38. Shaham Y, Adamson LK, Grocki S, Corrigall WA. Reinstatement and spontaneous recovery of nicotine seeking in rats. Psychopharmacology. 1997;130(4):396-403. doi: 10.1007/s002130050256.
39. Struik RF, De Vries TJ, Peters J. Detrimental effects of a retrieval-extinction procedure on nicotine seeking, but not cocaine seeking. Frontiers in Behavioral Neuroscience. 2019;13(243). doi: 10.3389/fnbeh.2019.00243.
40. LeCocq MR, Lahlou S, Chahine M, Padillo LN, Chaudhri N. Modeling relapse to pavlovian alcohol-seeking in rats using reinstatement and spontaneous recovery paradigms. Alcoholism: Clinical and Experimental Research. 2018;42(9):1795-806. doi: 10.1111/acer.13825.
41. Bouton ME, Swartzentruber D. Sources of relapse after extinction in Pavlovian and instrumental learning. Clinical Psychology Review. 1991;11(2):123-40. doi: 10.1016/0272-7358(91)90091-8.
42. Skinner BF. Are theories of learning necessary? Psychological Review. 1950;57(4):193-216. doi: 10.1037/h0054367.
43. Amsel A. The role of frustrative nonreward in noncontinuous reward situations. Psychological Bulletin. 1958;55(2):102-19. doi: 10.1037/h0043125.
44. Johnson JS, Escobar M, Kimble WL. Long-term maintenance of immediate or delayed extinction is determined by the extinction-test interval. Learning & Memory. 2010;17(12):639-44. doi: 10.1101/lm.1932310.
45. McSweeney FK, Hinson JM, Cannon CB. Sensitization-habituation may occur during operant conditioning. Psychological Bulletin. 1996;120(2):256-71. doi: 10.1037/0033-2909.120.2.256.
46. Storsve AB, McNally GP, Richardson R. US habituation, like CS extinction, produces a decrement in conditioned fear responding that is NMDA dependent and subject to renewal and reinstatement. Neurobiology of Learning and Memory. 2010;93(4):463-71. doi: 10.1016/j.nlm.2009.12.011.
47. Storsve AB, McNally GP, Richardson R. Renewal and reinstatement of the conditioned but not the unconditioned response following habituation of the unconditioned stimulus. Behavioural Processes. 2012;90(1):58-65. doi: 10.1016/j.beproc.2012.03.007.
48. McSweeney FK, Johnson KS. The effect of time between sessions on within-session patterns of responding. Behavioural Processes. 1994;31(2):207-17. doi: 10.1016/0376-6357(94)90007-8.
49. Grimm JW, Hope BT, Wise RA, Shaham Y. Incubation of cocaine craving after withdrawal. Nature. 2001;412(6843):141-2. doi: 10.1038/35084134.
50. Gawin FH, Kleber HD. Abstinence symptomatology and psychiatric diagnosis in cocaine abusers: Clinical observations. Archives of General Psychiatry. 1986;43(2):107-13. doi: 10.1001/archpsyc.1986.01800020013003.
51. Hollander JA, Carelli RM. Cocaine-associated stimuli increase cocaine seeking and activate accumbens core neurons after abstinence. The Journal of Neuroscience. 2007;27(13):3535-9. doi: 10.1523/jneurosci.3667-06.2007.
52. Nicolas C, Russell TI, Pierce AF, Maldera S, Holley A, You Z-B, et al. Incubation of cocaine craving after intermittent-access self-administration: Sex differences and estrous cycle. Biological Psychiatry. 2019;85:915-24. doi: 10.1016/j.biopsych.2019.01.015.
53. Krasnova IN, Marchant NJ, Ladenheim B, McCoy MT, Panlilio LV, Bossert JM, et al. Incubation of methamphetamine and palatable food craving after punishment-induced abstinence. Neuropsychopharmacology. 2014;39(8):2008-16. doi: 10.1038/npp.2014.50.
54. Pickens CL, Airavaara M, Theberge F, Fanous S, Hope BT, Shaham Y. Neurobiology of the incubation of drug craving. Trends in Neurosciences. 2011;34(8):411-20. doi: 10.1016/j.tins.2011.06.001.
55. Paulson PE, Robinson TE. Amphetamine-induced time-dependent sensitization of dopamine neurotransmission in the dorsal and ventral striatum: A microdialysis study in behaving rats. Synapse. 1995;19(1):56-65. doi: 10.1002/syn.890190108.
56. Delamater AR, Westbrook RF. Psychological and neural mechanisms of experimental extinction: A selective review. Neurobiology of Learning and Memory. 2014;108:38-51. doi: 10.1016/j.nlm.2013.09.016.
57. Perry CJ, McNally GP. Naloxone prevents the rapid reacquisition but not acquisition of alcohol seeking. Behavioral Neuroscience. 2012;126(4):599-604. doi: 10.1037/a0029079.
58. Bouton ME, Swartzentruber D. Slow reacquisition following extinction: Context, encoding, and retrieval mechanisms. Journal of Experimental Psychology: Animal Behavior Processes. 1989;15(1):43-53. doi: 10.1037/0097-7403.15.1.43.
59. Willcocks AL, McNally GP. The role of context in re-acquisition of extinguished alcoholic beer-seeking. Behavioral Neuroscience. 2011;125(4):541-50. doi: 10.1037/a0024100.
60. Willcocks AL, McNally GP. The role of medial prefrontal cortex in extinction and reinstatement of alcohol-seeking in rats. European Journal of Neuroscience. 2013;37(2):259-68. doi: 10.1111/ejn.12031.
61. Liu Y, Jean-Richard-dit-Bressel P, Yau JO-Y, Willing A, Prasad AA, Power JM, et al. The mesolimbic dopamine activity signatures of relapse to alcohol-seeking. The Journal of Neuroscience. 2020;40(33):6409-27. doi: 10.1523/jneurosci.0724-20.2020.
62. Marchant NJ, Li X, Shaham Y. Recent developments in animal models of drug relapse. Current Opinion in Neurobiology. 2013;23(4):675-83. doi: 10.1016/j.conb.2013.01.003.
63. Lattal KA, Cançado CRX, Cook JE, Kincaid SL, Nighbor TD, Oliver AC. On defining resurgence. Behavioural Processes. 2017;141:85-91. doi: 10.1016/j.beproc.2017.04.018.
64. Trask S. Cues associated with alternative reinforcement during extinction can attenuate resurgence of an extinguished instrumental response. Learning & Behavior. 2019;47(1):66-79. doi: 10.3758/s13420-018-0339-9.
65. Epstein R. On the rediscovery of the principle of resurgence. Mexican Journal of Behavior Analysis. 2015;41(2):19-43. doi: 10.5514/rmac.v41.i2.63722.
66. Hull CL. The rat's speed-of-locomotion gradient in the approach to food. Journal of Comparative Psychology. 1934;17(3):393-422. doi: 10.1037/h0071299.
67. Carey JP. Reinstatement of previously learned responses under conditions of extinction: a study of "regression." American Psychologist. 1951;6(7):284. doi: 10.1037/h0051240.
68. Leitenberg H, Rawson RA, Bath K. Reinforcement of competing behavior during extinction. Science. 1970;169(3942):301-3. doi: 10.1126/science.169.3942.301.
69. Podlesnik CA, Shahan TA. Extinction, relapse, and behavioral momentum. Behavioural Processes. 2010;84(1):400-11. doi: 10.1016/j.beproc.2010.02.001.
70. Shahan TA, Craig AR. Resurgence as choice. Behavioural Processes. 2017;141:100-27. doi: 10.1016/j.beproc.2016.10.006.
71. Stanger C, Budney AJ. Contingency management: Using incentives to improve outcomes for adolescent substance use disorders. Pediatric Clinics of North America. 2019;66(6):1183-92. doi: 10.1016/j.pcl.2019.08.007.
72. Higgins ST, Heil SH, Lussier JP. Clinical implications of reinforcement as a determinant of substance use disorders. Annual Review of Psychology. 2004;55(1):431-61. doi: 10.1146/annurev.psych.55.090902.142033.
73. Preston KL, Umbricht A, Epstein DH. Abstinence reinforcement maintenance contingency and one-year follow-up. Drug and Alcohol Dependence. 2002;67(2):125-37. doi: 10.1016/S0376-8716(02)00023-6.
74. Quick SL, Pyszczynski AD, Colston KA, Shahan TA. Loss of alternative non-drug reinforcement induces relapse of cocaine-seeking in rats: Role of dopamine D1 receptors. Neuropsychopharmacology. 2011;36(5):1015-20. doi: 10.1038/npp.2010.239.
75. Frye CCJ, Rung JM, Nall RW, Galizio A, Haynes JM, Odum AL. Continuous nicotine exposure does not affect resurgence of alcohol seeking in rats. PLOS ONE. 2018;13(8):e0202230. doi: 10.1371/journal.pone.0202230.
76. Podlesnik CA, Jimenez-Gomez C, Shahan TA. Resurgence of alcohol seeking produced by discontinuing non-drug reinforcement as an animal model of drug relapse. Behavioural Pharmacology. 2006;17(4). doi: 10.1097/01.fbp.0000224385.09486.ba.
77. Zironi I, Burattini C, Aicardi G, Janak PH. Context is a trigger for relapse to alcohol. Behavioural Brain Research. 2006;167(1):150-5. doi: 10.1016/j.bbr.2005.09.007.
78. Khoo SY-S, Sciascia JM, Brown A, Chaudhri N. Comparing ABA, AAB, and ABC renewal of appetitive Pavlovian conditioned responding in alcohol- and sucrose-trained male rats. Frontiers in Behavioral Neuroscience. 2020;14(5). doi: 10.3389/fnbeh.2020.00005.
79. Welker RL, McAuley K. Reductions in resistance to extinction and spontaneous recovery as a function of changes in transportational and contextual stimuli. Animal Learning & Behavior. 1978;6(4):451-7. doi: 10.3758/BF03209643.
80. Bouton ME, Bolles RC. Role of conditioned contextual stimuli in reinstatement of extinguished fear. Journal of Experimental Psychology: Animal Behavior Processes. 1979;5(4):368-78. doi: 10.1037/0097-7403.5.4.368.
81. Bouton ME, King DA. Contextual control of the extinction of conditioned fear: Tests for the associative value of the context. Journal of Experimental Psychology: Animal Behavior Processes. 1983;9(3):248-65. doi: 10.1037/0097-7403.9.3.248.
82. Rescorla RA, Wagner AR. A theory of Pavlovian conditioning: Variations in the effectiveness of reinforcement and nonreinforcement. In: Black AH, Prokasy WF, editors. Classical Conditioning II: Current Research and Theory. New York: Appleton-Century-Crofts; 1972. p. 64-99.
83. Bouton ME. Context and ambiguity in the extinction of emotional learning: Implications for exposure therapy. Behaviour Research and Therapy. 1988;26(2):137-49. doi: 10.1016/0005-7967(88)90113-1.
84. Hamlin AS, Newby J, McNally GP. The neural correlates and role of D1 dopamine receptors in renewal of extinguished alcohol-seeking. Neuroscience. 2007;146(2):525-36. doi: 10.1016/j.neuroscience.2007.01.063.
85. Kearns DN, Weiss SJ. Contextual renewal of cocaine seeking in rats and its attenuation by the conditioned effects of an alternative reinforcer. Drug and Alcohol Dependence. 2007;90(2):193-202. doi: 10.1016/j.drugalcdep.2007.03.006.
86. Hamlin AS, Clemens KJ, McNally GP. Renewal of extinguished cocaine-seeking. Neuroscience. 2008;151(3):659-70. doi: 10.1016/j.neuroscience.2007.11.018.
87. Crombag HS, Shaham Y. Renewal of drug seeking by contextual cues after prolonged extinction in rats. Behavioral Neuroscience. 2002;116(1):169-73. doi: 10.1037/0735-7044.116.1.169.
88. Bossert JM, Liu SY, Lu L, Shaham Y. A role of ventral tegmental area glutamate in contextual cue-induced relapse to heroin seeking. The Journal of Neuroscience. 2004;24(47):10726-30. doi: 10.1523/jneurosci.3207-04.2004.
89. Diergaarde L, de Vries W, Raasø H, Schoffelmeer ANM, De Vries TJ. Contextual renewal of nicotine seeking in rats and its suppression by the cannabinoid-1 receptor antagonist Rimonabant (SR141716A). Neuropharmacology. 2008;55(5):712-6. doi: 10.1016/j.neuropharm.2008.06.003.
90. Fuchs RA, Evans KA, Ledford CC, Parker MP, Case JM, Mehta RH, et al. The role of the dorsomedial prefrontal cortex, basolateral amygdala, and dorsal hippocampus in contextual reinstatement of cocaine seeking in rats. Neuropsychopharmacology. 2005;30(2):296-309. doi: 10.1038/sj.npp.1300579.
91. Todd TP. Mechanisms of renewal after the extinction of instrumental behavior. Journal of Experimental Psychology: Animal Behavior Processes. 2013;39(3):193-207. doi: 10.1037/a0032236.
92. Trask S, Shipman ML, Green JT, Bouton ME. Inactivation of the prelimbic cortex attenuates context-dependent operant responding. The Journal of Neuroscience. 2017;37(9):2317-24. doi: 10.1523/jneurosci.3361-16.2017.
93. Bouton ME, Schepers ST. Renewal after the punishment of free operant behavior. Journal of Experimental Psychology: Animal learning and cognition. 2015;41(1):81-90. doi: 10.1037/xan0000051.
94. Todd TP, Winterbauer NE, Bouton ME. Effects of the amount of acquisition and contextual generalization on the renewal of instrumental behavior after extinction. Learning & Behavior. 2012;40(2):145-57. doi: 10.3758/s13420-011-0051-5.
95. Bouton ME, Ricker ST. Renewal of extinguished responding in a second context. Animal Learning & Behavior. 1994;22(3):317-24. doi: 10.3758/BF03209840.
96. Nakajima S, Tanaka S, Urushihara K, Imada H. Renewal of extinguished lever-press responses upon return to the training context. Learning and Motivation. 2000;31(4):416-31. doi: 10.1006/lmot.2000.1064.
97. Bossert JM, Gray SM, Lu L, Shaham Y. Activation of group II metabotropic glutamate receptors in the nucleus accumbens shell attenuates context-induced relapse to heroin seeking. Neuropsychopharmacology. 2006;31(10):2197-209. doi: 10.1038/sj.npp.1300977.
98. Bossert JM, Poles GC, Sheffler-Collins SI, Ghitza UE. The mGluR2/3 agonist LY379268 attenuates context- and discrete cue-induced reinstatement of sucrose seeking but not sucrose self-administration in rats. Behavioural Brain Research. 2006;173(1):148-52. doi: 10.1016/j.bbr.2006.06.008.
99. Bossert JM, Poles GC, Wihbey KA, Koya E, Shaham Y. Differential effects of blockade of dopamine D1-family receptors in nucleus accumbens core or shell on reinstatement of heroin seeking induced by contextual and discrete cues. The Journal of Neuroscience. 2007;27(46):12655-63. doi: 10.1523/jneurosci.3926-07.2007.
100. Crombag HS, Bossert JM, Koya E, Shaham Y. Context-induced relapse to drug seeking: a review. Philosophical Transactions of the Royal Society B: Biological Sciences. 2008;363(1507):3233-43. doi: 10.1098/rstb.2008.0090.
101. Marchant NJ, Kaganovsky K, Shaham Y, Bossert JM. Role of corticostriatal circuits in context-induced reinstatement of drug seeking. Brain Research. 2015;1628, Part A:219-32. doi: 10.1016/j.brainres.2014.09.004.
102. Hamlin AS, Clemens KJ, Choi EA, McNally GP. Paraventricular thalamus mediates context-induced reinstatement (renewal) of extinguished reward seeking. European Journal of Neuroscience. 2009;29(4):802-12. doi: 10.1111/j.1460-9568.2009.06623.x.
103. Hamlin AS, Blatchford KE, McNally GP. Renewal of an extinguished instrumental response: Neural correlates and the role of D1 dopamine receptors. Neuroscience. 2006;143(1):25-38. doi: 10.1016/j.neuroscience.2006.07.035.
104. Westbrook RF, Iordanova M, McNally G, Richardson R, Harris JA. Reinstatement of fear to an extinguished conditioned stimulus: two roles for context. Journal of Experimental Psychology: Animal Behavior Processes. 2002;28(1):97. doi: 10.1037/0097-7403.28.1.97.
105. Kim JH, Richardson R. A developmental dissociation in reinstatement of an extinguished fear response in rats. Neurobiology of Learning and Memory. 2007;88(1):48-57. doi: 10.1016/j.nlm.2007.03.004.
106. Morris RW, Westbrook RF, Killcross AS. Reinstatement of extinguished fear by β-adrenergic arousal elicited by a conditioned context. Behavioral Neuroscience. 2005;119(6):1662. doi: 10.1037/0735-7044.119.6.1662.
107. Morris RW, Furlong TM, Westbrook RF. Recent exposure to a dangerous context impairs extinction and reinstates lost fear reactions. Journal of Experimental Psychology: Animal Behavior Processes. 2005;31(1):40. doi: 10.1037/0097-7403.31.1.40.
108. Rhodes SEV, Killcross S. Lesions of rat infralimbic cortex enhance recovery and reinstatement of an appetitive Pavlovian response. Learning & memory (Cold Spring Harbor, NY). 2004;11(5):611-6. doi: 10.1101/lm.79704.
109. Dirikx T, Hermans D, Vansteenwegen D, Baeyens F, Eelen P. Reinstatement of conditioned responses in human differential fear conditioning. Journal of Behavior Therapy and Experimental Psychiatry. 2007;38(3):237-51. doi: 10.1016/j.jbtep.2006.04.001.
110. Hermans D, Dirikx T, Vansteenwegenin D, Baeyens F, Van den Bergh O, Eelen P. Reinstatement of fear responses in human aversive conditioning. Behaviour Research and Therapy. 2005;43(4):533-51. doi: 10.1016/j.brat.2004.03.013.
111. Ebrahimi C, Koch SP, Pietrock C, Fydrich T, Heinz A, Schlagenhauf F. Opposing roles for amygdala and vmPFC in the return of appetitive conditioned responses in humans. Translational Psychiatry. 2019;9(1):148. doi: 10.1038/s41398-019-0482-x.
112. Torres SJ, Nowson CA. Relationship between stress, eating behavior, and obesity. Nutrition. 2007;23(11):887-94. doi: 10.1016/j.nut.2007.08.008.
113. Halladay L, Zelikowsky M, Blair H, Fanselow M. Reinstatement of extinguished fear by an unextinguished conditional stimulus. Frontiers in Behavioral Neuroscience. 2012;6(18). doi: 10.3389/fnbeh.2012.00018.
114. Krisch KA, Bandarian-Balooch S, Neumann DL, Zhong J. Eliciting and attenuating reinstatement of fear: Effects of an unextinguished CS. Learning and Motivation. 2020;71:101650. doi: 10.1016/j.lmot.2020.101650.
115. Shaham Y, Shalev U, Lu L, de Wit H, Stewart J. The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacology. 2003;168(1-2):3-20. doi: 10.1007/s00213-002-1224-x.
116. Stretch R, Gerber GJ, Wood SM. Factors affecting behavior maintained by response-contingent intravenous infusions of amphetamine in squirrel monkeys. Canadian Journal of Physiology and Pharmacology. 1971;49(6):581-9. doi: 10.1139/y71-075.
117. Gerber GJ, Stretch R. Drug-induced reinstatement of extinguished self-administration behavior in monkeys. Pharmacology Biochemistry and Behavior. 1975;3(6):1055-61. doi: 10.1016/0091-3057(75)90016-7.
118. Stretch R, Gerber GJ. Drug-induced reinstatement of amphetamine self-administration behaviour in monkeys. Canadian Journal of Psychology. 1973;27(2):168-77. doi: 10.1037/h0082466.
119. Davis WM, Smith SG. Role of conditioned reinforcers in the initiation, maintenance and extinction of drug-seeking behavior. The Pavlovian Journal of Biological Science. 1976;11(4):222-36.
120. de Wit H, Stewart J. Drug reinstatement of heroin-reinforced responding in the rat. Psychopharmacology. 1983;79(1):29-31. doi: 10.1007/BF00433012.
121. Stewart J. Reinstatement of heroin and cocaine self-administration behavior in the rat by intracerebral application of morphine in the ventral tegmental area. Pharmacology Biochemistry and Behavior. 1984;20(6):917-23. doi: 10.1016/0091-3057(84)90017-0.
122. Stewart J, de Wit H, Eikelboom R. Role of unconditioned and conditioned drug effects in the self-administration of opiates and stimulants. Psychological Review. 1984;91(2):251-68. doi: 10.1037/0033-295X.91.2.251.
123. de Wit H, Stewart J. Reinstatement of cocaine-reinforced responding in the rat. Psychopharmacology. 1981;75(2):134-43. doi: 10.1007/BF00432175.
124. Calu DJ, Kawa AB, Marchant NJ, Navarre BM, Henderson MJ, Chen B, et al. Optogenetic inhibition of dorsal medial prefrontal cortex attenuates stress-induced reinstatement of palatable food seeking in female rats. The Journal of Neuroscience. 2013;33(1):214-26. doi: 10.1523/jneurosci.2016-12.2013.
125. Bossert JM, Stern AL, Theberge FRM, Cifani C, Koya E, Hope BT, et al. Ventral medial prefrontal cortex neuronal ensembles mediate context-induced relapse to heroin. Nature Neuroscience. 2011;14(4):420-2. doi: 10.1038/nn.2758.
126. McLaughlin RJ, Floresco SB. The role of different subregions of the basolateral amygdala in cue-induced reinstatement and extinction of food-seeking behavior. Neuroscience. 2007;146(4):1484-94. doi: 10.1016/j.neuroscience.2007.03.025.
127. Ishikawa A, Ambroggi F, Nicola SM, Fields HL. Contributions of the amygdala and medial prefrontal cortex to incentive cue responding. Neuroscience. 2008;155(3):573-84. doi: 10.1016/j.neuroscience.2008.06.037.
128. Chen Y-W, Fiscella KA, Bacharach SZ, Tanda G, Shaham Y, Calu DJ. Effect of yohimbine on reinstatement of operant responding in rats is dependent on cue contingency but not food reward history. Addiction Biology. 2015;20(4):690-700. doi: 10.1111/adb.12164.
129. Skinner BF, Heron WT. Effects of caffeine and benzedrine upon conditioning and extinction. Psychological Record. 1937;1:340-6.
130. Shaham Y, Stewart J. Effects of opioid and dopamine receptor antagonists on relapse induced by stress and re-exposure to heroin in rats. Psychopharmacology. 1996;125(4):385-91. doi: 10.1007/bf02246022.
131. Mantsch JR, Baker DA, Funk D, Le AD, Shaham Y. Stress-induced reinstatement of drug seeking: 20 years of progress. Neuropsychopharmacology. 2016;41(1):335-56. doi: 10.1038/npp.2015.142.
132. Buffalari DM, See RE. Footshock stress potentiates cue-induced cocaine-seeking in an animal model of relapse. Physiology & Behavior. 2009;98(5):614-7. doi: 10.1016/j.physbeh.2009.09.013.
133. Reiner DJ, Fredriksson I, Lofaro OM, Bossert JM, Shaham Y. Relapse to opioid seeking in rat models: behavior, pharmacology and circuits. Neuropsychopharmacology. 2019;44(3):465-77. doi: 10.1038/s41386-018-0234-2.
134. Venniro M, Caprioli D, Shaham Y. Chapter 2 - Animal models of drug relapse and craving: From drug priming-induced reinstatement to incubation of craving after voluntary abstinence. In: Ekhtiari H, Paulus MP, editors. Neuroscience for Addiction Medicine: From Prevention to Rehabilitation - Methods and Interventions. vol 224 of Progress in Brain Research. Amsterdam: Elsevier; 2016. p. 25-52.
135. Vanderschuren LJMJ, Ahmed SH. Animal models of the behavioral symptoms of substance use disorders. Cold Spring Harbor Perspectives in Medicine. 2020;Advance online publication. doi: 10.1101/cshperspect.a040287.
136. Panlilio LV, Thorndike EB, Schindler CW. Reinstatement of punishment-suppressed opioid self-administration in rats: an alternative model of relapse to drug abuse. Psychopharmacology. 2003;168(1):229-35. doi: 10.1007/s00213-002-1193-0.
137. Farrell MR, Ruiz CM, Castillo E, Faget L, Khanbijian C, Liu S, et al. Ventral pallidum is essential for cocaine relapse after voluntary abstinence in rats. Neuropsychopharmacology. 2019;44(13):2174-85. doi: 10.1038/s41386-019-0507-4.
138. Venniro M, Russell TI, Zhang M, Shaham Y. Operant social reward decreases incubation of heroin craving in male and female rats. Biological Psychiatry. 2019;86(11):848-56. doi: 10.1016/j.biopsych.2019.05.018.
139. Marchant NJ, Khuc TN, Pickens CL, Bonci A, Shaham Y. Context-induced relapse to alcohol seeking after punishment in a rat model. Biological Psychiatry. 2013;73(3):256-62. doi: 10.1016/j.biopsych.2012.07.007.
140. Reiner DJ, Lofaro OM, Applebey SV, Korah H, Venniro M, Cifani C, et al. Role of projections between piriform cortex and orbitofrontal cortex in relapse to fentanyl seeking after palatable food choice-induced voluntary abstinence. The Journal of Neuroscience. 2020;40(12):2485-97. doi: 10.1523/jneurosci.2693-19.2020.
141. Marchant NJ, Campbell EJ, Pelloux Y, Bossert JM, Shaham Y. Context-induced relapse after extinction versus punishment: similarities and differences. Psychopharmacology. 2019;236(1):439-48. doi: 10.1007/s00213-018-4929-1.
142. Freese L, Durand A, Guillem K, Ahmed SH. Pre-trial cocaine biases choice toward cocaine through suppression of the nondrug option. Pharmacology Biochemistry and Behavior. 2018;173:65-73. doi: 10.1016/j.pbb.2018.07.010.
143. Hogarth L, Balleine BW, Corbit LH, Killcross S. Associative learning mechanisms underpinning the transition from recreational drug use to addiction. Annals of the New York Academy of Sciences. 2013;1282(1):12-24. doi: 10.1111/j.1749-6632.2012.06768.x.
144. Cunningham CL. Alcohol as a cue for extinction: State dependency produced by conditioned inhibition. Animal Learning & Behavior. 1979;7(1):45-52. doi: 10.3758/BF03209656.
145. Chen Y-W, Fiscella KA, Bacharach SZ, Calu DJ. Effect of cafeteria diet history on cue-, pellet-priming-, and stress-induced reinstatement of food seeking in female rats. PLOS ONE. 2014;9(7):e102213. doi: 10.1371/journal.pone.0102213.
146. Shaham Y, Stewart J. Stress reinstates heroin-seeking in drug-free animals: An effect mimicking heroin, not withdrawal. Psychopharmacology. 1995;119(3):334-41. doi: 10.1007/BF02246300.
147. Shaham Y, Rajabi H, Stewart J. Relapse to heroin-seeking in rats under opioid maintenance: the effects of stress, heroin priming, and withdrawal. The Journal of Neuroscience. 1996;16(5):1957-63. doi: 10.1523/jneurosci.16-05-01957.1996.
148. Baarendse PJJ, Limpens JHW, Vanderschuren LJMJ. Disrupted social development enhances the motivation for cocaine in rats. Psychopharmacology. 2014;231(8):1695-704. doi: 10.1007/s00213-013-3362-8.
149. Schepers ST, Bouton ME. Hunger as a context: Food seeking that is inhibited during hunger can renew in the context of satiety. Psychological Science. 2017;28(11):1640-8. doi: 10.1177/0956797617719084.
150. Schepers ST, Bouton ME. Stress as a context: Stress causes relapse of inhibited food seeking if it has been associated with prior food seeking. Appetite. 2019;132:131-8. doi: 10.1016/j.appet.2018.10.016.
151. Koob GF, Le Moal M. Drug addiction, dysregulation of reward, and allostasis. Neuropsychopharmacology. 2001;24(2):97-129. doi: 10.1016/S0893-133X(00)00195-0.
152. Koob GF, Le Moal M. Addiction and the brain antireward system. Annual Review of Psychology. 2008;59(1):29-53. doi: 10.1146/annurev.psych.59.103006.093548.
153. Solomon RL, Corbit JD. An opponent-process theory of motivation: I. Temporal dynamics of affect. Psychological Review. 1974;81(2):119-45. doi: 10.1037/h0036128.
154. Trask S, Thrailkill EA, Bouton ME. Occasion setting, inhibition, and the contextual control of extinction in Pavlovian and instrumental (operant) learning. Behavioural Processes. 2017;137:64-72. doi: 10.1016/j.beproc.2016.10.003.
155. Floresco SB, McLaughlin RJ, Haluk DM. Opposing roles for the nucleus accumbens core and shell in cue-induced reinstatement of food-seeking behavior. Neuroscience. 2008;154(3):877-84. doi: 10.1016/j.neuroscience.2008.04.004.
156. Yager LM, Robinson TE. Cue-induced reinstatement of food seeking in rats that differ in their propensity to attribute incentive salience to food cues. Behavioural Brain Research. 2010;214(1):30-4. doi: 10.1016/j.bbr.2010.04.021.
157. Brown RM, Kim AK, Khoo SY-S, Kim JH, Jupp B, Lawrence AJ. Orexin-1 receptor signalling in the prelimbic cortex and ventral tegmental area regulates cue-induced reinstatement of ethanol-seeking in iP rats. Addiction Biology. 2016;21(3):603-12. doi: 10.1111/adb.12251.
158. Moorman DE, James MH, Kilroy EA, Aston-Jones G. Orexin/hypocretin neuron activation is correlated with alcohol seeking and preference in a topographically specific manner. European Journal of Neuroscience. 2016;43(5):710-20. doi: 10.1111/ejn.13170.
159. Smith RJ, See RE, Aston-Jones G. Orexin/hypocretin signaling at the orexin 1 receptor regulates cue-elicited cocaine-seeking. European Journal of Neuroscience. 2009;30(3):493-503. doi: 10.1111/j.1460-9568.2009.06844.x.
160. Namba MD, Tomek SE, Olive MF, Beckmann JS, Gipson CD. The winding road to relapse: Forging a new understanding of cue-induced reinstatement models and their associated neural mechanisms. Frontiers in Behavioral Neuroscience. 2018;12(17). doi: 10.3389/fnbeh.2018.00017.
161. Perry CJ, Zbukvic I, Kim JH, Lawrence AJ. Role of cues and contexts on drug-seeking behaviour. British Journal of Pharmacology. 2014;171(20):4636-72. doi: 10.1111/bph.12735.
162. See RE. Neural substrates of cocaine-cue associations that trigger relapse. European Journal of Pharmacology. 2005;526(1):140-6. doi: 10.1016/j.ejphar.2005.09.034.
163. Kruzich PJ, See RE. Differential contributions of the basolateral and central amygdala in the acquisition and expression of conditioned relapse to cocaine-seeking behavior. The Journal of Neuroscience. 2001;21(14):RC155-RC. doi: 10.1523/JNEUROSCI.21-14-j0002.2001.
164. Buffalari DM, Feltenstein MW, See RE. The effects of varied extinction procedures on contingent cue-induced reinstatement in Sprague-Dawley rats. Psychopharmacology. 2013;230(2):319-27. doi: 10.1007/s00213-013-3156-z.
165. Torregrossa MM, Sanchez H, Taylor JR. D-Cycloserine reduces the context specificity of pavlovian extinction of cocaine cues through actions in the nucleus accumbens. The Journal of Neuroscience. 2010;30(31):10526-33. doi: 10.1523/jneurosci.2523-10.2010.
166. Perry CJ, Reed F, Zbukvic IC, Kim JH, Lawrence AJ. The metabotropic glutamate 5 receptor is necessary for extinction of cocaine-associated cues. British Journal of Pharmacology. 2016;173(6):1085-94. doi: 10.1111/bph.13437.
167. Zbukvic IC, Ganella DE, Perry CJ, Madsen HB, Bye CR, Lawrence AJ, et al. Role of dopamine 2 receptor in impaired drug-cue extinction in adolescent rats. Cerebral Cortex. 2016;26(6):2895-904. doi: 10.1093/cercor/bhw051.
168. Madsen HB, Zbukvic IC, Luikinga SJ, Lawrence AJ, Kim JH. Extinction of conditioned cues attenuates incubation of cocaine craving in adolescent and adult rats. Neurobiology of Learning and Memory. 2017;143:88-93. doi: 10.1016/j.nlm.2016.09.002.
169. Prasad AA, McNally GP. Ventral pallidum output pathways in context-induced reinstatement of alcohol seeking. The Journal of Neuroscience. 2016;36(46):11716-26. doi: 10.1523/jneurosci.2580-16.2016.
170. Williams BA. Conditioned reinforcement: Experimental and theoretical issues. The Behavior Analyst. 1994;17(2):261-85. doi: 10.1007/BF03392675.
171. Williams BA. Conditioned reinforcement: Neglected or outmoded explanatory construct? Psychonomic Bulletin & Review. 1994;1(4):457-75. doi: 10.3758/BF03210950.
172. Shahan TA. Conditioned reinforcement and response strength. Journal of the Experimental Analysis of Behavior. 2010;93(2):269-89. doi: 10.1901/jeab.2010.93-269.
173. Burke K, Franz T, Miller D, Schoenbaum G. Conditioned reinforcement can be mediated by either outcome-specific or general affective representations. Frontiers in Integrative Neuroscience. 2007;1(2). doi: 10.3389/neuro.07.002.2007.
174. Samaha AN, Minogianis EA, Nachar W. Cues paired with either rapid or slower self-administered cocaine injections acquire similar conditioned rewarding properties. PLoS ONE. 2011;6(10). doi: 10.1371/journal.pone.0026481.
175. Kawa AB, Valenta AC, Kennedy RT, Robinson TE. Incentive and dopamine sensitization produced by intermittent but not long access cocaine self-administration. European Journal of Neuroscience. 2019;50(4):2663-82. doi: 10.1111/ejn.14418.
176. Robinson TE, Berridge KC. The incentive sensitization theory of addiction: some current issues. Philosophical Transactions of the Royal Society B: Biological Sciences. 2008;363(1507):3137-46. doi: 10.1098/rstb.2008.0093.
177. Arroyo M, Markou A, Robbins TW, Everitt BJ. Acquisition, maintenance and reinstatement of intravenous cocaine self-administration under a second-order schedule of reinforcement in rats: effects of conditioned cues and continuous access to cocaine. Psychopharmacology. 1998;140(3):331-44. doi: 10.1007/s002130050774.
178. Smith SG, Werner TE, Davis WM. Alcohol-associated conditioned reinforcement. Psychopharmacology. 1977;53(3):223-6. doi: 10.1007/BF00492355.
179. Di Ciano P. Facilitated acquisition but not persistence of responding for a cocaine-paired conditioned reinforcer following sensitization with cocaine. Neuropsychopharmacology. 2008;33(6):1426-31. doi: 10.1038/sj.npp.1301542.
180. Di Ciano P, Everitt BJ. Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin or sucrose: implications for the persistence of addictive behaviour. Neuropharmacology. 2004;47:202-13. doi: 10.1016/j.neuropharm.2004.06.005.
181. Clemens KJ, Lay BPP, Holmes NM. Extended nicotine self-administration increases sensitivity to nicotine, motivation to seek nicotine and the reinforcing properties of nicotine-paired cues. Addiction Biology. 2017;22(2):400-10. doi: 10.1111/adb.12336.
182. Shahan TA. Moving beyond reinforcement and response strength. The Behavior Analyst. 2017;40(1):107-21. doi: 10.1007/s40614-017-0092-y.
183. Thrailkill EA, Shahan TA. Temporal integration and instrumental conditioned reinforcement. Learning & Behavior. 2014;42(3):201-8. doi: 10.3758/s13420-014-0138-x.
184. Ward RD, Gallistel CR, Jensen G, Richards VL, Fairhurst S, Balsam PD. Conditioned stimulus informativeness governs conditioned stimulus−unconditioned stimulus associability. Journal of Experimental Psychology: Animal Behavior Processes. 2012;38(3):217-32. doi: 10.1037/a0027621.
185. Parkinson JA, Roberts AC, Everitt BJ, Di Ciano P. Acquisition of instrumental conditioned reinforcement is resistant to the devaluation of the unconditioned stimulus. The Quarterly Journal of Experimental Psychology Section B. 2005;58(1b):19-30. doi: 10.1080/02724990444000023.
186. Plaza-Zabala A, Flores A, Martin-Garcia E, Saravia R, Maldonado R, Berrendero F. A role for hypocretin/orexin receptor-1 in cue-induced reinstatement of nicotine-seeking behavior. Neuropsychopharmacology. 2013;38(9):1724-36. doi: 10.1038/npp.2013.72.
187. Kumaresan V, Yuan M, Yee J, Famous KR, Anderson SM, Schmidt HD, et al. Metabotropic glutamate receptor 5 (mGluR5) antagonists attenuate cocaine priming- and cue-induced reinstatement of cocaine seeking. Behavioural Brain Research. 2009;202(2):238-44. doi: 10.1016/j.bbr.2009.03.039.
188. Guercio LA, Schmidt HD, Pierce RC. Deep brain stimulation of the nucleus accumbens shell attenuates cue-induced reinstatement of both cocaine and sucrose seeking in rats. Behavioural Brain Research. 2015;281:125-30. doi: 10.1016/j.bbr.2014.12.025.
189. Brown RM, Khoo SY-S, Lawrence AJ. Central orexin (hypocretin) 2 receptor antagonism reduces ethanol self-administration, but not cue-conditioned ethanol-seeking, in ethanol-preferring rats. The International Journal of Neuropsychopharmacology. 2013;16(9):2067-79. doi: 10.1017/S1461145713000333.
190. Tunstall BJ, Kearns DN. Cocaine can generate a stronger conditioned reinforcer than food despite being a weaker primary reinforcer. Addiction Biology. 2016;21(2):282-93. doi: 10.1111/adb.12195.
191. Caballero JP, Scarpa GB, Remage-Healey L, Moorman DE. Differential effects of dorsal and ventral medial prefrontal cortex inactivation during natural reward seeking, extinction, and cue-induced reinstatement. eneuro. 2019;6(5):ENEURO.0296-19.2019. doi: 10.1523/eneuro.0296-19.2019.
192. Deroche-Gamonet V, Piat F, Le Moal M, Piazza PV. Influence of cue-conditioning on acquisition, maintenance and relapse of cocaine intravenous self-administration. European Journal of Neuroscience. 2002;15(8):1363-70. doi: 10.1046/j.1460-9568.2002.01974.x.
193. Caggiula AR, Donny EC, White AR, Chaudhri N, Booth S, Gharib MA, et al. Cue dependency of nicotine self-administration and smoking. Pharmacology Biochemistry and Behavior. 2001;70(4):515-30. doi: 10.1016/S0091-3057(01)00676-1.
194. Caggiula AR, Donny EC, White AR, Chaudhri N, Booth S, Gharib MA, et al. Environmental stimuli promote the acquisition of nicotine self-administration in rats. Psychopharmacology. 2002;163(2):230-7. doi: 10.1007/s00213-002-1156-5.
195. Cohen C, Perrault G, Griebel G, Soubrié P. Nicotine-associated cues maintain nicotine-seeking behavior in rats several weeks after nicotine withdrawal: Reversal by the cannabinoid (CB1) receptor antagonist, rimonabant (SR141716). Neuropsychopharmacology. 2005;30(1):145-55. doi: 10.1038/sj.npp.1300541.
196. Liu X, Caggiula AR, Palmatier MI, Donny EC, Sved AF. Cue-induced reinstatement of nicotine-seeking behavior in rats: effect of bupropion, persistence over repeated tests, and its dependence on training dose. Psychopharmacology. 2008;196(3):365-75. doi: 10.1007/s00213-007-0967-9.
197. Cartoni E, Balleine B, Baldassarre G. Appetitive Pavlovian-instrumental Transfer: A review. Neuroscience & Biobehavioral Reviews. 2016;71:829-48. doi: 10.1016/j.neubiorev.2016.09.020.
198. Holmes NM, Marchand AR, Coutureau E. Pavlovian to instrumental transfer: A neurobehavioural perspective. Neuroscience & Biobehavioral Reviews. 2010;34(8):1277-95. doi: 10.1016/j.neubiorev.2010.03.007.
199. Trick L, Hogarth L, Duka T. Prediction and uncertainty in human Pavlovian to instrumental transfer. Journal of Experimental Psychology: Learning, Memory, and Cognition. 2011;37(3):757-65. doi: 10.1037/a0022310.
200. Derman RC, Ferrario CR. Enhanced incentive motivation in obesity-prone rats is mediated by NAc core CP-AMPARs. Neuropharmacology. 2018;131:326-36. doi: 10.1016/j.neuropharm.2017.12.039.
201. Alarcón DE, Delamater AR. Outcome-specific Pavlovian-to-instrumental transfer (PIT) with alcohol cues and its extinction. Alcohol. 2019;76:131-46. doi: 10.1016/j.alcohol.2018.09.003.
202. Krank MD. Pavlovian conditioning with ethanol: sign-tracking (autoshaping), conditioned incentive, and ethanol self-administration. Alcoholism: Clinical and Experimental Research. 2003;27(10):1592-8. doi: 10.1097/01.Alc.0000092060.09228.De.
203. Lamb RJ, Schindler CW, Pinkston JW. Conditioned stimuli’s role in relapse: preclinical research on Pavlovian-Instrumental-Transfer. Psychopharmacology. 2016;233(10):1933-44. doi: 10.1007/s00213-016-4216-y.
204. Manglani HR, Lewis AH, Wilson SJ, Delgado MR. Pavlovian-to-instrumental transfer of nicotine and food cues in deprived cigarette smokers. Nicotine & Tobacco Research. 2017;19(6):670-6. doi: 10.1093/ntr/ntx007.
205. Pielock SM, Lex B, Hauber W. The role of dopamine in the dorsomedial striatum in general and outcome-selective Pavlovian-instrumental transfer. European Journal of Neuroscience. 2011;33(4):717-25. doi: 10.1111/j.1460-9568.2010.07561.x.
206. Hall J, Parkinson JA, Connor TM, Dickinson A, Everitt BJ. Involvement of the central nucleus of the amygdala and nucleus accumbens core in mediating Pavlovian influences on instrumental behaviour. European Journal of Neuroscience. 2001;13(10):1984-92. doi: 10.1046/j.0953-816x.2001.01577.x.
207. Rescorla RA, Solomon RL. Two-process learning theory: Relationships between Pavlovian conditioning and instrumental learning. Psychological Review. 1967;74(3):151-82. doi: 10.1037/h0024475.
208. Estes WK. Discriminative conditioning. II. Effects of a Pavlovian conditioned stimulus upon a subsequently established operant response. Journal of Experimental Psychology. 1948;38(2):173-7. doi: 10.1037/h0057525.
209. Holland PC. Relations between Pavlovian-instrumental transfer and reinforcer devaluation. Journal of Experimental Psychology: Animal Behavior Processes. 2004;30(2):104-17. doi: 10.1037/0097-7403.30.2.104.
210. Augur IF, Wyckoff AR, Aston-Jones G, Kalivas PW, Peters J. Chemogenetic activation of an extinction neural circuit reduces cue-induced reinstatement of cocaine seeking. The Journal of Neuroscience. 2016;36(39):10174-80. doi: 10.1523/jneurosci.0773-16.2016.
211. Mahler SV, Brodnik ZD, Cox BM, Buchta WC, Bentzley BS, Quintanilla J, et al. Chemogenetic manipulations of ventral tegmental area dopamine neurons reveal multifaceted roles in cocaine abuse. The Journal of Neuroscience. 2019;39(3):503-18. doi: 10.1523/JNEUROSCI.0537-18.2018.
212. Smith RJ, Aston-Jones G. Orexin / hypocretin 1 receptor antagonist reduces heroin self-administration and cue-induced heroin seeking. European Journal of Neuroscience. 2012;35(5):798-804. doi: 10.1111/j.1460-9568.2012.08013.x.
213. Khoo SY-S, McNally GP, Clemens KJ. The dual orexin receptor antagonist TCS1102 does not affect reinstatement of nicotine-seeking. PLoS ONE. 2017;12(3):e0173967. doi: 10.1371/journal.pone.0173967.
214. Castino MR, Cornish JL, Clemens KJ. Inhibition of histone deacetylases facilitates extinction and attenuates reinstatement of nicotine self-administration in rats. PLoS ONE. 2015;10(4):e0124796. doi: 10.1371/journal.pone.0124796.
215. Rubio FJ, Quintana-Feliciano R, Warren BL, Li X, Witonsky KFR, Valle FSd, et al. Prelimbic cortex is a common brain area activated during cue-induced reinstatement of cocaine and heroin seeking in a polydrug self-administration rat model. European Journal of Neuroscience. 2019;49(2):165-78. doi: 10.1111/ejn.14203.
216. Leri F, Stewart J. Drug-induced reinstatement to heroin and cocaine seeking: A rodent model of relapse in polydrug use. Experimental and Clinical Psychopharmacology. 2001;9(3):297-306. doi: 10.1037/1064-1297.9.3.297.
217. Clemens KJ, Castino MR, Cornish JL, Goodchild AK, Holmes NM. Behavioral and neural substrates of habit formation in rats intravenously self-administering nicotine. Neuropsychopharmacology. 2014. doi: 10.1038/npp.2014.111.
218. Takahashi TT, Vengeliene V, Enkel T, Reithofer S, Spanagel R. Pavlovian to instrumental transfer responses do not correlate with addiction-like behavior in rats. Frontiers in Behavioral Neuroscience. 2019;13(129). doi: 10.3389/fnbeh.2019.00129.
219. Hogarth L. Addiction is driven by excessive goal-directed drug choice under negative affect: translational critique of habit and compulsion theory. Neuropsychopharmacology. 2020;45(5):720-35. doi: 10.1038/s41386-020-0600-8.
220. Belin D, Belin-Rauscent A, Murray JE, Everitt BJ. Addiction: failure of control over maladaptive incentive habits. Current Opinion in Neurobiology. 2013;23(4):564-72. doi: 10.1016/j.conb.2013.01.025.
221. Kalivas PW. Addiction as a pathology in prefrontal cortical regulation of corticostriatal habit circuitry. Neurotox Res. 2008;14(2-3):185-9. doi: 10.1007/BF03033809.
222. Bedi G, Preston KL, Epstein DH, Heishman SJ, Marrone GF, Shaham Y, et al. Incubation of cue-induced cigarette craving during abstinence in human smokers. Biological Psychiatry. 2011;69(7):708-11. doi: 10.1016/j.biopsych.2010.07.014.
223. Cannella N, Oliveira AMM, Hemstedt T, Lissek T, Buechler E, Bading H, et al. Dnmt3a2 in the nucleus accumbens shell is required for reinstatement of cocaine seeking. The Journal of Neuroscience. 2018;38(34):7516-28. doi: 10.1523/jneurosci.0600-18.2018.
224. Hull CL. Principles of behavior: An introduction to behavior theory. Elliott RM, editor. New York: Appleton-Century-Crofts Inc.; 1943.
225. Kamin LJ. The retention of an incompletely learned avoidance response. Journal of Comparative and Physiological Psychology. 1957;50(5):457-60. doi: 10.1037/h0044226.
226. Kamin LJ. Retention of an incompletely learned avoidance response: Some further analyses. Journal of Comparative and Physiological Psychology. 1963;56(4):713-8. doi: 10.1037/h0043941.
227. Tarpy RM. Incubation of anxiety as measured by response suppression. Psychonomic Science. 1966;4(1):189-90. doi: 10.3758/BF03342243.
228. Pinel JP, Mucha RF. Incubation and Kamin effects in the rat: Changes in activity and reactivity after footshock. Journal of Comparative and Physiological Psychology. 1973;84(3):661-8. doi: 10.1037/h0034890.
229. Anderson DC, Johnson L, Schwendiman G, Dunford G. Retention of an incompletely learned avoidance response: Some problems with replication. Psychonomic Science. 1966;6(1):23-4. doi: 10.3758/BF03327938.
230. Markou A, Li J, Tse K, Li X. Cue-induced nicotine-seeking behavior after withdrawal with or without extinction in rats. Addiction Biology. 2018;23(1):111-9. doi: 10.1111/adb.12480.
231. Sakurai T, Amemiya A, Ishii M, Matsuzaki I, Chemelli RM, Tanaka H, et al. Orexins and orexin receptors: A family of hypothalamic neuropeptides and G protein-coupled receptors that regulate feeding behavior. Cell. 1998;92(4):573-85. doi: 10.1016/s0092-8674(00)80949-6.
232. de Lecea L, Kilduff TS, Peyron C, Gao X-B, Foye PE, Danielson PE, et al. The hypocretins: Hypothalamus-specific peptides with neuroexcitatory activity. Proceedings of the National Academy of Sciences. 1998;95(1):322-7. doi: 10.1073/pnas.95.1.322.
233. Gotter AL, Webber AL, Coleman PJ, Renger JJ, Winrow CJ. International Union of Basic and Clinical Pharmacology. LXXXVI. Orexin receptor function, nomenclature and pharmacology. Pharmacological Reviews. 2012;64(3):389-420. doi: 10.1124/pr.111.005546.
234. Hauger RL, Grigoriadis DE, Dallman MF, Plotsky PM, Vale WW, Dautzenberg FM. International Union of Pharmacology. Xxxvi. Current status of the nomenclature for receptors for corticotropin-releasing factor and their ligands. Pharmacological Reviews. 2003;55(1):21-6. doi: 10.1124/pr.55.1.3.
235. Roger G. Hypothalamic hormones a.k.a. hypothalamic releasing factors. Journal of Endocrinology. 2005;184(1):11-28. doi: 10.1677/joe.1.05883.
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