Abstract
Finding effective long-lasting treatments for drug addiction has been an elusive goal. Consequently, researchers are beginning to investigate novel treatment strategies including manipulations of drug-associated memories. When environmental stimuli (cues) become associated with drug use, they become powerful motivators of continued drug use and relapse after abstinence. Reducing the strength of these cue–drug memories could decrease the number of factors that induce craving and relapse to aid in the treatment of addiction. Enhancing the consolidation of extinction learning and/or disrupting cue–drug memory reconsolidation are two strategies that have been proposed to reduce the strength of cues in motivating drug-seeking and drug-taking behavior. Here, we review the latest basic and clinical research elucidating the mechanisms underlying consolidation of extinction and reconsolidation of cue–drug memories in the hopes of developing pharmacological tools that exploit these signaling systems to treat addiction.
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Alberini CM (2005) Mechanisms of memory stabilization: are consolidation and reconsolidation similar or distinct processes? Trends Neurosci 28:51–56. doi:10.1016/j.tins.2004.11.001
Bassareo V, Di Chiara G (1999) Modulation of feeding-induced activation of mesolimbic dopamine transmission by appetitive stimuli and its relation of motivational state. Eur J Neurosci 11:4389–4397. doi:10.1046/j.1460-9568.1999.00843.x
Bassareo V, De Luca MA, Di Chiara G (2002) Differential expression of motivational stimulus properties of by dopamine in nucleus accumbens shell versus core and prefrontal cortex. J Neurosci 22:4709–4719
Bernardi RE, Lattal KM, Berger SP (2006) Postretrieval propranolol disrupts a cocaine conditioned place preference. Neuroreport 17:1443–1447. doi:10.1097/01.wnr.0000233098.20655.26
Botreau F, Paolone G, Stewart J (2006) D-cycloserine facilitates extinction of a cocaine-induced conditioned place preference. Behav Brain Res 15:173–178. doi:10.1016/j.bbr.2006.05.012
Bouton ME (2002) Context, ambiguity, and unlearning: sources of relapse after behavioral extinction. Biol Psychiatry 52:976–986. doi:10.1016/S0006-3223(02)01546-9
Bouton ME (2004) Context and behavioral processes in extinction. Learn Mem 11:485–494. doi:10.1101/lm.78804
Bouton ME, Bolles RC (1979) Role of conditioned contextual stimuli in reinstatement of conditioned fear. J Exp Psychol Anim Behav Process 5:368–378
Bozon B, Davis S, Laroche S (2003) A requirement for the immediate early gene zif268 in reconsolidation of recognition memory after retrieval. Neuron 40:695–701. doi:10.1016/S0896-6273(03)00674-3
Brown TE, Forquer MR, Cocking DL, Jansen HT, Harding JW, Sorg BA (2007) Role of matrix metalloproteinases in the acquisition and reconsolidation of cocaine-induced conditioned place preference. Learn Mem 14:214–223. doi:10.1101/lm.476207
Brown TE, Lee BR, Sorg BA (2008) The NMDA antagonist MK-801 disrupts reconsolidation of a cocaine-associated memory for conditioned place preference but not for self-administration in rats. Learn Mem 15:857–865. doi:10.1101/lm.1152808
Brunet A, Orr SP, Tremblay J, Robertson K, Nader K, Pitman RK (2008) Effect of post-retrieval propranolol on pscyhophysiologic responding during subsequent script-driven traumatic imagery in post-traumatic stress disorder. J Psychiatry Res 42:503–506. doi:10.1016/j.jpsychires.2007.05.006
Brunet A, Poundja J, Tremblay J, Bui E, Thomas E, Orr S, Azzoug A, Birmes P, Pitman RK (2011) Trauma reactivation under the influence of propranolol decreases posttraumatic stress symptoms and disorder: 3 open-label trials. J Clin Psychopharmacol 31:547–550. doi:10.1097/JCP.0b013e318222f360
Carter BL, Tiffany ST (1999) Meta-analysis of cue-reactivity in addiction research. Addiction 94:327–340. doi:10.1046/j.1360-0443.1999.9433273.x
Chan WY, Leung HT, Westbrook RF, McNally GP (2010) Effects of recent exposure to a conditioned stimulus on extinction of Pavlovian fear conditioning. Learn Mem 17:512–521. doi:10.1101/lm.1912510
Chaudhri N, Sahuque LL, Janak PH (2008) Context-induced relapse of conditioned behavioral responding to ethanol cues in rats. Biol Psychiatry 64:203–210. doi:10.1016/j.biopsych.2008.03.007
Clem RL, Huganir RL (2010) Calcium-permeable AMPA receptor dynamics mediate fear memory erasure. Science 330:1108–1112. doi:10.1126/science.1195298
Conklin CA, Tiffany ST (2002) Applying extinction research and theory to cue-exposure addiction treatments. Addiction 97:155–167. doi:10.1046/j.1360-0443.2002.00014.x
Corcoran KA, Maren S (2001) Hippocampal inactivation disrupts contextual retrieval of fear memory after extinction. J Neurosci 21:1720–1726
Corcoran KA, Maren S (2004) Factors regulating the effects of hippocampal inactivation on renewal of conditional fear after extinction. Learn Mem 11:598–603. doi:10.1101/lm.78704
de la Fuente V, Freudenthal R, Romano A (2011) Reconsolidation or extinction: transcription factor switch in the determination of memory course after retrieval. J Neurosci 31:5562–5573. doi:10.1523/JNEUROSCI.6066-10.2011
de Quervain DJ (2008) Glucocorticoid-induced reduction of traumatic memories: implications for the treatment of PTSD. Prog Brain Res 167:239–247. doi:10.1016/S0079-6123(07)67017-4
de Quervain DJ, Margraf J (2008) Glucocorticoids for the treatment of post-traumatic stress disorder and phobias: a novel therapeutic approach. Eur J Pharmacol 583:365–371. doi:10.1016/j.ejphar.2007.11.068
Debiec J, LeDoux JE (2006) Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: treatment implications for PTSD. Ann NY Acad Sci 1071:521–524. doi:10.1196/annals.1364.056
Debiec J, Doyere V, Nader K, LeDoux JE (2006) Directly reactivated, but not indirectly reactivated memories undergo reconsolidation in the amygdala. Proc Natl Acad Sci USA 103:3428–3433. doi:10.1073/pnas.0507168103
Debiec J, Diaz-Mataix L, Bush DEA, Doyere V, LeDoux JE (2010) The amygdala encodes specific sensory features of an aversive reinforcer. Nat Neurosci 13:536–537. doi:10.1038/nn.2520
Debiec J, Bush DE, LeDoux JE (2011) Noradrenergic enhancement of reconsolidation in the amygdala impairs extinction of conditioned fear in rats—a possible mechanism for the persistence of traumatic memories in PTSD. Depress Anxiety 28:186–193. doi:10.1002/da.20803
Di Chiara G (2002) Nucleus accumbens shell and core dopamine: differential role in behavior and addiction. Behav Brain Res 137:75–114. doi:10.1016/S0166-4328(02)00286-3
Di Ciano P, Everitt BJ (2004) Conditioned reinforcing properties of stimuli paired with self-administered cocaine, heroin, or sucrose: implications for the persistence of addictive behaviour. Neuropharmacol 47:202–213. doi:10.1016/jneuropharm.2004.06.005
Doyere V, Debiec J, Monfils MH, Schafe GE, LeDoux JE (2007) Synapse-specific reconsolidation of distinct fear memories in the lateral amygdala. Nat Neurosci 10:414–416. doi:10.1038/nn1871
Drummond DC (2000) What does cue-reactivity have to offer clinical research? Addiction 95:S129–144
Drummond DC, Glautier S (1994) A controlled trial of cue exposure treatment in alcohol dependence. J Consult Clin Psychol 62:809–817. doi:10.1037/0022-006X.62.4.809
Dudai Y (2004) The neurobiology of consolidations, or, how stable is the engram? Ann Rev Psychol 55:51–86. doi:10.1146/annurev.psych.55.090902.142050
Eisenberg M, Dudai Y (2004) Reconsolidation of fresh, remote, and extinguished fear memory in medaka: old fears don’t die. Eur J Neurosci 20:3397–3403. doi:10.1111/j.1460-9568.2004.03818.x
Eisenberg M, Kobilo T, Berman DE, Dudai Y (2003) Stability of retrieved memory: inverse correlation with trace dominance. Science 301:1102–1104. doi:10.1126/science.1086881
Eisenhardt D, Menzel R (2007) Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiol Learn Mem 87:167–173. doi:10.1016/j.nlm.2006.09.005
Feltenstein MW, See RE (2007) NMDA receptor blockade in the basolateral amygdala disrupts consolidation of stimulus–reward memory and extinction learning during reinstatement of cocaine-seeking in an animal model of relapse. Neurobiol Learn Mem 88:435–444. doi:10.1016/j.nlm.2007.05.006
Field M, Duka T (2002) Cues paired with a low dose of alcohol acquire conditioned incentive properties in social drinkers. Psychopharmacol 159:325–334. doi:10.1007/s00213-001-0923-z
Flavell CR, Barber DJ, Lee JL (2011) Behavioural memory reconsolidation of food and fear memories. Nat Commun 2:504. doi:10.1038/ncomms1515
Foltin RW, Haney M (2000) Conditioned effects of environmental stimuli paired with smoked cocaine in humans. Psychopharmacol 149:24–33. doi:10.1007/s002139900340
Font L, Cunningham CL (2012) Post-retrieval propranolol treatment does not modulate reconsolidation or extinction of ethanol-induced conditioned place preference. Pharmacol Biochem Behav 101:222–230. doi:10.1016/j.pbb.2012.01.009
Franken IH, de Haan HA, van der Meer CW, Haffmans PM, Hendriks VM (1999) Cue reactivity and effects of cue exposure in abstinent posttreatment drug users. J Subst Abuse Treat 16:81–85, PII: S0740-5472(98)00004-X
Freeman TP, Morgan CJ, Beesley T, Curran HV (2012) Drug cue induced overshadowing: selective disruption of natural reward processing by cigarette cues amongst abstinent but not satiated smokers. Psychol Med 42:161–171. doi:10.1017/S0033291711001139
Fuchs RA, Feltenstein MW, See RE (2006) The role of the basolateral amygdala in stimulus-reward memory and extinction memory consolidation and in subsequent conditioned cued reinstatement of cocaine seeking. Eur J Neurosci 23:2809–2813. doi:10.1111/j.1460-9568.2006.04806.x
Fuchs RA, Bell GH, Ramirez DR, Eaddy JL, Su ZI (2009) Basolateral amygdala involvement in memory reconsolidation processes that facilitate drug context-induced cocaine seeking. Eur J Neurosci 30:889–900. doi:10.1111/j.1460-9568.2009.06888.x
Hamlin AS, Clemens KJ, McNally GP (2008) Renewal of extinguished cocaine-seeking. Neurosci 151:650–670. doi:10.1016/j.neuroscience.2007.11.018
Hobin JA, Ji J, Maren S (2006) Ventral hippocampal muscimol disrupts context-specific fear memory retrieval after extinction in rats. Hippocampus 16:174–182. doi:10.1002/hipo.20144
Hofmann SG, Huweler R, Mackillop J, Kantak KM (2012) Effects of d-cycloserine on craving to alcohol cues in problem drinkers: preliminary findings. Am J Drug Alcohol Abuse 38:101–107. doi:10.3109/00952990.2011.600396
Hyman SE, Malenka RC, Nestler EJ (2006) Neural mechanisms of addiction: the role of reward-related learning and memory. Annu Rev Neurosci 29:565–598. doi:10.1146/annurev.neuro.29.051605.113009
Inda MC, Muravieva EV, Alberini CM (2011) Memory retrieval and the passage of time: from reconsolidation and strengthening to extinction. J Neurosci 31:1635–1643. doi:10.1523/JNEUROSCI.4736-10.2011
Itzhak Y, Anderson KL (2007) Memory reconsolidation of cocaine-associated context requires nitric oxide signaling. Synapse 61:1002–1005. doi:10.1002/syn.20446
Jentsch JD, Taylor JR (1999) Impulsivity resulting from frontostriatal dysfunction in drug abuse: implications for the control of behavior by reward-related stimuli. Pychopharmacol 146:373–390. doi:10.1007/PL00005483
Kalivas PW, Peters J, Knackstedt L (2006) Animal models and brain circuits in drug addiction. Mol Interven 6:339–344
Kamboj SK, Massey-Chase R, Rodney L, Das R, Almahdi B, Curran HV, Morgan CJA (2011a) Changes in cue reactivity and attentional bias following experimental cue exposure and response prevention: a laboratory of the effects of d-cycloserine in heavy drinkers. Psychopharmacol 217:25–37. doi:10.1007/s00213-011-2254-z
Kamboj SK, Joye A, Das RK, Gibson AJW, Morgan CJA, Curran HV (2011b) Cue exposure and response prevention with heavy smokers: a laboratory-based randomized placebo-controlled trial examining the effects of d-cycloserine on cue reactivity and attentional bias. Psychopharmacol. doi:10.1007/s00213-011-2571-2
Kearns DN, Weiss SJ (2007) Contextual renewal of cocaine seeking in rats and its attenuation by the conditioned effects of an alternative reinforcer. Drug Alcohol Depend 90:193–202. doi:10.1016/j.drugalcdep.2007.03.006
Kelamangalath L, Seymour CM, Wagner JJ (2009) D-serine facilitates the effects of extinction to reduce cocaine-primed reinstatement of drug-seeking behavior. Neurobiol Learn Mem 92:544–551. doi:10.1016/j.nlm.2009.07.004
Kelley JB, Anderson KL, Itzhak Y (2007) Long-term memory of cocaine-associated context: disruption and reinstatement. Neuroreport 18:777–780. doi:10.1097/WNR.0b013e3280c1e2e7
Kida S, Josselyn SA, de Ortiz SP, Kogan JH, Chevere I, Masushige S, Silva AJ (2002) CREB required for the stability of new and reactivated fear memories. Nat Neurosci 5:348–355. doi:10.1038/nn819
Kindt M, Soeter M (2011) Reconsolidation in a human fear conditioning study: a test of extinction as updating mechanism. Biol Psychol. doi:10.1016/j.biopsycho.2011.09.016
Kindt M, Soeter M, Vervliet B (2009) Beyond extinction: erasing human fear responses and preventing the return of fear. Nat Neurosci 12:256–258. doi:10.1038/nn.2271
Koya E, Uejima JL, Wihbey KA, Bossert JM, Hope BT, Shaham Y (2008) Role of ventral medial prefrontal cortex in incubation of cocaine craving. Neuropharmacol 56(Suppl 1):177–185. doi:10.1016/j.neuropharm.2008.04.022
Kuntze MF, Stoermer R, Mager R, Roessler A, Mueller-Spahn F, Bullinger AH (2001) Immersive virtual environments in cue exposure. Cyberpsychol Behav 4:497–501. doi:10.1089/109493101750527051
Ledgerwood L, Richardson R, Cranney J (2003) Effects of D-cycloserine on extinction of conditioned freezing. Behav Neurosci 117:341–349. doi:10.1037/0735-7044.117.2.341
Ledgerwood L, Richardson R, Cranney J (2004) D-cycloserine and the facilitation of extinction of conditioned fear: consequences for reinstatement. Behav Neurosci 118:505–513. doi:10.1037/0735-7044.118.3.505
Lee JL (2008) Memory reconsolidation mediates the strengthening of memories by additional learning. Nat Neurosci 11:1264–1266. doi:10.1038/nn.2205
Lee JL, Di Ciano P, Thomas KL, Everitt BJ (2005) Disrupting reconsolidation of drug memories reduces cocaine-seeking behavior. Neuron 47:795–801. doi:10.1016/j.neuron.2005.08.007
Lee JL, Milton AL, Everitt BJ (2006) Cue-induced cocaine seeking and relapse are reduced by disruption of drug memory reconsolidation. J Neurosci 26:5881–5887. doi:10.1523/JNEUROSCI.0323-06.2006
Lee J-H, Kwon H, Choi J, Yang B-H (2007) Cue-exposure therapy to decrease alcohol craving in virtual environment. Cyberpsychol Behav 10:617–623. doi:10.1089/cpb.2007.9978
Lee JL, Gardner RJ, Butler VJ, Everitt BJ (2009) D-cycloserine potentiates the reconsolidation of cocaine-associated memories. Learn Mem 16:82–85. doi:10.1101/lm.1186609
Leri F, Stewart J (2002) The consequences of different “lapses” on relapse to heroin seeking in rats. Exp Clin Psychopharmacol 10:339–349. doi:10.1037/1064-1297.10.4.339
Li FQ, Xue YX, Wang JS, Fang Q, Li YQ, Zhu WL, He YY, Liu JF, Xue LF, Shaham Y, Lu L (2010) Basolateral amygdala cdk5 activity mediates consolidation and reconsolidation of memories for cocaine cues. J Neurosci 30:10451–10359. doi:10.1523/JNEUROSCI.2112-10.2010
Li YQ, Xue YX, He YY, Li FQ, Xue LF, Xu CM, Sacktor TC, Shaham Y, Lu L (2011) Inhibition of PKMzeta in nucleus accumbens core abolishes long-term drug reward memory. J Neurosci 31:5436–5446. doi:10.1523/JNEUROSCI.5884-10.2011
Lindgren JL, Gallagher M, Holland PC (2003) Lesions of basolateral amygdala impair extinction of CS motivational value, but not of explicit conditioned responses, in Pavlovian appetitive second-order conditioning. Eur J Neurosci 17:160–166. doi:10.1046/j.1460-9568.2003.02421.x
Lynch WJ, Taylor JR (2005) Persistent changes in motivation to self-administer cocaine following modulation of cyclic AMP-dependent kinase A (PKA) activity in the nucleus accumbens. Eur J Neurosci 22:1214–1220. doi:10.1111/j.1460-9568.2005.04305.x
Ma X, Zhang JJ, Yu LC (2011) Post-retrieval extinction training enhances or hinders the extinction of morphine-induced conditioned place preference in rats dependent on the retrieval–extinction interval. Psychopharmacol. doi:10.1007/s00213-011-2545-4
Marissen MA, Franken IH, Blanken P, van den Brink W, Hendriks VM (2007) Cue exposure therapy for the treatment of opiate addiction: results of a randomized controlled clinical trial. Psychother Psychosom 76:97–105. doi:10.1159/000097968
McCleery JM, Harvey AG (2004) Integration of psychological and biological approaches to trauma memory: implications for pharmacological prevention of PTSD. J Trauma Stress 17:485–496
McLaughlin J, See RE (2003) Selective inactivation of the dorsomedial prefrontal cortex and the basolateral amygdala attenuates conditioned-cued reinstatement of extinguished cocaine-seeking behavior in rats. Psychopharmacol 168:57–65. doi:10.1007/s00213-002-1196-x
Meil WM, See RE (1997) Lesions of the basolateral amygdala abolish the ability of drug associated cues to reinstate responding during withdrawal from self-administered cocaine. Behav Brain Res 87:139–148. doi:10.1016/S0166-4328(96)02270-X
Merlo E, Romano A (2008) Memory extinction entails the inhibition of transcription factor NF-kappaB. PLoS One 3:e3687. doi:10.1371/journal.pone.0003687
Merlo E, Freudenthal R, Maldonado H, Romano A (2005) Activation of the transcription factor NF-kappaB by retrieval is required for long-term memory reconsolidation. Learn Mem 12:23–29. doi:10.1101/lm.82705
Mihinidou C, Vouillac C, Koob GF, Ahmed SH (2011) Preclinical validation of a novel cocaine exposure therapy for relapse prevention. Biol Psychiatry 70:593–598. doi:10.1016/j.biopsych.2011.03.036
Miller CA, Marshall JF (2005) Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47:873–884. doi:10.1016/j.neuron.2005.08.006
Milton AL, Lee JL, Butler VJ, Gardner R, Everitt BJ (2008a) Intra-amygdala and systemic antagonism of NMDA receptors prevents the reconsolidation of drug-associated memory and impairs subsequently both novel and previously acquired drug-seeking behaviors. J Neurosci 28:8230–8237. doi:10.1523/JNEUROSCI.1723-08.2008
Milton AL, Lee JLC, Everitt BJ (2008b) Reconsolidation of appetitive memories for both natural and drug reinforcement is dependent on B-adrenergic receptors. Learn Mem 15:88–92. doi:10.1101/lm.825008
Milton AL, Schramm MJW, Wawrzynski JR, Gore F, Oikonomou-Mpegeti F, Wang NQ, Samuel D, Economidou D, Everitt BJ (2012) Antagonism at NMDA receptors, but not beta-adrenergic receptors, disrupts the reconsolidation of Pavlovian conditioned approach and instrumental transfer for ethanol-associated conditioned stimuli. Psychopharmacol 219:751–761. doi:10.1007/s00213-011-2399-9
Monfils MH, Cowansage KK, Klann E, LeDoux JE (2009) Extinction–reconsolidation boundaries: key to persistent attenuation of fear memories. Science 324:951–955. doi:10.1126/science.1167975
Muller J, Corodimas KP, Fridel Z, LeDoux JE (1997) Functional inactivation of the lateral and basal nuclei of the amygdala by muscimol infusion prevents fear conditioning to an explicit conditioned stimulus and to contextual stimuli. Behav Neurosci 111:683–691
Muravieva EV, Alberini CM (2010) Limited efficacy of propranolol on the reconsolidation of fear memories. Learn Mem 17:306–313. doi:10.1101/lm.1794710
Nader K, Schafe GE, LeDoux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722–726. doi:10.1038/35021052
Nestler EJ (2004) Molecular mechanisms of drug addiction. Neuropharmacol 47:24–32. doi:10.1016/j.neuropharm.2004.06.031
Nic Dhonnchadha BA, Szalay JJ, Achat-Mendes C, Platt DM, Otto MW, Spealman RD, Kantak KM (2010) D-cycloserine deters reacquisition of cocaine self-administration by augmenting extinction learning. Neuropsychopharmacol 35:357–367. doi:10.1038/npp.2009.139
O’Brien CP, Childress AR, McLellan T, Ehrman R (1990) Integrating systemic cue exposure with standard treatment in recovering drug dependent patients. Addictive Behav 15:355–365
Otis JM, Mueller D (2011) Inhibition of beta-adrenergic receptors induces a persistent deficit in retrieval of a cocaine-associated memory providing protection against reinstatement. Neuropsychopharmacol 36:1912–1920. doi:10.1038/npp.2011.77
Paolone G, Botreau F, Stewart J (2009) The facilitative effects of D-cycloserine on extinction of a cocaine-induced conditioned place preference can be long lasting and resistant to reinstatement. Psychopharmacol 202:403–409. doi:10.1007/s00213-008-1280-y
Parker LA, Limebeer CL, Slomke J (2006) Renewal effect: context-dependent extinction of a cocaine- and a morphine-induced conditioned floor preference. Psychopharmacol 187:133–137. doi:10.1007/s00213-006-0422-3
Pedreira ME, Maldonado H (2003) Protein synthesis subserves reconsolidation or extinction depending on reminder duration. Neuron 38:863–869. doi:10.1016/S0896-6273(03)00352-0
Peters J, LaLumiere RT, Kalivas PW (2008) Infralimbic prefrontal cortex is responsible for inhibiting cocaine seeking in extinguished rats. J Neurosci 28:6046–6053. doi:10.1523/JNEUROSCI.1045-08.2008
Peters J, Kalivas PW, Quirk GJ (2009) Extinction circuits for fear and addiction overlap in prefrontal cortex. Learn Mem 16:279–288. doi:10.1101/lm.1041309
Peters J, Dieppa-Perea LM, Melendez LM, Quirk GJ (2010) Induction of fear extinction with hippocampal–infralimbic BDNF. Science 328:1288–1290
Pollandt S, Liu J, Orozco-Cabal L, Grigoriadis DE, Vale WW, Gallagher JP, Shinnick-Gallagher P (2006) Cocaine withdrawal enhances long-term potentiation induced by corticotropin-releasing factor at central amygdala glutamatergic synapses via CRF, NMDA receptors and PKA. Eur J Neurosci 24:1733–1743. doi:10.1111/j.1460-9568.2006.05049.x
Power AE, Berlau DJ, McGaugh JL, Steward O (2006) Anisomycin infused into the hippocampus fails to block "reconsolidation" but impairs extinction: the role of re-exposure duration. Learn Mem 13:27–34. doi:10.1101/lm.91206
Price KL, Baker NL, McRae-Clark AL, Saladin ME, DeSantis SM, Santa Ana EJ, Brady KT (2012) A randomized, placebo-controlled laboratory study of the effects of d-cycloserine on craving in cocaine-dependent individuals. Psychopharmacol. doi:10.1007/s00213-011-2592-x
Ramirez DR, Bell GH, Lasseter HC, Xie X, Traina SA, Fuchs RA (2009) Dorsal hippocampal regulation of memory reconsolidation processes that facilitate drug context-induced cocaine-seeking behavior in rats. Eur J Neurosci 30:901–912. doi:10.1111/j.1460-9568.2009.06889.x
Ressler KJ, Rothbaum BO, Tannenbaum L, Anderson P, Graap K, Zimand E, Hodges L, Davis M (2004) Cognitive enhancers as adjuncts to psychotherapy: use of D-cycloserine in phobic individuals to facilitate extinction of fear. Arch Gen Psychiatry 61:1136–1144
Robbins TW, Everitt BJ (2002) Limbic-striatal memory systems and drug addiction. Neurobiol Learn Mem 78:149–163. doi:10.1006/nlme.2002.4103
Robinson MJ, Franklin KB (2007) Central but not peripheral beta-adrenergic antagonism blocks reconsolidation for a morphine place preference. Behav Brain Res 182:129–134. doi:10.1016/j.bbr.2007.05.023
Robinson MJ, Franklin KB (2010) Reconsolidation of a morphine place preference: impact of the strength and age of memory on disruption by propranolol and midazolam. Behav Brain Res 213:201–207. doi:10.1016/j.bbr.2010.04.056
Robinson MJ, Ross EC, Franklin KB (2011a) The effect of propranolol dose and novelty of the reactivation procedure on the reconsolidation of a morphine place preference. Behav Brain Res 216:281–284. doi:10.1016/j.bbr.2010.08.009
Robinson MJ, Armson M, Franklin KB (2011b) The effect of propranolol and midazolam on the reconsolidation of a morphine place preference in chronically treated rats. Front Behav Neurosci 5:42. doi:10.3389/fnbeh.2011.00042
Sadler R, Herzig V, Schmidt WJ (2007) Repeated treatment with the NMDA antagonist MK-801 disrupts reconsolidation of memory for amphetamine-conditioned place preference. Behav Pharmacol 18:699–703. doi:10.1097/FBP.0b013e3282effb81
Sakurai S, Yu L, Tan SE (2007) Roles of hippocampal N-methyl-D-aspartate receptors and calcium/calmodulin-dependent protein kinase II in amphetamine-produced conditioned place preference in rats. Behav Pharmacol 18:497–506. doi:10.1097/FBP.0b013e3282ee7b62
Sanchez H, Quinn JJ, Torregrossa MM, Taylor JR (2010) Reconsolidation of a cocaine-paired stimulus requires amygdalar protein kinase A. J Neurosci 30:4401–4407. doi:10.1523/JNEUROSCI.3149-09.2010
Santa Ana EJ, Rounsaville BJ, Frankforter TL, Nich C, Babuscio T, Poling J, Gonsai K, Hill KP, Carroll KM (2009) D-cycloserine attenuates reactivity to smoking cues in nicotine dependent smokers: a pilot investigation. Drug Alcohol Depend 104:220–227. doi:10.1016/j.drugalcdep.2009.04.023
Schiller D, Monfils MH, Raio CM, Johnson DC, Ledoux JE, Phelps EA (2010) Preventing the return of fear in humans using reconsolidation update mechanisms. Nature 463:49–53. doi:10.1038/nature08637
Schroeder JP, Packard MG (2003) Systemic or intra-amygdala injections of glucose facilitate memory consolidation for extinction of drug-induced conditioned reward. Eur J Neurosci 17:1482–1488. doi:10.1046/j.1460-9568.2003.02578.x
Schroeder JP, Packard MG (2004) Facilitation of memory for extinction of drug-induced conditioned reward: role of amygdala and acetylcholine. Learn Mem 11:641–647. doi:10.1101/lm.78504
See RE (2002) Neural substrates of conditioned-cued relapse to drug-seeking behavior. Pharmacol Biochem Behav 71:517–529. doi:10.1016/S0091-3057(01)00682-7
Self DW, Choi KH (2004) Extinction-induced neuroplasticity attenuates stress-induced cocaine seeking: a state-dependent learning hypothesis. Stress 7:145–155. doi:10.1080/10253890400012677
Shabashov D, Shohami E, Yaka R (2011) Inactivation of PKMzeta in the NAc shell abolished cocaine-conditioned reward. J Mol Neurosci. doi:10.1007/s12031-011-9671-7
Shaham Y, Shalev U, Lu L, De Wit H, Stewart J (2003) The reinstatement model of drug relapse: history, methodology and major findings. Psychopharmacol 168:3–20. doi:10.1007/s00213-002-1224-x
Shalev U, Grimm JW, Shaham Y (2002) Neurobiology of relapse to heroin and cocaine seeking: a review. Pharmacol Rev 54:1–42. doi:10.1124/pr.54.1.1
Shema R, Sacktor TC, Dudai Y (2007) Rapid erasure of long-term memory associations in the cortex by an inhibitor of PKM zeta. Science 317:951–953. doi:10.1126/science.1144334
Sorg BA (2012) Reconsolidation of drug memories. Neurosci Biobehav Rev 36:1400–1417. doi:10.1016/j.neubiorev.2012.02.004
Sutton MA, Schmidt EF, Choi KH, Schad CA, Whisler K, Simmons D, Karanian DA, Monteggia LM, Neve RL, Self DW (2003) Extinction-induced upregulation in AMPA receptors reduces cocaine-seeking behaviour. Nature 421:70–75. doi:10.1038/nature01249
Suzuki A, Josselyn SA, Frankland PW, Masushige S, Silva AJ, Kida S (2004) Memory reconsolidation and extinction have distinct temporal and biochemical signatures. J Neurosci 24:4787–4795. doi:10.1523/JNEUROSCI.5491-03.2004
Taylor JR, Olausson P, Quinn JJ, Torregrossa MM (2009) Targeting extinction and reconsolidation mechanisms to combat the impact of drug cues on addiction. Neuropharmacology 56(Suppl 1):186–195. doi:10.1016/j.neuropharm.2008.07.027
Terwilliger RZ, Beitner-Johnson D, Sevarino KA, Crain SM, Nestler EJ (1991) A general role for adaptations in G-proteins and the cyclic AMP system in mediating the chronic actions of morphine and cocaine on neuronal function. Brain Res 548:100–110. doi:10.1016/0006-8993(91)91111-D
Torregrossa MM, Kalivas PW (2008) Microdialysis and the neurochemistry of addiction. Pharmacol Biochem Behav 90:261–272. doi:10.1016/j.pbb.2007.09.001
Torregrossa MM, Sanchez H, Taylor JR (2010) D-cycloserine reduces the context specificity of Pavlovian extinction of cocaine cues through actions in the nucleus accumbens. J Neurosci 30:10526–10533. doi:10.1523/JNEUROSCI.2523-10.2010
Torregrossa MM, Corlett PR, Taylor JR (2011) Aberrant learning and memory in addiction. Neurobiol Learn Mem 96:609–623. doi:10.1016/j.nlm.2011.02.014
Toyomitsu Y, Nishijo H, Uwano T, Kuratsu J, Ono T (2002) Neuronal responses of the rat amygdala during extinction and reassociation learning in elementary and configural associative tasks. Eur J Neurosci 15:753–768. doi:10.1046/j.1460-9568.2002.01889.x
Tronson NC, Taylor JR (2007) Molecular mechanisms of memory reconsolidation. Nature Rev Neurosci 8:262–275. doi:10.1038/nrn2090
Tronson NC, Wiseman SL, Olausson P, Taylor JR (2006) Bidirectional behavioral plasticity of memory reconsolidation depends on amygdalar protein kinase A. Nat Neurosci 9:167–169. doi:10.1038/nn1628
Tzeng WY, Chang WT, Chuang JY, Lin KY, Cherng CG, Yu L (2012) Disruption of memory reconsolidation impairs storage of other, non-reactivated memory. Neurobiol Learn Mem 97:241–249. doi:10.1016/j.nlm.2012.01.001
Tzschentke TM (2007) Measuring reward with the conditioned place preference (CPP) paradigm: update of the last decade. Addict Biol 12:227–462. doi:10.1111/j.1369-1600.2007.00070.x
Valjent E, Corbillé AG, Bertran-Gonzalez J, Hervé D, Girault JA (2006) Inhibition of ERK pathway or protein synthesis during reexposure to drugs of abuse erases previously learned place preference. Proc Nat Acad Sci 103:2932–2937. doi:10.1073/pnas.0511030103
Vansteenwegen D, Vervliet B, Iberico C, Baeyens F, Van den Bergh O, Hermans D (2007) The repeated confrontation with videotapes of spiders in multiple contexts attenuates renewal of fear in spider-anxious students. Behav Res Ther 45:1169–1179. doi:10.1016/j.brat.2006.08.023
von der Goltz C, Vengeliene V, Bilbao A, Perreau-Lenz S, Pawlak CR, Kiefer F, Spanagel R (2009) Cue-induced alcohol-seeking behavior is reduced by disrupting the reconsolidation of alcohol-related memories. Psychopharmacol 205:389–397. doi:10.1007/s00213-009-1544-1
Vurbic D, Gold B, Bouton ME (2011) Effects of D-cycloserine on the extinction of appetitive operant learning. Behav Neurosci 125:551–559. doi:10.1037/a0024-403
Wang XY, Zhao M, Ghitza UE, Li YQ, Lu L (2008) Stress impairs reconsolidation of drug memory via glucocorticoid receptors in the basolateral amygdala. J Neurosci 28:5602–5610. doi:10.1523/JNEUROSCI.0750-08.2008
Watson BJ, Wilson S, Griffin L, Kalk NJ, Taylor LG, Munafo MR, Lingford-Hughes AR, Nutt DJ (2011) A pilot study of the effectiveness of d-cycloserine during cue-exposure therapy in abstinent alcohol-dependent subjects. Psychopharmacol 216:121–129. doi:10.1007/s00213-011-2199-2
Weiss F, Martin-Fardon R, Ciccocioppo R, Kerr TM, Smith DL, Ben-Shahar O (2001) Enduring resistance to extinction of cocaine-seeking behavior induced by drug-related cues. Neuropsychopharmacol 25:361–372. doi:361-372.10.1038/S0893-133X(01)00238-X
Wilensky AE, Schafe GE, Kristensen MP, LeDoux JE (2006) Rethinking the fear circuit: the central nucleus of the amygdala is required for the acquisition, consolidation, and expression of Pavlovian fear conditioning. J Neurosci 26:12387–12396. doi:10.1523/JNEUROSCI.4316-06.2006
Winters BD, Tucci MC, DaCosta-Furtado M (2009) Older and stronger object memories are selectively destabilized by reactivation in the presence of new information. Learn Mem 16:545–553. doi:10.1101/lm.1509909
Woods AM, Bouton ME (2006) D-cycloserine facilitates extinction but does not eliminate renewal of the conditioned emotional response. Behav Neurosci 120:1159–1162. doi:10.1037/0735-7044.120.5.1159
Wouda JA, Diergaarde L, Riga D, van Mourik Y, Schoffelmeer AN, De Vries TJ (2010) Disruption of long-term alcohol-related memory reconsolidation: role of beta-adrenoceptors and NMDA receptors. Front Behav Neurosci 4:179. doi:10.3389/fnbeh.2010.00179
Wu P, Xue YX, Ding ZB, Xue LF, Xu CM, Lu L (2011) Glycogen synthase kinase 3B in the basolateral amygdala is critical for the reconsolidation of cocaine reward memory. J Neurochem 118:113–125. doi:10.1111/j.1471-4159.2011.07277.x
Xue YX, Luo YX, Wu P, Shi HS, Xue LF, Chen C, Zhu WL, Ding ZB, Bao YP, Shi J, Epstein DH, Shaham Y, Lu L (2012) A memory retrieval–extinction procedure to prevent drug craving and relapse. Science 336:241–245. doi:10.1126/science.1215070
Zhai H, Wu P, Chen S, Li F, Liu Y, Lu L (2008) Effects of scopolamine and ketamine on reconsolidation of morphine conditioned place preference in rats. Behav Pharmacol 19:211–216. doi:10.1097/FBP.0b013e3282fe88a0
Zhao LY, Zhang XL, Shi J, Epstein DH, Lu L (2009) Psychosocial stress after reactivation of drug-related memory impairs later recall in abstinent heroin addicts. Psychopharmacol 203:599–608. doi:10.1007/s00213-008-1406-2
Zhao LY, Sun LL, Shi J, Li P, Zhang Y, Lu L (2011) Effects of beta-adrenergic receptor blockade on drug-related memory reconsolidation in abstinent heroin addicts. Drug Alcohol Depend 118:224–229. doi:10.1016/j.drugalcdep.2011.03.025
Zhou W, Kalivas PW (2008) N-acetylcysteine reduces extinction responding and induces enduring reductions in cue- and heroin-induced drug-seeking. Biol Psychiatry 63:338–340. doi:10.1016/j.biopsych.2007.06.008
Zhou SJ, Xue LF, Wang XY, Jiang WG, Xue YX, Liu JF, He YY, Luo YX, Lu L (2011) NMDA receptor glycine modulatory site in the ventral tegmental area regulates the acquisition, retrieval, and reconsolidation of cocaine reward memory. Psychopharmacol. doi:10.1007/s00213-011-2551-6
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Torregrossa, M.M., Taylor, J.R. Learning to forget: manipulating extinction and reconsolidation processes to treat addiction. Psychopharmacology 226, 659–672 (2013). https://doi.org/10.1007/s00213-012-2750-9
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DOI: https://doi.org/10.1007/s00213-012-2750-9