Amygdala dopamine receptors are required for the destabilization of a reconsolidating appetitive memory

eNeuro

Volumn 2, Issue 1, 2015, Pages

  Merlo, Emiliano ^a   Ratano, Patrizia ^a   Ilioi, Elena C ^a   Robbins, Miranda A L S ^a   Everitt, Barry J ^a   Milton, Amy L ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

Amygdala; Dopamine; Reconsolidation

Indexed keywords

EID: 85040951819     PISSN: None     EISSN: 23732822     Source Type: Journal    
DOI: 10.1523/ENEURO.0024-14.2015     Document Type: Article

References (73)

1. Alleweireldt AT, Hobbs RJ, Taylor AR, Neisewander JL (2006) Effects of SCH-23390 infused into the amygdala or adjacent cortex and basal ganglia on cocaine seeking and self-administration in rats. Neuropsychopharmacology 31:363–374. CrossRef Medline
2. Arguello AA, Hodges MA, Wells AM, Lara H 3rd, Xie X, Fuchs RA (2014) Involvement of amygdalar protein kinase a, but not calcium/ calmodulin-dependent protein kinase II, in the reconsolidation of cocaine-related contextual memories in rats. Psychopharmacology 231:55–65. CrossRef
3. Asan E (1997) Ultrastructural features of tyrosine-hydroxylase-immunoreactive afferents and their targets in the rat amygdala. Cell Tissue Res 288:449–469. Medline
4. Barak S, Liu F, Ben Hamida S, Yowell QV, Neasta J, Kharazia V, Janak PH, Ron D (2013) Disruption of alcohol-related memories by mTORC1 inhibition prevents relapse. Nat Neurosci 16:1111–1117. CrossRef Medline
5. Ben Mamou C, Gamache K, Nader K (2006) NMDA receptors are critical for unleashing consolidated auditory fear memories. Nat Neurosci 9:1237–1239. CrossRef Medline
6. Berglind WJ, Case JM, Parker MP, Fuchs RA, See RE (2006) Dopamine D1 or D2 receptor antagonism within the basolateral amygdala differentially alters the acquisition of cocaine-cue associations necessary for cue-induced reinstatement of cocaine seeking. Neuroscience 137:699–706. CrossRef Medline
7. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Rev 28:309–369. Medline
8. Bissière S, Humeau Y, Lüthi A (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6:587–592. CrossRef Medline
9. 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. Medline
10. Brinley-Reed M, McDonald AJ (1999) Evidence that dopaminergic axons provide a dense innervation of specific neuronal subpopu-lations in the rat basolateral amygdala. Brain Res 850:127–135. Medline
11. Brischoux F, Chakraborty S, Brierley DI, Ungless MA (2009) Phasic excitation of dopamine neurons in ventral VTA by noxious stimuli. Proc Natl Acad Sci USA106:4894–4899. CrossRef Medline
12. Burns LH, Everitt BJ, Robbins TW (1999) Effects of excitotoxic lesions of the basolateral amygdala on conditional discrimination learning with primary and conditioned reinforcement. Behav Brain Res 100:123–133. Medline
13. Cardinal RN (2000) Whisker control. www.whiskercontrol.com
14. Cardinal RN (2005) Conditioned reinforcement. http://egret.psychol. cam.ac.uk/whisker/tasks.shtml#ConditionedReinforcement
15. Cardinal RN, Aitken MR (2006) ANOVA for the behavioural sciences researcher. London: Lawrence Erlbaum.
16. Cardinal RN, Parkinson JA, Hall J, Everitt BJ (2002) Emotion and motivation: the role of the amygdala, ventral striatum, and prefrontal cortex. Neurosci Biobehav Rev 26:321–352. Medline
17. Corlett PR, Krystal JH, Taylor JR, Fletcher PC (2009) Why do delusions persist? Front Hum Neurosci 3:12[PMC] [CrossRef ][Med-line]
18. Dębiec J, LeDoux JE (2006) Noradrenergic signaling in the amygdala contributes to the reconsolidation of fear memory: treatment implications for PTSD. Ann N Y Acad Sci 1071:521–524.
19. Di Ciano P, Everitt BJ (2004) Direct interactions between the basolateral amygdala and nucleus accumbens core underlie cocaine-seeking behavior by rats. J Neurosci 24:7167–7173. CrossRef Medline
20. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Lüthi A (2009) Amygdala inhibitory circuits and the control of fear memory. Neuron 62:757–771. CrossRef Medline
21. Eisenhardt D, Menzel R (2007) Extinction learning, reconsolidation and the internal reinforcement hypothesis. Neurobiol Learn Mem 87:167–173. CrossRef Medline
22. Esber GR, Roesch MR, Bali S, Trageser J, Bissonette GB, Puche AC, Holland PC, Schoenbaum G (2012) Attention-related Pearce-Kaye-hall signals in basolateral amygdala require the midbrain dopaminergic system. Biol Psychiatry 72:1012–1019. CrossRef Medline
23. Alleweireldt AT, Hobbs RJ, Taylor AR, Neisewander JL (2006) Effects of SCH-23390 infused into the amygdala or adjacent cortex and basal ganglia on cocaine seeking and self-administration in rats. Neuropsychopharmacology 31:363–374. CrossRef Medline
24. Finnie PS, Nader K (2012) The role of metaplasticity mechanisms in regulating memory destabilization and reconsolidation. Neurosci Biobehav Rev 36:1667–1707. CrossRef Medline
25. Forcato C, Burgos VL, Argibay PF, Molina VA, Pedreira ME, Maldonado H (2007) Reconsolidation of declarative memory in humans. Learn Memory 14:295–303. CrossRef Medline
26. Forcato C, Argibay PF, Pedreira ME, Maldonado H (2009) Human reconsolidation does not always occur when a memory is retrieved: the relevance of the reminder structure. Neurobiol Learn Mem 91:50–57. CrossRef Medline
27. Fotros A, Casey KF, Larcher K, Verhaeghe JA, Cox SM, Gravel P, Reader AJ, Dagher A, Benkelfat C, Leyton M (2013) Cocaine cue-induced dopamine release in amygdala and hippocampus: a high-resolution PET [(18)F]fallypride study in cocaine dependent participants. Neuropsychopharmacology 38:1780–1788.CrossRef
28. Greba Q, Kokkinidis L (2000) Peripheral and intraamygdalar administration of the dopamine D 1 receptor antagonist SCH 23390 blocks fear-potentiated startle but not shock reactivity of the shock sensitization of acoustic startle. Behav Neurosci 114:262– 272.CrossRef
29. 1 dopamine receptor involvement in pavlovian fear conditioning. Brain Res 827:28–40. Medline
30. 2 dopamine receptor antagonist on pavlovian fear conditioning. Behav Neurosci 114:647–651. Medline
31. Harmer CJ, Phillips GD (1999) Enhanced dopamine efflux in the amygdala by a predictive, but not a non-predictive, stimulus: facilitation by prior repeated D-amphetamine. Neuroscience 90: 119–130. Medline
32. Kaang BK, Lee SH, Kim H (2009) Synaptic protein degradation as a mechanism in memory reorganization. Neuroscientist 15:430–435. CrossRef Medline
33. Kröner S, Rosenkranz JA, Grace AA, Barrionuevo G (2005) Dopamine modulates excitability of basolateral amygdala neurons in vitro. J Neurophysiol 93:1598–1610. CrossRef Medline
34. LaLumiere RT, Nguyen LT, McGaugh JL (2004) Post-training intra-basolateral amygdala infusions of dopamine modulate consolidation of inhibitory avoidance memory: involvement of noradrenergic and cholinergic systems. Eur J Neurosci 20:2804–2810. CrossRef Medline
35. 1 receptor antagonist SCH 23390 into the amygdala blocks fear expression in a potentiated startle paradigm. Brain Res 795:128–136. Medline
36. Lee JL (2009) Reconsolidation: maintaining memory relevance. Trends Neurosci 32:413–420. CrossRef Medline
37. Lee JL, Di Ciano P, Thomas KL, Everitt BJ (2005) Disrupting reconsolidation of drug memories reduces cocaine seeking behavior. Neuron 47:795–801. CrossRef Medline
38. 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. CrossRef Medline
39. Lorétan K, Bissière S, Lüthi A (2004) Dopaminergic modulation of spontaneous inhibitory network activity in the lateral amygdala. Neuropharmacology 47:631–639. CrossRef Medline
40. Mackintosh NJ (1974) The psychology of animal learning. London: Academic.
41. Maltais S, Côté S, Drolet G, Falardeau P (2000) Cellular colocaliza-tion of dopamine D1 mRNA and D2 receptor in rat brain using a D2 dopamine receptor specific polyclonal antibody. Prog Neuropsy-chopharmacol Biol Psychiatry 24:1127–1149. Medline
42. Marowsky A, Yanagawa Y, Obata K, Vogt KE (2005) A specialized subclass of interneurons mediates dopaminergic facilitation of amygdala function. Neuron 48:1025–1037. CrossRef Medline
43. Milton AL, Everitt BJ (2010) The psychological and neurochemical mechanisms of drug memory reconsolidation: implications for the treatment of addiction. Eur J Neurosci 31:2308–2319. CrossRef Medline
44. Milton AL, Everitt BJ (2012) The persistence of maladaptive memory: addiction, drug memories and anti-relapse treatments. Neurosci Biobehav Rev 36:1119–1139. CrossRef Medline
45. Milton AL, Lee JLC, Butler VJ, Gardner RJ, Everitt BJ (2008) 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.CrossRef
46. Milton AL, Merlo E, Ratano P, Gregory BL, Dumbreck JK, Everitt BJ (2013) Double dissociation of the requirement for GluN2B- and GluN2A-containing NMDA receptors in the destabilization and restabilization of a reconsolidating memory. J Neurosci 33:1109– 1115. CrossRef Medline
47. Nader K, Schafe GE, Le Doux JE (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406:722–726. CrossRef Medline
48. Olshavsky ME, Song BJ, Powell DJ, Jones CE, Monfils MH, Lee HJ (2014) Updating appetitive memory during reconsolidation window: critical role of cue-directed behavior and amygdala central nucleus. Front Behav Neurosci 7:186
49. Paxinos G, Watson C (2004) The rat brain in stereotaxic coordinates, 5th Ed. New York: Academic.
50. Alleweireldt AT, Hobbs RJ, Taylor AR, Neisewander JL (2006) Effects of SCH-23390 infused into the amygdala or adjacent cortex and basal ganglia on cocaine seeking and self-administration in rats. Neuropsychopharmacology 31:363–374. CrossRef Medline
51. Pickel VM, Colago EE, Mania I, Molosh AI, Rainnie DG (2006) Dopamine D1 receptors co-distribute with N-methyl-D-aspartic acid type-1 subunits and modulate synaptically-evoked N-methyl-D-aspartic acid currents in rat basolateral amygdala. Neuroscience 142:671–690. CrossRef Medline
52. Reichelt AC, Exton-McGuinness MT, Lee JL (2013) Ventral tegmental dopamine dysregulation prevents appetitive memory destabilization. J Neurosci 33:14205–14210. CrossRef Medline
53. Alleweireldt AT, Hobbs RJ, Taylor AR, Neisewander JL (2006) Effects of SCH-23390 infused into the amygdala or adjacent cortex and basal ganglia on cocaine seeking and self-administration in rats. Neuropsychopharmacology 31:363–374. CrossRef Medline
54. Rosenkranz JA, Grace AA (1999) Modulation of basolateral amygdala neuronal firing and afferent drive by dopamine receptor activation in vivo. J Neurosci 19:11027–11039. Medline
55. Rossato JI, Kohler CA, Radiske A, Lima RH, Bevilaqua LR, Camma-rota M (2014) State-dependent effect of dopamine D/D receptors inactivation on memory destabilization and reconsolidation. Behav Brain Res. Advance online publication. doi:10.1016/j.bbr.2014.09.009.
56. Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76:470–485. CrossRef Medline
57. Sanchez H, Quinn JJ, Torregrossa MM, Taylor JR (2010) Reconsolidation of a cocaine-associated stimulus requires amygdalar protein kinase A. J Neurosci 30:4401–4407. CrossRef Medline
58. Schultz W, Apicella P, Ljungberg T (1993) Responses of monkey dopamine neurons to reward and conditioned stimuli during successive steps of learning a delayed response task. J Neurosci 13:900–913.
59. Schultz W, Dayan P, Montague PR (1997) A neural substrate of prediction and reward. Science 275:1593–1599. Medline
60. Sevenster D, Beckers T, Kindt M (2013) Prediction error governs pharmacologically induced amnesia for learned fear. Science 339: 830–833. CrossRef Medline
61. Sherry JM, Hale MW, Crowe SF (2005) The effects of the dopamine D1 receptor antagonist SCH23390 on memory reconsolidation following reminder-activated retrieval in day-old chicks. Neurobiol Learn Mem 83:104–112. CrossRef Medline
62. Stoof JC, Kebabian JW (1981) Opposing roles for D-1 and D-2 dopamine receptors in efflux of cyclic AMP from rat neostriatum. Nature 294:366–368. Medline
63. Takahashi YK, Roesch MR, Stalnaker TA, Haney RZ, Calu DJ, Taylor AR, Burke KA, Schoenbaum G (2009) The orbitofrontal cortex and ventral tegmental area are necessary for learning from unexpected outcomes. Neuron 62:269–280. CrossRef Medline
64. Théberge FR, Milton AL, Belin D, Lee JL, Everitt BJ (2010) The basolateral amygdala and nucleus accumbens core mediate dissociable aspects of drug memory reconsolidation. Learn Mem 17:444–453. CrossRef Medline
65. Tronson NC, Taylor JR (2013) Addiction: a drug-induced disorder of memory reconsolidation. Curr Opin Neurobiol 23:573–580. Cross-Ref Medline
66. Tye KM, Cone JJ, Schairer WW, Janak PH (2010) Amygdala neural encoding of the absence of reward during extinction. J Neurosci 30:116–125. CrossRef Medline
67. von Hertzen LS, Giese KP (2005) Memory reconsolidation engages only a subset of immediate-early genes induced during consolidation. J Neurosci 25:1935–1942. CrossRef Medline
68. Weiskrantz L (1956) Behavioral changes associated with ablation of the amygdaloid complex in monkeys. J Comp Physiol Psychol 49:381–391. Medline
69. Wells AM, Arguello AA, Xie X, Blanton MA, Lasseter HC, Reittinger AM, Fuchs RA (2013) Extracellular signal-regulated kinase in the basolateral amygdala, but not the nucleus accumbens core, is critical for context-response-cocaine memory reconsolidation in rats. Neuropsychopharmacology 38:753–762. CrossRef Medline
70. Wise RA, Rompre PP (1989) Brain dopamine and reward. Annu Rev Psychol 40:191–225. CrossRef Medline
71. Yan Y, Newman AH, Xu M (2014) Dopamine D1 and D3 receptors mediate reconsolidation of cocaine memories in mouse models of drug self-administration. Neuroscience 278:154–164. CrossRef Medline
72. Yan Y, Kong H, Wu EJ, Newman AH, Xu M (2013) Dopamine D3 receptors regulate reconsolidation of cocaine memory. Neuroscience 241:32–40. CrossRef Medline
73. Yang K, Trepanier C, Sidhu B, Xie Y-F, Li H, Lei G, Salter MW, Orser BA, Nakazawa T, Yamamoto T, Jackson MF, MacDonald JF (2012) Metaplasticity gated through differential regulation of GluN2A versus GluN2B receptors by src family kinases. EMBO J 31:805–816. CrossRef Medline