Early versus Late-Phase Consolidation of Opiate Reward Memories Requires Distinct Molecular and Temporal Mechanisms in the Amygdala-Prefrontal Cortical Pathway

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Gholizadeh, Shervin ^a   Sun, Ninglei ^a   De Jaeger, Xavier ^a   Bechard, Melanie ^a   Coolen, Lique ^a   Laviolette, Steven R ^a  

^a WESTERN UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; MORPHINE; OPIATE;

AMYGDALOID NUCLEUS; ANIMAL CELL; ARTICLE; BASOLATERAL AMYGDALA; CONTROLLED STUDY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; MALE; MEMORY CONSOLIDATION; NERVE CELL PLASTICITY; NONHUMAN; PLACE PREFERENCE; PREFRONTAL CORTEX; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS INHIBITION; RAT; RECALL; REWARD; SIGNAL TRANSDUCTION; VENTROMEDIAL PREFRONTAL CORTEX;

AMYGDALA; ANALGESICS, OPIOID; ANIMALS; MALE; MEMORY; PREFRONTAL CORTEX; RATS;

EID: 84877825841     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063612     Document Type: Article

References (46)

1. Izquierdo I, Barros DM, Souza ME, de Souza MM, Izquierdo LA, et al. (1998) Mechanisms of memory types differ. Nature 393: 635-636.
2. Frankland PW, Ding HK, Takahashi E, Suzuki A, Kida S, et al. (2006) Stability of recent and remote contextual fear memory. Learning & Mem. 13: 451-457.
3. McGaugh JL, (1966) Time-dependent processes in memory storage. Science. 153: 1351-1358.
4. Milekic MH, Alberini CM, (2002) Temporally graded requirement for protein synthesis following memory reactivation. Neuron. 36: 521-525.
5. Frankland PW, Bontempi B, Talton LE, Kaczmarek L, Silva AJ, (2004) The involvement of the anterior cingulate cortex in remote contextual fear memory. Science 304: 881-883.
6. Han JH, Kushner SA, Yiu AP, Hsiang HL, Buch T, et al. (2009) Selective erasure of a fear memory. Science. 323: 1492-1496.
7. Nader K, Schafe GE, Le Doux JE, (2000) Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature. 406: 722-726.
8. Frenois F, Stinus L, Di Blasi F, Cador M, Le Moine C, (2005) A specific limbic circuit underlies opiate withdrawal memories. J Neurosci 25: 1366-1374.
9. Lintas A, Chi N, Lauzon NM, Bishop SF, Gholizadeh S, et al. (2011) Identification of a dopamine receptor-mediated opiate reward memory switch in the basolateral amygdala-nucleus accumbens circuit. J Neurosci. 31: 11172-11183.
10. Sun N, Chi N, Lauzon N, Bishop S, Tan H, et al. (2011) Acquisition, Extinction, and Recall of Opiate Reward Memory Are Signalled by Dynamic Neuronal Activity Patterns in the Prefrontal Cortex. Cereb Cortex 21: 2665-2680.
11. Tan H, Lauzon NM, Bishop SF, Bechard MA, Laviolette SR, (2010) Integrated cannabinoid CB1 receptor transmission within the amygdala-prefrontal cortical pathway modulates neuronal plasticity and emotional memory encoding. Cereb Cortex 20: 1486-96.
12. Ford CP, Mark GP, Williams JT, (2006) Properties and opioid inhibition of mesolimbic dopamine neurons vary according to target location. J Neurosci 26: 2788-2797.
13. Sun N, Laviolette SR, (2012) Inactivation of the basolateral amygdala during opiate reward learning disinhibits prelimbic cortical neurons and modulates associative memory extinction. Psychopharmacology 222: 645-661.
14. Laviolette SR, Lipski WJ, Grace AA, (2005) A subpopulation of neurons in the medial prefrontal cortex encodes emotional learning through burst and frequency codes through a dopamine D4 receptor-dependent basolateral amygdala input. J Neurosci 25: 6066-6075.
15. Bishop SF, Lauzon NM, Bechard M, Gholizadeh S, Laviolette SR, (2011) NMDA receptor hypofunction in the prelimbic cortex increases sensitivity to the rewarding properties of opiates via dopaminergic and amygdalar substrates. Cereb Cortex 21: 61-80.
16. Laviolette SR, Gallegos RA, Henriksen SJ, van der Kooy D, (2004) Opiate state controls bi-directional reward signaling via GABAA receptors in the ventral tegmental area. Nat Neurosci 7: 160-169.
17. Paxinos G, Watson C (2005) The rat brain in stereotaxic coordinates. Amsterdam: Elsevier Academic Press.
18. Valjent E, Corbille AG, Bertran-Gonzales J, Herve D, Girault JA, (2006) Inhibition of ERK pathway or protein synthesis during re-exposure to drugs of abuse erases previously learned place preference. PNAS 103: 2932-2937.
19. Valjent E, Corvol JC, Pages C, Besson MJ, Maldonado R, et al. (1999) Involvement of the extracellular signal-related kinase cascade for cocaine rewarding properties J Neurosci. 19: 8685-8695.
20. Berhow MT, Hiroi N, Nestler EJ, (1996) Regulation of ERK (extracellular signal regulated kinase), part of the neurotrophin signal transduction cascade, in the rat mesolimbic dopamine system by chronic exposure to morphine or cocaine. J Neurosci 16: 4707-4715.
21. Frankland PW, O'Brien C, Ohno M, Kirkwood A, Silva AJ, (2001) Alpha-CaMKII-dependent plasticity in the cortex is required for permanent memory. Nature 411: 309-313.
22. Lai YT, Fan HY, Cherng CG, Chiang CY, Kao GS, et al. (2008) Activation of amygdaloid PKC pathway is necessary for conditioned cues-provoked cocaine memory performance. Neurobiol Learn Mem 90: 164-70.
23. Alvarez-Jaimes L, Feliciano-Rivera M, Centeno-González M, Maldonado-Vlaar CS, (2005) Contributions of the mitogen-activated protein kinase and protein kinase C cascades in spatial learning and memory mediated by the nucleus accumbens. J Pharmacol Exp Ther 314: 1144-1157.
24. Almeida RC, Souza DG, Soletti RC, López MG, Rodrigues AL, et al. (2006) Involvement of PKA, MAPK/ERK and CaMKII, but not PKC in the acute antidepressant-like effect of memantine in mice. Neurosci Lett 395: 93-97.
25. Yim AJ, Morase CRG, Ferreira TL, Oliveira MGM, (2006) Protein synthesis in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference. Behav Brain Res 171: 162-169.
26. Shalev U, Robarts P, Shaham Y, Morales M, (2003) Selective induction of c-Fos immunoreactivity in the prelimbic cortex during reinstatement of heroin seeking induced by acute food deprivation in rats. Behav Brain Res. 145: 79-88.
27. Luo F, Xi ZX, Wu G, Liu C, Gardner EL, et al. (2004) Attenuation of brain response to heroin correlates with the reinstatement of heroin-seeking in rats by fMRI. Neuroimage 22: 1328-1335.
28. Langleben DD, Ruparel K, Elman I, Busch-Winokur S, Pratiwadi R, et al. (2008) Acute effect of methadone maintenance dose on brain fMRI response to heroin-related cues. Am J Psych 165: 390-394.
29. Daglish MRC, Weinstein A, Malizia AL, Wilson S, Melichar JK, et al. (2001) Changes in regional cerebral blood flow elicited by craving memories in abstinent opiate-dependent subjects. Am J Psych 158: 1680-1686.
30. Rosenkranz JA, Moore H, Grace AA, (2003) The prefrontal cortex regulates lateral amygdala neuronal plasticity and responses to previously conditioned stimuli. J Neurosci 23: 11054-11064.
31. Maroun M, Richter-Lavin G, (2003) Exposure to acute stress blocks the induction of long-term potentiation in the amygdala-prefrontal cortex pathway in vivo. J Neurosci 23: 4406-4409.
32. Wu J, Rowan MJ, Anwyl R, (2006) Long-term potentiation is mediated by multiple kinase cascades involving CaMKII or either PKA or p42/44 MAPK in the adult dentate gyrus in vitro. J Neurophysiol 95: 3519-3527.
33. Igaz LM, Winograd M, Cammarota M, Izquierdo LA, Alonso M, et al. (2006) Early activation of extracellular signal-regulated kinase signalling pathway in the hippocampus is required for short-term memory formation of fear-motivated learning. Cell Mol Neurobiol 26: 989-997.
34. Miller CA, Marshall JF, (2005) Molecular substrates for retrieval and reconsolidation of cocaine-associated contextual memory. Neuron 47: 873-84.
35. Languille S, Davis S, Richer P, Alacer C, Laroche S, et al. (2009) Extracellular signal-related kinase activation is required for consolidation and reconsolidation of memory at an early state of ontogenesis. Eur J Neurosci 30: 1923-1930.
36. Schafe GE, Atkins CM, Swank MW, Bauer EP, Sweatt JD, et al. (2000) Activation of ERK/MAP kinase in the amygdala is required for memory consolidation of Pavlovian fear-conditioning. J Neurosci 20: 8177-8187.
37. Olmstead MC, Franklin KB, (1997) The development of a conditioned place preference to morphine: effects of microinjections into various CNS sites. Behav Neurosci 111: 1324-1334.
38. Nader K, van der Kooy D, (1997) Deprivation state switches the neurobiological substrates mediating opiate reward in the ventral tegmental area. J Neurosci 17: 383-90.
39. Bissière S, Humeau Y, Lüthi A, (2003) Dopamine gates LTP induction in lateral amygdala by suppressing feedforward inhibition. Nat Neurosci 6: 587-592.
40. Kroner SK, Rosenkranz JA, Grace AA, Barrionuevo G, (2005) Dopamine modulates excitability of basolateral amygdala neurons in vitro. J Neurophysiol 93: 1598-1610.
41. Carr DB, O'Donnell P, Card JP, Sesack SR, (1999) Dopamine terminals in the rat prefrontal cortex synapse on pyramidal cells that project to the nucleus accumbens. J Neurosci 19: 11049-11060.
42. Carr DB, Sesack SR, (2000) Dopamine terminals synapse on callosal projection neurons in the rat prefrontal cortex. J Comp Neurol 425: 275-283.
43. De Jaeger X, Bishop SF, Ahmad T, Lyons D, Ng GA, et al. (2012) The effects of AMPA receptor blockade in the prelimbic cortex on systemic and ventral tegmental area opiate reward sensitivity. Psychopharmacology 225: 687-695.
44. Floresco SB, Tse MT, (2007) Dopaminergic regulation of inhibitory and excitatory transmission in the basolateral amygdala-prefrontal cortical pathway. J Neurosci 27: 2045-2057.
45. Rosenkranz JA, Grace AA, (2002) Dopamine-mediated modulation of odour-evoked amygdala potentials during Pavlovian conditioning. Nature 417: 282-287.
46. Laviolette SR, Grace AA, (2006) Cannabinoids Potentiate Emotional Learning Plasticity in Neurons of the Medial Prefrontal Cortex through Basolateral Amygdala Inputs. J Neurosci 26: 6458-68.