A role for the insular cortex in long-term memory for context-evoked drug craving in rats

Neuropsychopharmacology

Volumn 37, Issue 9, 2012, Pages 2101-2108

  Contreras, Marco ^a   Billeke, Pablo ^a   Vicencio, Sergio ^b   Madrid, Carlos ^a   Perdomo, Guetón ^a   González, Marcela ^a   Torrealba, Fernando ^a  

^a PONTIFICIA UNIVERSIDAD CATÓLICA DE CHILE   (Chile)

^b UNIVERSITY OF CHILE   (Chile)

Author keywords

addiction; amphetamine; conditioned place preference; craving; insula; memory reconsolidation

Indexed keywords

AMPHETAMINE; ANISOMYCIN; BRAIN PROTEIN; PROTEIN ZIF268; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; CONTROLLED STUDY; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; INSULA; LONG TERM MEMORY; MALE; MEMORY CONSOLIDATION; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REVIEW; WITHDRAWAL SYNDROME;

AMPHETAMINE; ANIMALS; ANISOMYCIN; ASSOCIATION LEARNING; BEHAVIOR, ADDICTIVE; CEREBRAL CORTEX; CONDITIONING (PSYCHOLOGY); MALE; MEMORY, LONG-TERM; MICROINJECTIONS; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84863987965     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2012.59     Document Type: Review

References (55)

1. Abdolahi A, Acosta G, Breslin FJ, Hemby SE, Lynch WJ (2010). Incubation of nicotine seeking is associated with enhanced protein kinase A-regulated signaling of dopamine-and cAMPregulated phosphoprotein of 32 kDa in the insular cortex. Eur J Neurosci 31: 733-741.
2. Alberini CM (2008). The role of protein synthesis during the labile phases of memory: revisiting the skepticism. Neurobiol Learn Mem 89: 234-246.
3. Allen GV, Saper CB, Hurley KM, Cechetto DF (1991). Organization of visceral and limbic connections in the insular cortex of the rat. J Comp Neurol 311: 1-16.
4. BermudezRattoni F (2004). Molecular mechanisms of tasterecognition memory. Nat Rev Neurosci 5: 209-217.
5. Cechetto DF, Saper CB (1987). Evidence for a viscerotopic sensory representation in the cortex and thalamus in the rat. J Comp Neurol 262: 27-45.
6. Contreras M, Ceric F, Torrealba F (2007). Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318: 655-658.
7. Craig AD (2004). Interoception: the sense of the physiological condition of the body. Curr Opin Neurobiol 13: 500-505.
8. Damasio AR, Grabowski TJ, Bechara A, Damasio H, Ponto LL, Parvizi J et al (2000). Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci 3: 1049-1056.
9. Davis M, Whalen PJ (2001). The amygdala: vigilance and emotion. Mol Psychiatry 6: 13-34.
10. Farnham MM, Pilowsky PM (2009). Local anaesthetics for acute reversible blockade of the sympathetic baroreceptor reflex in the rat. J Neurosci Methods 179: 58-62.
11. Forget B, Pushparaj A, Le Foll B (2010). Granular insular cortex inactivation as a novel therapeutic strategy for nicotine addiction. Biol Psychiatry 68: 265-271.
12. Gabbott PLA, Warner TA, Jays PRL, Bacon SJ (2003). Areal and synaptic interconnectivity of prelimbic (Area 32), infralimbic (Area 25) and insular cortices in the rat. Brain Res 993: 59-71.
13. Gauriau C, Bernard JF (2004). Posterior triangular thalamic neurons convey nociceptive messages to the secondary somatosensory and insular cortices in the rat. J Neurosci 24: 752-761.
14. Gilbert CD, Li W, Piech V (2009). Perceptual learning and adult cortical plasticity. J Physiol 587: 2743-2751.
15. Groenewegen HJ, Witter MP (2004). Thalamus. In: Paxinos G (ed) The Rat Nervous System. Elsevier Academic Press: London. pp 407-453.
16. Hall J, Thomas KL, Everitt BJ (2001). Cellular imaging of zif268 expression in the hippocampus and amygdala during contextual and cued fear memory retrieval: selective activation of hippocampal CA1 neurons during the recall of contextual memories. J Neurosci 21: 2186-2193.
17. Hollander JA, Lu Q, Cameron MD, Kamenecka TM, Kenny PJ (2008). Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci USA 105: 19480-19485.
18. Hsu E, Packard MG (2008). Medial prefrontal cortex infusions of bupivacaine or AP-5 block extinction of amphetamine conditioned place preference. Neurobiol Learn Mem 89: 504-512.
19. Insausti R, Herrero MT, Witter MP (1997). Entorhinal cortex of the rat: cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus 7: 146-183.
20. Ito S (1994). Electrophysiological evidence for projections of myelinated and non-myelinated primary vagal afferents to the rat insular cortex. Neurosci Lett 179: 32.
21. Jasmin L, Burkey AR, Granato A, Ohara PT (2004). Rostral agranular insular cortex and pain areas of the central nervous system: a tract-tracing study in the rat. J Comp Neurol 468: 425-440.
22. Kasanetz F, Deroche-Gamonet V, Berson N, Balado E, Lafourcade M, Manzoni O et al (2010). Transition to addiction is associated with a persistent impairment in synaptic plasticity. Science 328: 1709-1712.
23. Kerr KM, Agster KL, Furtak SC, Burwell RD (2007). Functional neuroanatomy of the parahippocampal region: the lateral and medial entorhinal areas. Hippocampus 17: 697-708.
24. Kimura A, Imbe H, Donishi T (2010). Efferent connections of an auditory area in the caudal insular cortex of the rat: anatomical nodes for cortical streams of auditory processing and crossmodal sensory interactions. Neuroscience 166: 1140-1157.
25. Kleim JA, Bruneau R, Calder K, Pocock D, VandenBerg PM, MacDonald E et al (2003). Functional organization of adult motor cortex is dependent upon continued protein synthesis. Neuron 40: 167-176.
26. Krettek JE, Price JL (1977). The cortical projections of the mediodorsal nucleus and adjacent thalamic nuclei in the rat. J Comp Neurol 171: 157-191.
27. Li FQ, Xue YX, Wang JS, Fang Q, Li YQ, Zhu WL et al (2010). Basolateral amygdala cdk5 activity mediates consolidation and reconsolidation of memories for cocaine cues. J Neurosci 30: 10351-10359.
28. Maren S (2011). Seeking a spotless mind: extinction, deconsolidation, and erasure of fear memory. Neuron 70: 830-845.
29. Maviel T, Durkin TP, Menzaghi F, Bontempi B (2004). Sites of neocortical reorganization critical for remote spatial memory. Science 305: 96-99.
30. Milekic MH, Brown SD, Castellini C, Alberini CM (2006). Persistent disruption of an established morphine conditioned place preference. J Neurosci 26: 3010-3020.
31. Nader K, Schafe GE, Le Doux JE (2000). Fear memories require protein synthesis in the amygdala for reconsolidation after retrieval. Nature 406: 722-726.
32. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007). Damage to the insula disrupts addiction to cigarette smoking. Science 315: 531-534.
33. O'Brien CP (1997). A range of research-based pharmacotherapies for addiction. Science 278: 66-70.
34. Paulus MP, Tapert SF, Schuckit MA (2005). Neural activation patterns of methamphetamine-dependent subjects during decision making predict relapse. Arch Gen Psychiatry 62: 761-768.
35. Pessoa L, Adolphs R (2010). Emotion processing and the amygdala: from a 'low road' to 'many roads' of evaluating biological significance. Nat Rev Neurosci 11: 773-783.
36. Robbins TW, Ersche KD, Everitt BJ (2008). Drug addiction and the memory systems of the brain. Ann N Y Acad Sci 1141: 1-21.
37. Rosenblum K, Meiri N, Dudai Y (1993). Taste memory: the role of protein synthesis in gustatory cortex. Behav Neural Biol 59: 49-56.
38. Rothbaum BO, Davis M (2003). Applying learning principles to the treatment of post-trauma reactions. Ann N Y Acad Sci 1008: 112-121.
39. Rudy JW, Biedenkapp JC, Moineau J, Bolding K (2006). Anisomycin and the reconsolidation hypothesis. Learn Mem 13: 1-3.
40. Sacco T, Sacchetti B (2010). Role of secondary sensory cortices in emotional memory storage and retrieval in rats. Science 329: 649-656.
41. Sanfey AG, Rilling JK, Aronson JA, Nystrom LE, Cohen JD (2003). The neural basis of economic decision-making in the Ultimatum Game. Science 300: 1755-1758.
42. Sara SJ (2000). Strengthening the shaky trace through retrieval. Nat Rev Neurosci 1: 212-213.
43. Sara SJ (2010). Reactivation, retrieval, replay and reconsolidation in and out of sleep: connecting the dots. Front Behav Neurosci 4: 185.
44. Scott D, Hiroi N (2011). Deconstructing craving: dissociable cortical control of cue reactivity in nicotine addiction. Biol Psychiatry 69: 1052-1059.
45. Shi CJ, Cassell MD (1998). Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399: 440-468.
46. Squire LR (2006). Lost forever or temporarily misplaced? The long debate about the nature of memory impairment. Learn Mem 13: 522-529.
47. Squire LR (2009). Memory and brain systems: 1969-2009. J Neurosci 29: 12711-12716.
48. Stehberg J, AcunaGoycolea C, Ceric F, Torrealba F (2001). The visceral sector of the thalamic reticular nucleus in the rat. Neuroscience 106: 745-755.
49. Swanson LW (1998). Brain Maps: Structure of the Rat Brain. Elsevier BV: Amsterdam, 267pp.
50. Taubenfeld SM, Muravieva EV, Garcia-Osta A, Alberini CM (2010). Disrupting the memory of places induced by drugs of abuse weakens motivational withdrawal in a context-dependent manner. Proc Natl Acad Sci USA 107: 12345-12350.
51. Tronson NC, Taylor JR (2007). Molecular mechanisms of memory reconsolidation. Nat Rev Neurosci 8: 262-275.
52. Volkow N, Li TK (2005). The neuroscience of addiction. Nat Neurosci 8: 1429-1430.
53. Wanisch K, Wotjak CT (2008). Time course and efficiency of protein synthesis inhibition following intracerebral and systemic anisomycin treatment. Neurobiol Learn Mem 90: 485-494.
54. Weinberger NM (2007). Associative representational plasticity in the auditory cortex: a synthesis of two disciplines. Learn Mem 14: 1-16.
55. Xiong W, Kojic LZ, Zhang L, Prasad SS, Douglas R, Wang Y et al (2006). Anisomycin activates p38 MAP kinase to induce LTD in mouse primary visual cortex. Brain Res 1085: 68-76.