Effects of inactivating the agranular or granular insular cortex on the acquisition of the morphine-induced conditioned place preference and naloxone-precipitated conditioned place aversion in rats

Journal of Psychopharmacology

Volumn 27, Issue 9, 2013, Pages 837-844

  Li, Chun Lu ^a,b   Zhu, Ning ^a   Meng, Xiao Lu ^a,b   Li, Yong Hui ^a   Sui, Nan ^a  

^a INSTITUTE OF PSYCHOLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

Author keywords

agranular; conditioned place aversion; conditioned place preference; granular; insular cortex; Morphine; naloxone

Indexed keywords

MORPHINE; NALOXONE;

AGRANULAR INSULAR CORTEX; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; AVERSION; BRAIN FUNCTION; BRAIN REGION; CONTROLLED STUDY; ELECTROENCEPHALOGRAM; ESCAPE BEHAVIOR; GRANULAR INSULAR CORTEX; INSULA; LATENT PERIOD; MALE; MAZE TEST; MENTAL CAPACITY; MOTOR PERFORMANCE; NONHUMAN; PLACE PREFERENCE; PRIORITY JOURNAL; RAT; SPATIAL LEARNING; SWIMMING;

AGRANULAR; CONDITIONED PLACE AVERSION; CONDITIONED PLACE PREFERENCE; GRANULAR; INSULAR CORTEX; MORPHINE; NALOXONE;

ANALGESICS, OPIOID; ANIMALS; CEREBRAL CORTEX; CONDITIONING (PSYCHOLOGY); LEARNING; MALE; MORPHINE; MOTOR ACTIVITY; NALOXONE; OPIOID-RELATED DISORDERS; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANCE WITHDRAWAL SYNDROME;

EID: 84883398328     PISSN: 02698811     EISSN: 14617285     Source Type: Journal    
DOI: 10.1177/0269881113492028     Document Type: Article

References (46)

1. Accolla R, Carleton A. Internal body state influences topographical plasticity of sensory representations in the rat gustatory cortex. Proc Natl Acad Sci U S A. 2008 ; 105: 4010-4015
2. Allen GV, Saper CB, Hurley KM, et al. Organization of visceral and limbic connections in the insular cortex of the rat. J Comp Neurol. 1991 ; 311: 1-16
3. Azar MR, Jones BC, Schulteis G. Conditioned place aversion is a highly sensitive index of acute opioid dependence and withdrawal. Psychopharmacology. 2003 ; 170: 42-50
4. Azorlosa JL, Stitzer ML, Greenwald MK, et al. Opioid physical dependence development: Effects of single versus repeated morphine pretreatments and of subjects' opioid exposure history. Psychopharmacology. 1994 ; 114: 71-80
5. Baker T, Piper M, McCarthy D, et al. Addiction motivation reformulated: An affective processing model of negative reinforcement. Psychol Rev. 2004 ; 111: 33-51
6. Bardo MT, Bevins RA. Conditioned place preference: What does it add to our preclinical understanding of drug reward?. Psychopharmacology. 2000 ; 153: 31-43
7. Buccafusco JJ, Terry AV Methods of Behavior Analysis in Neuroscience. 2009 ) Methods of Behavior Analysis in Neuroscience. 2nd edition, Boca Raton, CRC Press. Boca Raton: CRC Press ; 2009 :
8. Cechetto D. Central representation of visceral function. Fed Proc. 1987 ; 46: 17-23
9. Chikama M, McFarland NR, Amaral DG, et al. Insular cortical projections to functional regions of the striatum correlate with cortical cytoarchitectonic organization in the primate. J Neurosci. 1997 ; 17: 9686-9705
10. Contreras M, Billeke P, Vicencio S, et al. A role for the insular cortex in long-term memory for context-evoked drug craving in rats. Neuropsychopharmacology. 2012 ; 37: 2101-2108
11. Contreras M, Ceric F, Torrealba F. Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science. 2007 ; 318: 655-657
12. Craig A. How do you feel? Interoception: The sense of the physiological condition of the body. Nat Rev Neurosci. 2002 ; 3: 655-666
13. Cubero I, Puerto A. Electrical stimulation of the insular cortex induces flavor-preferences in rats. Brain Res. 2000 ; 872: 134-140
14. Damasio AR, Grabowski TJ, Bechara A, et al. Subcortical and cortical brain activity during the feeling of self-generated emotions. Nat Neurosci. 2000 ; 3: 1049-1056
15. Di Ciano P, Everitt BJ. Contribution of the ventral tegmental area to cocaine-seeking maintained by a drug-paired conditioned stimulus in rats. Eur J Neurosci. 2004 ; 19: 1661-1667
16. Escobar ML, Alcocer I, Chao V. The NMDA receptor antagonist CPP impairs conditioned taste aversion and insular cortex long-term potentiation in vivo. Brain Res. 1998 ; 812: 246-251
17. Ferreira G, Miranda M, Cruz V, et al. Basolateral amygdala glutamatergic activation enhances taste aversion through NMDA receptor activation in the insular cortex. Eur J Neurosci. 2005 ; 22: 2596-2604
18. Forget B, Pushparaj A, Le Foll B. Granular insular cortex inactivation as a novel therapeutic strategy for nicotine addiction. Biol Psychiatry. 2010 ; 68: 265-271
19. Gao J, Zhu N, Feng M, et al. Intra-nucleus-accumbens SKF38393 improved the impaired acquisition of morphine-conditioned place preference in depression-like rats. PsyCh Journal. 2012 ; 1: 2-14
20. Hollander J, Lu Q, Cameron M, et al. Insular hypocretin transmission regulates nicotine reward. Proc Natl Acad Sci U S A. 2008 ; 105: 19480-19485
21. Insausti R, Herrero M, Witter MP, et al. Entorhinal cortex of the rat: Cytoarchitectonic subdivisions and the origin and distribution of cortical efferents. Hippocampus. 1997 ; 7: 146-183
22. Jasmin L, Rabkin SD, Granato A, et al. Analgesia and hyperalgesia from GABA-mediated modulation of the cerebral cortex. Nature. 2003 ; 424: 316-320
23. Jasmin L, Granato A, Ohara PT. Rostral agranular insular cortex and pain areas of the central nervous system: A tract-tracing study in the rat. J Comp Neurol. 2004 ; 468: 425-440
24. Kerr KM, Agster KL, Furtak SC, et al. Functional neuroanatomy of the parahippocampal region: The lateral and medial entorhinal areas. Hippocampus. 2007 ; 17: 697-708
25. Koh M, Bernstein I. Mapping conditioned taste aversion associations using c-Fos reveals a dynamic role for insular cortex. Behav Neurosci. 2005 ; 119: 388-398
26. Lin J, Roman C, Reilly S. Morphine-induced suppression of conditioned stimulus intake: Effects of stimulus type and insular cortex lesions. Brain Res. 2009 ; 1292: 52-60
27. McDonald RJ, Yim TT, Lehmann H, et al. Expression of a conditioned place preference or spatial navigation task following muscimol-induced inactivations of the amygdala or dorsal hippocampus: A double dissociation in the retrograde direction. Brain Res Bull. 2010 ; 83: 29-37
28. McFarland K, Kalivas PW. The circuitry mediating cocaine-induced reinstatement of drug-seeking behavior. J Neurosci. 2001 ; 21: 8655-8663
29. Mackey W, Keller J, Van der Kooy D. Visceral cortex lesions block conditioned taste aversions induced by morphine. Pharmacol Biochem Behav. 1986 ; 24: 71-78
30. Martin JH, Ghez C. Pharmacological inactivation in the analysis of the central control of movement. J Neurosci Meth. 1999 ; 86: 145-159
31. Meyer DA, Richer E, Benkovic SA, et al. Striatal dysregulation of Cdk5 alters locomotor responses to cocaine, motor learning, and dendritic morphology. Proc Natl Acad Sci U S A. 2008 ; 105: 18561-18566
32. Miranda M, Quirarte G, Rodriguez-Garcia G, et al. Glucocorticoids enhance taste aversion memory via actions in the insular cortex and basolateral amygdala. Learn Mem. 2008 ; 15: 468-476
33. Naqvi NH, Rudrauf D, Damasio H, et al. Damage to the insula disrupts addiction to cigarette smoking. Science. 2007 ; 315: 531-534
34. O'Brien CP. Evidence-based treatments of addiction. Philos Trans R Soc Lond B Biol Sci. 2008 ; 363: 3277-3286
35. Ohara PT, Granato A, Moallem TM, et al. Dopaminergic input to GABAergic neurons in the rostral agranular insular cortex of the rat. J Neurocytol. 2003 ; 32: 131-141
36. Paxinos G, Watson C The Rat Brain in Stereotaxic Coordinates. 2005 ) The Rat Brain in Stereotaxic Coordinates, 5th ed.New York: Academic Press. New York: Academic Press ; 2005 :
37. Rezayof A, Nazari-Serenjeh F, Zarrindast MR, et al. Morphine-induced place preference: Involvement of cholinergic receptors of the ventral tegmental area. Eur J Pharmacol. 2007 ; 562: 92-102
38. Schulteis G, Koob GF. Reinforcement processes in opiate addiction: A homeostatic model. Neurochem Res. 1996 ; 21: 1437-1454
39. Van Duuren E, van der Plasse G, van der Blom R, et al. Pharmacological manipulation of neuronal ensemble activity by reverse microdialysis in freely moving rats: A comparative study of the effects of tetrodotoxin, lidocaine, and muscimol. J Pharmacol Exp Ther. 2007 ; 323: 61-69
40. Verdejo-García A, Bechara A. A somatic marker theory of addiction. Neuropharmacology. 2009 ; 56: 48-62
41. Watanabe T, Nakagawa T, Yamamoto R, et al. Involvement of noradrenergic system within the central nucleus of the amygdala in naloxone-precipitated morphine withdrawal-induced conditioned place aversion in rats. Psychopharmacology. 2003 ; 170: 80-88
42. Wu Y, Li Y, Gao J, et al. Differential effect of NMDA receptor antagonist in the nucleus accumbens on reconsolidation of morphine -related positive and aversive memory in rats. Eur J Pharmacol. 2012a ; 674: 321-326
43. Wu Y, Li Y, Yang X. Differential effect of beta-adrenergic receptor antagonism in basolateral amygdala on reconsolidation of aversive and appetitive memories associated with morphine in rats. Addict Biol. 2012b ;:
44. Yim AJ, Moraes CRG, Ferreira TL, et al. Protein synthesis inhibition in the basolateral amygdala following retrieval does not impair expression of morphine-associated conditioned place preference. Behav Brain Res. 2006 ; 171: 162-169
45. Yonghui L, Xigeng Z, Yunjing B. Opposite effects of MK-801 on the expression of food and morphine-induced conditioned place preference in rats. J Psychopharmacol. 2006 ; 20: 40-46
46. Zito K, Bechara A, Greenwood C, et al. The dopamine innervation of the visceral cortex mediates the aversive effects of opiates. Pharmacol Biochem Behav. 1988 ; 30: 693-699