Differential involvement of the agranular vs granular insular cortex in the acquisition and performance of choice behavior in a rodent gambling task

Neuropsychopharmacology

Volumn 40, Issue 12, 2015, Pages 2832-2842

  Pushparaj, Abhiram ^a   Kim, Aaron S ^a   Musiol, Martin ^a   Zangen, Abraham ^b   Daskalakis, Zafiris J ^a,c   Zack, Martin ^c,d   Winstanley, Catharine A ^e   Le Foll, Bernard ^a,c,d  

^a UNIVERSITY OF TORONTO   (Canada)

^b BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^c CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

^d UNIVERSITY OF TORONTO   (Canada)

^e UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; AMINO ACID RECEPTOR STIMULATING AGENT; IBOTENIC ACID;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN REGION; CAUDAL GRANULAR INSULAR CORTEX; CONTROLLED STUDY; DECISION MAKING; GAMBLING; INSULA; LATENT PERIOD; MALE; NONHUMAN; PRIORITY JOURNAL; PUNISHMENT; RAT; REWARD; ROSTRAL AGRANULAR INSULAR CORTEX; TASK PERFORMANCE; ANALYSIS OF VARIANCE; ANIMAL; BRAIN CORTEX; DRUG EFFECTS; INJURIES; LONG EVANS RAT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; PSYCHOLOGY; REACTION TIME; REINFORCEMENT;

ANALYSIS OF VARIANCE; ANIMALS; CEREBRAL CORTEX; CHOICE BEHAVIOR; DECISION MAKING; EXCITATORY AMINO ACID AGONISTS; GABA AGONISTS; GAMBLING; IBOTENIC ACID; MALE; RATS; RATS, LONG-EVANS; REACTION TIME; REINFORCEMENT (PSYCHOLOGY);

EID: 84944441581     PISSN: 0893133X     EISSN: 1740634X     Source Type: Journal    
DOI: 10.1038/npp.2015.133     Document Type: Article

References (58)

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. 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.
3. APA (2013). Diagnostic and Statistical Manual of Mental Disorders, 5th edn. American Psychiatric Publishing: Washington, D. C., Washington, D.C.
4. Ayton P, Fischer I (2004). The hot hand fallacy and the gamblers fallacy: two faces of subjective randomness? Mem Cognit 32: 1369-1378.
5. Bar-On R, Tranel D, Denburg NL, Bechara A (2003). Exploring the neurological substrate of emotional and social intelligence. Brain 126: 1790-1800.
6. Billieux J, Van der Linden M, Khazaal Y, Zullino D, Clark L (2012). Trait gambling cognitions predict near-miss experiences and persistence in laboratory slot machine gambling. Br J Psychol 103: 412-427.
7. 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.
8. Clark L (2010). Decision-making during gambling: an integration of cognitive and psychobiological approaches. Philos Trans R Soc Lond B Biol Sci 365: 319-330.
9. Clark L, Bechara A, Damasio H, Aitken MR, Sahakian BJ, Robbins TW (2008). Differential effects of insular and ventromedial prefrontal cortex lesions on risky decision-making. Brain 131: 1311-1322.
10. Clark L, Crooks B, Clarke R, Aitken MR, Dunn BD (2012). Physiological responses to near-miss outcomes and personal control during simulated gambling. J Gambl Stud 28: 123-137.
11. Clark L, Lawrence AJ, Astley-Jones F, Gray N (2009). Gambling near-misses enhance motivation to gamble and recruit winrelated brain circuitry. Neuron 61: 481-490.
12. Clark L, Studer B, Bruss J, Tranel D, Bechara A (2014). Damage to insula abolishes cognitive distortions during simulated gambling. Proc Natl Acad Sci USA 111: 6098-6103.
13. Contreras M, Billeke P, Vicencio S, Madrid C, Perdomo G, Gonzalez M et al (2012). A role for the insular cortex in longterm memory for context-evoked drug craving in rats. Neuropsychopharmacology 37: 2101-2108.
14. Contreras M, Ceric F, Torrealba F (2007). Inactivation of the interoceptive insula disrupts drug craving and malaise induced by lithium. Science 318: 655-658.
15. Craig AD (2002). How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci 3: 655-666.
16. Craig AD (2004). Human feelings: why are some more aware than others? Trends Cogn Sci 8: 239-241.
17. Craig AD (2009). How do you feel-now? The anterior insula and human awareness. Nat Rev Neurosci 10: 59-70.
18. Craig AD (2010). The sentient self. Brain Struct Funct 214: 563-577.
19. Critchley HD, Mathias CJ, Dolan RJ (2001). Neural activity in the human brain relating to uncertainty and arousal during anticipation. Neuron 29: 537-545.
20. Damasio AR (1996). The somatic marker hypothesis and the possible functions of the prefrontal cortex. Philos Trans R Soc Lond B Biol Sci 351: 1413-1420.
21. 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.
22. Di Pietro NC, Mashhoon Y, Heaney C, Yager LM, Kantak KM (2008). Role of dopamine D1 receptors in the prefrontal dorsal agranular insular cortex in mediating cocaine self-administration in rats. Psychopharmacology (Berl) 200: 81-91.
23. 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.
24. 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.
25. Goldman-Rakic PS (1998). The cortical dopamine system: role in memory and cognition. Adv Pharmacol 42: 707-711.
26. Hardy SG (1985). Analgesia elicited by prefrontal stimulation. Brain Res 339: 281-284.
27. Hiebert NM, Vo A, Hampshire A, Owen AM, Seergobin KN, MacDonald PA (2014)Striatum in stimulus-response learning via feedback and in decision making. Neuroimage 101C: 448-457.
28. 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.
29. Hosking JG, Cocker PJ, Winstanley CA (2014). Dissociable contributions of anterior cingulate cortex and basolateral amygdala on a rodent cost/benefit decision-making task of cognitive effort. Neuropsychopharmacology 39: 1558-1567.
30. Ishii H, Ohara S, Tobler PN, Tsutsui K, Iijima T (2012). Inactivating anterior insular cortex reduces risk taking. J Neurosci 32: 16031-16039.
31. Jones CL, Minati L, Harrison NA, Ward J, Critchley HD (2011). Under pressure: response urgency modulates striatal and insula activity during decision-making under risk. PLoS One 6: e20942.
32. 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.
33. Kuhnen CM, Knutson B (2005). The neural basis of financial risk taking. Neuron 47: 763-770.
34. McGeorge AJ, Faull RL (1989). The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 29: 503-537.
35. Naqvi NH, Gaznick N, Tranel D, Bechara A (2014). The insula: a critical neural substrate for craving and drug seeking under conflict and risk. Ann N Y Acad Sci 1316: 53-70.
36. Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007). Damage to the insula disrupts addiction to cigarette smoking. Science 315: 531-534.
37. Pattij T, Schetters D, Schoffelmeer AN (2014). Dopaminergic modulation of impulsive decision making in the rat insular cortex. Behav Brain Res 270: 118-124.
38. Paulus MP, Rogalsky C, Simmons A, Feinstein JS, Stein MB (2003). Increased activation in the right insula during risk-taking decision making is related to harm avoidance and neuroticism. Neuroimage 19: 1439-1448.
39. Paulus MP, Stein MB (2006). An insular view of anxiety. Biol Psychiatry 60: 383-387.
40. Paxinos G, Watson C (1986). The Rat Brain in Stereotaxic Coordinates. 2nd edn. Academic Press: New York.
41. Preuschoff K, Bossaerts P, Quartz SR (2006). Neural differentiation of expected reward and risk in human subcortical structures. Neuron 51: 381-390.
42. Pushparaj A, Hamani C, Yu W, Shin DS, Kang B, Nobrega JN et al (2013). Electrical stimulation of the insular region attenuates nicotine-taking and nicotine-seeking behaviors. Neuropsychopharmacology 38: 690-698.
43. Rudorf S, Preuschoff K, Weber B (2012). Neural correlates of anticipation risk reflect risk preferences. J Neurosci 32: 16683-16692.
44. Scott D, Hiroi N (2011). Deconstructing craving: dissociable cortical control of cue reactivity in nicotine addiction. Biol Psychiatry 69: 1052-1059.
45. Seif T, Chang SJ, Simms JA, Gibb SL, Dadgar J, Chen BT et al (2013). Cortical activation of accumbens hyperpolarization-active NMDARs mediates aversion-resistant alcohol intake. Nat Neurosci 16: 1094-1100.
46. Shi CJ, Cassell MD (1998a). Cascade projections from somatosensory cortex to the rat basolateral amygdala via the parietal insular cortex. J Comp Neurol 399: 469-491.
47. Shi CJ, Cassell MD (1998b). Cortical, thalamic, and amygdaloid connections of the anterior and posterior insular cortices. J Comp Neurol 399: 440-468.
48. Singer T, Critchley HD, Preuschoff K (2009). A common role of insula in feelings, empathy and uncertainty. Trends Cogn Sci 13: 334-340.
49. St Onge JR, Floresco SB (2010). Prefrontal cortical contribution to risk-based decision making. Cereb Cortex 20: 1816-1828.
50. Sterzer P, Kleinschmidt A (2010). Anterior insula activations in perceptual paradigms: often observed but barely understood. Brain Struct Funct 214: 611-622.
51. Tremblay M, Cocker PJ, Hosking JG, Zeeb FD, Rogers RD, Winstanley CA (2014). Dissociable effects of basolateral amygdala lesions on decision making biases in rats when loss or gain is emphasized. Cogn Affect Behav Sci 14: 1184-1195.
52. Van der Werf YD, Witter MP, Groenewegen HJ (2002). The intralaminar and midline nuclei of the thalamus. Anatomical and functional evidence for participation in processes of arousal and awareness. Brain Res Brain Res Rev 39: 107-140.
53. Vertes RP (2004). Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51: 32-58.
54. Watanabe M, Kodama T, Hikosaka K (1997). Increase of extracellular dopamine in primate prefrontal cortex during a working memory task. J Neurophysiol 78: 2795-2798.
55. Weller JA, Levin IP, Shiv B, Bechara A (2009). The effects of insula damage on decision-making for risky gains and losses. Soc Neurosci 4: 347-358.
56. Xue G, Lu Z, Levin IP, Bechara A (2010). The impact of prior risk experiences on subsequent risky decision-making: the role of the insula. Neuroimage 50: 709-716.
57. Zeeb FD, Robbins TW, Winstanley CA (2009). Serotonergic and dopaminergic modulation of gambling behavior as assessed using a novel rat gambling task. Neuropsychopharmacology 34: 2329-2343.
58. Zeeb FD, Winstanley CA (2011). Lesions of the basolateral amygdala and orbitofrontal cortex differentially affect acquisition and performance of a rodent gambling task. J Neurosci 31: 2197-2204.