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:: Volume 23, Issue 2 (Bimonthly 2019) ::
Feyz 2019, 23(2): 143-152 Back to browse issues page
Evaluation of the effect of orexin-1 receptors in the nucleus accumbens shell on cost-benefit decision making in male rats
Saeedeh Nasrollahi , Sara Karimi , Alireza Abed , Gholamali Hamidi *
Physiology Research Center, Kashan University of Medical Sciences, Kashan, I.R. Iran. , hamiidi@yahoo.com
Abstract:   (174 Views)
Background: Cost-benefit decision-making is a one of the decision-making models in which the animal achieves a final benefit (reward) by evaluating the cost (effort or delay). The role of different brain regions such as nucleus accumbens in this process has been proven. Orexin is a neuropeptide expressed exclusively by lateral hypothalamus area neurons and orexin-producing neurons project their axons throughout the brain such as nucleus accumbens. The nucleus accumbens is a region of neural system that serves effort-based decision-making and orexin 1 receptor is distributed extensively throughout nucleus accumbens. Different physiological acts for erixin have been shown including cognitive actions and rewards. Since there is limited knowledge about this subject, this study aimed to examine the effect of orexin 1 receptor in the nucleus accumbens shell on effort-based decision-making.
Materials and Methods: In this study, T-maze was used to investigate cost-benefit decision-making based on effort, and the effect of SB334867 (30, 100, 300 nM/0.5µlDMSO), as selective orexin 1 receptor antagonist, within the nucleus accumbens shell was examined.
Results: SB334867 300 nM/0.5µl DMSO (injection in the shell of nucleus accumbens) significantly decreased the percentage of high reward choice (P<0.01) than the control group.
Conclusion: SB334867 affects the animal's preference for crossing the barrier and achieving more rewards, and the animal chooses to lower reward, without any effort.
Keywords: Cost-benefit decision-making, Orexin, Nucleus accumbens
Full-Text [PDF 349 kb]   (47 Downloads)    
Type of Study: Research | Subject: General
Received: 2019/01/24 | Accepted: 2019/04/27 | Published: 2019/06/10
1. Khani A, Kermani M, Hesam S, Haghparast A, Argandoña EG, Rainer G. Activation of cannabinoid system in anterior cingulate cortex and orbitofrontal cortex modulates cost-benefit decision making. Psychopharmacology 2015; 232(12): 2097-112.
2. Schulz S, Becker T, Nagel U, von Ameln-Mayerhofer A, Koch M. Chronic co-administration of the cannabinoid receptor agonist WIN55, 212-2 during puberty or adulthood reverses 3, 4 methylenedioxymetamphetamine (MDMA)-induced deficits in recognition memory but not in effort-based decision making. Pharmacol Biochem Behav 2013; 106: 91-100.
3. Bardgett ME, Depenbrock M, Downs N, Points M, Green L. Dopamine modulates effort-based decision making in rats. Behav Neurosci 2009; 123(2): 242.
4. Walton ME, Bannerman DM, Rushworth MF. The role of rat medial frontal cortex in effort-based decision making. J Neuroscience 2002; 22(24): 10996-1003.
5. Floresco SB, Maric T, Ghods-Sharifi S. Dopaminergic and glutamatergic regulation of effort-and delay-based decision making. Neuropsychopharmacology 2008; 33(8): 1966.
6. Salamone JD, Cousins MS, Bucher S. Anhedonia or anergia? Effects of haloperidol and nucleus accumbens dopamine depletion on instrumental response selection in a T-maze cost/benefit procedure. Behav Brain Res 1994; 65(2): 221-9.
7. Floresco SB, Ghods-Sharifi S. Amygdala-prefrontal cortical circuitry regulates effort-based decision making. Cereb Cortex 2006; 17(2): 251-60.
8. Walton ME, Bannerman DM, Alterescu K, Rushworth MF. Functional specialization within medial frontal cortex of the anterior cingulate for evaluating effort-related decisions. J Neuroscience 2003; 23(16): 6475-9.
9. Denk F, Walton M, Jennings K, Sharp T, Rushworth M, Bannerman D. Differential involvement of serotonin and dopamine systems in cost-benefit decisions about delay or effort. Psychopharmacology 2005; 179(3): 587-96.
10. Karimi S, Hamidi G, Fatahi Z, Haghparast A. Orexin 1 receptors in the anterior cingulate and orbitofrontal cortex regulate cost and benefit decision-making. Prog Neuropsychopharmacol Biol Psychiatry 2019; 89: 227-35.
11. Peyron C, Tighe DK, Van Den Pol AN, De Lecea L, Heller HC, Sutcliffe JG, et al. Neurons containing hypocretin (orexin) project to multiple neuronal systems. J Neuroscience 1998; 18(23): 9996-10015.
12. Narita M, Nagumo Y, Hashimoto S, Narita M, Khotib J, Miyatake M, et al. Direct involvement of orexinergic systems in the activation of the mesolimbic dopamine pathway and related behaviors induced by morphine. J Neuroscience 2006; 26(2): 398-405.
13. Borgland SL, Chang SJ, Bowers MS, Thompson JL, Vittoz N, Floresco SB, et al. Orexin A/hypocretin-1 selectively promotes motivation for positive reinforcers. J Neuroscience 2009; 29(36): 11215-25.
14. Mahler SV, Smith RJ, Moorman DE, Sartor GC, Aston-Jones G. Multiple roles for orexin/hypocretin in addiction. Prog Brain Res 2012; 198: 79-121.
15. Moorman DE, Aston-Jones G. Orexin/hypocretin modulates response of ventral tegmental dopamine neurons to prefrontal activation: diurnal influences. J Neurosci 2010; 30(46): 15585-99.
16. Sunter D, Morgan I, Edwards CMB, Dakin CL, Murphy KG, Gardiner J, et al. Orexins: effects on behavior and localisation of orexin receptor 2 messenger ribonucleic acid in the rat brainstem. Brain Res 2001; 907(1-2): 27-34.
17. Hervieu G, Cluderay J, Harrison D, Roberts J, Leslie R. Gene expression and protein distribution of the orexin-1 receptor in the rat brain and spinal cord. Neuroscience 2001; 103(3): 777-97.
18. Brown RE, Sergeeva OA, Eriksson KS, Haas HL. Convergent excitation of dorsal raphe serotonin neurons by multiple arousal systems (orexin/hypocretin, histamine and noradrenaline). J Neurosci 2002; 22(20): 8850-9.
19. Li J, Hu Z, Lecea L. The hypocretins/orexins: integrators of multiple physiological functions. Br J Pharmacol 2014; 171(2): 332-50.
20. Borgland SL, Ungless MA, Bonci A. Convergent actions of orexin/hypocretin and CRF on dopamine neurons: emerging players in addiction. Brain Res 2010; 1314: 139-44.
21. Sokolowski J, Salamone J. The role of accumbens dopamine in lever pressing and response allocation: effects of 6-OHDA injected into core and dorsomedial shell. Pharmacol Biochem Behav 1998; 59(3): 557-66.
22. Harris GC, Aston-Jones G. Arousal and reward: a dichotomy in orexin function. Trends Neurosci 2006; 29(10): 571-7.
23. Shirayama Y, Chaki S. Neurochemistry of the nucleus accumbens and its relevance to depression and antidepressant action in rodents. Curr Neuropharmacol 2006; 4(4): 277-91.
24. Salamone J, Cousins M, Snyder B. Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci Biobehav Rev 1997; 21(3): 341-59.
25. Walton M, Croxson P, Rushworth M, Bannerman D. The mesocortical dopamine projection to anterior cingulate cortex plays no role in guiding effort-related decisions. Behav Neurosci 2005; 119(1): 323.
26. Aston-Jones G, Smith RJ, Sartor GC, Moorman DE, Massi L, Tahsili-Fahadan P, et al. Lateral hypothalamic orexin/hypocretin neurons: a role in reward-seeking and addiction. Brain Res 2010; 1314: 74-90.
27. Sutcliffe JG, de Lecea L. The hypocretins: setting the arousal threshold. Nat Rev Neurosci 2002; 3(5): 339.
28. Sakurai T. The neural circuit of orexin (hypocretin): maintaining sleep and wakefulness. Nat Rev Neurosci 2007; 8(3): 171.
29. Akbari E, Naghdi N, Motamedi F. Functional inactivation of orexin 1 receptors in CA1 region impairs acquisition, consolidation and retrieval in Morris water maze task. Behav Brain Res 2006; 173(1): 47-52.
30. Akbari E, Naghdi N, Motamedi F. The selective orexin 1 receptor antagonist SB-334867-A impairs acquisition and consolidation but not retrieval of spatial memory in Morris water maze. Peptides 2007; 28(3): 650-6.
31. Jaeger LB, Farr SA, Banks WA, Morley JE. Effects of orexin-A on memory processing. Peptides 2002; 23(9): 1683-8.
32. Lei K, Wegner SA, Yu JH, Mototake A, Hu B, Hopf FW. Nucleus accumbens shell and mPFC but not insula orexin-1 receptors promote excessive alcohol drinking. Frontiers Neurosci 2016; 10: 400.
33. Hutton S, Murphy F, Joyce E, Rogers R, Cuthbert I, Barnes T, et al. Decision making deficits in patients with first-episode and chronic schizophrenia. Schizophr Res 2002; 55(3): 249-57.
34. Shurman B, Horan WP, Nuechterlein KH. Schizophrenia patients demonstrate a distinctive pattern of decision-making impairment on the Iowa Gambling Task. Schizophr Res 2005; 72(2-3): 215-24.
35. Pagonabarraga J, García‐Sánchez C, Llebaria G, Pascual‐Sedano B, Gironell A, Kulisevsky J. Controlled study of decision‐making and cognitive impairment in Parkinson's disease. Mov Disord 2007; 22(10): 1430-5.
36. Must A, Szabó Z, Bódi N, Szász A, Janka Z, Kéri S. Sensitivity to reward and punishment and the prefrontal cortex in major depression. J Affect Disord 2006; 90(2-3): 209-15.
37. Fadel J, Deutch A. Anatomical substrates of orexin–dopamine interactions: lateral hypothalamic projections to the ventral tegmental area. Neuroscience 2002; 111(2): 379-87.
38. Patyal R, Woo EY, Borgland SL. Local hypocretin-1 modulates terminal dopamine concentration in the nucleus accumbens shell. Front Behav Neurosci 2012; 6: 82.
39. Aston-Jones G, Smith RJ, Moorman DE, Richardson KA. Role of lateral hypothalamic orexin neurons in reward processing and addiction. Neuropharmacology 2009; 56: 112-21.
40. Balcita-Pedicino JJ, Sesack SR. Orexin axons in the rat ventral tegmental area synapse infrequently onto dopamine and gamma-aminobutyric acid neurons. J Comp Neurol 2007; 503(5): 668-84.
41. Salamone JD, Correa M, Farrar A, Mingote SM. Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 2007; 191(3): 461-82.
42. Bayer HM, Glimcher PW. Midbrain dopamine neurons encode a quantitative reward prediction error signal. Neuron 2005; 47(1): 129-41.
43. Hollerman JR, Schultz W. Dopamine neurons report an error in the temporal prediction of reward during learning. Nat Neurosci 1998; 1(4): 304.
44. Schultz W, Dayan P, Montague PR. A neural substrate of prediction and reward. Science 1997; 275(5306): 1593-9.
45. Berridge KC. The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology 2007; 191(3): 391-431.
46. Cagniard B, Balsam PD, Brunner D, Zhuang X. Mice with chronically elevated dopamine exhibit enhanced motivation, but not learning, for a food reward. Neuropsychopharmacology 2006; 31(7): 1362.
47. Salamone JD, Correa M, Mingote S, Weber S. Nucleus accumbens dopamine and the regulation of effort in food-seeking behavior: implications for studies of natural motivation, psychiatry, and drug abuse. J Pharmacol Exp Ther 2003; 305(1): 1-8.
48. Wise RA. Dopamine, learning and motivation. Nat Rev Neurosci 2004; 5(6): 483.
49. Hamill S, Trevitt J, Nowend K, Carlson B, Salamone J. Nucleus accumbens dopamine depletions and time-constrained progressive ratio performance: effects of different ratio requirements. Pharmacol Biochem Behav 1999; 64(1): 21-7.
50. Hosking JG, Floresco SB, Winstanley CA. Dopamine antagonism decreases willingness to expend physical, but not cognitive, effort: a comparison of two rodent cost/benefit decision-making tasks. Neuropsychopharmacology 2015; 40(4): 1005.
51. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN, Monsma FJ, et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 1990; 250(4986): 1429-32.
52. Kawaguchi Y. Neostriatal cell subtypes and their functional roles. Neurosci Res 1997; 27(1): 1-8.
53. Kravitz AV, Tye LD, Kreitzer AC. Distinct roles for direct and indirect pathway striatal neurons in reinforcement. Nat Neurosci 2012; 15(6): 816.
54. Flores Á, Maldonado R, Berrendero F. Cannabinoid-hypocretin cross-talk in the central nervous system: what we know so far. Frontiers Neurosci 2013; 7: 256.
55. Watkins BA, Kim J. The endocannabinoid system: directing eating behavior and macronutrient metabolism. Frontiers Psychol 2015; 5: 1506.
56. Thompson MD, Xhaard H, Sakurai T, Rainero I, Kukkonen JP. OX1 and OX2 orexin/hypocretin receptor pharmacogenetics. Frontiers Neurosci 2014; 8: 57.
57. Xu T-R, Ward RJ, Pediani JD, Milligan G. The orexin OX1 receptor exists predominantly as a homodimer in the basal state: potential regulation of receptor organization by both agonist and antagonist ligands. Biochem J 2011; 439(1): 171-83.
58. Ward RJ, Pediani JD, Milligan G. Hetero-multimerization of the cannabinoid CB1 receptor and the orexin OX1 receptor generates a unique complex in which both protomers are regulated by orexin A. J Biol Chem 2011:jbc. M111. 287649.
59. Tung LW, Lu GL, Lee YH, Yu L, Lee HJ, Leishman E, et al. Orexins contribute to restraint stress-induced cocaine relapse by endocannabinoid-mediated disinhibition of dopaminergic neurons. Nat Commun 2016; 7: 12199.
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Nasrollahi S, Karimi S, Abed A, Hamidi G. Evaluation of the effect of orexin-1 receptors in the nucleus accumbens shell on cost-benefit decision making in male rats. Feyz. 2019; 23 (2) :143-152
URL: http://feyz.kaums.ac.ir/article-1-3800-en.html

Volume 23, Issue 2 (Bimonthly 2019) Back to browse issues page
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