Selection of sucrose concentration depends on the effort required to obtain it: Studies using tetrabenazine, D1, D2, and D3 receptor antagonists

Psychopharmacology

Volumn 232, Issue 13, 2015, Pages 2377-2391

  Pardo, Marta ^a   López Cruz, Laura ^a   Miguel, Noemí San ^a   Salamone, John D ^b   Correa, Mercè ^a,b  

^a UNIVERSITAT JAUME I   (Spain)

^b UNIVERSITY OF CONNECTICUT   (United States)

Author keywords

Anergia; Anhedonia; Decision making; Depression; Dopamine; Motivation

Indexed keywords

4' ACETYL N [4 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]BUTYL]BIPHENYL 4 CARBOXAMIDE; DOPAMINE; DOPAMINE 1 RECEPTOR; DOPAMINE 2 RECEPTOR; DOPAMINE 3 RECEPTOR; ECOPIPAM; HALOPERIDOL; TETRABENAZINE; DOPAMINE 2 RECEPTOR BLOCKING AGENT; DOPAMINE RECEPTOR BLOCKING AGENT; SUCROSE;

ADULT; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; CONCENTRATION (PARAMETERS); DECISION MAKING; DEPLETION; DOPAMINE DEPLETION; DOPAMINE RECEPTOR BLOCKING; DRUG EFFECT; FOOD PREFERENCE; MALE; MOTIVATION; NONHUMAN; PRIORITY JOURNAL; SUGAR INTAKE; TASK PERFORMANCE; TASTE; ANIMAL; ANTAGONISTS AND INHIBITORS; DOSE RESPONSE; DRUG EFFECTS; PHYSIOLOGY; RAT; SPRAGUE DAWLEY RAT;

ANIMALS; CHOICE BEHAVIOR; DOPAMINE ANTAGONISTS; DOPAMINE D2 RECEPTOR ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; MALE; MOTIVATION; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, DOPAMINE D1; RECEPTORS, DOPAMINE D2; RECEPTORS, DOPAMINE D3; SUCROSE; TETRABENAZINE;

EID: 84930869228     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-015-3872-7     Document Type: Article

References (91)

1. Alburges ME, Hunt ME, McQuade RD, Wamsley JK (1992) D1-receptor antagonists: comparison of [3H]SCH39166 to [3H]SCH23390. J Chem Neuroanat 5(5):357-366
2. Audinot V, Newman-Tancredi A, Gobert A, Rivet JM, Brocco M, Lejeune F, Gluck L, Desposte I, Bervoets K, Dekeyne A, Millan MJ (1998) A comparative in vitro and in vivo pharmacological characterization of the novel dopamine D3 receptor antagonists (+)-S 14297, nafadotride, GR 103,691 and U 99194. J Pharmacol Exp Ther 287(1):187-197
3. Bai Y, Li Y, Lv Y, Liu Z, Zheng X (2014) Complex motivated behaviors for natural rewards following a binge-like regimen of morphine administration: mixed phenotypes of anhedonia and craving after short-term withdrawal. Front Behav Neurosci 8:23
4. Baldo BA, Sadeghian K, Basso AM, Kelley AE (2002) Effects of selective dopamine D1 or D2 receptor blockade within nucleus accumbens subregions on ingestive behavior and associated motor activity. Behav Brain Res 137(1-2):165-177
5. Barbano MF, Cador M (2006) Differential regulation of the consummatory, motivational and anticipatory aspects of feeding behavior by dopaminergic and opioidergic drugs. Neuropsychopharmacology 31(7):1371-1381
6. Barbano MF, Cador M (2007) Opioids for hedonic experience and dopamine to get ready for it. Psychopharmacology (Berl) 191(3):497-506
7. Barch DM, Treadway MT, Schoen N (2014) Effort, anhedonia, and function in schizophrenia: reduced effort allocation predicts amotivation and functional impairment. J Abnorm Psychol 123(2):387-397
8. Bardgett ME, Depenbrock M, Downs N, Points M, Green L (2009) Dopamine modulates effort-based decision making in rats. Behav Neurosci 123(2):242-251
9. Berridge KC (2000) Measuring hedonic impact in animals and infants: microstructure of affective taste reactivity patterns. Neurosci Biobehav Rev 24(2):173-198
10. Berridge KC (2007) The debate over dopamine's role in reward: the case for incentive salience. Psychopharmacology (Berl) 191(3):391-431
11. Berridge KC, Kringelbach ML (2008) Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology (Berl) 199(3):457-480
12. Berridge KC, Robinson TE (1998) What is the role of dopamine in reward: hedonic impact, reward learning, or incentive salience? Brain Res Brain Res Rev 28(3):309-369
13. Berridge KC, Robinson TE (2003) Parsing reward. Trends Neurosci 26(9):507-513. Review. Erratum in. Trends Neurosci 26(11):581
14. Cagniard B, Balsam PD, Brunner D, Zhuang X (2006) Mice with chronically elevated dopamine exhibit enhanced motivation, but not learning, for a food reward. Neuropsychopharmacology 31(7):1362-1370
15. Cannon CM, Bseikri MR (2004) Is dopamine required for natural reward? Physiol Behav 81(5):741-748
16. Cannon CM, Palmiter RD (2003) Reward without dopamine. J Neurosci 23(34):10827-10831
17. Clifford JJ, Waddington JL (1998) Heterogeneity of behavioural profile between three new putative selective D3 dopamine receptor antagonists using an ethologically based approach. Psychopharmacology (Berl) 136(3):284-290
18. Cocker PJ, Hosking JG, Benoit J, Winstanley CA (2012) Sensitivity to cognitive effort mediates psychostimulant effects on a novel rodent cost/benefit decision-making task. Neuropsychopharmacol 37:1825-1837
19. Cofer CN, Appley MH (1964) Motivation: Theory and Research. John Wiley and Sons, New York
20. Cousins MS, Wei W, Salamone JD (1994) Pharmacological characterization of performance on a concurrent lever pressing/feeding choice procedure: effects of dopamine antagonist, cholinomimetic, sedative and stimulant drugs. Psychopharmacology (Berl) 116(4):529-537
21. Das S, Fowler SC (1996) Similarity of clozapine's and olanzapine's acute effects on rats' lapping behavior. Psychopharmacology (Berl) 123(4):374-378
22. Diaz MR, Chappell AM, Christian DT, Anderson NJ, McCool BA (2011) Dopamine D3-like receptors modulate anxiety-like behavior and regulate GABAergic transmission in the rat lateral/basolateral amygdala. Neuropsychopharmacology 36(5):1090-1103
23. Fasano A, Bentivoglio AR (2009) Tetrabenazine. Expert Opin Pharmacother 10(17):2883-2896
24. Floresco SB, St Onge JR, Ghods-Sharifi S, Winstanley CA (2008) Cortico-limbic-striatal circuits subserving different forms of cost-benefit decision making. Cogn Affect Behav Neurosci 8(4):375-389
25. Fowler SC, Mortell C (1992) Low doses of haloperidol interfere with rat tongue extensions during licking: a quantitative analysis. Behav Neurosci 106(2):386-395
26. Gerlach M, Bartoszyk GD, Riederer P, Dean O, van den Buuse M (2011) Role of dopamine D3 and serotonin 5-HT 1A receptors in L:-DOPA-induced dyskinesias and effects of sarizotan in the 6-hydroxydopamine-lesioned rat model of Parkinson's disease. J Neural Transm 118(12):1733-1742
27. Gold JM, Strauss GP, Waltz JA, Robinson BM, Brown JK, Frank MJ (2013) Negative symptoms of schizophrenia are associated with abnormal effort-cost computations. Biol Psychiatry 74(2):130-136
28. Guay DR (2010) Tetrabenazine, a monoamine-depleting drug used in the treatment of hyperkinetic movement disorders. Am J Geriatr Pharmacother 8(4):331-373
29. Higley AE, Kiefer SW, Li X, Gaál J, Xi ZX, Gardner EL (2011) Dopamine D(3) receptor antagonist SB-277011A inhibits methamphetamine self-administration and methamphetamine-induced reinstatement of drug-seeking in rats. Eur J Pharmacol 659(2-3):187-192
30. Hsiao S, Chen BH (1995) Complex response competition and dopamine blocking: choosing of high cost sucrose solution versus low cost water in rats. Chin J Physiol 38(2):99-109
31. Hurley LL, Akinfiresoye L, Kalejaiye O, Tizabi Y (2014) Antidepressant effects of resveratrol in an animal model of depression. Behav Brain Res 268:1-7
32. Ikemoto S, Panksepp J (1996) Dissociations between appetitive and consummatory responses by pharmacological manipulations of reward-relevant brain regions. Behav Neurosci 110(2):331-345
33. Keppel G (1991) Design and Analysis: a researcher's handbook. Prentice-Hall, Englewood Cliffs, NJ
34. Koch M, Schmid A, Schnitzler HU (2000) Role of nucleus accumbens dopamine D1 and D2 receptors in instrumental and Pavlovian paradigms of conditioned reward. Psychopharmacology (Berl) 152(1):67-73
35. Koob GF, Riley SJ, Smith SC, Robbins TW (1978) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. J Comp Physiol Psychol 92(5):917-927
36. Levine AS, Kotz CM, Gosnell BA (2003) Sugars: hedonic aspects, neuroregulation, and energy balance. Am J Clin Nutr 78(4):834S-842S
37. Mai B, Sommer S, Hauber W (2012) Motivational states influence effort-based decision making in rats: the role of dopamine in the nucleus accumbens. Cogn Affect Behav Neurosci 12:74-84
38. Markou A, Salamone JD, Bussey TJ, Mar AC, Brunner D, Gilmour G, Balsam P (2013) Measuring reinforcement learning and motivation constructs in experimental animals: relevance to the negative symptoms of schizophrenia. Neurosci Biobehav Rev 37(9):2149-2165
39. Martinez-Hernandez J, Lanuza E, Martínez-García F (2012) Lesions of the dopaminergic innervation of the nucleus accumbens medial shell delay the generation of preference for sucrose, but not of sexual pheromones. Behav Brain Res 226(2):538-547
40. Mott AM, Nunes EJ, Collins LE, Port RG, Sink KS, Hockemeyer J, Müller CE, Salamone JD (2009) The adenosine A2A antagonist MSX-3 reverses the effects of the dopamine antagonist haloperidol on effort-related decision making in a T-maze cost/benefit procedure. Psychopharmacology (Berl) 204(1):103-112
41. Muscat R, Willner P (1989) Effects of dopamine receptor antagonists on sucrose consumption and preference. Psychopharmacology (Berl) 99(1):98-102
42. Nowend KL, Arizzi M, Carlson BB, Salamone JD (2001) D1 or D2 antagonism in nucleus accumbens core or dorsomedial shell suppresses lever pressing for food but leads to compensatory increases in chow consumption. Pharmacol Biochem Behav 69(3-4):373-382
43. Nunes EJ, Randall PA, Santerre JL, Given AB, Sager TN, Correa M, Salamone JD (2010) Differential effects of selective adenosine antagonists on the effort-related impairments induced by dopamine D1 and D2 antagonism. Neuroscience 170(1):268-280
44. Nunes EJ, Randall PA, Hart EE, Freeland C, Yohn SE, Baqi Y, Müller CE, López-Cruz L, Correa M, Salamone JD (2013) Effort-related motivational effects of the VMAT-2 inhibitor tetrabenazine: implications for animal models of the motivational symptoms of depression. J Neurosci 33(49):19120-19130
45. Orsetti M, Canonico PL, Dellarole A, Colella L, Di Brisco F, Ghi P (2007) Quetiapine prevents anhedonia induced by acute or chronic stress. Neuropsychopharmacology 32(8):1783-1790
46. Pardo M, Lopez-Cruz L, Valverde O, Ledent C, Baqi Y, Müller CE, Salamone JD, Correa M (2012) Adenosine A2A receptor antagonism and genetic deletion attenuate the effects of dopamine D2 antagonism on effort-based decision making in mice. Neuropharmacology 62(5-6):2068-2077
47. Peciña S, Berridge KC, Parker LA (1997) Pimozide does not shift palatability: separation of anhedonia from sensorimotor suppression by taste reactivity. Pharmacol Biochem Behav 58(3):801-811
48. Pettibone DJ, Totaro JA, Pflueger AB (1984) Tetrabenazine-induced depletion of brain monoamines: characterization and interaction with selected antidepressants. Eur J Pharmacol 102(3-4):425-430
49. Phillips PE, Walton ME, Jhou TC (2007) Calculating utility: preclinical evidence for cost-benefit analysis by mesolimbic dopamine. Psychopharmacology (Berl) 191(3):483-495
50. Pizzagalli DA (2014) Depression, stress, and anhedonia: toward a synthesis and integrated model. Annu Rev Clin Psychol 10:393-423
51. Podurgiel SJ, Nunes EJ, Yohn SE, Barber J, Thompson A, Milligan M, Lee CA, López-Cruz L, Pardo M, Valverde O, Lendent C, Baqi Y, Müller CE, Correa M, Salamone JD (2013) The vesicular monoamine transporter (VMAT-2) inhibitor tetrabenazine induces tremulous jaw movements in rodents: implications for pharmacological models of parkinsonian tremor. Neuroscience. 250:507-519
52. Randall PA, Pardo M, Nunes EJ, López Cruz L, Vemuri VK, Makriyannis A, Baqi Y, Müller CE, Correa M, Salamone JD (2012) Dopaminergic modulation of effort-related choice behavior as assessed by a progressive ratio chow feeding choice task: pharmacological studies and the role of individual differences. PLoS One 7(10):e47934
53. Randall PA, Lee CA, Nunes EJ, Yohn SE, Nowak V, Khan B, Shah P, Vemuri K, Makriyannis A, Baqi Y, Müller CE, Correa M, Salamone JD (2014) The VMAT-2 inhibitor tetrabenazine affects effort-related decision making in a progressive ratio/chow feeding choice task: reversal with antidepressant drugs. PLoS ONE 9(6):e99320
54. Reynolds SM, Berridge KC (2002) Positive and negative motivation in nucleus accumbens shell: bivalent rostrocaudal gradients for GABA-elicited eating, taste «liking»/«disliking» reactions, place preference/avoidance, and fear. J Neurosci 22:7308-7320
55. Roitman MF, Stuber GD, Phillips PE, Wightman RM, Carelli RM (2004) Dopamine operates as a subsecond modulator of food seeking. J Neurosci 24(6):1265-1271
56. Rolls ET, Rolls BJ, Kelly PH, Shaw SG, Wood RJ, Dale R (1974) The relative attenuation of self-stimulation, eating and drinking produced by dopamine-receptor blockade. Psychopharmacologia 38(3):219-230
57. Salamone JD (1988) Dopaminergic involvement in activational aspects of motivation: effects of haloperidol on schedule induced activity, feeding and foraging in rats. Psychobiology 16:196-206
58. Salamone JD (1992) Complex motor and sensorimotor functions of striatal and accumbens dopamine: involvement in instrumental behavior processes. Psychopharmacology 107:160-174
59. Salamone JD, Correa M (2002) Motivational views of reinforcement: implications for understanding the behavioral functions of nucleus accumbens dopamine. Behav Brain Res 137(1-2):3-25
60. Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76(3):470-485
61. Salamone JD, Steinpreis RE, McCullough LD, Smith P, Grebel D, Mahan K (1991) Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology (Berl) 104(4):515-521
62. Salamone JD, Mahan K, Rogers S (1993) Ventrolateral striatal dopamine depletions impair feeding and food handling in rats. Pharmacol Biochem Behav 44(3):605-610
63. Salamone JD, Cousins MS, Bucher S (1994) 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 65(2):221-229
64. Salamone JD, Cousins MS, Snyder BJ (1997) Behavioral functions of nucleus accumbens dopamine: empirical and conceptual problems with the anhedonia hypothesis. Neurosci Biobehav Rev 21(3):341-359
65. Salamone JD, Arizzi M, Sandoval MD, Cervone KM, Aberman JE (2002) Dopamine antagonists alter response allocation but do not suppress appetite for food in rats: contrast between the effects of SKF 83566, raclopride and fenfluramine on a concurrent choice task. Psychopharmacology (Berl) 160(4):371-380
66. Salamone JD, Correa M, Mingote S, Weber SM (2003) 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 305(1):1-8
67. Salamone JD, Correa M, Mingote SM, Weber SM (2005) Beyond the reward hypothesis: alternative functions of nucleus accumbens dopamine. Curr Opin Pharmacol 5(1):34-41
68. Salamone JD, Correa M, Mingote SM, Weber SM, Farrar AM (2006) Nucleus accumbens dopamine and the forebrain circuitry involved in behavioral activation and effort-related decision making: implications of understanding anergia and psychomotor slowing in depression. Curr Psychiat Rev 2(2):267-280
69. Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology (Berl) 191(3):461-482
70. Salamone JD, Correa M, Farrar AM, Nunes EJ, Pardo M (2009) Dopamine, behavioral economics, and effort. Front Behav Neurosci 3:13
71. Schneider JS, Pope A, Simpson K, Taggart J, Smith MG, DiStefano L (1992) Recovery from experimental parkinsonism in primates with GM1 ganglioside treatment. Science 256(5058):843-846
72. Sclafani A, Nissenbaum JW (1987) Taste preference thresholds for Polycose, maltose, and sucrose in rats. Neurosci Biobehav Rev 11(2):181-185
73. Sink KS, Vemuri VK, Olszewska T, Makriyannis A, Salamone JD (2008) Cannabinoid CB1 antagonists and dopamine antagonists produce different effects on a task involving response allocation and effort-related choice in food-seeking behavior. Psychopharmacology (Berl) 196(4):565-574
74. Smith GP (1995) Dopamine and food reward. Progress Psychobiol Physiol Psychol 16:83-144
75. Smith KS, Berridge KC, Aldridge JW (2011) Disentangling pleasure from incentive salience and learning signals in brain reward circuitry. Proc Natl Acad Sci U S A 108(27):E255-264
76. Sommer S, Danysz W, Russ H, Valastro B, Flik G, Hauber W (2014) The dopamine reuptake inhibitor MRZ-9547 increases progressive ratio responding in rats. Int J Neuropsychopharmacol [Epub ahead of print]
77. Song R, Bi GH, Zhang HY, Yang RF, Gardner EL, Li J, Xi ZX (2014) Blockade off D3 receptors by YQA14 inhibits cocaine's rewarding effects and relapse to drug-seeking behavior in rats. Neuropharmacology 77:398-405
78. Tanra AJ, Kagaya A, Okamoto Y, Muraoka M, Motohashi N, Yamawaki S (1995) TJS-010, a new prescription of oriental medicine, antagonizes tetrabenazine-induced suppression of spontaneous locomotor activity in rats. Prog Neuropsychopharmacol Biol Psychiatry 19(5):963-971
79. Treadway MT, Zald DH (2011) Reconsidering anhedonia in depression: lessons from translational neuroscience. Neurosci Biobehav Rev 35(3):537-555
80. Treadway MT, Bossaller NA, Shelton RC, Zald DH (2012) Effort-based decision-making in major depressive disorder: a translational model of motivational anhedonia. J Abnorm Psychol 121(3):553-558
81. Treit D, Berridge KC (1990) A comparison of benzodiazepine, serotonin, and dopamine agents in the taste-reactivity paradigm. Pharmacol Biochem Behav 37(3):451-456
82. Trifilieff P, Feng B, Urizar E, Winiger V, Ward RD, Taylor KM, Martinez D, Moore H, Balsam PD, Simpson EH, Javitch JA (2013) Increasing dopamine D2 receptor expression in the adult nucleus accumbens enhances motivation. Mol Psychiatry 18(9):1025-1033
83. Ungerstedt U (1971) Adipsia and aphagia after 6-hydroxydopamine induced degeneration of the nigro-striatal dopamine system. Acta Physiol Scand Suppl 367:95-122
84. Vezina P, Lorrain DS, Arnold GM, Austin JD, Suto N (2002) Sensitization of midbrain dopamine neuron reactivity promotes the pursuit of amphetamine. J Neurosci 22(11):4654-4662
85. Wakabayashi KT, Fields HL, Nicola SM (2004) Dissociation of the role of nucleus accumbens dopamine in responding to reward-predictive cues and waiting for reward. Behav Brain Res 154(1):19-30
86. Ward RD, Simpson EH, Richards VL, Deo G, Taylor K, Glendinning JI, Kandel ER, Balsam PD (2012) Dissociation of hedonic reaction to reward and incentive motivation in an animal model of the negative symptoms of schizophrenia. Neuropsychopharmacology 37(7):1699-1707
87. Westerink BH, Kwint HF, de Vries JB (1997) Eating-induced dopamine release from mesolimbic neurons is mediated by NMDA receptors in the ventral tegmental area: a dual-probe microdialysis study. J Neurochem 69(2):662-668
88. 2A antagonist MSX-3 reverses the effort-related effects of dopamine blockade: differential interaction with D1 and D2 family antagonists. Psychopharmacology (Berl) 203(3):489-499
89. Yamamoto T (2003) Brain mechanisms of sweetness and palatability of sugars. Nutr Rev 61:S5-9
90. Yohn SE, Thompson C, Randall PA, Lee CA, Müller CE, Baqi Y, Correa M, Salamone JD (2014) The VMAT-2 inhibitor tetrabenazine alters effort-related decision making as measured by the T-maze barrier choice task: reversal with the adenosine A2A antagonist MSX-3 and the catecholamine uptake blocker bupropion. Psychopharmacology (in press)
91. Zheng G, Dwoskin LP, Crooks PA (2006) Vesicular monoamine transporter 2: role as a novel target for drug development. AAPS J 8(4):E682-92