Lorcaserin and CP-809101 reduce motor impulsivity and reinstatement of food seeking behavior in male rats: Implications for understanding the anti-obesity property of 5-HT2C receptor agonists

Psychopharmacology

Volumn 233, Issue 14, 2016, Pages 2841-2856

  Higgins, Guy A ^a,d   Silenieks, Leo B ^a   Altherr, Everett B ^c   MacMillan, Cam ^b   Fletcher, Paul J ^d,e   Pratt, Wayne E ^c  

^a InterVivo Solutions Inc   (Canada)

^b Vivocore   (Canada)

^c WAKE FOREST UNIVERSITY   (United States)

^d UNIVERSITY OF TORONTO   (Canada)

^e CENTRE FOR ADDICTION AND MENTAL HEALTH   (Canada)

Author keywords

5 HT2C receptor; Binge eating disorder; CP 809101; Food reinstatement; Impulsivity; Lorcaserin; Prefeeding; Rat

Indexed keywords

CP 809101; LORCASERIN; SEROTONIN 2C AGONIST; UNCLASSIFIED DRUG; BENZAZEPINE DERIVATIVE; CP-809,101; PIPERAZINE DERIVATIVE; PYRAZINE DERIVATIVE; SEROTONIN 2 AGONIST;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BINGE EATING DISORDER; COMPARATIVE EFFECTIVENESS; CONTROLLED STUDY; CROSSOVER PROCEDURE; DISEASE ASSOCIATION; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFECT; EXPERIMENTAL HYPOACTIVITY; FOOD DEPRIVATION; FOOD INTAKE; FOOD SEEKING BEHAVIOR; IMPULSIVENESS; MALE; NONHUMAN; OBESITY; PRIORITY JOURNAL; RAT; REINFORCEMENT; RELAPSE; REWARD; SATIETY; ANIMAL; DECISION MAKING; DRUG EFFECTS; FEEDING BEHAVIOR;

ANIMALS; BENZAZEPINES; CHOICE BEHAVIOR; DOSE-RESPONSE RELATIONSHIP, DRUG; FEEDING BEHAVIOR; IMPULSIVE BEHAVIOR; MALE; OBESITY; PIPERAZINES; PYRAZINES; RATS; REWARD; SEROTONIN 5-HT2 RECEPTOR AGONISTS;

EID: 84973161248     PISSN: 00333158     EISSN: 14322072     Source Type: Journal    
DOI: 10.1007/s00213-016-4329-3     Document Type: Article

References (86)

1. Aronne L, Shanahan W, Fain R, Glicklich A, Soliman W, Li Y, Smith S (2014) Safety and efficacy of lorcaserin: a combined analysis of the BLOOM and BLOSSOM trials. Postgrad Med 126:7–18
2. Avena NM (2010) The study of food addiction using animal models of binge eating. Appetite 55:734–737
3. Baldo BA, Pratt WE, Will MJ, Hanlon EC, Bakshi VP, Cador M (2013) Principles of motivation revealed by the diverse functions of neuropharmacological and neuroanatomical substrates underlying feeding behavior. Neurosci Biobehav Rev 37:1985–1998
4. Berg KA, Clarke WP, Cunningham KA, Spampinato U (2008) Fine-tuning serotonin2c receptor function in the brain: molecular and functional implications. Neuropharmacology 55:969–976
5. Berridge KC (2007) The debate over dopamine’s role in reward: the case for incentive salience. Psychopharmacology (Berl) 191:391–431
6. Berthoud H-R (2011) Metabolic and hedonic drives in the neural control of appetite: who is the boss? Curr Opin Neurobiol 21:888–896
7. Betley JN, Cao ZF, Ritola KD, Sternson SM (2013) Parallel, redundant circuit organization for homeostatic control of feeding behavior. Cell 155:1337–1150
8. Bizarro L, Stolerman IP (2003) Attentional effects of nicotine and amphetamine in rats at different levels of motivation. Psychopharmacology (Berl) 170:271–277
9. Bray GA, Ryan DH (2014) Update on obesity pharmacotherapy. Ann N Y Acad Sci 1311:1–13
10. Burke LK, Heisler LK (2015) 5-Hydroxytryptamine medications for the treatment of obesity. J Neuroendocrinol 27:389–398
11. Calu DJ, Chen YW, Kawa AB, Nair SG, Shaham Y (2014) The use of the reinstatement model to study relapse to palatable food seeking during dieting. Neuropharmacology 76:395–406
12. Cardinal RN, Robbins TW, Everitt BJ (2000) The effects of d-amphetamine, chlordiazepoxide, alpha-flupenthixol and behavioural manipulations on choice of signalled and unsignalled delayed reinforcement in rats. Psychopharmacology (Berl) 152:362–375
13. Carli M, Samanin R (1992) Serotonin2 receptor agonists and serotonergic anorectic drugs affect rats’ performance differently in a five-choice serial reaction time task. Psychopharmacology (Berl) 106:228–234
14. Carli M, Samanin R (2000) The 5-HT(1A) receptor agonist 8-OH-DPAT reduces rats’ accuracy of attentional performance and enhances impulsive responding in a five-choice serial reaction time task: role of presynaptic 5-HT(1A) receptors. Psychopharmacology (Berl) 149:259–268
15. 2C receptor agonist and d-fenfluramine on feeding patterns in the rat. Psychopharmacology (Berl) 152:256–67
16. Corwin RL, Avena NM, Boggiano MM (2011) Feeding and reward: perspectives from three rat models of binge eating. Physiol Behav 104:87–97
17. 2C receptor activation suppresses the reinforcing efficacy of cocaine and sucrose but differentially affects the incentive-salience value of cocaine- vs. sucrose-associated cues. Neuropharmacology 61:513–523
18. Dalley JW, Everitt BJ, Robbins TW (2011) Impulsivity, compulsivity, and top-down cognitive control. Neuron 69:680–694
19. Diergaarde L, Pattij T, Poortvliet I, Hogenboom F, de Vries W, Schoffelmeer AN, De Vries TJ (2008) Impulsive choice and impulsive action predict vulnerability to distinct stages of nicotine seeking in rats. Biol Psychiatry 63:301–308
20. Di Matteo V, Cacchio M, Di Giulio C, Esposito E (2002) Role of serotonin(2C) receptors in the control of brain dopaminergic function. Pharmacol Biochem Behav 71:727–734
21. Evenden JL (1999) Varieties of impulsivity. Psychopharmacology (Berl) 146:348–361
22. Evenden JL, Ryan CN (1996) The pharmacology of impulsive behaviour in rats: the effects of drugs on response choice with varying delays of reinforcement. Psychopharmacology (Berl) 128:161–170
23. Fidler MC, Sanchez M, Raether B, Weissman NJ, Smith SR, Shanahan WR, Anderson CM (2011) A one-year randomized trial of lorcaserin for weight loss in obese and overweight adults: the BLOSSOM trial. J Clin Endocrinol Metab 96:3067–3077
24. 2C receptor antagonists in the rat and mouse on premature responding in the five-choice serial reaction time test. Psychopharmacology (Berl) 195:223–234
25. Floresco SB, McLaughlin RJ, Haluk DM (2008) Opposing roles for the nucleus accumbens core and shell in cue-induced reinstatement of food-seeking behavior. Neuroscience 154:877–884
26. Grottick AJ, Higgins GA (2000) Effect of subtype selective nicotinic compounds on attention as assessed by the five-choice serial reaction time task. Behav Brain Res 117:197–208
27. 2C receptors on cocaine- and food-maintained behavior. J Pharmacol Exp Ther 295:1183–1191
28. Guy EG, Choi E, Pratt WE (2011) Nucleus accumbens dopamine and mu-opioid receptors modulate the reinstatement of food-seeking behavior by food-associated cues. Behav Brain Res 219:265–272
29. Hamilton KR, Mitchell MR, Wing VC, Balodis IM, Bickel WK, Fillmore M, Lane SD, Lejuez CW, Littlefield AK, Luijten M, Mathias CW, Mitchell SH, Napier TC, Reynolds B, Schütz CG, Setlow B, Sher KJ, Swann AC, Tedford SE, White MJ, Winstanley CA, Yi R, Potenza MN, Moeller FG (2015) Choice impulsivity: definitions, measurement issues, and clinical implications. Personal Disord 6:182–198
30. Halford JC, Harrold JA, Lawton CL, Blundell JE (2005) Serotonin (5-HT) drugs: effects on appetite expression and use for the treatment of obesity. Curr Drug Targets 6:201–213
31. 2C receptor compounds on ventral tegmental area self-stimulation thresholds in rats. Psychopharmacology (Berl) 203:579–588
32. Harrison AA, Everitt BJ, Robbins TW (1997) Central 5-HT depletion enhances impulsive responding without affecting the accuracy of attentional performance: interactions with dopaminergic mechanisms. Psychopharmacology (Berl) 133:329–342
33. Harrison AA, Everitt BJ, Robbins TW (1999) Central serotonin depletion impairs both the acquisition and performance of a symmetrically reinforced go/no-go conditional visual discrimination. Behav Brain Res 100:99–112
34. Heal DJ, Gosden J, Smith S (2012) What is the prognosis for new centrally-acting anti-obesity drugs? Neuropharmacology 63:132–146
35. Heisler LK, Cowley MA, Tecott LH, Fan W, Low MJ, Smart JL, Rubinstein M, Tatro JB, Marcus JN (2002) Activation of central melanocortin pathways by fenfluramine. Science 297(5581):609–611
36. Hewitt KN, Lee MD, Dourish CT, Clifton PG (2002) Serotonin 2C receptor agonists and the behavioural satiety sequence in mice. Pharmacol Biochem Behav 71:691–700
37. 2C receptor agonist lorcaserin on efficacy and safety measures in a rat model of diet-induced obesity. Pharmacol Res Perspect 3(1):e00084
38. 2A receptor antagonist M100,907 attenuates motor and ‘impulsive-type’ behaviours produced by NMDA receptor antagonism. Psychopharmacology (Berl) 170:309–319
39. 2C receptors. Eur J Pharmacol 480:151–162
40. 2C receptor agonists on behaviours motivated by food and nicotine and on side effect profiles. Psychopharmacology (Berl) 226:475–490
41. 2C receptor agonist lorcaserin reduces nicotine self-administration, discrimination and reinstatement: relationship to feeding behavior and impulse control. Neuropsychopharmacology 37:1177–1191
42. 6 receptor antagonist, SB-742457, promote satiety; a microstructural analysis of feeding behaviour. Psychopharmacology (Berl) 233:417–424
43. 2C receptors on brain stimulation reward and the reward-facilitating effect of cocaine. Psychopharmacology (Berl) 213:337–354
44. Kelley AE, Baldo BA, Pratt WE, Will MJ (2005) Corticostriatal-hypothalamic circuitry and food motivation: integration of energy, reward, and action. Physiology and Behavior 86:773–795
45. Kennett GA, Clifton PG (2010) New approaches to the pharmacological treatment of obesity: can they break through the efficacy barrier? Pharmacol Biochem Behav 97:63–83
46. Kenny PJ (2011) Reward mechanisms in obesity: new insights and future directions. Neuron 69:644–679
47. Kolokotroni KZ, Rodgers RJ, Harrison AA (2011) Acute nicotine increases both impulsive choice and behavioural disinhibition in rats. Psychopharmacology (Berl) 217:455–473
48. 2C receptor agonist promotes hypophagia via downstream activation of melanocortin 4 receptors. Endocrinology 149:1323–1328
49. 2C agonist, decreases nicotine self-administration in female rats. J Pharmacol Exp Ther 338:890–896
50. Lin W, Pratt WE (2014) Inactivation of the nucleus accumbens core or medial shell attenuates reinstatement of sugar-seeking behavior following sugar priming or exposure to food-associated cues. PLoS One 9(6):e99301
51. Martin CK, Redman LM, Zhang J, Sanchez M, Anderson CM, Smith SR, Ravussin E (2011) Lorcaserin, a 5-HT(2C) receptor agonist, reduces body weight by decreasing energy intake without influencing energy expenditure. J Clin Endocrinol Metab 96:837–845
52. Mobbs O, Crépin C, Thiéry C, Golay A, Van der Linden M (2010) Obesity and the four facets of impulsivity. Patient Educ Couns 79:372–377
53. Mobini S, Chiang TJ, Ho MY, Bradshaw CM, Szabadi E (2000) Effects of central 5-hydroxytryptamine depletion on sensitivity to delayed and probabilistic reinforcement. Psychopharmacology (Berl) 152:390–397
54. Myerson J, Green L, Warusawitharana M (2001) Area under the curve as a measure of discounting. J Exp Anal Behav 76:235–243
55. Nair SG, Adams-Deutsch T, Epstein DH, Shaham Y (2009) The neuropharmacology of relapse to food seeking: methodology, main findings, and comparison with relapse to drug seeking. Prog Neurobiol 89:18–45
56. Navarra R, Comery TA, Graf R, Rosenzweig-Lipson S, Day M (2008) The 5-HT(2C) receptor agonist WAY-163909 decreases impulsivity in the 5-choice serial reaction time test. Behav Brain Res 188:412–415
57. Pattij T, De Vries TJ (2013) The role of impulsivity in relapse vulnerability. Curr Opin Neurobiol 23:700–705
58. Pickens CL, Cifani C, Navarre BM, Eichenbaum H, Theberge FR, Baumann MH, Calu DJ, Shaham Y (2012) Effect of fenfluramine on reinstatement of food seeking in female and male rats: implications for the predictive validity of the reinstatement model. Psychopharmacology (Berl) 221:341–353
59. Powell AG, Apovian CM, Aronne LJ (2011) New drug targets for the treatment of obesity. Clin Pharmacol Ther 90:40–51
60. Pratt WE, Ford RT (2013) Systemic treatment with D-fenfluramine, but not sibutramine, blocks cue-induced reinstatement of food-seeking behavior in the rat. Neurosci Lett 556:232–237
61. Quarta D, Naylor CG, Stolerman IP (2007) The serotonin2C receptor agonist Ro-60-0175 attenuates effects of nicotine in the five-choice serial reaction time task and in drug discrimination. Psychopharmacology (Berl) 193:391–402
62. Richards JB, Mitchell SH, de Wit H, Seiden LS (1997) Determination of discount functions in rats with an adjusting-amount procedure. J Exp Anal Behav 67:353–366
63. Robbins TW (2002) The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 163:362–380
64. Salamone JD, Correa M (2012) The mysterious motivational functions of mesolimbic dopamine. Neuron 76(3):470–485
65. Schag K, Schönleber J, Teufel M, Zipfel S, Giel KE (2013) Food-related impulsivity in obesity and binge eating disorder–a systematic review. Obes Rev 14:477–495
66. Serafine KM, Rice KC, France CP (2015) Directly observable behavioral effects of lorcaserin in rats. J Pharmacol Exp Ther 355:381–385
67. 2C agonist, shows activity in animal models of antipsychotic activity. Neuropharmacology 52:279–290
68. 2C receptor agonist for the treatment of obesity. J Med Chem 51:305–313
69. Smith DG, Robbins TW (2013) The neurobiological underpinnings of obesity and binge eating: a rationale for adopting the food addiction model. Biol Psychiatry 73:804–810
70. Smith SR, Weissman NJ, Anderson CM, Sanchez M, Chuang E, Stubbe S, Bays H, Shanahan WR, Behavioral Modification and Lorcaserin for Overweight and Obesity Management (BLOOM) Study Group (2010) Multicentre, placebo-controlled trial of lorcaserin for weight management. N Eng J Med 263:245–256
71. Sohn JW, Xu Y, Jones JE, Wickman K, Williams KW, Elmquist JK (2011) Serotonin 2C receptor activates a distinct population of arcuate pro-opiomelanocortin neurons via TRPC channels. Neuron 71:488–497
72. St Onge JR, Chiu YC, Floresco SB (2010) Differential effects of dopaminergic manipulations on risky choice. Psychopharmacology (Berl) 211:209–221
73. Tanno T, Maguire DR, Henson C, France CP (2014) Effects of amphetamine and methylphenidate on delay discounting in rats: interactions with order of delay presentation. Psychopharmacology (Berl) 231:85–95
74. Thomsen WJ, Grottick AJ, Menzaghi F, Reyes-Saldana H, Espita S, Yuskin D, Whelan K, Martin M, Morgan M, Chen W, Al-Shamma H, Smith B, Chalmers D, Behan D (2008) Lorcaserin, a novel selective human 5-hydroxytryptamine2C agonist: in vitro and in vivo pharmacological characterization. J Pharmacol Exp Ther 325:577–587
75. Velázquez-Sánchez C, Ferragud A, Moore CF, Everitt BJ, Sabino V, Cottone P (2014) High trait impulsivity predicts food addiction-like behavior in the rat. Neuropsychopharmacology 39:2463–2472
76. 2C receptor mutant mice. Psychopharmacology (Berl) 143:309–314
77. Vickers SP, Dourish CT, Kennett GA (2001) Evidence that hypophagia induced by d-fenfluramine and d-norfenfluramine in the rat is mediated by 5-HT2C receptors. Neuropharmacology 41:200–209
78. Vickers SP, Hackett D, Murray F, Hutson PH, Heal DJ (2015) Effects of lisdexamfetamine in a rat model of binge-eating. J Psychopharmacol 29:1290–1307
79. Volkow ND, Wang GJ, Tomasi D, Baler RD (2013) Obesity and addiction: neurobiological overlaps. Obes Rev 14:2–18
80. Volkow ND, Wise RA (2005) How can drug addiction help us understand obesity? Nat Neurosci 8:555–560
81. Winstanley CA (2011) The utility of rat models of impulsivity in developing pharmacotherapies for impulse control disorders. Br J Pharmacol 164:1301–1321
82. Winstanley CA, Dalley JW, Theobald DE, Robbins TW (2004a) Fractionating impulsivity: contrasting effects of central 5-HT depletion on different measures of impulsive behavior. Neuropsychopharmacology 29:1331–1343
83. 2C receptor antagonists have opposing effects on a measure of impulsivity: interactions with global 5-HT depletion. Psychopharmacology (Berl) 176:376–385
84. Wogar MA, Bradshaw CM, Szabadi E (1993) Effect of lesions of the ascending 5-hydroxytryptaminergic pathways on choice between delayed reinforcers. Psychopharmacology (Berl) 111:239–243
85. Zeeb FD, Higgins GA, Fletcher PJ (2015) The serotonin 2C receptor agonist lorcaserin attenuates intracranial self-stimulation and blocks the reward-enhancing effects of nicotine. ACS Chem Neurosci 6:1231–1240
86. Zlebnik NE, Carroll ME (2015) Effects of the combination of wheel running and atomoxetine on cue- and cocaine-primed reinstatement in rats selected for high or low impulsivity. Psychopharmacology (Berl) 232:1049–1059