Pregabalin- and topiramate-mediated regulation of cognitive and motor impulsivity in DBA/2 mice

British Journal of Pharmacology

Volumn 167, Issue 1, 2012, Pages 183-195

  Navarrete, Francisco ^a,c   Pérez Ortiz, José M ^b   Manzanares, Jorge ^a,c  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b HOSPITAL GENERAL UNIVERSITARIO DE ALBACETE   (Spain)

^c INSTITUTO DE SALUD CARLOS III   (Spain)

Author keywords

adrenaline; DBA 2 mice; dopamine; drug abuse; gene expression; impulsivity; pregabalin; topiramate

Indexed keywords

PREGABALIN; TOPIRAMATE;

ALPHA 2A ADRENOCEPTOR GENE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR DISORDER; COGNITIVE DEFECT; CONTROLLED STUDY; D2 RECEPTOR GENE; DOSE RESPONSE; DRUG EFFECT; DRUG MEGADOSE; GENE; GENE EXPRESSION; GENE LOCATION; IMPULSIVENESS; MALE; MENTAL TASK; MENTAL TEST; MOTOR DYSFUNCTION; MOUSE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; REINFORCEMENT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE DRUG DOSE; TH GENE; TRANQUILIZING ACTIVITY; TREATMENT DURATION; TREATMENT RESPONSE; VENTRAL TEGMENTUM;

ANIMALS; ANTICONVULSANTS; ANXIETY; BEHAVIOR, ANIMAL; COGNITION; FRUCTOSE; GAMMA-AMINOBUTYRIC ACID; IMPULSIVE BEHAVIOR; MALE; MICE; MICE, INBRED DBA; MOTOR ACTIVITY; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; RECEPTORS, ADRENERGIC, ALPHA-2; RECEPTORS, DOPAMINE D2; VENTRAL TEGMENTAL AREA;

EID: 84864650952     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/j.1476-5381.2012.01981.x     Document Type: Article

References (102)

1. Adriani W, Zoratto F, Romano E, Laviola G, (2010). Cognitive impulsivity in animal models: role of response time and reinforcing rate in delay intolerance with two-choice operant tasks. Neuropharmacology 58: 694-701.
2. Andrews N, Loomis S, Blake R, Ferrigan L, Singh L, McKnight AT, (2001). Effect of gabapentin-like compounds on development and maintenance of morphine-induced conditioned place preference. Psychopharmacology (Berl) 157: 381-387.
3. Aracil-Fernandez A, Almela P, Manzanares J, (2011). Pregabalin and topiramate regulate behavioural and brain gene transcription changes induced by spontaneous cannabinoid withdrawal in mice. Addict Biol doi: 10.1111/j.1369-1600.2011.00406.x.
4. August GJ, Garfinkel BD, (1989). Behavioral and cognitive subtypes of ADHD. J Am Acad Child Adolesc Psychiatry 28: 739-748.
5. Backstrom P, Hyytia P, (2003). Attenuation of cocaine-seeking behaviour by the AMPA/kainate receptor antagonist CNQX in rats. Psychopharmacology (Berl) 166: 69-76.
6. Basar K, Sesia T, Groenewegen H, Steinbusch HW, Visser-Vandewalle V, Temel Y, (2010). Nucleus accumbens and impulsivity. Prog Neurobiol 92: 533-557.
7. Bisaga A, Aharonovich E, Garawi F, Levin FR, Rubin E, Raby WN, et al,. (2006). A randomized placebo-controlled trial of gabapentin for cocaine dependence. Drug Alcohol Depend 81: 267-274.
8. Bockbrader HN, Radulovic LL, Posvar EL, Strand JC, Alvey CW, Busch JA, et al,. (2010). Clinical pharmacokinetics of pregabalin in healthy volunteers. J Clin Pharmacol 50: 941-950.
9. Boes AD, Bechara A, Tranel D, Anderson SW, Richman L, Nopoulos P, (2009). Right ventromedial prefrontal cortex: a neuroanatomical correlate of impulse control in boys. Soc Cogn Affect Neurosci 4: 1-9.
10. Bourgeois BF, (1996). New antiepileptic drugs. Curr Opin Pediatr 8: 543-548.
11. Braga MF, Aroniadou-Anderjaska V, Li H, Rogawski MA, (2009). Topiramate reduces excitability in the basolateral amygdala by selectively inhibiting GluK1 (GluR5) kainate receptors on interneurons and positively modulating GABAA receptors on principal neurons. J Pharmacol Exp Ther 330: 558-566.
12. Buckholtz JW, Treadway MT, Cowan RL, Woodward ND, Li R, Ansari MS, et al,. (2010). Dopaminergic network differences in human impulsivity. Science 329: 532.
13. Crawley J, Goodwin FK, (1980). Preliminary report of a simple animal behavior model for the anxiolytic effects of benzodiazepines. Pharmacol Biochem Behav 13: 167-170.
14. Cubells JF, (2006). Topiramate for cocaine dependence. Curr Psychiatry Rep 8: 130-131.
15. Cummings JA, Gowl BA, Westenbroek C, Clinton SM, Akil H, Becker JB, (2011). Effects of a selectively bred novelty-seeking phenotype on the motivation to take cocaine in male and female rats. Biol Sex Differ 2: 1-10.
16. Dalley JW, Fryer TD, Brichard L, Robinson ES, Theobald DE, Laane K, et al,. (2007). Nucleus accumbens D2/3 receptors predict trait impulsivity and cocaine reinforcement. Science 315: 1267-1270.
17. Dalley JW, Mar AC, Economidou D, Robbins TW, (2008). Neurobehavioral mechanisms of impulsivity: fronto-striatal systems and functional neurochemistry. Pharmacol Biochem Behav 90: 250-260.
18. Dellu-Hagedorn F, (2006). Relationship between impulsivity, hyperactivity and working memory: a differential analysis in the rat. Behav Brain Funct 2: 10.
19. Di Nicola M, Martinotti G, Tedeschi D, Frustaci A, Mazza M, Sarchiapone M, et al,. (2010). Pregabalin in outpatient detoxification of subjects with mild-to-moderate alcohol withdrawal syndrome. Hum Psychopharmacol 25: 268-275.
20. Dolengevich Segal H, Rodriguez Salgado B, Conejo Garcia A, San Sebastian Cabases J, (2006). Efficacy of topiramate in children and adolescent with problems in impulse control: preliminary results. Actas Esp Psiquiatr 34: 280-282.
21. Dougherty DM, Bjork JM, Harper RA, Marsh DM, Moeller FG, Mathias CW, et al,. (2003). Behavioral impulsivity paradigms: a comparison in hospitalized adolescents with disruptive behavior disorders. J Child Psychol Psychiatry 44: 1145-1157.
22. Evenden J, (1999a). Impulsivity: a discussion of clinical and experimental findings. J Psychopharmacol 13: 180-192.
23. Evenden JL, (1999b). Varieties of impulsivity. Psychopharmacology (Berl) 146: 348-361.
24. Evren C, Durkaya M, Evren B, Dalbudak E, Cetin R, (2012). Relationship of relapse with impulsivity, novelty seeking and craving in male alcohol-dependent inpatients. Drug Alcohol Rev 31: 81-90.
25. Fahy T, Eisler I, (1993). Impulsivity and eating disorders. Br J Psychiatry 162: 193-197.
26. Feng J, Sobell JL, Heston LL, Goldman D, Cook E, Jr, Kranzler HR, et al,. (1998). Variants in the alpha2A AR adrenergic receptor gene in psychiatric patients. Am J Med Genet 81: 405-410.
27. Frampton JE, Foster RH, (2006). Pregabalin: in the treatment of generalised anxiety disorder. CNS Drugs 20: 685-693. discussion 694-5.
28. Furieri FA, Nakamura-Palacios EM, (2007). Gabapentin reduces alcohol consumption and craving: a randomized, double-blind, placebo-controlled trial. J Clin Psychiatry 68: 1691-1700.
29. Gajraj NM, (2005). Pregabalin for pain management. Pain Pract 5: 95-102.
30. Gibbs JW, 3rd, Sombati S, DeLorenzo RJ, Coulter DA, (2000). Cellular actions of topiramate: blockade of kainate-evoked inward currents in cultured hippocampal neurons. Epilepsia 41 (Suppl. 1): S10-S16.
31. Griebel G, Belzung C, Perrault G, Sanger DJ, (2000). Differences in anxiety-related behaviours and in sensitivity to diazepam in inbred and outbred strains of mice. Psychopharmacology (Berl) 148: 164-170.
32. Hamidovic A, Dlugos A, Skol A, Palmer AA, de Wit H, (2009). Evaluation of genetic variability in the dopamine receptor D2 in relation to behavioral inhibition and impulsivity/sensation seeking: an exploratory study with d-amphetamine in healthy participants. Exp Clin Psychopharmacol 17: 374-383.
33. Helms CM, Reeves JM, Mitchell SH, (2006). Impact of strain and d-amphetamine on impulsivity (delay discounting) in inbred mice. Psychopharmacology (Berl) 188: 144-151.
34. Hyman SE, Malenka RC, (2001). Addiction and the brain: the neurobiology of compulsion and its persistence. Nat Rev Neurosci 2: 695-703.
35. James AS, Groman SM, Seu E, Jorgensen M, Fairbanks LA, Jentsch JD, (2007). Dimensions of impulsivity are associated with poor spatial working memory performance in monkeys. J Neurosci 27: 14358-14364.
36. Jensen JM, Pettinati HM, Evans BD, Meyers K, Valliere VN, (1990). Impulsivity and substance abusers: changes with treatment and recovery. NIDA Res Monogr 105: 287-288.
37. Johnson BA, (2004a). Progress in the development of topiramate for treating alcohol dependence: from a hypothesis to a proof-of-concept study. Alcohol Clin Exp Res 28: 1137-1144.
38. Johnson BA, (2004b). Topiramate-induced neuromodulation of cortico-mesolimbic dopamine function: a new vista for the treatment of comorbid alcohol and nicotine dependence? Addict Behav 29: 1465-1479.
39. Johnson BA, Ait-Daoud N, (2010). Topiramate in the new generation of drugs: efficacy in the treatment of alcoholic patients. Curr Pharm Des 16: 2103-2112.
40. Johnson BA, Ait-Daoud N, Bowden CL, DiClemente CC, Roache JD, Lawson K, et al,. (2003). Oral topiramate for treatment of alcohol dependence: a randomised controlled trial. Lancet 361: 1677-1685.
41. Kampman KM, Pettinati H, Lynch KG, Dackis C, Sparkman T, Weigley C, et al,. (2004). A pilot trial of topiramate for the treatment of cocaine dependence. Drug Alcohol Depend 75: 233-240.
42. Kavoussi RJ, Coccaro EF, (1998). Divalproex sodium for impulsive aggressive behavior in patients with personality disorder. J Clin Psychiatry 59: 676-680.
43. Kelley AE, Smith-Roe SL, Holahan MR, (1997). Response-reinforcement learning is dependent on N-methyl-D-aspartate receptor activation in the nucleus accumbens core. Proc Natl Acad Sci USA 94: 12174-12179.
44. Kenna GA, Lomastro TL, Schiesl A, Leggio L, Swift RM, (2009). Review of topiramate: an antiepileptic for the treatment of alcohol dependence. Curr Drug Abuse Rev 2: 135-142.
45. Kilkenny C, Browne W, Cuthill IC, Emerson M, Altman DG, (2010). NC3Rs Reporting Guidelines Working Group. Br J Pharmacol 160: 1577-1579.
46. Kim S, Lee D, (2010). Prefrontal cortex and impulsive decision making. Biol Psychiatry 69: 1140-1146.
47. Kim S, Bobeica I, Gamo NJ, Arnsten AF, Lee D, (2011). Effects of alpha-2A adrenergic receptor agonist on time and risk preference in primates. Psychopharmacology (Berl) 219: 363-375.
48. Lange LA, Kampov-Polevoy AB, Garbutt JC, (2010). Sweet liking and high novelty seeking: independent phenotypes associated with alcohol-related problems. Alcohol Alcohol 45: 431-436.
49. Lauria-Horner BA, Pohl RB, (2003). Pregabalin: a new anxiolytic. Expert Opin Investig Drugs 12: 663-672.
50. Lee B, London ED, Poldrack RA, Farahi J, Nacca A, Monterosso JR, et al,. (2009). Striatal Dopamine D2/D3 Receptor Availability Is Reduced in Methamphetamine Dependence and Is Linked to Impulsivity. J Neurosci 29: 14734-14740.
51. Leshner AI, Koob GF, (1999). Drugs of abuse and the brain. Proc Assoc Am Physicians 111: 99-108.
52. Livak KJ, Schmittgen TD, (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
53. Marazziti D, Baroni S, Masala I, Golia F, Consoli G, Massimetti G, et al,. (2010). Impulsivity, gender, and the platelet serotonin transporter in healthy subjects. Neuropsychiatr Dis Treat 6: 9-15.
54. Martinotti G, Di Nicola M, Romanelli R, Andreoli S, Pozzi G, Moroni N, et al,. (2007). High and low dosage oxcarbazepine versus naltrexone for the prevention of relapse in alcohol-dependent patients. Hum Psychopharmacol 22: 149-156.
55. Martinotti G, Di Nicola M, Tedeschi D, Mazza M, Janiri L, Bria P, (2008). Efficacy and safety of pregabalin in alcohol dependence. Adv Ther 25: 608-618.
56. Martinotti G, Di Nicola M, Tedeschi D, Andreoli S, Reina D, Pomponi M, et al,. (2010). Pregabalin versus naltrexone in alcohol dependence: a randomised, double-blind, comparison trial. J Psychopharmacol 24: 1367-1374.
57. McGrath J, Drummond G, Kilkenny C, Wainwright C, (2010). Guidelines for reporting experiments involving animals: the ARRIVE guidelines. Br J Pharmacol 160: 1573-1576.
58. Miranda R, Jr, MacKillop J, Monti PM, Rohsenow DJ, Tidey J, Gwaltney C, et al,. (2008). Effects of topiramate on urge to drink and the subjective effects of alcohol: a preliminary laboratory study. Alcohol Clin Exp Res 32: 489-497.
59. Navarrete F, Perez-Ortiz JM, Manzanares J, (2012). Cannabinoid CB(2) receptor-mediated regulation of impulsive-like behaviour in DBA/2 mice. Br J Pharmacol 165: 260-273.
60. Nguyen SA, Malcolm R, Middaugh LD, (2007). Topiramate reduces ethanol consumption by C57BL/6 mice. Synapse 61: 150-156.
61. Ohl F, Roedel A, Binder E, Holsboer F, (2003). Impact of high and low anxiety on cognitive performance in a modified hole board test in C57BL/6 and DBA/2 mice. Eur J Neurosci 17: 128-136.
62. Otobe T, Makino J, (2004). Impulsive choice in inbred strains of mice. Behav Processes 67: 19-26.
63. Oulis P, Konstantakopoulos G, (2010). Pregabalin in the treatment of alcohol and benzodiazepines dependence. CNS Neurosci Ther 16: 45-50.
64. Palkovits M, (1983). Punch sampling biopsy technique. Methods Enzymol 103: 368-376.
65. Patel S, Stolerman IP, Asherson P, Sluyter F, (2006). Attentional performance of C57BL/6 and DBA/2 mice in the 5-choice serial reaction time task. Behav Brain Res 170: 197-203.
66. Patton JH, Stanford MS, Barratt ES, (1995). Factor structure of the Barratt impulsiveness scale. J Clin Psychol 51: 768-774.
67. Paxinos G, Franklin KBJ, (2001). The Mouse Brain in Stereotaxic Coordinates. Academic Press. Harcourt Science and Technology Company: New York.
68. Petry NM, (2001). Substance abuse, pathological gambling, and impulsiveness. Drug Alcohol Depend 63: 29-38.
69. Phillips AG, Fibiger HC, (1973). Dopaminergic and noradrenergic substrates of positive reinforcement: differential effects of d- and l-amphetamine. Science 179: 575-577.
70. Pickering C, Avesson L, Lindblom J, Liljequist S, Schioth HB, (2007). To press or not to press? Differential receptor expression and response to novelty in rats learning an operant response for reward. Neurobiol Learn Mem 87: 181-191.
71. Poulsen CF, Simeone TA, Maar TE, Smith-Swintosky V, White HS, Schousboe A, (2004). Modulation by topiramate of AMPA and kainate mediated calcium influx in cultured cerebral cortical, hippocampal and cerebellar neurons. Neurochem Res 29: 275-282.
72. Prestes AP, Marques FZ, Hutz MH, Roman T, Bau CH, (2007). Tobacco smoking and the ADRA2A C-1291G polymorphism. J Neural Transm 114: 1503-1506.
73. Rapport MD, DuPaul GJ, Stoner G, Birmingham BK, Masse G, (1985). Attention deficit disorder with hyperactivity: differential effects of methylphenidate on impulsivity. Pediatrics 76: 938-943.
74. Reis AD, Castro LA, Faria R, Laranjeira R, (2008). Craving decrease with topiramate in outpatient treatment for cocaine dependence: an open label trial. Rev Bras Psiquiatr 30: 132-135.
75. Reis J, Tergau F, Hamer HM, Muller HH, Knake S, Fritsch B, et al,. (2002). Topiramate selectively decreases intracortical excitability in human motor cortex. Epilepsia 43: 1149-1156.
76. Rubio G, Martinez-Gras I, Manzanares J, (2009). Modulation of impulsivity by topiramate: implications for the treatment of alcohol dependence. J Clin Psychopharmacol 29: 584-589.
77. Scahill L, (2009). Alpha-2 adrenergic agonists in children with inattention, hyperactivity and impulsiveness. CNS Drugs 23 (Suppl. 1): 43-49.
78. Schmitz M, Denardin D, Silva TL, Pianca T, Roman T, Hutz MH, et al,. (2006). Association between alpha-2a-adrenergic receptor gene and ADHD inattentive type. Biol Psychiatry 60: 1028-1033.
79. Shank RP, Maryanoff BE, (2008). Molecular pharmacodynamics, clinical therapeutics, and pharmacokinetics of topiramate. CNS Neurosci Ther 14: 120-142.
80. Siefert HM, Domdey-Bette A, Henninger K, Hucke F, Kohlsdorfer C, Stass HH, (1999). Pharmacokinetics of the 8-methoxyquinolone, moxifloxacin: a comparison in humans and other mammalian species. J Antimicrob Chemother 43 (Suppl. B): 69-76.
81. Smathers SA, Wilson JG, Nigro MA, (2003). Topiramate effectiveness in Prader-Willi syndrome. Pediatr Neurol 28: 130-133.
82. Stahl SM, (2004). Mechanism of action of alpha2delta ligands: voltage sensitive calcium channel (VSCC) modulators. J Clin Psychiatry 65: 1033-1034.
83. Stopponi S, Somaini L, Cippitelli A, de Guglielmo G, Kallupi M, Cannella N, et al,. (2011). Pregabalin reduces alcohol drinking and relapse to alcohol seeking in the rat. Psychopharmacology (Berl) 220: 87-96.
84. Takeuchi Y, Takasu K, Ono H, Tanabe M, (2007). Pregabalin, S-(+)-3-isobutylgaba, activates the descending noradrenergic system to alleviate neuropathic pain in the mouse partial sciatic nerve ligation model. Neuropharmacology 53: 842-853.
85. Taverna S, Sancini G, Mantegazza M, Franceschetti S, Avanzini G, (1999). Inhibition of transient and persistent Na+ current fractions by the new anticonvulsant topiramate. J Pharmacol Exp Ther 288: 960-968.
86. Taylor CP, Angelotti T, Fauman E, (2007). Pharmacology and mechanism of action of pregabalin: the calcium channel alpha2-delta (alpha2-delta) subunit as a target for antiepileptic drug discovery. Epilepsy Res 73: 137-150.
87. van Gaalen MM, van Koten R, Schoffelmeer AN, Vanderschuren LJ, (2006). Critical involvement of dopaminergic neurotransmission in impulsive decision making. Biol Psychiatry 60: 66-73.
88. Vengeliene V, Heidbreder CA, Spanagel R, (2007). The effects of lamotrigine on alcohol seeking and relapse. Neuropharmacology 53: 951-957.
89. Vogelaer J, (1981). Carbamazepine in the treatment of psychotic and behavioral disorders. A pilot study. Acta Psychiatr Belg 81: 532-541.
90. Wade TR, de Wit H, Richards JB, (2000). Effects of dopaminergic drugs on delayed reward as a measure of impulsive behavior in rats. Psychopharmacology (Berl) 150: 90-101.
91. Wang HD, Takigawa M, Hamada K, Shiratani T, Takenouchi K, (2002). A shift in information flow between prefrontal cortex and the ventral tegmental area in methamphetamine-sensitized rats. Int J Psychophysiol 44: 251-259.
92. White HS, Brown SD, Woodhead JH, Skeen GA, Wolf HH, (1997). Topiramate enhances GABA-mediated chloride flux and GABA-evoked chloride currents in murine brain neurons and increases seizure threshold. Epilepsy Res 28: 167-179.
93. White HS, Brown SD, Woodhead JH, Skeen GA, Wolf HH, (2000). Topiramate modulates GABA-evoked currents in murine cortical neurons by a nonbenzodiazepine mechanism. Epilepsia 41 (Suppl. 1): S17-S20.
94. Wilcox J, (1994). Divalproex sodium in the treatment of aggressive behavior. Ann Clin Psychiatry 6: 17-20.
95. Wilcox JA, (1995). Divalproex sodium as a treatment for borderline personality disorder. Ann Clin Psychiatry 7: 33-37.
96. Wilson EA, Brodie MJ, (1996). New antiepileptic drugs. Baillieres Clin Neurol 5: 723-747.
97. Winstanley CA, Eagle DM, Robbins TW, (2006). Behavioral models of impulsivity in relation to ADHD: translation between clinical and preclinical studies. Clin Psychol Rev 26: 379-395.
98. Xu C, Schachar R, Tannock R, Roberts W, Malone M, Kennedy JL, et al,. (2001). Linkage study of the alpha2A adrenergic receptor in attention-deficit hyperactivity disorder families. Am J Med Genet 105: 159-162.
99. Yang B, Bankir L, (2005). Urea and urine concentrating ability: new insights from studies in mice. Am J Physiol Renal Physiol 288: F881-F896.
100. Yilmazer-Hanke DM, Roskoden T, Zilles K, Schwegler H, (2003). Anxiety-related behavior and densities of glutamate, GABAA, acetylcholine and serotonin receptors in the amygdala of seven inbred mouse strains. Behav Brain Res 145: 145-159.
101. Zona C, Ciotti MT, Avoli M, (1997). Topiramate attenuates voltage-gated sodium currents in rat cerebellar granule cells. Neurosci Lett 231: 123-126.
102. Zullino DF, Khazaal Y, Hattenschwiler J, Borgeat F, Besson J, (2004). Anticonvulsant drugs in the treatment of substance withdrawal. Drugs Today (Barc) 40: 603-619.