Modafinil restores methamphetamine induced object-in-place memory deficits in rats independent of glutamate N-methyl-d-aspartate receptor expression

Drug and Alcohol Dependence

Volumn 134, Issue 1, 2014, Pages 115-122

  Reichel, Carmela M ^a   Gilstrap, Meghin G ^a   Ramsey, Lauren A ^a   See, Ronald E ^a  

^a MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

Glutamate; Memory; Methamphetamine; Object recognition; Perirhinal cortex; Self administration

Indexed keywords

CALNEXIN; GLUTAMATE RECEPTOR; METHAMPHETAMINE; MODAFINIL; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SODIUM CHLORIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DOWN REGULATION; DRUG WITHDRAWAL; EXPLORATORY BEHAVIOR; HIPPOCAMPUS; MALE; MEMORY DISORDER; METHAMPHETAMINE DEPENDENCE; NONHUMAN; OBJECT MANIPULATION; PERIRHINAL CORTEX; PREFRONTAL CORTEX; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; RECOGNITION; SPATIAL MEMORY; TASK PERFORMANCE; TREATMENT OUTCOME; WESTERN BLOTTING;

RATTUS;

GLUTAMATE; MEMORY; METHAMPHETAMINE; OBJECT RECOGNITION; PERIRHINAL CORTEX; SELF-ADMINISTRATION;

ANIMALS; BENZHYDRYL COMPOUNDS; BRAIN; GENE EXPRESSION REGULATION; MALE; MEMORY DISORDERS; METHAMPHETAMINE; RATS; RATS, LONG-EVANS; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 84890162301     PISSN: 03768716     EISSN: 18790046     Source Type: Journal    
DOI: 10.1016/j.drugalcdep.2013.09.018     Document Type: Article

References (73)

1. Ahmed S.H., Walker J.R., Koob G.F. Persistent increase in the motivation to take heroin in rats with a history of drug escalation. Neuropsychopharmacology 2000, 22:413-421.
2. Anderson A.L., Li S.-H., Biswas K., McSherry F., Holmes T., Iturriaga E., Kahn R., Chiang N., Beresford T., Campbell J., Haning W., Mawhinney J., McCann M., Rawson R., Stock C., Weis D., Yu E., Elkashef A.M. Modafinil for the treatment of methamphetamine dependence. Drug Alcohol Depend. 2012, 120:135-141.
3. Barker G., Warburton E. NMDA receptor plasticity in the perirhinal and prefrontal cortices Is crucial for the acquisition of long-term object-in-place associative memory. J. Neurosci. 2008, 28:2837-2844.
4. Barker G.R.I., Bird F., Alexander V., Warburton E.C. Recognition memory for objects, place, and temporal order: a disconnection analysis of the role of the medial prefrontal cortex and perirhinal cortex. J. Neurosci. 2007, 27:2948-2957.
5. Barker G.R.I., Warburton E.C. When is the hippocampus involved in recognition memory?. J. Neurosci. 2011, 31:10721-10731.
6. Barker G.R.I., Warburton E.C., Koder T., Dolman N.P., More J.C.A., Aggleton J.P., Bashir Z.I., Auberson Y.P., Jane D.E., Brown M.W. The different effects on recognition memory of perirhinal kainate and NMDA glutamate receptor antagonism: implications for underlying plasticity mechanisms. J. Neurosci. 2006, 26:3561-3566.
7. Belcher A., O'dell S., Marshall J. Impaired object recognition memory following methamphetamine, but not p-chloroamphetamine- or d-amphetamine-induced neurotoxicity. Neuropsychopharmacology 2005, 30:2026-2034.
8. Belcher A.M., Feinstein E.M., O'Dell S.J., Marshall J.F. Methamphetamine influences on recognition memory: comparison of escalating and single-day dosing regimens. Neuropsychopharmacology 2008, 33:1453-1463.
9. Belcher A.M., O'Dell S.J., Marshall J.F. A sensitizing regimen of methamphetamine causes impairments in a novelty preference task of object recognition. Behav. Brain Res. 2006, 170:167-172.
10. Berlyne D.E. Novelty and curiosity as determinants of exploratory behaviour. Br. J. Psychol. 1950, 41:68-80.
11. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. J. Neurosci. 2000, 20:4320-4324.
12. Bisagno V., Ferguson D., Luine V.N. Short toxic methamphetamine schedule impairs object recognition task in male rats. Brain Res. 2002, 940:95-101.
13. Cappon G.D., Pu C., Vorhees C.V. Time-course of methamphetamine-induced neurotoxicity in rat caudate-putamen after single-dose treatment. Brain Res. 2000, 863:106-111.
14. Cho K., Kemp N., Noel J., Aggleton J.P., Brown M.W., Bashir Z.I. A new form of long-term depression in the perirhinal cortex. Nat. Neurosci. 2000, 3:150-156.
15. Dackis C.A., Lynch K.G., Yu E., Samaha F.F., Kampman K.M., Cornish J.W., Rowan A., Poole S., White L., O'Brien C.P. Modafinil and cocaine: a double-blind, placebo-controlled drug interaction study. Drug Alcohol Depend. 2003, 70:29-37.
16. Dalley J.W., Lääne K., Theobald D.E., Peña Y., Bruce C.C., Huszar A.C., Wojcieszek M., Everitt B.J., Robbins T.W. Enduring deficits in sustained visual attention during withdrawal of intravenous methylenedioxymethamphetamine self-administration in rats: results from a comparative study with d-amphetamine and methamphetamine. Neuropsychopharmacology 2007, 32:1195-1206.
17. De La Garza R., Zorick T., London E., Newton T. Evaluation of modafinil effects on cardiovascular, subjective, and reinforcing effects of methamphetamine in methamphetamine-dependent volunteers. Drug Alcohol Depend. 2009, 106:173-180.
18. Dean A.C., Sevak R.J., Monterosso J.R., Hellemann G., Sugar C.A., London E.D. Acute modafinil effects on attention and inhibitory control in methamphetamine-dependent humans. J. Stud. Alcohol Drugs 2011, 72:943-953.
19. Demakis G.J. A meta-analytic review of the sensitivity of the Wisconsin card sorting test to frontal and lateralized frontal brain damage. Neuropsychology 2003, 17:255-264.
20. Dickerson B.C., Eichenbaum H. The episodic memory system: neurocircuitry and disorders. Neuropsychopharmacology 2010, 35:86-104.
21. Ennaceur A. One-trial object recognition in rats and mice: methodological and theoretical issues. Behav. Brain Res. 2010, 215:244-254.
22. Ennaceur A., Delacour J. A new one-trial test for neurobiological studies of memory in rats. 1: Behavioral data. Behav. Brain Res. 1988, 31:47-59.
23. Ersche K.D., Clark L., London M., Robbins T.W., Sahakian B.J. Profile of executive and memory function associated with amphetamine and opiate dependence. Neuropsychopharmacology 2006, 31:1036-1047.
24. Ferraro L., Antonelli T., O'Connor W.T., Tanganelli S., Rambert F., Fuxe K. The antinarcoleptic drug modafinil increases glutamate release in thalamic areas and hippocampus. Neuroreport 1997, 8:2883-2887.
25. Ferraro L., Antonelli T., O'Connor W.T., Tanganelli S., Rambert F.A., Fuxe K. The effects of modafinil on striatal, pallidal and nigral GABA and glutamate release in the conscious rat: evidence for a preferential inhibition of striato-pallidal GABA transmission. Neurosci. Lett. 1998, 253:135-138.
26. Ferraro L., Antonelli T., Beggiato S., Tomasini M.C., Fuxe K., Tanganelli S. The vigilance promoting drug modafinil modulates serotonin transmission in the rat prefrontal cortex and dorsal raphe nucleus: possible relevance for its postulated antidepressant activity. Mini Rev. Med. Chem. 2013, 13:478-492.
27. Fumagalli F., Frasca A., Racagni G., Riva M.A. Dynamic regulation of glutamatergic postsynaptic activity in rat prefrontal cortex by repeated administration of antipsychotic drugs. Mol. Pharmacol. 2008, 73:1484-1490.
28. Ghahremani D.G., Tabibnia G., Monterosso J., Hellemann G., Poldrack R.A., London E.D. Effect of modafinil on learning and task-related brain activity in methamphetamine-dependent and healthy individuals. Neuropsychopharmacology 2011, 36:950-959.
29. Groc L., Choquet D. AMPA and NMDA glutamate receptor trafficking: multiple roads for reaching and leaving the synapse. Cell Tissue Res. 2006, 326:423-438.
30. Hadamitzky M., Markou A., Kuczenski R. Extended access to methamphetamine self-administration affects sensorimotor gating in rats. Behav. Brain Res. 2011, 217:386-390.
31. Heinzerling K.G., Swanson A.-N., Kim S., Cederblom L., Moe A., Ling W., Shoptaw S. Randomized, double-blind, placebo-controlled trial of modafinil for the treatment of methamphetamine dependence. Drug Alcohol Depend. 2010, 109:20-29.
32. Holtz N.A., Lozama A., Prisinzano T.E., Carroll M.E. Reinstatement of methamphetamine seeking in male and female rats treated with modafinil and allopregnanolone. Drug Alcohol Depend. 2012, 100:233-237.
33. Hotchkiss A.J., Gibb J.W. Long-term effects of multiple doses of methamphetamine on tryptophan hydroxylase and tyrosine hydroxylase activity in rat brain. J. Pharmacol. Exp. Ther. 1980, 214:257-262.
34. Ishizuka T., Murotani T., Yamatodani A. Action of modafinil through histaminergic and orexinergic neurons. Vitam. Horm. 2012, 89:259-278.
35. Iudicello J.E., Weber E., Grant I., Weinborn M., Woods S.P. Misremembering future intentions in methamphetamine-dependent individuals. Clin. Neuropsychol. 2011, 25:269-286. HIV Neurobehavioral Research Center, (HNRC) Group.
36. Kalechstein A.D., De La Garza R., Newton T.F. Modafinil administration improves working memory in methamphetamine-dependent individuals who demonstrate baseline impairment. Am. J. Addict. 2010, 19:340-344.
37. Kalechstein A.D., Newton T.F., Green M. Methamphetamine dependence is associated with neurocognitive impairment in the initial phases of abstinence. J. Neuropsychiatry Clin. Neurosci. 2003, 15:215-220.
38. Kitamura O., Wee S., Specio S., Koob G., Pulvirenti L. Escalation of methamphetamine self-administration in rats: a dose-effect function. Psychopharmacology 2006, 186:48-53.
39. Lee N., Pennay A., Hester R., McKetin R., Nielsen S., Ferris J. A pilot randomised controlled trial of modafinil during acute methamphetamine withdrawal: feasibility, tolerability and clinical outcomes. Drug Alcohol Rev. 2013, 32:88-95.
40. Ling W., Rawson R., Shoptaw S., Ling W. Management of methamphetamine abuse and dependence. Curr. Psychiatry Rep. 2006, 8:345-354.
41. Mahler S.V., Hensley-Simon M., Tahsili-Fahadan P., LaLumiere R.T., Thomas C., Fallon R.V., Kalivas P.W., Aston-Jones G. Modafinil attenuates reinstatement of cocaine seeking: role for xystine-glutamate exchange and metabotropic glutamate receptors. Addiction Biology 2012, ahead of print.
42. Mandyam C., Wee S., Eisch A., Richardson H., Koob G. Methamphetamine self-administration and voluntary exercise have opposing effects on medial prefrontal cortex gliogenesis. J. Neurosci. 2007, 27:11442-11450.
43. Mandyam C.D., Wee S., Crawford E.F., Eisch A.J., Richardson H.N., Koob G.F. Varied access to intravenous methamphetamine self-administration differentially alters adult hippocampal neurogenesis. Biol. Psychiatry 2008, 64:958-965.
44. Massey P.V., Bashir Z.I. Long-term depression: multiple forms and implications for brain function. Trends Neurosci. 2007, 30:176-184.
45. Massey P.V., Johnson B.E., Moult P.R., Auberson Y.P., Brown M.W., Molnar E., Collingridge G.L., Bashir Z.I. Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression. J. Neurosci. 2004, 24:7821-7828.
46. McGaugh J., Mancino M.J., Feldman Z., Chopra M.P., Gentry W.B., Cargile C., Oliveto A. Open-label pilot study of modafinil for methamphetamine dependence. J. Clin. Psychopharmacol. 2009, 29:488-491.
47. Minzenberg M.J., Carter C.S. Modafinil: a review of neurochemical actions and effects on cognition. Neuropsychopharmacology 2008, 33:1477-1502.
48. Nguyen T.-L., Tian Y.-H., You I.-J., Lee S.-Y., Jang C.-G. Modafinil-induced conditioned place preference via dopaminergic system in mice. Synapse 2011, 65:733-741.
49. O'Dell S.J., Feinberg L.M., Marshall J.F. A neurotoxic regimen of methamphetamine impairs novelty recognition as measured by a social odor-based task. Behav. Brain Res. 2011, 216:396-401.
50. Parsegian A., Glen W.B., Lavin A., See R.E. Methamphetamine self-administration produces attentional set-shifting deficits and alters prefrontal cortical neurophysiology in rats. Biol. Psychiatry 2011, 69:253-259.
51. Paterson N.E., Markou A. Increased motivation for self-administered cocaine after escalated cocaine intake. Neuroreport 2003, 14:2229-2232.
52. Paxinos G., Watson C. The Rat Brain in Sterotaxic Coordinates 2007, Academic press, San Diego.
53. Reichel C.M., Chan C.H., Ghee S.M., See R.E. Sex differences in escalation of methamphetamine self-administration: cognitive and motivational consequences in rats. Psychopharmacology 2012, 223:371-380.
54. Reichel C.M., Ramsey L.A., Schwendt M., Mcginty J.F., See R.E. Methamphetamine-induced changes in the object recognition memory circuit. Neuropharmacology 2012, 62:1119-1126.
55. Reichel C.M., Schwendt M., McGinty J.F., Olive M.F., See R.E. Loss of object recognition memory produced by extended access to methamphetamine self-administration is reversed by positive allosteric modulation of metabotropic glutamate receptor 5. Neuropsychopharmacology 2011, 36:782-792.
56. Reichel C.M., See R.E. Modafinil effects on reinstatement of methamphetamine seeking in a rat model of relapse. Psychopharmacology 2010, 210:337-346.
57. Reichel C.M., See R.E. Chronic modafinil effects on drug-seeking following methamphetamine self-administration in rats. Int. J. Neuropsychopharmacol. 2012, 15:919-929.
58. Riedel G., Platt B., Micheau J. Glutamate receptor function in learning and memory. Behav. Brain Res. 2003, 140:1-47.
59. Rogers J., Santis S., See R. Extended methamphetamine self-administration enhances reinstatement of drug seeking and impairs novel object recognition in rats. Psychopharmacology 2008, 199:615-624.
60. Sase S., Khan D., Sialana F., Höger H., Russo-Schlaff N., Lubec G. Modafinil improves performance in the multiple T-Maze and modifies GluR1, GluR2, D2 and NR1 receptor complex levels in the C57BL/6J mouse. Amino Acids 2012, 43:2285-2292.
61. Schwendt M.R., Reichel C.M., See R.E. Extinction-dependent alterations in corticostriatal metabotropic glutamate receptor 2/3 and 7 following chronic methamphetamine self-administration in rats. PLoS One 2012, 7:e34299.
62. Scott J.C., Woods S.P., Matt G.E., Meyer R.A., Heaton R.K., Atkinson J.H., Grant I. Neurocognitive effects of methamphetamine: a critical review and meta-analysis. Neuropsychol. Rev. 2007, 17:275-297.
63. Shearer J., Darke S., Rodgers C., Slade T., van Beek I., Lewis J., Brady D., McKetin R., Mattick R.P., Wodak A. A double-blind, placebo-controlled trial of modafinil (200mg/day) for methamphetamine dependence. Addiction 2009, 104:224-233.
64. Simon S.L., Dacey J., Glynn S., Rawson R., Ling W. The effect of relapse on cognition in abstinent methamphetamine abusers. J. Subst. Abuse Treat. 2004, 27:59-66.
65. Turner D.C., Clark L., Dowson J., Robbins T.W., Sahakian B.J. Modafinil improves cognition and response inhibition in adult attention-deficit/hyperactivity disorder. Biol. Psychiatry 2004, 55:1031-1040.
66. Turner D.C., Robbins T.W., Clark L., Aron A.R., Dowson J., Sahakian B.J. Cognitive enhancing effects of modafinil in healthy volunteers. Psychopharmacology 2003, 165:260-269.
67. Vanderschuren L.J.M.J., Everitt B.J. Drug seeking becomes compulsive after prolonged cocaine self-administration. Science 2004, 305:1017-1019.
68. Vocci F.J., Appel N.M. Approaches to the development of medications for the treatment of methamphetamine dependence. Addiction 2007, 102(Suppl. 1):96-106.
69. Wagner G.C., Ricaurte G.A., Seiden L.S., Schuster C.R., Miller R.J., Westley J. Long-lasting depletions of striatal dopamine and loss of dopamine uptake sites following repeated administration of methamphetamine. Brain Res. 1980, 181:151-160.
70. Wan H., Aggleton J.P., Brown M.W. Different contributions of the hippocampus and perirhinal cortex to recognition memory. J. Neurosci. 1999, 19:1142-1148.
71. Warburton E.C., Brown M.W. Findings from animals concerning when interactions between perirhinal cortex, hippocampus and medial prefrontal cortex are necessary for recognition memory. Neuropsychologia 2009, 48:2262-2272.
72. Watson H.C., Lee A.C.H. The perirhinal cortex and recognition memory interference. J. Neurosci. 2013, 33:4192-4200.
73. Zolkowska D., Jain R., Rothman R.B., Partilla J.S., Roth B.L., Setola V., Prisinzano T.E., Baumann M.H. Evidence for the involvement of dopamine transporters in behavioral stimulant effects of modafinil. J. Pharmacol. Exp. Ther. 2009, 329:738-746.