Effects of risperidone, clozapine and the 5-HT6 antagonist GSK-742457 on PCP-induced deficits in reversal learning in the two-lever operant task in male Sprague Dawley rats

Behavioural Brain Research

Volumn 244, Issue , 2013, Pages 15-28

  de Bruin, N M W J ^a   van Drimmelen, M ^a,b   Kops, M ^a,c   van Elk, J ^a,d   Wetering, M Middelveld van de ^a,e   Schwienbacher, I ^a,f  

^a Solvay Pharmaceuticals Inc   (Netherlands)

^b ACE Pharmaceuticals BV   (Netherlands)

^c UTRECHT UNIVERSITY   (Netherlands)

^d NETHERLANDS CANCER INSTITUTE   (Netherlands)

^e Sandoz BV   (Netherlands)

^f MERZ PHARMACEUTICALS GMBH   (Germany)

Author keywords

Antipsychotics; Dizocilpine (MK 801); Extinction; GSK 742457; Phencyclidine (PCP); Reversal learning; Skinner box

Indexed keywords

3 PHENYLSULFONYL 8 (1 PIPERAZINYL)QUINOLINE; CLONAZEPAM; DIZOCILPINE; RISPERIDONE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COGNITION; CONTROLLED STUDY; DRUG EFFICACY; DRUG MEGADOSE; DRUG TREATMENT FAILURE; LEARNING DISORDER; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SPATIAL DISCRIMINATION; STIMULUS RESPONSE; TASK PERFORMANCE; TREATMENT RESPONSE;

EID: 84874381856     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.01.035     Document Type: Article

References (89)

1. Keefe R.S.E., Bilder R.M., Davis S.M., Harvey P.D., Rosenheck R.A., Perkins D.O., et al. Neurocognitive effects of antipsychotic medications in patients with chronic schizophrenia in the CATIE trial. Archives of General Psychiatry 2007, 64:633-647.
2. Young J.W., Powell S.B., Risbrough V., Marston H.M., Geyer M.A. Using the MATRICS to guide development of a preclinical cognitive test battery for research in schizophrenia. Pharmacology and Therapeutics 2009, 122(May):150-202.
3. Davidson M., Galderisi S., Weiser M., Werbeloff N., Fleischhacker W.W., Keefe R.S., et al. Cognitive effects of antipsychotic drugs in first-episode schizophrenia and schizophreniform disorder: a randomized, open-label clinical trial (EUFEST). American Journal of Psychiatry 2009, 166:675-682.
4. Nuechterlein K.H., Green M.F., Kern R.S., Baade L.E., Barch D.M., Cohen J.D., et al. The MATRICS Consensus Cognitive Battery, part 1: test selection, reliability, and validity. American Journal of Psychiatry 2008, 165:203-213.
5. Kern R.S., Gold J.M., Dickinson D., Green M.F., Nuechterlein K.H., Baade L.E., et al. The MCCB impairment profile for schizophrenia outpatients: results from the MATRICS psychometric and standardization study. Schizophrenia Research 2011, 126:124-131.
6. Green M.F., Nuechterlein K.H., Gold J.M., Barch D.M., Cohen J., Essock S., et al. Approaching a consensus cognitive battery for clinical trials in schizophrenia: the NIMH-MATRICS conference to select cognitive domains and test criteria. Biological Psychiatry 2004, 56:301-307.
7. Geyer M.A., Olivier B., Joëls M., Kahn R.S. From antipsychotic to anti-schizophrenia drugs: role of animal models. Trends in Pharmacological Sciences 2012, 33:515-521.
8. Leeson V.C., Robbins T.W., Matheson E., Hutton S.B., Ron M.A., Barnes T.R.E., et al. Discrimination learning, reversal, and set-shifting in first-episode schizophrenia: stability over six years and specific associations with medication type and disorganization syndrome. Biological Psychiatry 2009, 66:586-593.
9. Pantelis C., Barber F.Z., Barnes T.R., Nelson H.E., Owen a.M., Robbins T.W. Comparison of set-shifting ability in patients with chronic schizophrenia and frontal lobe damage. Schizophrenia Research 1999, 37:251-270.
10. Pantelis C., Wood S.J., Proffitt T.M., Testa R., Mahony K., Brewer W.J., et al. Attentional set-shifting ability in first-episode and established schizophrenia: relationship to working memory. Schizophrenia Research 2009, 112:104-113.
11. Birrell J.M., Brown V.J. Medial frontal cortex mediates perceptual attentional set shifting in the rat. Journal of Neuroscience 2000, 20:4320-4324.
12. Ragozzino M.E., Wilcox C., Raso M., Kesner R.P. Involvement of rodent prefrontal cortex subregions in strategy switching. Behavioral Neuroscience 1999, 113:32-41.
13. Widholm J.J., Clarkson G.B., Strupp B.J., Crofton K.M., Seegal R.F., Schantz S.L. Spatial reversal learning in Aroclor 1254-exposed rats: sex-specific deficits in associative ability and inhibitory control. Toxicology and Applied Pharmacology 2001, 174:188-198.
14. Abdul-Monim Z., Reynolds G.P., Neill J.C. The atypical antipsychotic ziprasidone, but not haloperidol, improves phencyclidine-induced cognitive deficits in a reversal learning task in the rat. Journal of Psychopharmacology 2003, 17:57-66.
15. Abdul-Monim Z., Reynolds G.P., Neill J.C. The effect of atypical and classical antipsychotics on sub-chronic PCP-induced cognitive deficits in a reversal-learning paradigm. Behavioural Brain Research 2006, 169:263-273.
16. Idris N.F., Repeto P., Neill J.C., Large C.H. Investigation of the effects of lamotrigine and clozapine in improving reversal-learning impairments induced by acute phencyclidine and d-amphetamine in the rat. Psychopharmacology 2005, 179:336-348.
17. Arnt J., Olsen C.K. 5-HT6 receptor ligands and their antipsychotic potential, IV. Effects in models of CIAS (Cognitive Impairment Associated with Schizophrenia). International Review of Neurobiology 2011, vol. 96:150-156. Elsevier, Amsterdam.
18. Neill J.C., Barnes S., Cook S., Grayson B., Idris N.F., McLean S.L., et al. Animal models of cognitive dysfunction and negative symptoms of schizophrenia: focus on NMDA receptor antagonism. Pharmacology and Therapeutics 2010, 128:419-432.
19. Rodefer J.S., Murphy E.R., Baxter M.G. PDE10A inhibition reverses subchronic PCP-induced deficits in attentional set-shifting in rats. European Journal of Neuroscience 2005, 21:1070-1076.
20. Idris N., Neill J., Grayson B., Bang-Andersen B., Witten L.M., Brennum L.T., et al. Sertindole improves sub-chronic PCP-induced reversal learning and episodic memory deficits in rodents: involvement of 5-HT(6) and 5-HT (2A) receptor mechanisms. Psychopharmacology 2010, 208:23-36.
21. Goetghebeur P., Dias R. Comparison of haloperidol, risperidone, sertindole, and modafinil to reverse an attentional set-shifting impairment following subchronic PCP administration in the rat-a back translational study. Psychopharmacology 2009, 202:287-293.
22. Featherstone R.E., Rizos Z., Nobrega J.N., Kapur S., Fletcher P.J. Gestational methylazoxymethanol acetate treatment impairs select cognitive functions: parallels to schizophrenia. Neuropsychopharmacology 2007, 32:483-492.
23. Egerton A., Reid L., McGregor S., Cochran S.M., Morris B.J., Pratt J.A. Subchronic and chronic PCP treatment produces temporally distinct deficits in attentional set shifting and prepulse inhibition in rats. Psychopharmacology (Berlin) 2008, 198:37-49.
24. Broberg B.V., Dias R., Glenthøj B.Y., Olsen C.K. Evaluation of a neurodevelopmental model of schizophrenia-early postnatal PCP treatment in attentional set-shifting. Behavioural Brain Research 2008, 190:160-163.
25. Jentsch J.D., Taylor J.R. Impaired inhibition of conditioned responses produced by subchronic administration of phencyclidine to rats. Neuropsychopharmacology 2001, 24:66-74.
26. Abdul-Monim Z., Neill J.C., Reynolds G.P. Sub-chronic psychotomimetic phencyclidine induces deficits in reversal learning and alterations in parvalbumin-immunoreactive expression in the rat. Journal of Psychopharmacology 2007, 21:198-205.
27. Van der Meulen J.A.J., Bilbija L., Joosten R.N.J.M.A., De Bruin J.P.C., Feenstra C.A.M.G.P. The NMDA-receptor antagonist MK-801 selectively disrupts reversal learning in rats. Neuroreport 2003, 14:2225-2228.
28. Andrzejewski M.E., Schochet T.L., Feit E.C., Harris R., McKee B.L., Kelley A.E. A comparison of adult and adolescent rat behavior in operant learning, extinction, and behavioral inhibition paradigms. Behavioral Neuroscience 2011, 125:93-105.
29. Butter C., Mishkin M., Rosvold H. Conditioning and extinction of a food-rewarded response after selective ablations of frontal cortex in rhesus monkeys. Experimental Neurology 1963, 7.
30. Finger E.C., Mitchell D.G.V., Jones M., Blair R.J.R. Dissociable roles of medial orbitofrontal cortex in human operant extinction learning. NeuroImage 2008, 43:748-755.
31. Boulougouris V., Dalley J.W., Robbins T.W. Effects of orbitofrontal, infralimbic and prelimbic cortical lesions on serial spatial reversal learning in the rat. Behavioural Brain Research 2007, 179:219-228.
32. Chudasama Y., Robbins T.W. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. Journal of Neuroscience 2003, 23:8771-8780.
33. McAlonan K., Brown V.J. Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behavioural Brain Research 2003, 146:97-103.
34. Schoenbaum G., Chiba A.A., Gallagher M. Changes in functional connectivity in orbitofrontal cortex and basolateral amygdala during learning and reversal training. Journal of Neuroscience 2000, 20:5179-5189.
35. Ragozzino M.E. The contribution of the medial prefrontal cortex, orbitofrontal cortex, and dorsomedial striatum to behavioral flexibility. Annals of the New York Academy of Sciences 2007, 1121:355-375.
36. Bouton M.E., Woods A.M. Extinction: behavioral mechanisms and their Implications. Learning and memory: A comprehensive reference 2008, vol. 1:151-171. Elsevier, Oxford.
37. Vurbic D., Gold B., Bouton M. Effects of d-cycloserine on the extinction of appetitive operant learning. Behavioral Neuroscience 2011, 125:551-559.
38. Bouton M.E. Context and behavioral processes in extinction. Learning and Memory 2004, 11:485-494.
39. Quirk G.J., Mueller D. Neural mechanisms of extinction learning and retrieval. Neuropsychopharmacology 2008, 33:56-72.
40. Holt D.J., Lebron-Milad K., Milad M.R., Rauch S.L., Pitman R.K., Orr S.P., et al. Extinction memory is impaired in schizophrenia. Biological Psychiatry 2009, 65:455-463.
41. Myers K.M., Davis M. Mechanisms of fear extinction. Molecular Psychiatry 2007, 12:120-150.
42. McLean S.L., Neill J.C., Idris N.F., Marston H.M., Wong E.H.F., Shahid M. Effects of asenapine, olanzapine, and risperidone on psychotomimetic-induced reversal-learning deficits in the rat. Behavioural Brain Research 2010, 214:240-247.
43. Mitchell E.S., Neumaier J.F. 5-HT6 receptors: a novel target for cognitive enhancement. Pharmacology and Therapeutics 2005, 108:320-333.
44. Rodefer J.S., Nguyen T.N., Karlsson J.-J., Arnt J. Reversal of subchronic PCP-induced deficits in attentional set shifting in rats by sertindole and a 5-HT6 receptor antagonist: comparison among antipsychotics. Neuropsychopharmacology 2008, 33:2657-2666.
45. Borsini F. Pharmacology of 5-HT6 receptors, Part II. International Review of Neurobiology 2011, vol. 96:1-250. Elsevier, Amsterdam.
46. Hatcher P.D., Brown V.J., Tait D.S., Bate S., Overend P., Hagan J.J., et al. 5-HT6 receptor antagonists improve performance in an attentional set shifting task in rats. Psychopharmacology 2005, 181:253-259.
47. Johnson C.N., Ahmed M., Miller N.D. 5-HT6 receptor antagonists: prospects for the treatment of cognitive disorders including dementia. Current Opinion in Drug Discovery and Development 2008, 11:642-654.
48. Hirst W.D., Stean T.O., Rogers D.C., Sunter D., Pugh P., Moss S.F., et al. SB-399885 is a potent, selective 5-HT6 receptor antagonist with cognitive enhancing properties in aged rat water maze and novel object recognition models. European Journal of Pharmacolgy 2006, 553:109-119.
49. 6 receptor in cognitive function. Neuropharmacology 2008, 55:1015-1022.
50. Mohler E.G., Baker P.M., Gannon K.S., Jones S.S., Shacham S., Sweeney J.A., et al. The effects of PRX-07034, a novel 5-HT(6) antagonist, on cognitive flexibility and working memory in rats. Psychopharmacology (Berlin) 2012, 220:687-696.
51. Codony X., Vela J.M., Ramírez M.J. 5-HT(6) receptor and cognition. Current Opinion in Pharmacology 2011, 11:94-100.
52. de Bruin N.M.W.J., Prickaerts J., van Loevezijn A., Venhorst J., de Groote L., Houba P., et al. Two novel 5-HT6 receptor antagonists ameliorate scopolamine-induced memory deficits in the object recognition and object location tasks in Wistar rats. Neurobiology of Learning and Memory 2011, 96:392-402.
53. Olney J.W., Farber N.B. Glutamate receptor dysfunction and schizophrenia. Archives of General Psychiatry 1995, 52:998-1007.
54. Castellani S., Adams P.M. Acute and chronic phencyclidine effects on locomotor activity, stereotypy and ataxia in rats. European Journal of Pharmacology 1981, 73:143-154.
55. Kalinichev M., Robbins M.J., Hartfield E.M., Maycox P.R., Moore S.H., Savage K.M., et al. Comparison between intraperitoneal and subcutaneous phencyclidine administration in Sprague-Dawley rats: a locomotor activity and gene induction study. Progress in Neuro-Psychopharmacology and Biological Psychiatry 2008, 32:414-422.
56. Andiné P., Widermark N., Axelsson R., Nyberg G., Olofsson U., Mårtensson E., et al. Characterization of MK-801-induced behavior as a putative rat model of psychosis. Journal of Pharmacology and Experimental Therapeutics 1999, 290:1393-1408.
57. Cochran S.M., Kennedy M., McKerchar C.E., Steward L.J., Pratt J.A., Morris B.J. Induction of metabolic hypofunction and neurochemical deficits after chronic intermittent exposure to phencyclidine: differential modulation by antipsychotic drugs. Neuropsychopharmacology 2003, 28:265-275.
58. Pratt J.A., Winchester C., Egerton A., Cochran S.M., Morris B.J. Modelling prefrontal cortex deficits in schizophrenia: implications for treatment. British Journal of Pharmacology 2008, 153(Suppl.):S465-S470.
59. Pratt J., Winchester C., Dawson N., Morris B. Advancing schizophrenia drug discovery: optimizing rodent models to bridge the translational gap. Nature Reviews Drug Discovery 2012, 11:560-579.
60. Chadman K.K., Watson D.J., Stanton M.E. NMDA receptor antagonism impairs reversal learning in developing rats. Behavioral Neuroscience 2006, 120:1071-1083.
61. Dix S., Gilmour G., Potts S., Smith J.W., Tricklebank M. A within-subject cognitive battery in the rat: differential effects of NMDA receptor antagonists. Psychopharmacology 2010, 212:227-242.
62. Gilmour G., Pioli E.Y., Dix S.L., Smith J.W., Conway M.W., Jones W.T., et al. Diverse and often opposite behavioural effects of NMDA receptor antagonists in rats: implications for NMDA antagonist modelling of schizophrenia. Psychopharmacology 2009, 205:203-216.
63. Pechnick R.N., Bresee C.J., Poland R.E. The role of antagonism of NMDA receptor-mediated neurotransmission and inhibition of the dopamine reuptake in the neuroendocrine effects of phencyclidine. Life Sciences 2006, 78:2006-2011.
64. Rothman R.B., Reid A.A., Monn J.A., Jacobson A.E., Rice K.C. The psychotomimetic drug phencyclidine labels two high affinity binding sites in guinea pig brain: evidence for N-methyl-d-aspartate-coupled and dopamine reuptake carrier-associated phencyclidine binding sites. Molecular Pharmacology 1989, 36:887-896.
65. Mele A., Wozniak K.M., Hall F.S., Pert A. The role of striatal dopaminergic mechanisms in rotational behavior induced by phencyclidine and phencyclidine-like drugs. Psychopharmacology 1998, 135:107-118.
66. Callado L.F., Hopwood S.E., Hancock P.J., Stamford J.A. Effects of dizocilpine (MK-801) on noradrenaline, serotonin and dopamine release and uptake. Neuroreport 2000, 11:173-176.
67. Kapur S., Seeman P. NMDA receptor antagonists ketamine and PCP have direct effects on the dopamine D(2) and serotonin 5-HT(2)receptors-implications for models of schizophrenia. Molecular Psychiatry 2002, 7:837-844.
68. Gilmour G., Dix S., Fellini L., Gastambide F., Plath N., Steckler T., et al. NMDA receptors, cognition and schizophrenia - tsting the validity of the NMDA receptor hypofunction hypothesis. Neuropharmacology 2011, 62:1401-1412.
69. Holahan M.R., Clarke M.J., Hines D.D. Dopamine-mediated MK-801-induced elevation in food-based extinction responding in rats and associated changes in region-specific phosphorylated ERK. Psychopharmacology 2010, 212:393-403.
70. Holahan M.R., Westby E.P., Albert K. Comparison of the MK-801-induced appetitive extinction deficit with pressing for reward and associated pERK1/2 staining in prefrontal cortex and nucleus accumbens. Behavioural Brain Research 2012, 228:194-202.
71. Santini E., Muller R.U., Quirk G.J. Consolidation of extinction learning involves transfer from NMDA-independent to NMDA-dependent memory. Journal of Neuroscience 2001, 21:9009-9017.
72. Palencia C.A., Ragozzino M.E. The influence of NMDA receptors in the dorsomedial striatum on response reversal learning. Neurobiology of Learning and Memory 2004, 82:81-89.
73. Podhorna J., Didriksen M. Performance of male C57BL/6J mice and Wistar rats in the water maze following various schedules of phencyclidine treatment. Behavioural Pharmacology 2005, 16:25-34.
74. Overton D.A. Contextual stimulus effects of drugs and internal states. Context and learning 1985, 357-384. Erlbaum, Hillsdale. P.D. Balsam, A. Tomie (Eds.).
75. Castañé A., Theobald D.E.H., Robbins T.W. Selective lesions of the dorsomedial striatum impair serial spatial reversal learning in rats. Behavioural Brain Research 2010, 210:74-83.
76. Keefe R.S.E., Buchanan R.W., Marder S.R., Schooler N.R., Dugar A., Zivkov M., et al. Clinical trials of potential cognitive-enhancing drugs in schizophrenia: what have we learned so far?. Schizophrenia Bulletin 2011, 2-11. 10.1093/schbul/sbr153.
77. Buchanan R.W., Keefe R.S.E., Umbricht D., Green M.F., Laughren T., Marder S.R. The FDA-NIMH-MATRICS guidelines for clinical trial design of cognitive-enhancing drugs: what do we know 5 years later?. Schizophrenia Bulletin 2011, 37:1209-1217.
78. Di Chiara G., Valentini V., Fenu S. Behavioral and neurochemical pharmacology of 5-HT6 receptors related to reward and reinforcement. International Review of Neurobiology 2011, vol. 96:111-139. Elsevier, Amsterdam.
79. Dawson L.A., Nguyen H.Q., Li P. The 5-HT(6) receptor antagonist SB-271046 selectively enhances excitatory neurotransmission in the rat frontal cortex and hippocampus. Neuropsychopharmacology 2001, 25:662-668.
80. Dawson L.A., Nguyen H.Q., Li P. Potentiation of amphetamine-induced changes in dopamine and 5-HT by a 5-HT(6) receptor antagonist. Brain Research Bulletin 2003, 59:513-521.
81. Lacroix L.P., Dawson L.A., Hagan J.J., Heidbreder C.A. 5-HT6 receptor antagonist SB-271046 enhances extracellular levels of monoamines in the rat medial prefrontal cortex. Synapse 2004, 51:158-164.
82. Riemer C., Borroni E., Levet-trafit B., Martin J.R., Poli S., Porter R.H.P., et al. Influence of the 5-HT6 receptor on acetylcholine release in the cortex: pharmacological characterization of 4-(2-bromo-6-pyrrolidin-1-ylpyridine-4-sulfonyl)phenylamine, a potent and selective 5-HT6 receptor antagonist. Journal of Medicinal Chemistry 2003, 46:1273-1276.
83. Schechter L.E., Lin Q., Smith D.L., Zhang G., Shan Q., Platt B., et al. Neuropharmacological profile of novel and selective 5-HT6 receptor agonists: WAY-181187 and WAY-208466. Neuropsychopharmacology 2008, 33:1323-1335.
84. Woolley M.L., Marsden C.A., Fone K.C. 5-HT6 receptors. Curr Drug Targets 2004, 3:59-79.
85. Dawson L.A. The central role of 5-HT6 receptors in modulating brain neurochemistry. International Review of Neurobiology 2011, vol. 96:1-26. Elsevier, Amsterdam.
86. Chuang A.T.T., Foley A., Pugh P.L., Sunter D., Tong X., Regan C., et al. 5-HT6 receptor antagonist SB-742457 as a novel cognitive enhancing agent for Alzheimer's disease. Alzheimer's Dementia 2006, 2:S631-S632.
87. Foley A.G., Hirst W.D., Gallagher H.C., Barry C., Hagan J.J., Upton N., et al. The selective 5-HT6 receptor antagonists SB-271046 and SB-399885 potentiate NCAM PSA immunolabeling of dentate granule cells, but not neurogenesis, in the hippocampal formation of mature Wistar rats. Neuropharmacology 2008, 54:1166-1174.
88. Brennaman L.H., Maness P.F. NCAM in neuropsychiatric and neurodegenerative disorders. Advances in Experimental Medicine and Biology 2010, 663:299-317.
89. Barbeau D., Liang J.J., Robitalille Y., Quirion R., Srivastava L.K. Decreased expression of the embryonic form of the neural cell adhesion molecule in schizophrenic brains. Proceedings of the National Academy of Sciences of the United States of America 1995, 92:2785-2789.