Chronic administration of clozapine alleviates reversal-learning impairment in isolation-reared rats

Behavioural Pharmacology

Volumn 18, Issue 2, 2007, Pages 135-145

  Li, Nanxin ^a   Wu, Xihong ^a   Li, Liang ^a,b  

^a PEKING UNIVERSITY   (China)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Animal model; Clozapine; Isolation rearing; Rat; Reversal learning; Schizophrenia; T maze

Indexed keywords

CLOZAPINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DATA ANALYSIS; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFECT; INHIBITION (PSYCHOLOGY); LEARNING; LEARNING DISORDER; MALE; MAZE TEST; NEUROPATHOLOGY; NONHUMAN; RAT; REARING; SCHIZOPHRENIA; SOCIAL ISOLATION; TREATMENT RESPONSE; VISUAL DISCRIMINATION;

ANIMALS; ANTIPSYCHOTIC AGENTS; CLOZAPINE; DISCRIMINATION LEARNING; DOSE-RESPONSE RELATIONSHIP, DRUG; LEARNING DISORDERS; MALE; MAZE LEARNING; RATS; RATS, SPRAGUE-DAWLEY; REVERSAL LEARNING; SOCIAL ISOLATION; VISUAL PERCEPTION;

EID: 33947123173     PISSN: 09558810     EISSN: None     Source Type: Journal    
DOI: 10.1097/FBP.0b013e3280d3ee83     Document Type: Article

References (113)

1. Abdul-Monim Z, Reynolds GP, Neill JC (2003). The atypical antipsychotic ziprasidone, but not haloperidol, improves phencyclidine-induced cognitive deficits in a reversal learning task in the rat. J Psychopharmacol 17:57-65.
2. Abdul-Monim Z, Reynolds GP, Neill JC (2006). The effect of atypical and classical antipsychotics on sub-chronic PCP-induced cognitive deficits in a reversal-learning paradigm. Behav Brain Res 169:263-273.
3. Altar CA, Wasley AM, Neale RF, Stone GA (1986). Typical and atypical antipsychotic occupancy of D2 and S2 receptors: an autoradiographic analysis in rat brain. Brain Res Bull 16:517-525.
4. Arakawa H (2005). Interaction between isolation rearing and social development on exploratory behavior in male rats. Behav process 70:223-234.
5. Bardgett ME, Griffith MS, Foltz RF (2006). The effects of clozapine on delayed spatial alternation deficits in rats with hippocampal damage. Neurobiol Learn Mem 85:86-94.
6. Barr AM, Young CE, Sawada K, Trimble WS, Phillips AG, Honer WG (2004). Abnormalities of presynaptic protein CDCrel-1 in striatum of rats reared in social isolation: relevance to neural connectivity in schizophrenia. Eur J Neurosci 20:303-307.
7. Bembenek A (2005). Seasonality of birth in schizophrenia patients: literary review. Psychiatr Pol 39:259-270.
8. Bender S, Dittmann-Balcar A, Schall U (2006). Influence of atypical neuroleptics on executive functioning in patients with schizophrenia: a randomized, double-blind comparison of olanzapine vs. clozapine. Int J Neuropsychopharmacol 9:135-145.
9. Bickerdike MJ, Wright IK, Marsden CA (1993). Social isolation attenuates rat forebrain 5-HT release induced by KCl stimulation and exposure to a novel environment. Behav Pharmacol 4:231-236.
10. Bortolozzi A, az-Mataix LD, Scorza C, Celada P, Artigas F (2004). Atypical antipsychotics modulate a prefrontal 5-HT2A receptormediated activation of the mesocortical dopaminergic pathway. Abstract Viewer/Itinerary Planner Washington, DC: Society for Neuroscience Program No. 45.10.
11. Braff DL, Geyer MA, Swerdlow NR (2001). Human studies of prepulse inhibition of startle: normal subjects, patient groups, and pharmacological studies. Psychopharmacology 156:234-258.
12. Chudasama Y, Robbins TW (2003). 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. J Neurosci 23:8771-8780.
13. Cilia J, Hatcher PD, Reavill C (2005). Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats: an update. Psychopharmacology 180:57-62.
14. Cilia J, Reavill C, Hagan JJ (2001). Long-term evaluation of isolation-rearing induced prepulse inhibition deficits in rats. Psychopharmacology 156:327-337.
15. Clarke HF, Dalley JW, Crofts HS, Robbins TW, Roberts AC (2004). Cognitive inflexibility after prefrontal serotonin depletion. Science 304:878-880.
16. Clarke HF, Walker SC, Crofts HS, Dalley JW, Robbins TW, Roberts AC (2005). Prefrontal serotonin depletion affects reversal learning but not attentional set shifting. J Neurosci 25:532-538.
17. Crespi F, Wright IK, Mobius C (1992). Isolation rearing of rats alters release of 5-hydroxytryptamine and dopamine in the frontal cortex: an in vivo electrochemical study. Exp Brain Res 88:495-501.
18. Crider A (1997). Perseveration in schizophrenia. Schizophr Bul 23:63-74.
19. Dalley JW, Theobald DE, Pereira EAC, Li PMMC, Robbins TW (2002). Specific abnormalities in serotonin release in the prefrontal cortex of isolation-reared rats measured during behavioural performance of a task assessing visuospatial attention and impulsivity. Psychopharmacology 164:329-340.
20. Day-Wilson KM, Jones DNC, Southam E, Cilia J, Totterdell S (2006). Medial prefrontal cortex volume loss in rats with isolation rearing-induced deficits in prepulse inhibition of acoustic startle. Neuroscience 141:1113-1121.
21. Demakis GJ (2003). A meta-analytic review of the sensitivity of the Wisconsin Card Sorting Test to frontal and lateralized frontal brain damage. Neuropsychology 17:255-264.
22. Deutch AY, Moghaddam B, Innis RB, Krystal JH, Aghajanian GK, Bunney BS, Charney DS (1991). Mechanism of action atypical antipsychotic-drugs implications for novel therapeutic strategies for schizophrenia. Schizophr Res 4:121-156.
23. Eells JB, Misler JA, Nikodem VM (2006). Early postnatal isolation reduces dopamine levels, elevates dopamine turnover and specifically disrupts prepulse inhibition in Nurr1-null heterozygous mice. Neuroscience 140:1117-1126.
24. Ellenbroek BA, Cools AR (1998). The neurodevelopment hypothesis of schizophrenia: clinical evidence and animal models. Neurosci Res Commun 22:127-136.
25. Flagstad P, Glenthøj BY, Didriksen M (2005). Cognitive deficits caused by late gestational disruption of neurogenesis in rats: a preclinical model of schizophrenia. Neuropsychopharmacology 30:250-260.
26. 2C receptor responsiveness occurs on rearing rats in social isolation. Psychopharmacology 123:346-352.
27. Geyer MA, Wilkinson LS, Humby T, Robbins TW (1993). Isolation rearing of rats produces a deficit in prepulse inhibition of acoustic startle similar to that in schizophrenia. Biol Psychiatry 34:361-372.
28. Geyer MA, Kirsten K, Braff DL, Swerdlow NR (2001). Pharmacological studies of prepulse inhibition models of sensorimotor gating deficits in schizophrenia: a decade in review. Psychopharmacology 156:117-154.
29. Galletly CA, Clark CR, McFarlane AC (2005). Clozapine improves working memory updating in schizophrenia. Eur Neuropsychopharmacol 15:601-608.
30. Hall FS, Ghaed S, Pert A, Xing G (2002). The effects of isolation rearing on glutamate receptor NMDAR1A mRNA expression determined by in situ hybridization in Fawn hooded and Wistar rats. Pharmacol Biochem Behav 73:185-191.
31. Harte MK, Powell SB, Reynolds LM, Swerdlow NR, Geyer MA, Reynolds GP (2004). Reduced N-acetylaspartate in the temporal cortex of rats reared in isolation. Biol Psychiatry 56:296-299.
32. Hartmann B, Gunturkun O (1998). Selective deficits in reversal learning after neostriatum caudolaterale lesions in pigeons: possible behavioral equivalencies to the mammalian prefrontal system. Behav Brain Res 96:125-133.
33. Heidbreder CA, Foxton R, Cilia J, Hughes ZA, Shah AJ, Atkins A, et al. (2001). Increased responsiveness of dopamine to atypical, but not typical anti-psychotics in the medial prefrontal cortex of rats reared in isolation. Psychopharmacology 156:338-351.
34. Heidbreder CA, Weiss IC, Domeney AM, Pryce C, Homber J, Hedou G, et al. (2000). Behavioral, neurochemical and endocrinological characterization of the early isolation syndrome. Neuroscience 100:749-768.
35. Hitchcock JM, Lister S, Fischer TR, Wettstein JG (1997). Disruption of latent inhibition in the rat by the 5-HT2 agonist DOI: effects of MDL 100 907, clozapine, risperidone and haloperidol. Behav Brain Res 88:43-49.
36. 1A receptor activation: a possible mechanism of atypical antipsychotic-induced cortical dopamine release. J Neurochem 76:1521-1531.
37. Idris NF, Repeto P, Neill JC (2005). Investigation of the effects of lamotrigine and clozapine in improving reversal-learning impairments induced by acute phencyclidine and D-amphetamine in the rat. Psychopharmacology 179:336-348.
38. Janowsky JS, Shimamura AP, Kritchevsky M, Squire LR (1989). Cognitive impairment following frontal lobe damage and its relevance to human amnesia. Behav Neurosci 103:548-560.
39. Jardemark KE, Liang X, Arvanov V, Wang RY (2000). Subchronic treatment with either clozapine, olanzapine or haloperidol produces a hyposensitive response of the rat cortical cells to N-methyl-D-aspartate. Neuroscience 100:1-9.
40. Jentsch JD, Taylor JR (2001). Impaired inhibition of conditioned responses produced by subchronic administration of phencyclidine to rats. Neuropsychopharmacology 24:66-74.
41. Joel D, Weiner I, Feldon J (1997). Electrolytic lesions of the medial prefrontal cortex in rats disrupt performance on an analog of the Wisconsin Card Sorting Test, but do not disrupt latent inhibition: implications for animal models of schizophrenia. Behav Brain Res 85:187-201.
42. Jones GH, Hernandez TD, Kendall DA (1992). Dopaminergic and serotonergic function following isolation rearing in rats: study of behavioral-response and postmortem and in vivo neurochemistry. Pharmacol Biochem Behav 43:17-35.
43. Jones GH, Marsden CA, Robbins TW (1991). Behavioural rigidity and rule-learning deficits following isolation-rearing in the rat: neurochemical correlates. Behav Brain Res 43:35-50.
44. Kolb B, Whishaw IQ (1983). Performance of schizophrenic patients on tests sensitive to left or right frontal, temporal, or parietal function in neurological patients. J Nerv Ment Dis 171:435-443.
45. Krech D, Rosenzweig MR, Bennett EL (1962). Relations between brain chemistry and problem-solving among rats raised in enriched and impoverished environments. J Comp Physiol Psychol 55:801-807.
46. Kumari V, Soni W, Mathew VM, Sharma T (2000). Prepulse inhibition of the startle response in men with schizophrenia: effects of age of onset of illness, symptoms, and medication. Arch Gen Psychiatry 57:609-614.
47. Kumari V, Soni W, Sharma T (1999). Normalization of information processing deficits in schizophrenia with clozapine. Am J Psychiatry 156:1046-1051.
48. Kumari V, Soni W, Sharma T (2002). Prepulse inhibition of the startle response in risperidone-treated patients: comparison with typical antipsychotics. Schizophr Res 55:139-146.
49. Lanser MG, Berger HJC, Ellenbroek BA, Cools AR, Zitman FG (2002). Perseveration in schizophrenia: failure to generate a plan and relationship with the psychomotor poverty subsyndrome. Psych Res 112:13-26.
50. Lapiz MDS, Mateo Y, Parker T (2000). Effects of noradrenaline depletion in the brain on response to novelty in isolation-reared rats. Psychopharmacology 152:312-320.
51. Lehmann K, Hundsdorfer B, Hartmann T, Teuchert-Noodt G (2004). The acetylcholine fiber density of the neocortex is altered by isolated rearing and early methamphetamine intoxication in rodents. Exp Neurol 189:131-140.
52. Lehmann K, Lesting J, Polascheck D, Teuchert-Noodt G (2003). Serotonin fibre densities in subcortical areas: differential effects of isolated rearing and methamphetamine. Dev Brain Res 147:143-152.
53. Leumann L, Feldon J, Vollenweider FX, Ludewig K (2002). Effects of typical and atypical antipsychotics on prepulse inhibition and latent inhibition in chronic schizophrenia. Biol Psychiatry 52:729-739.
54. Levin ED, Christopher NC (2006). Effects of clozapine on memory function in the rat neonatal hippocampal lesion model of schizophrenia. Prog Neuropsychopharmacol Biol Psychiatry 30:223-229.
55. Li L, Shao J (1998). Restricted lesions to ventral prefrontal subareas block reversal learning but not visual discrimination learning in rats. Physiol Behav 65:371-379.
56. Li L, Yue Q (2002). Auditory gating processes and binaural inhibition in the inferior colliculus. Hear Res 168:113-124.
57. Mackintosh NJ, Holgate V (1969). Serial reversal training and nonreversal shift learning. J Comp Physiol Psychol 67:89-93.
58. Marenco S, Weinberger DR (2000). The neurodevelopmental hypothesis of schizophrenia: following a trail of evidence from cradle to grave. Dev Psychopathol 12:501-527.
59. McAlonan K, Brown VJ (2003). Orbital prefrontal cortex mediates reversal learning and not attentional set shifting in the rat. Behav Brain Res 146:97-103.
60. Mcelroy SL, Dessain EC, Pope HG, Cole Jo, Keck PE, Frankenberg FR, et al. (1991). Clozapine in the treatment of psychotic mood disorders, schizo-affective disorder, and schizophrenia. J Clin Psychiatry 52:411-414.
61. McGrath JJ, Feron FP, Burne THJ, Mackay-Sim A, Eyles DW (2003). The neurodevelopmental hypothesis of schizophrenia: a review of recent developments. Ann Med 35:86-93.
62. Meltzer HY (1989). Clinical studies of the mechanism of action of clozapine-the dopamine-serotonin hypothesis of schizophrenia. Psychopharmacology 99:S18-S27.
63. Meltzer HY, McGurk SR (1999). The effects of clozapine, risperidone, and olanzapine on cognitive function in schizophrenia. Schizophr Bull 25:233-255.
64. Meyera U, Feldon J, Schedlowskib M, Yee BK (2005). Towards an immuno-precipitated neurodevelopmental animal model of schizophrenia. Neurosci Biobehav Rev 29:913-947.
65. Milner B (1963). Effects of different brain lesions on card sorting. Arch Neurol 9:90-100.
66. Miura H, Qiao H, Ohta T (2002). Attenuating effects of the isolated rearing condition on increased brain serotonin and dopamine turnover elicited by novelty stress. Brain Res 926:10-17.
67. Muchimapura S, Mason R, Marsden CA (2003). Effect of isolation rearing on pre- and post-synaptic serotonergic function in the rat dorsal hippocampus. Synapse 47:209-217.
68. Nagahama Y, Okina T, Suzuki N, Nabatame H, Matsuda M (2005). The cerebral correlates of different types of perseveration in the Wisconsin Card Sorting Test. J Neurol Neurosurg Psychiatry 76:169-175.
69. Oranje B, Van Oel CJ, Gispen-De Wied CC, Verbaten MN, Kahn RS (2002). Effects of typical and atypical antipsychotics on the prepulse inhibition of the startle reflex in patients with schizophrenia. J Clin Psychopharmacol 22:359-365.
70. Ortega-Alvaro A, Gibert-Rahola J, Mico JA (2006). Influence of chronic treatment with olanzapine, clozapine and scopolamine on performance of a learned 8-arm radial maze task in rats. Prog Neuropsychopharmacol Biol Psychiatry 30:104-111.
71. O'Connor TG, Rutter M (1996). Risk mechanisms in development: some conceptual and methodological considerations. Dev Psychol 32:787-795.
72. Paulus MP, Bakshi VP, Geyer MA (1998). Isolation rearing affects sequential organization of motor behavior in post-pubertal but not pre-pubertal Lister and Sprague-Dawley rats. Behav Brain Res 94:271-280.
73. Pehek EA, Nocjar C, Roth BL, Byrd TA, Mabrouk OS (2006). Evidence for the preferential involvement of 5-HT2A serotonin receptors in stress- and drug-induced dopamine release in the rat medial prefrontal cortex. Neuropsychopharmacology 31:265-277.
74. Peters YM, O'Donnell P (2005). Social isolation rearing affects prefrontal cortical response to ventral tegmental area stimulation. Biol Psychiatry 57:1205-1208.
75. Pickar D, Owen RR, Litman RE, Konicki PE, Gutierrez R, Rapaport MH (1992). Clinical and biologic response to clozapine in patients with schizophrenia: crossover comparison with fluphenazine. Arch Gen Psychiatry 49:345-353.
76. Powell CM, Miyakawa T (2006). Schizophrenia-relevant behavioral testing in rodent models: a uniquely human disorder? Biol Psychiatry 59:1198-1207.
77. Powell SB, Risbrough VB, Geyer MA (2003). Potential use of animal models to examine antipsychotic prophylaxis for schizophrenia. Clin Neurosci Res 3:289-296.
78. Powell SB, Swerdlow NR, Pitcher LK, Geyer MA (2002). Isolation rearing-induced deficits in prepulse inhibition and locomotor habituation are not potentiated by water deprivation. Physiol Behav 77:55-64.
79. Preece MA, Dalley JW, Theobald DH (2004). Region specific changes in forebrain 5-hydroxytryptamine(1A) and 5-hydroxytryptamine(2A) receptors in isolation-reared rats: an in vitro autoradiography study. Neuroscience 123:725-732.
80. Ragozzino ME, Jih J, Tzavos A (2002). Involvement of the dorsomedial striatum in behavioral flexibility: role of muscarinic cholinergic receptors. Brain Res 953:205-214.
81. Reboucas R, Schimdek WR (1997). Handing and isolation in three strains of rats affect open field, exploration, hoarding and predation. Physiol Behav 62:1159-1164.
82. Rehn AE, Rees SM (2005). Investigating the neurodevelopmental hypothesis of schizophrenia. Clin Exp Pharmacol Physiol 32:687-696.
83. Ritter LM, Meador-Woodruff JH, Dalack GW (2004). Neurocognitive measures of prefrontal cortical dysfunction in schizophrenia. Schizophr Res 68:65-73.
84. Robbins TW (2005). Chemistry of the mind: neurochemical modulation of prefrontal cortical function. J Comp Neurol 493:140-146.
85. Robertson GS, Fibiger HC (1992). Neuroleptics increase c-fos expression in the forebrain contrasting effects of haloperidol and clozapine. Neuroscience 46:315-328.
86. Rogers RD, Andrews TC, Grasby PM (2000). Contrasting cortical and subcortical activations produced by attentional-set shifting and reversal learning in humans. J Cogn Neurosci 12:142-162.
87. Russig H, Durrer A, Yee BK, Murphy CA, Feldon J (2003). The acquisition, retention and reversal of spatial learning in the Morris water maze task following withdrawal from an escalating dosage schedule of amphetamine in Wistar rats. Neuroscience 119:167-179.
88. Salazara RF, White W, Lacroix L, Feldon J, White IA (2004). NMDA lesions in the medial prefrontal cortex impair the ability to inhibit responses during reversal of a simple spatial discrimination. Behav Brain Res 152:413-424.
89. Schoenbaum G, Nugent SL, Saddoris MP, Setlow B (2002). Orbitofrontal lesions in rats impair reversal but not acquisition of go, no-go odor discriminations. Neuroreport 13:885-890.
90. Schrijver NCA, Pallier PN, Brown VJ, Wurbel H (2004). Double dissociation of social and environmental stimulation on spatial learning and reversal learning in rats. Behav Brain Res 152:307-314.
91. Schrijver NCA, Würbel H (2001). Early social deprivation disrupts attentional, but not affective, shifts in rats. Behav Neurosci 115:437-442.
92. Schwabe K, Enkel T, Klein S, Schutte M, Koch M (2004). Effects of neonatal lesions of the medial prefrontal cortex on adult rat behaviour. Behav Brain Res 153:21-34.
93. 2A-receptors. Br J Pharmacol 135:65-78.
94. Sharma T, Hughes C, Soni W, Kumari V (2003). Cognitive effects of olanzapine and clozapine treatment in chronic schizophrenia. Psychopharmacology, 169:398-403.
95. Sperling SE (1965). Reversal learning and resistance to extinction: a review of the rat literature. Psychol Bull 63:281-297.
96. Sullivan R, Wilson DA, Feldon J, Yee BK, Meyer U, Richter-Levin G, et al. (2006). The international society for developmental psychobiology annual meeting symposium: impact of early life experiences on brain and behavioral development. Dev Psychobiol 48:583-602.
97. Swerdlow NR, Geyer MA (1993). Clozapine and haloperidol in an animal model of sensorimotor gating deficits in schizophrenia. Pharmacol Biochem Behav 44:741-744.
98. Swerdlow NR, Geyer MA, Braff DL (2001). Neural circuit regulation of prepulse inhibition of startle in the rat: current knowledge and future challenges. Psychopharmacology 156:194-215.
99. Tanaka Y, Obata T, Sassa T, Yoshitome E, Asai Y, Ikehira H, et al. (2006). Quantitative magnetic resonance spectroscopy of schizophrenia: relationship between decreased N-acetylaspartate and frontal lobe dysfunction. Psychiatry Clin Neurosci 60:365-372.
100. Tochigi M, Okazaki Y, Kato N, Sasaki T (2004). What causes seasonality of birth in schizophrenia? Neurosci Res 48:1-11.
101. Varty GB, Geyer MA (1998). Effects of isolation rearing on startle reactivity, habituation, and prepulse inhibition in male Lewis, Sprague-Dawley, and Fischer F344 rats. Behav Neurosci 112:1450-1457.
102. Varty GB, Higgins GA (1995). Examination of drug-induced and isolation-induced disruptions of prepulse Inhibition as models to screen antipsychotic drugs. Psychopharmacology 122:15-26.
103. Varty GB, Paulus MP, Braff DL, Geyer MA (2000). Environmental enrichment and isolation rearing in the rat: effects on locomotor behavior and startle response plasticity. Biol Psychiatry 47:864-873.
104. Van den Buuse M, Garner B, Koch M (2003). Neurodevelopmental animal models of schizophrenia: effects on prepulse inhibition. Curr Mol Med 3:459-471.
105. Van der Meulen JAJ, Bilbija L, Joosten RNJMA (2003). The NMDA-receptor antagonist MK-801 selectively disrupts reversal learning in rats. Neuroreport 14:2225-2228.
106. Van den Buuse M, Garner B, Gogos A, Kusljic S (2005). Importance of animal models in schizophrenia research. Aust NZ J Psychiatry 39:550-557.
107. Weinberger DR (1987). Implications of normal brain-development for the pathogenesis of schizophrenia. Arch Gen Psychiatry 44:660-669.
108. Weinberger DR (1996). On the plausibility of 'the neurodevelopmental hypothesis' of schizophrenia. Neuropsychopharmacology 14 (Suppl):S1-S11.
109. Weiss IC, Domeney AM, Moreau J, Russig H, Feldon J (2001). Dissociation between the effects of pre-weaning and/or post-weaning social isolation on prepulse inhibition and latent inhibition in adult Sprague-Dawley rats. Behav Brain Res 121:207-218.
110. Weiss IC, Feldon J (2001). Environmental animal models for sensorimotor gating deficiencies in schizophrenia: a review. Psychopharmacology 156:305-326.
111. Whitaker-Azmitia P, Zhou F, Hobin J, Borella A (2000). Isolation-fearing of rats produces deficits as adults in the serotonergic innervation of hippocampus. Peptides 21:1755-1759.
112. Wilkinson LS, Killcross SS, Humby T, Hall FS, Geyer MA, Robbins TW (1994). Social-isolation in the rat produces developmentally specific deficits in prepulse inhibition of the acoustic startle response without disturbing latent inhibition. Neuropsychopharmacology 10:61-72.
113. Wongwitdecha N, Marsden CA (1996). Effects of social isolation rearing on learning in the Morris water maze. Brain Res 1:119-124.