Fine-Tuning of Awake Prefrontal Cortex Neurons by Clozapine: Comparison With Haloperidol and N-Desmethylclozapine

Biological Psychiatry

Volumn 61, Issue 5, 2007, Pages 679-687

  Homayoun, Houman ^a   Moghaddam, Bita ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

Author keywords

Atypical antipsychotic drugs; cognition; dopamine; ensemble unit electrophysiology; NMDA receptor antagonist; schizophrenia

Indexed keywords

CLOZAPINE; DIZOCILPINE; HALOPERIDOL; NORCLOZAPINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BEHAVIOR; CONTROLLED STUDY; DRUG ACTIVITY; DRUG EFFECT; MALE; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; STEREOTYPY; WAKEFULNESS;

ACTION POTENTIALS; ANALYSIS OF VARIANCE; ANIMALS; ANTIPSYCHOTIC AGENTS; CLOZAPINE; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; EXCITATORY AMINO ACID ANTAGONISTS; HALOPERIDOL; MALE; NEURONS; PREFRONTAL CORTEX; RATS; RATS, SPRAGUE-DAWLEY; STEREOTYPED BEHAVIOR; WAKEFULNESS;

EID: 33847289217     PISSN: 00063223     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.biopsych.2006.05.016     Document Type: Article

References (90)

1. Adams B., and Moghaddam B. Corticolimbic dopamine neurotransmission is temporally dissociated from the cognitive and locomotor effects of phencyclidine. J Neurosci 18 (1998) 5545-5554
2. Arango C., Breier A., McMahon R., Carpenter W.J., and Buchanan R. The relationship of clozapine and haloperidol treatment response to prefrontal, hippocampal, and caudate brain volumes. Am J Psychiatry 160 (2003) 1421-1427
3. Arvanov V., Liang X., Schwartz J., Grossman S., and Wang R. Clozapine and haloperidol modulate N-methyl-D-aspartate- and non-N-methyl-D-aspartate receptor-mediated neurotransmission in rat prefrontal cortical neurons in vitro. J Pharm Exp Thera 283 (1997) 226-234
4. Arvanov V., and Wang R. Clozapine, but not haloperidol, prevents the functional hyperactivity of N-methyl-D-aspartate receptors in rat cortical neurons induced by subchronic administration of phencyclidine. J Pharmacol Exp Ther 289 (1999) 1000-1006
5. Baeg E.H., Kim Y.B., Jang J., Kim H.T., Mook-Jung I., and Jung M.W. Fast spiking and regular spiking neural correlates of fear conditioning in the medial prefrontal cortex of rats. Cereb Cortex 11 (2001) 441-451
6. Bakshi V.P., Swerdlow N.R., and Geter M.A. Clozapine antagonizes phencyclidine-induced deficits in sensorimotor gating of the startle response. J Pharmacol Exp Ther 271 (1994) 787-794
7. Bartho P., Hirase H., Monconduit L., Zugaro M., Harris K.D., and Buzsaki G. Characterization of neocortical principal cells and interneurons by network interactions and extracellular features. J Neurophysiol 92 (2004) 600-608
8. Bechara A., Tranel D., and Damasio H. Characterization of the decision-making deficit of patients with ventromedial prefrontal cortex lesions. Brain 123 (2000) 2189-2202
9. Braver T., and Barch D. A theory of cognitive control, aging cognition, and neuromodulation. Neurosci Biobehav Rev 26 (2002) 809-817
10. Carlsson A., Waters N., and Carlsson M. Neurotransmitter interactions in schizophrenia: Therapeutic implications. Biol Psychiatry 46 (1999) 1388-1395
11. Castner S., Goldman-Rakic P., and Williams G. Animal models of working memory: Insights for targeting cognitive dysfunction in schizophrenia. Psychopharmacology (Berl) 174 (2004) 111-125
12. Chen L., and Yang C. Interaction of dopamine D1 and NMDA receptors mediates acute clozapine potentiation of glutamate EPSPs in rat prefrontal cortex. J Neurophysiol 87 (2002) 2324-2336
13. Conley R., and Kelly D. Management of treatment resistance in schizophrenia. Biol Psychiatry 50 (2001) 898-911
14. Creese I., Burt D., and Snyder S. Dopamine receptor binding predicts clinical and pharmacological potencies of antischizophrenic drugs. Science 192 (1976) 481-483
15. Davies M., Compton-Toth B., Hufeisen S., Meltzer H., and Roth B. The highly efficacious actions of N-desmethylclozapine at muscarinic receptors are unique and not a common property of either typical or atypical antipsychotic drugs: Is M1 agonism a pre-requisite for mimicking clozapine's actions?. Psychopharmacology (Berl) 178 (2005) 451-460
16. Davis J. The choice of drugs for schizophrenia. N Engl J Med 354 (2006) 518-520
17. Delfs J., and Kelley A. The role of D1 and D2 dopamine receptors in oral stereotypy induced by dopaminergic stimulation of the ventrolateral striatum. Neurosci 39 (1990) 59-67
18. Deutch A., and Duman R. The effects of antipsychotic drugs on Fos protein expression in the prefrontal cortex: Cellular localization and pharmacological characterization. Neurosci 70 (1996) 377-389
19. Dreher J., and Burnod Y. An integrative theory of the phasic and tonic modes of dopamine modulation in the prefrontal cortex. Neural Networks 15 (2002) 583-602
20. Duncan G., Leipzig J., Mailman R., and Lieberman J. Differential effects of clozapine and haloperidol on ketamine-induced brain metabolic activation. Brain Res 812 (1998) 65-75
21. Durstewitz D., and Seamans J. The computational role of dopamine D1 receptors in working memory. Neural Networks 15 (2002) 651-672
22. Durstewitz D., Seamans J., and Sejnowski T. Dopamine-mediated stabilization of delay-period activity in a network model of prefrontal cortex. J Neurophysiol 83 (2000) 1733-1750
23. Freedman R. The choice of antipsychotic drugs for schizophrenia. N Engl J Med 353 (2005) 1286-1288
24. Friedman J. Cholinergic targets for cognitive enhancement in schizophrenia: Focus on cholinesterase inhibitors and muscarinic agonists. Psychopharmacology (Berl) 174 (2004) 45-53
25. Funahashi S., Bruce C., and Goldman-Rakic P. Dorsolateral prefrontal lesions and oculomotor delayed-response performance: Evidence for mnemonic "scotomas.". J Neurosci 13 (1993) 1479-1497
26. Fuster J.M. The prefrontal cortex, mediator of cross-temporal contingencies. Human Neurobiol 4 (1985) 169-179
27. Gemperle A., Enz A., Pozza M., Luthi A., and Olpe H. Effects of clozapine, haloperidol and iloperidone on neurotransmission and synaptic plasticity in prefrontal cortex and their accumulation in brain tissue: An in vitro study. Neurosci 117 (2003) 681-695
28. Gold J., and Weinberger D. Cognitive deficits and the neurobiology of schizophrenia. Curr Opin Neurobiol 5 (1995) 225-230
29. Gorelick D., and Balster R. Phencyclidine (PCP). In: Bloom F., and Kupfer D. (Eds). Psychopharmacology, The Fourth Generation of Progress (1994), Raven Press, New York 1767-1776
30. Greene R. Circuit analysis of NMDAR hypofunction in the hippocampus, in vitro, and psychosis of schizophrenia. Hippocampus 11 (2001) 569-577
31. Homayoun H., Jackson M.E., and Moghaddam B. Activation of metabotropic glutamate 2/3 (mGlu2/3) receptors reverses the effects of NMDA receptor hypofunction on prefrontal cortex unit activity in awake rats. J Neurophysiol 93 (2004) 1989-2001
32. Izaki Y., Maruki K., Hori K., and Nomura M. Effects of rat medial prefrontal cortex temporal inactivation on a delayed alternation task. Neurosci Lett 315 (2001) 129-132
33. Jackson M., Homayoun H., and Moghaddam B. NMDA receptor hypofunction produces concomitant firing rate potentiation and burst activity reduction in the prefrontal cortex. Proc Natl Acad Sci U S A 101 (2004) 6391-6396
34. Jardemark K., Ninan I., Liang X., and Wang R. Protein kinase C is involved in clozapine's facilitation of N-methyl-D-aspartate- and electrically evoked responses in pyramidal cells of the medial prefrontal cortex. Neurosci 118 (2003) 501-512
35. Javitt D.C., and Zukin S.R. Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148 (1991) 1301-1308
36. Jentsch J.D., Tran A., Taylor J.R., and Roth R.H. Prefrontal cortical involvement in phencyclidine-induced activation of the mesolimbic dopamine system: Behavioral and neurochemical evidence. Psychopharmacol 138 (1998) 89-95
37. Kane J., Honigfeld G., Singer J., and Meltzer H. Clozapine for the treatment-resistant schizophrenic. A double-blind comparison with chlorpromazine. Arch Gen Psychiatry 45 (1988) 789-796
38. Karoum F., and Egan M. Dopamine release and metabolism in the rat frontal cortex, nucleus accumbens, and striatum: A comparison of acute clozapine and haloperidol. Br J Pharmacol 105 (1992) 703-707
39. Keefe R.S., Silva S.G., Perkins D.O., and Lieberman J.A. The effects of atypical antipsychotic drugs on neurocognitive impairment in schizophrenia: A review and meta-analysis. Schizophr Bull 25 (1999) 201-222
40. Konicki P., Kwon K., Steele V., White J., Fuller M., Jurjus G., and Jaskiw G. Prefrontal cortical sulcal widening associated with poor treatment response to clozapine. Schizo Res 48 (2001) 173-176
41. Krystal J.H., Karper L.P., Seibyl J.P., Freeman G.K., Delaney R., Bremner J.D., et al. Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans: Psychotomimetic, perceptual, cognitive, and neuroendocrine responses. Arch Gen Psychiatry 51 (1994) 199-214
42. Kumari V., Soni W., and Sharma T. Normalization of information processing deficits in schizophrenia with clozapine. Am J Psychiatry 156 (1999) 1046-1051
43. Kuoppamaki M.S., and Hietala J. Clozapine and N-desmethylclozapine are potent 5-HT1C receptor antagonists. E. Eur J Pharmacol 245 (1993) 179-182
44. Kuroki T., Meltzer H., and Ichikawa J. Effects of antipsychotic drugs on extracellular dopamine levels in rat medial prefrontal cortex and nucleus accumbens. J Pharmacol Exp Ther 288 (1999) 774-781
45. Lahti A., Holcomb H., Weiler M., Medoff D., Frey K., Hardin M., and Tamminga C. Clozapine but not haloperidol re-establishes normal task-activated rCBF patterns in schizophrenia within the anterior cingulate cortex. Neuropsychopharmacology 29 (2004) 171-178
46. Lieberman J.A., Stroup T.S., McEvoy J.P., Swartz M.S., Rosenheck R.A., Perkins D.O., et al., Clinical Antipsychotic Trials of Intervention Effectiveness (CATIE) Investigators. Effectiveness of antipsychotic drugs in patients with chronic schizophrenia. N Eng J Med 353 (2005) 1209-1223
47. Lee M., Jayathilake K., and Meltzer H. A comparison of the effect of clozapine with typical neuroleptics on cognitive function in neuroleptic-responsive schizophrenia. Schizophr Res 37 (1999) 1-11
48. Lewis D., Hashimoto T., and Volk D. Cortical inhibitory neurons and schizophrenia. Nat Rev Neurosci 6 (2005) 312-324
49. Malhotra A.K., Adler C.M., Kennison S.D., Elman I., Pickar D., and Breier A. Clozapine blunts N-methyl-D-aspartate antagonist-induced psychosis: A study with ketamine. Biol Psychiatry 42 (1997) 664-668
50. Manes F., Sahakian B., Clark L., Rogers R., Antoun N., Aitken M., and Robbins T. Decision-making processes following damage to the prefrontal cortex. Brain 125 (2002) 624-639
51. Maurel-Remy S., Bervoets K., and Millan M.J. Blockade of phencyclidine-induced hyperlocomotion by clozapine and MDL in rats reflects antagonism of 5-HT2A receptors. Eur J Pharmacol 280 (1995) R9-R11
52. McCormick D.A., Connors B.W., Lighthall J.W., and Prince D.A. Comparative electrophysiology of pyramidal and sparsely spiny stellate neurons of the neocortex. J Neurophysiol 54 (1985) 782-806
53. McEvoy J.P., Lieberman J.A., Stroup T.S., Davis S.M., Meltzer H.Y., Rosenheck R.A., et al., CATIE Investigators. Effectiveness of clozapine versus olanzapine, quetiapine, and risperidone in patients with chronic schizophrenia who did not respond to prior atypical antipsychotic treatment. Am J Psychiatry 163 (2006) 600-610
54. McGurk S. The effects of clozapine on cognitive functioning in schizophrenia. J Clin Psychiatry 60 suppl 1 (1999) 24-29
55. Meltzer H., Alphs L., Green A., Altamura A., Anand R., Bertoldi A., et al. Clozapine treatment for suicidality in schizophrenia: International Suicide Prevention Trial (InterSePT). Arch Gen Psychiatry 60 (2003) 82-91
56. Meltzer H., and McGurk S. The effects of clozapine, risperidone, and olanzapine on cognitive function in schizophrenia. Schizophr Bull 25 (1999) 233-255
57. Meltzer H.Y., Matsubara S., and Lee J.C. Classification of typical and atypical antipsychotic drugs on the basis of dopamine D-1, D-2 and seratonin2 pKi values. J Pharmacol Exp Ther 251 (1989) 238-246
58. Miller P., Lawrie S.M., Hodges A., Clafferty R., Cosway R., and Johnstone E.C. Genetic liability, illicit drug use, life stress and psychotic symptoms: Preliminary findings from the Edinburgh study of people at high risk for schizophrenia. Soc Psychiatry Psychiatr Epidemiol 36 (2001) 338-342
59. Miyamoto S., Duncan G., Marx C., and Lieberman J. Treatments for schizophrenia: A critical review of pharmacology and mechanisms of action of antipsychotic drugs. Mol Psychiatry 10 (2005) 79-104
60. Moghaddam B., Adams B., Verma A., and Daly D. Activation of glutamatergic neurotransmission by ketamine: A novel step in the pathway from NMDA receptor blockade to dopaminergic and cognitive disruptions associated with the prefrontal cortex. J Neurosci 17 (1997) 2921-2927
61. Moghaddam B., and Bunney B.S. Acute effects of typical and atypical antipsychotic drugs on the release of dopamine from prefrontal cortex, nucleus accumbens, and striatum of the rat: An in vivo microdialysis study. J Neurosci 54 (1990) 1755-1760
62. Molina V., Reig S., Sarramea F., Sanz J., Francisco Artaloytia J., Luque R., et al. Anatomical and functional brain variables associated with clozapine response in treatment-resistant schizophrenia. Psychiat Res 124 (2003) 153-161
63. Nicolelis M.A.L., Dimitrov D., Carmena J.M., Crist R., Lehew G., Kralik J.D., and Wise S.P. Chronic, multisite, multielectrode recordings in macaque monkeys. Proc Natl Acad Sci U S A 100 (2003) 11041-11046
64. O'Donnell P. Dopamine gating of forebrain neural ensembles. Eur J Neurosci 17 (2003) 429-435
65. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, San Diego
66. Peters Y., Barnhardt N., and O'Donnell P. Prefrontal cortical up states are synchronized with ventral tegmental area activity. Synapse 52 (2004) 143-152
67. Piscitelli S., Frazier J., McKenna K., Albus K., Grothe D., Gordon C., and Rapoport J. Plasma clozapine and haloperidol concentrations in adolescents with childhood-onset schizophrenia: Association with response. J Clin Psychiatry 55 suppl B (1994) 94-97
68. Robertson G., and Fibiger H. Neuroleptics increase c-fos expression in the forebrain: Contrasting effects of haloperidol and clozapine. Neurosci 46 (1992) 315-328
69. Roth B., Sheffler D., and Kroeze W. Magic shotguns versus magic bullets: Selectively non-selective drugs for mood disorders and schizophrenia. Nat Rev Drug Discov 3 (2004) 353-359
70. Sams-Dodd F. A test of the predictive validity of animal models of schizophrenia based on phencyclidine and D-amphetamine. Neuropsychopharmacology 18 (1998) 293-304
71. Sawaguchi T., and Iba M. Prefrontal cortical representation of visuospatial working memory in monkeys examined by local inactivation with muscimol. J Neurophysiol 86 (2001) 2041-2053
72. Seeman P., Lee T., Chau-Wong M., and Wong K. Antispsychotic drug doses and neuroleptic/dopamine receptors. Nature 261 (1976) 717-719
73. Sharma T. Cognitive effects of conventional and atypical antipsychotics in schizophrenia. Br J Psychiatry Suppl 38 (1999) 44-51
74. Spivak B., Shabash E., Sheitman B., Weizman A., and Mester R. The effects of clozapine versus haloperidol on measures of impulsive aggression and suicidality in chronic schizophrenia patients: An open, nonrandomized, 6-month study. J Clin Psychiatry 64 (2003) 755-760
75. Stockmeier C., DiCarlo J., Zhang Y., Thompson P., and Meltzer H. Characterization of typical and atypical antipsychotic drugs based on in vivo occupancy of serotonin2 and dopamine2 receptors. J Pharmacol Exp Ther 266 (1993) 1374-1384
76. Sur C., Mallorga P.J., Wittmann M., Jacobson M.A., Pascarella D., Williams J.B., et al. N-desmethylclozapine, an allosteric agonist at muscarinic 1 receptor, potentiates N-methyl-D-aspartate receptor activity. Proc Natl Acad Sci U S A 100 (2003) 13674-13679
77. Svensson T. Alpha-adrenoceptor modulation hypothesis of antipsychotic atypicality. Biol Psychiatry 27 (2003) 1145-1158
78. Takahata R., and Moghaddam B. Activation of glutamate neurotransmission in the prefrontal cortex sustains the motoric and dopaminergic effects of phencyclidine. Neuropsychopharmacology 28 (2003) 1117-1124
79. Tiedtke P.I., Bischoff C., and Schmidt W.J. MK-801-induced stereotypy and its antagonism by neuroleptic drugs. J Neural Trans 81 (1990) 173-182
80. Tierney P., Degenetais E., Thierry A., Glowinski J., and Gioanni Y. Influence of the hippocampus on interneurons of the rat prefrontal cortex. Eur J Neurosci 20 (2004) 514-524
81. Verma A., and Moghaddam B. NMDA receptor antagonists impair prefrontal cortex function as assessed via spatial delayed alternation performance in rats: Modulation by dopamine. J Neurosci 16 (1996) 373-379
82. Wahlbeck K., Cheine M., and Essali M. Clozapine versus typical neuroleptic medication for schizophrenia. Cochrane Database Syst Rev 2 (2000) CD000059
83. Weiner D., Meltzer H., Veinbergs I., Donohue E., Spalding T., Smith T., et al. The role of M1 muscarinic receptor agonism of N-desmethylclozapine in the unique clinical effects of clozapine. Psychopharmacology (Berl) 177 (2004) 207-216
84. Williams G.V., and Goldman-Rakic P.S. Modulation of memory fields by dopamine D1 receptors in prefrontal cortex. Nature 376 (1995) 393-401
85. Winterer G., and Weinberger D. Genes, dopamine and cortical signal-to-noise ratio in schizophrenia. Trends Neurosci 27 (2004) 683-690
86. Yamamoto B., Pehek E., and Meltzer H. Brain region effects of clozapine on amino acid and monoamine transmission. J Clin Psychiatry 55 suppl B (1994) 8-14
87. Yang C., and Seamans J. Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: Modulation of dendritic-somatic signal integration. J Neurosci 16 (1996) 1922-1935
88. Young C., Meltzer H., and Deutch A. Effects of desmethylclozapine on Fos protein expression in the forebrain: In vivo biological activity of the clozapine metabolite. Neuropsychopharmacology 19 (1998) 99-103
89. Youngren K.D., Inglis F.M., Pivirotto P.J., Jedema H.P., Bradberry C.W., Goldman-Rakic P.S., et al. Clozapine preferentially increases dopamine release in the rhesus monkey prefrontal cortex compared with the caudate nucleus. Neuropsychopharmacology 20 (1999) 403-412
90. Youngren K.D., Moghaddam B., Bunney B.S., and Roth R.H. Preferential activation of dopamine overflow in prefrontal cortex produced by chronic clozapine treatment. Neurosci Lett 165 (1994) 41-44