Corticolimbic dopamine neurotransmission is temporally dissociated from the cognitive and locomotor effects of phencyclidine

Journal of Neuroscience

Volumn 18, Issue 14, 1998, Pages 5545-5554

  Adams, Barbara ^a   Moghaddam, Bita ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Drug abuse; Glutamate; Ketamine; Microdialysis; NMDA; Nucleus accumbens; PCP; Prefrontal cortex; Schizophrenia; Working memory

Indexed keywords

DOPAMINE; GLUTAMIC ACID; KETAMINE; PHENCYCLIDINE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; COGNITION; CONTROLLED STUDY; DOPAMINERGIC SYSTEM; DRUG ABUSE; DRUG MECHANISM; LIMBIC SYSTEM; MALE; NONHUMAN; NUCLEUS ACCUMBENS; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SCHIZOPHRENIA; WORKING MEMORY;

EID: 0032527894     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.18-14-05545.1998     Document Type: Article

References (94)

1. Bakker CB, Amini FB (1961) Observations on the psychotomimetic effects of sernyl. Compr Psychiatry 2:269-280.
2. Bakshi VP, Swerdlow NR, Geyer MA (1994) Clozapine antagonizes phencyclidine-induced deficits in sensorimotor gating of the startle response. J Pharmacol Exp Ther 271:787-794.
3. Breier, A, Su TP, Saunders R, Carson RE, Kolachana BS, de Bartolomeis A, Weinberger DR, Weisenfeld N, Malhorta AK, Eckelman WC, Pickar D (1977) Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method, Proc Natl Acad Sci USA 94:2569-2574.
4. Breier A, Adler C, Weisenfeld NI, Elman I, Picken L, Malhotra AK, Pickar D (1998) Effects of NMDA antagonism on striatal dopamine release in healthy subjects: application of a novel PET approach. Synapse 29:142-147.
5. Bristow LJ, Hutson PH, Thorn L, Tricklebank MD (1993) The glycine/NMDA receptor antagonist, R-(+)-HA-966, blocks activation of the mesolimbic dopaminergic system induced by phencyclidine and dizocilpine (MK-801) in rodents. Br J Pharmacol 108:1156-1163.
6. Bubser M, Schmidt WJ (1990) 6-Hydroxydopamine lesion of the rat prefrontal cortex increases locomotor activity, impairs acquisition of delayed alternation tasks, but does not affect uninterrupted tasks in the radial maze. Behav Brain Res 37:157-168.
7. Bubser M, Tzschentke T, Hauber W (1995) Behavioral and neurochemical interactions of the AMPA antagonist GYKI 52466 and the non-competitive NMDA antagonist dizocilpine in rats. J Neural Transm Gen Sect 101:115-126.
8. Burns RS, Lerner LS (1976) Perspectives: acute phencyclidine intoxication. Clin Toxicol 9:477-501.
9. Byrd LD, Standish LJ, Howell LL (1987) Behavioral effects of phencyclidine and ketamine alone and in combination with other drugs. Eur J Pharmacol 144:331-341.
10. Carboni E, Imperato A, Perezzani L, Di Chiara G (1989) Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats. Neuroscience 28:653-661.
11. Carlezon Jr WA, Wise RA (1996) Rewarding actions of phencyclidine and related drugs in nucleus accumbens shell and frontal cortex. J Neurosci 16:3112-3122.
12. Carlsson A, Svensson A, Carlsson ML (1993) Future strategies in the discovery of new antipsychotic agents: focus on dopamine-glutamate interactions. In: New generation of antipsychotic drugs: novel mechanisms of action, Vol 4 (Brunello N, Mendlewicz J, Racagni G, eds), pp 118-129. Basel: Basel.
13. Carlsson M, Carlsson A (1989) The NMDA antagonist MK-801 causes marked locomotor stimulation in monamine-depleted mice. J Neural Transm 75:221-226.
14. Castellani S, Adams PM (1981) Effects of dopaminergic drugs on phencyclidine-induced behavior in the rat. Neuropharmacology 20:371-374.
15. Davies BM, Beech DR (1960) The effect of the 1-arylcyclohexylamine (sernyl) on twelve normal volunteers. J Ment Sci 106:912-924.
16. Deuten AY, Tam S-Y, Freeman AS, Bowers Jr MB, Roth RH (1987) Mesolimbic and mesocortical dopamine activation induced by phencyclidine: contrasting pattern to striatal response. Eur J Pharmacol 134:257-264.
17. Doherty JD, Simonovic M, So R, Meltzer HY (1980) The effect of phencyclidine on dopamine synthesis and metabolism in rat striamm. Eur J Pharmacol 65:139-149.
18. Druhan JP, Rajabi H, Stewart J (1996) MK-801 increases locomotor activity without elevating extracellular dopamine levels in the nucleus accumbens. Synapse 24:135-146.
19. Filtz TM, Artymyshyn RP, Guan W, Molinoff PB (1993) Paradoxical regulation of dopamine receptors in transfected 293 cells. Mol Pharmacol 44:371-379.
20. Freed WJ, Weinberger DR, Bing LA, Wyatt RJ (1980) Neuropharmacological studies of phencyclidine (PCP)-induced behavioral stimulation in mice. Psychopharmacology 71:291-297.
21. Freeman J, Stanton M (1992) Medial prefrontal cortex lesions and spatial delayed alternation in the developing rat: recovery or sparing? Behav Neurosci 106:924-932.
22. French ED (1986) Effects of n-allyl normetazocine (SKF 10,047), phencyclidine and other psychomotor stimulants in the rat following 6-hydroxydopamine lesion of the ventral tegmental area. Neuropharmacology 25:447-450.
23. French ED (1994) Phencyclidine and the midbrain dopamine system: electrophysiology and behavior. Neurotoxicol Teratol 4:355-362.
24. Gleason SD, Shannon HE (1997) Blockade of phencyclidine-induced hyperlocomotion by olanzapine, clozapine and serotonin receptor subtype selective antagonists in mice. Psychopharmacology 129:79-84.
25. Goldman-Rakic PS (1996) Memory: recording experience in cells and circuits: diversity in memory research. Proc Natl Acad Sci USA 93:13435-13447.
26. Greenburg BD, Segal DS (1985) Acute and chronic behavioral interactions between phencyclidine (PCP) and amphetamine: evidence for a dopaminergic role in some PCP-induced behaviors. Pharmacol Biochem Behav 23:99-105.
27. Handelmann GE, Contreras PC, O'Donohue TL (1987) Selective memory impairment by phencyclidine in rats. Eur J Pharmacol 140:69-73.
28. Hauber W, Andersen R (1993) The non-NMDA glutamate receptor antagonist GYKI 52466 counteracts locomotor stimulation and anticataleptic activity induced by the NMDA antagonist dizocilpine. Naunyn-Schmiedeberg's Arch Pharmacol 348:486-490.
29. Hertel P, Mathe JM, Nomikos GG, Iurlo M, Mathe AA, Svensson TH (1996) Effects of D-amphetamine and phencyclidine on behavior and extracellular concentrations of neurotensin and dopamine in the ventral striatum and the medial prefrontal cortex of the rat. Behav Brain Res 72:103-114.
30. Hondo H, Yonezawa Y, Nakahara T, Nakamura K, Hirano M, Uchimura H, Tashiro N (1994) Effects of phencyclidine on dopamine release in the rat prefrontal cortex: an in vivo microdialysis study. Brain Res 633:337-342.
31. Hudzik TJ, Wenger GR (1993) Effects of drugs of abuse and cholinergic agents on delayed matching-to-sample responding in the squirrel monkey. J Pharmacol Exp Ther 265:120-127.
32. Hurd YL, Ungerstedt U (1989) Cocaine: an in vivo microdialysis evaluation of its acute action on dopamine transmission in rat striatum. Synapse 3:48-54.
33. Hutson PH, Hogg JE (1996) Effects of and interactions between antagonists for different sites on the NMDA receptor complex on hippocampal and striatal acetylcholine efflux in vivo. Eur J Pharmacol 295:45-52.
34. Iversen SD (1995) Interactions between excitatory amino acids and dopamine systems in the forebrain: implications for schizophrenia and Parkinson's disease. Behav Pharmacol 6:478-491.
35. Jackson DM, Johansson C, Lindgren LM, Bengtsson A (1994) Dopamine receptor antagonists block amphetamine and phencyclidine-induced motor stimulation in rats. Pharmacol Biochem Behav 48:465-471.
36. Javitt DC, Zukin SR (1991) Recent advances in the phencyclidine model of schizophrenia. Am J Psychiatry 148:1301-1308.
37. Javitt DC, Steinschneider M, Schroeder CE, Arezzo JC (1996) Role of cortical N-methyl-D-aspartate receptors in auditory sensory memory and mismatch negativity generation: implications for schizophrenia. Proc Natl Acad Sci USA 93:11962-11967.
38. Jedema HP, Moghaddam B (1996) Characterization of excitatory amino acid modulation of dopamine release in the prefrontal cortex of conscious rats. J Neurochem 66:1448-1453.
39. Jentsch JD, Redmond Jr DE, Elsworth JD, Taylor JR, Youngren KD, Roth RH (1997a) Enduring cognitive deficits and cortical dopamine dysfunction in monkeys after long-term administration of phencyclidine. Science 277:953-955.
40. Jentsch JD, Tran A, Le D, Youngren KD, Roth RH (1997b) Subchronic phencyclidine administration reduces mesoprefrontal dopamine utilization and impairs prefrontal cortical-dependent cognition in the rat. Neuropsychopharmacology 17:92-99.
41. Johnson KM, Jones SM (1990) Neuropharmacology of phencyclidine: basic mechanisms and therapeutic potential. Annu Rev Pharmacol Toxicol 30:707-750.
42. Jones KA, Wilding TJ, Huettner JE, Costa AM (1997) Desensitization of kainate receptors by kainate, glutamate and diastereomers of 4-methylglutamate. Neuropharmacology 36:853-863.
43. Karreman M, Westerink BHC, Moghaddam B (1996) Excitatory amino acid receptors in the ventral tegmental area regulate dopamine release in the ventral striatum. J Neurochem 67:601-607.
44. Keith VA, Mansbach RS, Geyer MA (1991) Failure of haloperidol to block the effects of phencyclidine and dizocilpine on prepulse inhibition of startle. Biol Psychiatry 30:557-566.
45. Kelley AE, Delfs JM (1994) Excitatory amino acid receptors mediate orafacial stereotypy elicited by dupaminergic stimulation of the ventro-lateral striatum. Neuroscience 60:85-95.
46. Kelly PH, Iversen SD (1976) Selective 6-OHDA-induced destruction of mesolimbic dopamine neurons: abolition of psychostimulant-induced locomotor activity in rats. Eur J Pharmacol 40:45-56.
47. Kiskin NI, Krishtal OA, Tsyndrenko AY (1986) Excitatory amino acid receptors in hippocampal neurons: kainate fails to desensitize them. Neurosci Lett 63:225-230.
48. Kitaichi K, Yamada K, Hasegawa T, Furukawa H, Nabeshima T (1994) Effects of risperidone on phencyclidine-induced behaviors: comparison with haloperidol and ritanserin. Jpn J Pharmacol 66:181-189.
49. Koob GF, Riley SJ, Smith SC, Robbins TW (1978) Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi and olfactory tubercle on feeding, locomotor activity, and amphetamine anorexia in the rat. J Comp Physiol Psychol 92:917-927.
50. Kornhuber J, Riederer P, Beckmann H (1990) The dopaminergic and glutamatergic systems in schizophrenia. In: Neuropsychopharmacology, pp 714-720. Berlin: Springer.
51. Krystal JH, Karper LP, Seibyl JP, Freeman GK, Delaney R, Bremner JD, Heninger GR, Bowers Jr MB, Charney DS (1994) Subanesthetic effects of the noncompetitive NMDA antagonist, ketamine, in humans. Arch Gen Psychiatry 51:199-214.
52. Krystal J, Karper L, Bennett A, Abi-Saab D, Souza C, Abi-Dargham A, Charney D (1995) Modulating ketamine-induced thought disorder with lorazepam and haloperidol in humans [abstract]. Schizophr Res 15:156.
53. Kuczenski R, Segal DS (1989) Concomitant characterization of behavioral and striatal neurotransmitter response to amphetamine using in vivo microdialysis. J Neurosci 9:2051-2065.
54. Kuczenski R, Melega WP, Cho AK, Segal DS (1997) Extracellular dopamine and amphetamine after systemic amphetamine administration: comparison to the behavioral response. J Pharm Exp Ther 282:591-596.
55. Laruelle M, Abi-Dargham A, van Dyck C, Gil R, D'Souza CD, Erdos J, McCane E, Rosenblatt W, Fingado C, Zoghbi S, Baldwin RM, Seibyl JP, Krystal JH, Charney DS, Innis RB (1996) SPECT imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proc Natl Acad Sci USA 93:9235-9240.
56. Lindefors N, Barati S, O'Connor WT (1997) Differential effects of single and repeated ketamine administration on dopamine, serotonin, and GABA transmission in rat medial prefrontal cortex. Brain Res 759:205-212.
57. Liu J, Moghaddam B (1995) Regulation of glutamate efflux by excitatory amino acid receptors: evidence for tonic inhibitory and phasic excitatory regulation. J Pharm Exp Ther 274:1209-1215.
58. Luby ED, Cohen BD, Rosenbaum G, Gottlieb JS, Kelley R (1959) Study of a new schizophrenomimetic drug - sernyl. Am Med Assoc Arch Neurol Psychiatry 81:363-369.
59. Malhotra AK, Pinals DA, Weingartner H, Sirocco K, Missar CD, Pickar D, Breier A (1996) NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology 14:301-307.
60. McCullough LD, Salamone JD (1992) Anxiogenic drugs beta-CCE and FG 7142 increase extracellular dopamine levels in nucleus accumbens. Psychopharmacology 109:379-382.
61. Moghaddam B, Bunney BS (1989) Differential effect of cocaine on extracellular dopamine levels in rat medial prefrontal cortex and nucleus accumbens: comparison to amphetamine. Synapse 4:156-161.
62. Moghaddam B, Adams B, Verma A, Daly D (1997) 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 17:2921-2927.
63. Ng GY, Varghese G, Chung HT, Trogadis J, Seeman P, O'Dowd BF, George SR (1997) Resistance of the dopamine D2L receptor to desensitization accompanies the up-regulation of receptors on the surface of Sf9 cells. Endocrinology 138:4199-4206.
64. Nishijima K, Kashiwa A, Hashimoto A, Iwama H, Umino A, Nishikawa T (1996) Differential effects of phencyclidine and methamphetamine on dopamine metabolism in rat frontal cortex and striatum as revealed by in vivo dialysis. Synapse 22:304-312.
65. Ogawa SI, Okuyama S, Araki H, Otomo S (1994) Effect of NE-100, a novel σ receptor ligand, on phencyclidine-induced cognitive dysfunction. Eur J Pharmacol 263:9-15.
66. Ogren SO, Goldstein M (1994) Phencyclidine and dizocilpine-induced hyperlocomotion are differentially mediated. Neuropsychopharmacology 11:167-177.
67. Olney JW, Farber NB (1995) Glutamate receptor dysfunction and schizophrenia. Arch Gen Psychiatry 52:998-1007.
68. Otis T, Zhang S, Trussell LO (1996) Direct measurement of AMPA receptor desensitization induced by glutamatergic synaptic transmission. J Neurosci 16:7496-7504.
69. Ouagazzal A, Nieoullon A, Amalric M (1994) Locomotor activation induced by MK-801 in the rat: postsynaptic interactions with dopamine receptors in the ventral striatum. Eur J Pharmacol 251:229-236.
70. Paxinos G, Watson C (1982) The rat brain in stereotaxic coordinates. New York: Academic.
71. Perry DC (1975) Pharm Chem Newsletter 4:9.
72. Sams-Dodd R (1996) Phencyclidine-induced stereotyped behaviour and social isolation in the rat: a possible animal model of schizophrenia. Behav Pharmacol 7:3-23.
73. Schlemmer Jr RF, Jackson JA, Preston KL, Bederka Jr JP, Garver DL, Davis JM (1978) Phencyclidine-induced stereotyped behavior in monkeys: antagonism by pimozide. Eur J Pharmacol 52:379-384.
74. Sesack SR, Hawrylak VA, Guido MA, Levey AI (1998) Dopamine axon varicosities in the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 18:2697-2708.
75. Sharp JW, Petersen DL, Langford MT (1995) DNQX inhibits phencyclidine (PCP) and ketamine induction of the hsp70 heat shock gene in the rat cingulate and retrosplenial cortex. Brain Res 687:114-124.
76. Simon H (1981) Dopaminergic A10 neurons and frontal system. J Physiol (Lond) 77:81-95.
77. 11C-raclopride in normal human subjects. Neuropsychopharmacology 18:18-25.
78. Steinpreis R (1996) The behavioral and neurochemical effects of phencyclidine in humans and animals: some implications for modeling psychosis. Behav Brain Res 74:45-55.
79. Steinpreis RE, Salamone JD (1993) The role of the nucleus accumbens dopamine in the neurochemical and behavioral effects of phencyclidine: a microdialysis and behavioral study. Brain Res 612:263-270.
80. Steinpreis RE, Sokolowski JD, Papanikolaou A, Salamone JD (1994) The effects of haloperidol and clozapine on PCP and amphetamine induced suppression of social behavior. Pharmacol Biochem Behav 47:579-585.
81. Sturgeon RD, Fessier RG, Meltzer HY (1979) Behavioral rating scales for assessing phencyclidine-induced locomotor activity, stereotyped behavior and ataxia in rats. Eur J Pharmacol 59:169-179.
82. Takahata R, Moghaddam B (1998) Glutamatergic regulation of basal and stimulus-activated dopamine release in the prefrontal cortex. J Neurochem, in press.
83. Timmerman W, Westerink BHC (1997) Brain microdialysis of GABA and glutamate: what does it signify? Synapse 27:242-261.
84. Verma A, Moghaddam B (1996) NMDA receptor antagonists impair prefrontal cortex function as assessed via spatial delayed alternation performance in rats: modulation by dopamine. J Neurosci 16:373-379.
85. Waters N, Lundgren C, Hansson LO, Carlsson ML (1996) Concurrent locomotor stimulation and decrease in dopamine release in rats and mice after treatment with the competitive NMDA receptor antagonists D-CPPene and CGS 19755. J Neural Transm 103:117-129.
86. Wedzony K, Golembiowska K, Zazula M (1994) Differential effects of CGP 37849 and MK-801, competitive and noncompetitive NMDA antagonists, with respect to the modulation of sensorimotor gating and dopamine outflow in the prefrontal cortex of rats. Naunyn-Schmiedeberg's Arch Pharmacol 350:555-562.
87. Wesierska M, Macias-Gonzalez R, Bures J (1990) Differential effect of ketamine on the reference and working memory versions of the Morris water maze task. Behav Neurosci 104:74-83.
88. Westerink BHC, Kwint HF, deVries JB (1996) The pharmacology of mesolimbic dopamine neurons: a dual-probe microdialysis study in the ventral tegmental area and nucleus accumbens of the rat brain. J Neurosci 16:2605-2611.
89. White F (1996) Synaptic regulation of mesocorticolimbic dopamine neurons, Annu Rev Neurosci 19:405-436.
90. Wilding TJ, Huettner JE (1997) Activation and desensitization of hippocampal kainate receptors. J Neurosci 17:2713-2721.
91. Williams SM, Goldman-Rakic PS (1993) Characterization of the dopaminergic innervation of the primate frontal cortex using a dopamine-specific antibody. Cereb Cortex 3:199-222.
92. Willins DL, Narayanan S, Wallace LJ, Uretsky NJ (1993) The role of dopamine and AMPA/kainate receptors in the nucleus accumbens in the hypermotility response to MK801. Pharmacol Biochem Behav 46:881-887.
93. Wilson FAW, O'Scalaidhe SP, Goldman-Rakic PS (1994) Functional synergism between putative γ-aminobutyrate-containing neurons and pyramidal neurons in prefrontal cortex. Proc Natl Acad Sci USA 91:4009-4013.
94. Zahrt J, Taylor JR, Mathew RG, Arnsten AFT (1997) Supranormal stimulation of D1 dopamine receptors in the rodent prefrontal cortex impairs spatial working memory performance. J Neurosci 17:8528-8535.