Ketamine increases striatal dopamine release and hyperlocomotion in adult rats after postnatal functional blockade of the prefrontal cortex

Behavioural Brain Research

Volumn 256, Issue , 2013, Pages 229-237

  Usun, Y ^a   Eybrard, S ^a   Meyer, F ^a   Louilot, A ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

Dopamine; Dorsal striatum; In vivo voltammetry; Ketamine; Neonatal functional blockade; Prefrontal cortex

Indexed keywords

GLUTAMATE RECEPTOR; KETAMINE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; TETRODOTOXIN; AMINO ACID RECEPTOR BLOCKING AGENT; DOPAMINE;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BRAIN DEVELOPMENT; BRAIN REGION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE RELEASE; DOPAMINERGIC ACTIVITY; DOPAMINERGIC TRANSMISSION; IN VIVO STUDY; LOCOMOTION; MALE; MENTAL DISEASE; MENTAL HEALTH; NERVE BLOCK; NERVE CONDUCTION; NONHUMAN; PERINATAL PERIOD; POTENTIOMETRY; PREFRONTAL CORTEX; PRIORITY JOURNAL; PSYCHOSIS; RAT; SCHIZOPHRENIA; ANIMAL; DOSE RESPONSE; DRUG EFFECTS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOTOR ACTIVITY; NEWBORN; PATHOPHYSIOLOGY; SPRAGUE DAWLEY RAT; TIME; TOXICITY;

ANIMALS; ANIMALS, NEWBORN; CORPUS STRIATUM; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; EXCITATORY AMINO ACID ANTAGONISTS; KETAMINE; MALE; MOTOR ACTIVITY; PREFRONTAL CORTEX; RATS, SPRAGUE-DAWLEY; SCHIZOPHRENIA; TETRODOTOXIN; TIME FACTORS;

EID: 84883305436     PISSN: 01664328     EISSN: 18727549     Source Type: Journal    
DOI: 10.1016/j.bbr.2013.08.017     Document Type: Article

References (89)

1. Lawrie S.M., Buechel C., Whalley H.C., Frith C.D., Friston K.J., Johnstone E.C. Reduced frontotemporal functional connectivity in schizophrenia associated with auditory hallucinations. Biological Psychiatry 2002, 51:1008-1011.
2. Stephan K.E., Friston K.J., Frith C.D. Dysconnection in schizophrenia: from abnormal synaptic plasticity to failures of self-monitoring. Schizophrenia Bulletin 2009, 35:509-527.
3. Garey L. When cortical development goes wrong: schizophrenia as a neurodevelopmental disease of microcircuits. Journal of Anatomy 2010, 217:324-333.
4. Yang Y., Fung S.J., Rothwell A., Tianmei S., Weickert C.S. Increased interstitial white matter neuron density in the dorsolateral prefrontal cortex of people with schizophrenia. Biological Psychiatry 2011, 69:63-70.
5. Nesvåg R., Bergmann Ø., Rimol L.M., Lange E.H., Haukvik U.K., Hartberg C.B., et al. A 5-year follow-up study of brain cortical and subcortical abnormalities in a schizophrenia cohort. Schizophrenia Research 2012, 142:209-216.
6. Palaniyappan L., Liddle P.F. Aberrant cortical gyrification in schizophrenia: a surface-based morphometry study. Journal of Psychiatry & Neuroscience 2012, 37:399-406.
7. Carlsson A., Waters N., Holm-Waters S., Tedroff J., Nilsson M., Carlsson M.L. Interactions between monoamines, glutamate, and GABA in schizophrenia: new evidence. Annual Review of Pharmacology and Toxicology 2001, 41:237-260.
8. Laruelle M., Frankle W.G., Narendran R., Kegeles L.S., Abi-Dargham A. Mechanism of action of antipsychotic drugs: from dopamine D(2) receptor antagonism to glutamate NMDA facilitation. Clinical Therapeutics 2005, 27(Suppl. A):S16-S24.
9. Kuepper R., Skinbjerg M., Abi-Dargham A. The dopamine dysfunction in schizophrenia revisited: new insights into topography and course. Handbook of Experimental Pharmacology 2012, 212:1-26.
10. Hietala J., Syvälahti E., Vuorio K., Räkköläinen V., Bergman J., Haaparanta M., et al. Presynaptic dopamine function in striatum of neuroleptic-naive schizophrenic patients. Lancet 1995, 346:1130-1131.
11. Hietala J., Syvälahti E., Vilkman H., Vuorio K., Räkköläinen V., Bergman J., et al. Depressive symptoms and presynaptic dopamine function in neuroleptic-naive schizophrenia. Schizophrenia Research 1999, 35:41-50.
12. Laruelle M., Abi-Dargham A., van Dyck C.H., Gil R., D'Souza C.D., Erdos J., et al. Single photon emission computerized tomography imaging of amphetamine-induced dopamine release in drug-free schizophrenic subjects. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:9235-9240.
13. Breier A., Su T.P., Saunders R., Carson R.E., Kolachana B.S., de Bartolomeis A., et al. Schizophrenia is associated with elevated amphetamine-induced synaptic dopamine concentrations: evidence from a novel positron emission tomography method. Proceedings of the National Academy of Sciences of the United States of America 1997, 94:2569-2574.
14. Dao-Castellana M.H., Paillère-Martinot M.L., Hantraye P., Attar-Lévy D., Rémy P., Crouzel C., et al. Presynaptic dopaminergic function in the striatum of schizophrenic patients. Schizophrenia Research 1997, 23:167-174.
15. Abi-Dargham A., Gil R., Krystal J., Baldwin R.M., Seibyl J.P., Bowers M., et al. Increased striatal dopamine transmission in schizophrenia: confirmation in a second cohort. The American Journal of Psychiatry 1998, 155:761-767.
16. Lindström L.H., Gefvert O., Hagberg G., Lundberg T., Bergström M., Hartvig P., et al. Increased dopamine synthesis rate in medial prefrontal cortex and striatum in schizophrenia indicated by l-(beta-11C) DOPA and PET. Biological Psychiatry 1999, 46:681-688.
17. Howes O.D., Montgomery A.J., Asselin M-C., Murray R.M., Grasby P.M., McGuire P.K. Molecular imaging studies of the striatal dopaminergic system in psychosis and predictions for the prodromal phase of psychosis. The British Journal of Psychiatry Supplement 2007, 51:s13-s18.
18. Kegeles L.S., Abi-Dargham A., Zea-Ponce Y., Rodenhiser-Hill J., Mann J.J., Van Heertum R.L., et al. Modulation of amphetamine-induced striatal dopamine release by ketamine in humans: implications for schizophrenia. Biological Psychiatry 2000, 48:627-640.
19. Stephan K.E., Baldeweg T., Friston K.J. Synaptic plasticity and dysconnection in schizophrenia. Biological Psychiatry 2006, 59:929-939.
20. Zhou Y., Liang M., Jiang T., Tian L., Liu Y., Liu Z., et al. Functional dysconnectivity of the dorsolateral prefrontal cortex in first-episode schizophrenia using resting-state fMRI. Neuroscience Letters 2007, 417:297-302.
21. Carlsson M.L., Carlsson A., Nilsson M. Schizophrenia: from dopamine to glutamate and back. Current Medicinal Chemistry 2004, 11:267-277.
22. Stone J.M., Morrison P.D., Pilowsky L.S. Glutamate and dopamine dysregulation in schizophrenia-a synthesis and selective review. Journal of Psychopharmacology 2007, 21:440-452.
23. Tost H., Meyer-Lindenberg A. Dopamine-glutamate interactions: a neural convergence mechanism of common schizophrenia risk variants. Biological Psychiatry 2011, 69:912-913.
24. 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. Archives of General Psychiatry 1994, 51:199-214.
25. Malhotra A.K., Pinals D.A., Weingartner H., Sirocco K., Missar C.D., Pickar D., et al. NMDA receptor function and human cognition: the effects of ketamine in healthy volunteers. Neuropsychopharmacology 1996, 14:301-307.
26. Newcomer J.W., Farber N.B., Jevtovic-Todorovic V., Selke G., Melson A.K., Hershey T., et al. Ketamine-induced NMDA receptor hypofunction as a model of memory impairment and psychosis. Neuropsychopharmacology 1999, 20:106-118.
27. Hetem L.A., Danion J.M., Diemunsch P., Brandt C. Effect of a subanesthetic dose of ketamine on memory and conscious awareness in healthy volunteers. Psychopharmacology 2000, 152:283-288.
28. Lahti A.C., Koffel B., LaPorte D., Tamminga C.A. Subanesthetic doses of ketamine stimulate psychosis in schizophrenia. Neuropsychopharmacology 1995, 13:9-19.
29. Malhotra A.K., Pinals D.A., Adler C.M., Elman I., Clifton A., Pickar D., et al. Ketamine-induced exacerbation of psychotic symptoms and cognitive impairment in neuroleptic-free schizophrenics. Neuropsychopharmacology 1997, 17:141-150.
30. Jentsch J.D., Roth R.H. The neuropsychopharmacology of phencyclidine: from NMDA receptor hypofunction to the dopamine hypothesis of schizophrenia. Neuropsychopharmacology 1999, 20:201-225.
31. Stevens M., Peigneur S., Tytgat J. Neurotoxins and their binding areas on voltage-gated sodium channels. Frontiers in Pharmacology 2011, 2:71.
32. Weinberger D.R., Lipska B.K. Cortical maldevelopment, anti-psychotic drugs, and schizophrenia: a search for common ground. Schizophrenia Research 1995, 16:87-110.
33. Fatemi S.H., Folsom T.D. The neurodevelopmental hypothesis of schizophrenia, revisited. Schizophrenia Bulletin 2009, 35:528-548.
34. Stryker M.P., Harris W.A. Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. Journal of Neuroscience 1986, 6:2117-2133.
35. Katz L.C., Shatz C.J. Synaptic activity and the construction of cortical circuits. Science 1996, 274:1133-1138.
36. Drakew A., Frotscher M., Heimrich B. Blockade of neuronal activity alters spine maturation of dentate granule cells but not their dendritic arborization. Neuroscience 1999, 94:767-774.
37. Hutchins B.I., Kalil K. Differential outgrowth of axons and their branches is regulated by localized calcium transients. Journal of Neuroscience 2008, 28:143-153.
38. Spitzer N.C. Electrical activity in early neuronal development. Nature 2006, 444:707-712.
39. Lipska B.K., Weinberger D.R. To model a psychiatric disorder in animals: schizophrenia as a reality test. Neuropsychopharmacology 2000, 23:223-239.
40. Geyer M.A., Moghaddam B. Animal models relevant to schizophrenia disorders. Neuropsychopharmacology: The fifth generation of progress 2001, 689-701. Lippincott Williams & Wilkins, Philadelphia. K.L. Davis, D. Charney, J.T. Coyle, C. Nemeroff (Eds.).
41. Zhuravin I.A., Bures J. Extent of the tetrodotoxin induced blockade examined by pupillary paralysis elicited by intracerebral injection of the drug. Experimental Brain Research 1991, 83:687-690.
42. Meyer F.F., Louilot A. Latent inhibition-related dopaminergic responses in the nucleus accumbens are disrupted following neonatal transient inactivation of the ventral subiculum. Neuropsychopharmacology 2011, 36:1421-1432.
43. Meyer F., Louilot A. Early prefrontal functional blockade in rats results in schizophrenia-related anomalies in behavior and dopamine. Neuropsychopharmacology 2012, 37:2233-2243.
44. Malpeli J.G. Reversible inactivation of subcortical sites by drug injection. Journal of Neuroscience Methods 1999, 86:119-128.
45. Rothfeld J.M., Harlan R.E., Shivers B.D., Pfaff D.W. Reversible disruption of lordosis via midbrain infusions of procaine and tetrodotoxin. Pharmacology, Biochemistry, and Behavior 1986, 25:857-863.
46. Sierra-Mercado D., Corcoran K.A., Lebron-Milad K., Quirk G.J. Inactivation of the ventromedial prefrontal cortex reduces expression of conditioned fear and impairs subsequent recall of extinction. European Journal of Neuroscience 2006, 24:1751-1758.
47. Martin J.H., Ghez C. Differential impairments in reaching and grasping produced by local inactivation within the forelimb representation of the motor cortex in the cat. Experimental Brain Research 1993, 94:429-443.
48. Louilot A., Serrano A., D'Angio M. A novel carbon fiber implantation assembly for cerebral voltammetric measurements in freely moving rats. Physiology & Behavior 1987, 41:227-231.
49. Paxinos G., Watson C. The rat brain in stereotaxic coordinates, compact 2009, Academic Press, New York. 6th edn.
50. Castagné V., Wolinsky T., Quinn L., Virley D. Differential behavioral profiling of stimulant substances in the rat using the LABORAS® system. Pharmacology, Biochemistry, and Behavior 2012, 101:553-563.
51. Imre G., Fokkema D.S., Den Boer J.A., Ter Horst G.J. Dose-response characteristics of ketamine effect on locomotion, cognitive function and central neuronal activity. Brain Research Bulletin 2006, 69:338-345.
52. Gonzalez-Mora J.L., Guadalupe T., Fumero B., Mas M. Mathematical resolution of mixed in vivo voltammetry signals. Models, equipment, assessment by simultaneous microdialysis sampling. Journal of Neuroscience Methods 1991, 39:231-244.
53. Peterschmitt Y., Meyer F., Louilot A. Neonatal functional blockade of the entorhinal cortex results in disruption of accumbal dopaminergic responses observed in latent inhibition paradigm in adult rats. European Journal of Neuroscience 2007, 25:2504-2513.
54. Meyer F., Peterschmitt Y., Louilot A. Postnatal functional inactivation of the entorhinal cortex or ventral subiculum has different consequences for latent inhibition-related striatal dopaminergic responses in adult rats. European Journal of Neuroscience 2009, 29:2035-2048.
55. Rosenthal R., Rosnow R.L. Contrast analysis, focused comparisons in the analysis of variance 1985, Cambridge University Press, Cambridge.
56. Rosenthal R., Rosnow R.L., Rubin D.B. Contrasts and effect sizes in behavioral research 2000, Cambridge University Press, New York.
57. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1998, Academic Press, San Diego. 4th edn.
58. Hunt M.J., Raynaud B., Garcia R. Ketamine dose-dependently induces high-frequency oscillations in the nucleus accumbens in freely moving rats. Biological Psychiatry 2006, 60:1206-1214.
59. Hakami T., Jones N.C., Tolmacheva E.A., Gaudias J., Chaumont J., Salzberg M., et al. NMDA receptor hypofunction leads to generalized and persistent aberrant gamma oscillations independent of hyperlocomotion and the state of consciousness. PLoS ONE 2009, 4:e6755.
60. Nicolás M.J., López-Azcárate J., Valencia M., Alegre M., Pérez-Alcázar M., Iriarte J., et al. Ketamine-induced oscillations in the motor circuit of the rat basal ganglia. PLoS ONE 2011, 6:e21814.
61. Phillips K.G., Cotel M.C., McCarthy A.P., Edgar D.M., Tricklebank M., O'Neill M.J., et al. Differential effects of NMDA antagonists on high frequency and gamma EEG oscillations in a neurodevelopmental model of schizophrenia. Neuropharmacology 2012, 62:1359-1370.
62. Carboni E., Imperato A., Perezzani L., Di Chiara G. Amphetamine, cocaine, phencyclidine and nomifensine increase extracellular dopamine concentrations preferentially in the nucleus accumbens of freely moving rats. Neuroscience 1989, 28:653-661.
63. Irifune M., Shimizu T., Nomoto M. Ketamine-induced hyperlocomotion associated with alteration of presynaptic components of dopamine neurons in the nucleus accumbens of mice. Pharmacology, Biochemistry, and Behavior 1991, 40:399-407.
64. Littlewood C.L., Jones N., O'Neill M.J., Mitchell S.N., Tricklebank M., Williams S.C.R. Mapping the central effects of ketamine in the rat using pharmacological MRI. Psychopharmacology 2006, 186:64-81.
65. Matulewicz P., Kasicki S., Hunt M.J. The effect of dopamine receptor blockade in the rodent nucleus accumbens on local field potential oscillations and motor activity in response to ketamine. Brain Research 2010, 1366:226-232.
66. Hertel P., Mathé J.M., Nomikos G.G., Iurlo M., Mathé A.A., Svensson T.H. 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. Behavioural Brain Research 1995, 72:103-114.
67. Monaghan D.T., Cotman C.W. Distribution of N-methyl-d-aspartate-sensitive l-[3H]glutamate-binding sites in rat brain. Journal of Neuroscience 1985, 5:2909-2919.
68. McGeorge A.J., Faull R.L. The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience 1989, 29:503-537.
69. Fonnum F., Storm-Mathisen J., Divac I. Biochemical evidence for glutamate as neurotransmitter in corticostriatal and corticothalamic fibres in rat brain. Neuroscience 1981, 6:863-873.
70. Hassler R., Haug P., Nitsch C., Kim J.S., Paik K. Effect of motor and premotor cortex ablation on concentrations of amino acids, monoamines, and acetylcholine and on the ultrastructure in rat striatum. A confirmation of glutamate as the specific cortico-striatal transmitter. Journal of Neurochemistry 1982, 38:1087-1098.
71. Krebs M.O., Trovero F., Desban M., Gauchy C., Glowinski J., Kemel M.L. Distinct presynaptic regulation of dopamine release through NMDA receptors in striosome- and matrix-enriched areas of the rat striatum. Journal of Neuroscience 1991, 11:1256-1262.
72. Hernandez L.F., Segovia G., Mora F. Effects of activation of NMDA and AMPA glutamate receptors on the extracellular concentrations of dopamine, acetylcholine, and GABA in striatum of the awake rat: a microdialysis study. Neurochemical Research 2003, 28:1819-1827.
73. Carlsson A., Hansson L.O., Waters N., Carlsson M.L. A glutamatergic deficiency model of schizophrenia. The British Journal of Psychiatry Supplement 1999, 37:2-6.
74. Keita H., Lecharny J.B., Henzel D., Desmonts J.M., Mantz J. Is inhibition of dopamine uptake relevant to the hypnotic action of i.v. anaesthetics?. British Journal of Anaesthesia 1996, 77:254-256.
75. Nishimura M., Sato K., Okada T., Yoshiya I., Schloss P., Shimada S., et al. Ketamine inhibits monoamine transporters expressed in human embryonic kidney 293 cells. Anesthesiology 1998, 88:768-774.
76. Berendse H.W., Galis-de Graaf Y., Groenewegen H.J. Topographical organization and relationship with ventral striatal compartments of prefrontal corticostriatal projections in the rat. Journal of Comparative Neurology 1992, 316:314-347.
77. Groenewegen H.J., Wright C.I., Uylings H.B. The anatomical relationships of the prefrontal cortex with limbic structures and the basal ganglia. Journal of Psychopharmacology 1997, 11:99-106.
78. Heidbreder Ca, Groenewegen H.J. The medial prefrontal cortex in the rat: evidence for a dorso-ventral distinction based upon functional and anatomical characteristics. Neuroscience & Biobehavioral Reviews 2003, 27:555-579.
79. Voorn P., Vanderschuren L.J.M.J., Groenewegen H.J., Robbins T.W., Pennartz C.M.A. Putting a spin on the dorsal-ventral divide of the striatum. Trends in Neurosciences 2004, 27:468-474.
80. Van Eden C.G., Uylings H.B. Cytoarchitectonic development of the prefrontal cortex in the rat. Journal of Comparative Neurology 1985, 241:253-267.
81. van Eden C.G., Kros J.M., Uylings H.B. The development of the rat prefrontal cortex. Its size and development of connections with thalamus, spinal cord and other cortical areas. Progress in Brain Research 1990, 85:169-183.
82. Demerens C., Stankoff B., Logak M., Anglade P., Allinquant B., Couraud F., et al. Induction of myelination in the central nervous system by electrical activity. Proceedings of the National Academy of Sciences of the United States of America 1996, 93:9887-9892.
83. Schneider M., Koch M. Behavioral and morphological alterations following neonatal excitotoxic lesions of the medial prefrontal cortex in rats. Experimental Neurology 2005, 195:185-198.
84. Klein S., Koch M., Schwabe K. Neuroanatomical changes in the adult rat brain after neonatal lesion of the medial prefrontal cortex. Experimental Neurology 2008, 209:199-212.
85. Kiyosue K., Hiyama T.Y., Nakayama K., Kasai M., Taguchi T. Re-expression of NR2B-containing NMDA receptors in vitro by suppression of neuronal activity. International Journal of Developmental Neuroscience 2004, 22:59-65.
86. Rodríguez-Paz J.M., Anantharam V., Treistman S.N. Block of the N-methyl-d-aspartate receptor by phencyclidine-like drugs is influenced by alternative splicing. Neuroscience Letters 1995, 190:147-150.
87. El-Rawas R., Saadé N.E., Thiriet N., Atweh S., Jaber M., Al-Amin H.A. Developmental changes in the mRNA expression of neuropeptides and dopamine and glutamate receptors in neonates and adult rats after ventral hippocampal lesion. Schizophrenia Research 2009, 113:298-307.
88. Kantrowitz J.T., Javitt D.C. N-methyl-d-aspartate (NMDA) receptor dysfunction or dysregulation: the final common pathway on the road to schizophrenia. Brain Research Bulletin 2010, 83:108-121.
89. Vollenweider F.X., Vontobel P., Oye I., Hell D., Leenders K.L. Effects of (S)-ketamine on striatal dopamine: a [11C]raclopride PET study of a model psychosis in humans. Journal of Psychiatric Research 2000, 34:35-43.