Synergistic interaction of dopamine D1 and glutamate N-methyl-d-aspartate receptors in the rat dorsal striatum controls attention

Neuroscience

Volumn 185, Issue , 2011, Pages 39-49

  Agnoli, L ^a   Carli, M ^a  

^a MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

5 CSRT task; Attention; D1 receptors; Dorsomedial striatum; NMDA receptors

Indexed keywords

DOPAMINE 1 RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ACCURACY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DENDRITIC SPINE; MALE; MENTAL PERFORMANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; RECEPTOR BLOCKING; REINFORCEMENT; SELECTIVE ATTENTION; STIMULUS RESPONSE; TASK PERFORMANCE; VISUAL DISCRIMINATION;

ANALYSIS OF VARIANCE; ANIMALS; ATTENTION; BENZAZEPINES; CORPUS STRIATUM; DISCRIMINATION (PSYCHOLOGY); DOPAMINE ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; EXCITATORY AMINO ACID ANTAGONISTS; MALE; PHOTIC STIMULATION; PIPERAZINES; RATS; REACTION TIME; RECEPTORS, DOPAMINE D1; RECEPTORS, N-METHYL-D-ASPARTATE;

EID: 79956275091     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.04.044     Document Type: Article

References (87)

1. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986, 9:357-381.
2. Amalric M., Ouagazzal A., Baunez C., Nieoullon A. Functional interactions between glutamate and dopamine in the rat striatum. Neurochem Int 1994, 25:123-131.
3. Anden N.E., Hfuxe K., Hamberger B., Hokfelt T. A quantitative study on the nigro-neostriatal dopamine neuron system in the rat. Acta Physiol Scand 1966, 67:306-312.
4. Baldwin A.E., Sadeghian K., Kelley A.E. Appetitive instrumental learning requires coincident activation of NMDA and dopamine D1 receptors within the medial prefrontal cortex. J Neurosci 2002, 22:1063-1071.
5. Baunez C., Robbins T.W. Effects of dopamine depletion of the dorsal striatum and further interaction with subthalamic nucleus lesions in an attentional task in the rat. Neuroscience 1999, 92:1343-1356.
6. Baviera M., Invernizzi R.W., Carli M. Haloperidol and clozapine have dissociable effects in a model of attentional performance deficits induced by blockade of NMDA receptors in the mPFC. Psychopharmacology (Berl) 2008, 196:269-280.
7. Cagniard B., Beeler J.A., Britt J.P., McGehee D.S., Marinelli M., Zhuang X. Dopamine scales performance in the absence of new learning. Neuron 2006, 51:541-547.
8. Carli M. Serotonergic modulation of attentional processes in the rat prefrontal cortex. Life science 2006, 123-147. Open University, London, UK.
9. Carli M., Robbins T.W., Evenden J.L., Everitt B.J. Effects of lesions to ascending noradrenergic neurones on performance of a 5-choice serial reaction task in rats; implications for theories of dorsal noradrenergic bundle function based on selective attention and arousal. Behav Brain Res 1983, 9:361-380.
10. Carli M., Samanin R. Serotonin2 receptor agonists and serotonergic anorectic drugs affect rats' performance differently in a five-choice serial reaction time task. Psychopharmacology 1992, 106:228-234.
11. Cepeda C., Buchwald N.A., Levine M.S. Neuromodulatory actions of dopamine in the neostriatum are dependent upon the excitatory amino acid receptor subtypes activated. Proc Natl Acad Sci U S A 1993, 90:9576-9580.
12. Cepeda C., Colwell C.S., Itri J.N., Chandler S.H., Levine M.S. Dopaminergic modulation of NMDA-induced whole cell currents in neostriatal neurons in slices: contribution of calcium conductances. J Neurophysiol 1998, 79:82-94.
13. Cepeda C., Levine M.S. Where do you think you are going?. The NMDA-D1 receptor trap. Sci STKE 2006, 2006:pe20.
14. Chase T.N., Oh J.D. Striatal dopamine- and glutamate-mediated dysregulation in experimental parkinsonism. Trends Neurosci 2000, 23:S86-S91.
15. Choi W.Y., Balsam P.D., Horvitz J.C. Extended habit training reduces dopamine mediation of appetitive response expression. J Neurosci 2005, 25:6729-6733.
16. Christakou A., Robbins T.W., Everitt B.J. Functional disconnection of a prefrontal cortical-dorsal striatal system disrupts choice reaction time performance: implications for attentional function. Behav Neurosci 2001, 115:812-825.
17. Christakou A., Robbins T.W., Everitt B.J. Prefrontal cortical-ventral striatal interactions involved in affective modulation of attentional performance: implications for corticostriatal circuit function. J Neurosci 2004, 24:773-780.
18. Christakou A., Robbins T.W., Everitt B.J. Prolonged neglect following unilateral disruption of a prefrontal cortical-dorsal striatal system. Eur J Neurosci 2005, 21:782-792.
19. Chudasama Y., Passetti F., Rhodes S.E., Lopian D., Desai A., Robbins T.W. Dissociable aspects of performance on the 5-choice serial reaction time task following lesions of the dorsal anterior cingulate, infralimbic and orbitofrontal cortex in the rat: differential effects on selectivity, impulsivity and compulsivity. Behav Brain Res 2003, 146:105-119.
20. Chudasama Y., Robbins T.W. Dopaminergic modulation of visual attention and working memory in the rodent prefrontal cortex. Neuropsychopharmacology 2004, 29:1628-1636.
21. Chudasama Y., Robbins T.W. Functions of frontostriatal systems in cognition: comparative neuropsychopharmacological studies in rats, monkeys and humans. Biol Psychol 2006, 73:19-38.
22. Cole B.J., Robbins T.W. Effects of 6-hydroxydopamine lesions of the nucleus accumbens septi on performance of a 5-choice serial reaction time task in rats: implications for theories of selective attention and arousal. Behav Brain Res 1989, 33:165-179.
23. Cools R., Barker R.A., Sahakian B.J., Robbins T.W. Mechanisms of cognitive set flexibility in Parkinson's disease. Brain 2001, 124:2503-2512.
24. Cools R., Rogers R., Barker R.A., Robbins T.W. Top-down attentional control in Parkinson's disease: salient considerations. J Cogn Neurosci 2010, 22:848-859.
25. Cools R., Stefanova E., Barker R.A., Robbins T.W., Owen A.M. Dopaminergic modulation of high-level cognition in Parkinson's disease: the role of the prefrontal cortex revealed by PET. Brain 2002, 125:584-594.
26. Corbetta M., Miezin F.M., Dobmeyer S., Shulman G.L., Petersen S.E. Selective and divided attention during visual discriminations of shape, color, and speed: functional anatomy by positron emission tomography. J Neurosci 1991, 11:2383-2402.
27. Dagher A., Owen A.M., Boecker H., Brooks D.J. The role of the striatum and hippocampus in planning: a PET activation study in Parkinson's disease. Brain 2001, 124:1020-1032.
28. Dalley J.W., Everitt B.J., Robbins T.W. Impulsivity, compulsivity, and top-down cognitive control. Neuron 2011, 69:680-694.
29. David H.N., Ansseau M., Abraini J.H. Dopamine-glutamate reciprocal modulation of release and motor responses in the rat caudate-putamen and nucleus accumbens of "intact" animals. Brain Res Brain Res Rev 2005, 50:336-360.
30. Di Chiara G., Morelli M., Consolo S. Modulatory functions of neurotransmitters in the striatum: ACh/dopamine/NMDA interactions. Trends Neurosci 1994, 17:228-233.
31. Evenden J.L. Varieties of impulsivity. Psychopharmacology (Berl) 1999, 146:348-361.
32. Ferretti V., Florian C., Costantini V.J., Roullet P., Rinaldi A., De Leonibus E., Oliverio A., Mele A. Co-activation of glutamate and dopamine receptors within the nucleus accumbens is required for spatial memory consolidation in mice. Psychopharmacology (Berl) 2005, 179:108-116.
33. Flores-Hernandez J., Cepeda C., Hernandez-Echeagaray E., Calvert C.R., Jokel E.S., Fienberg A.A., Greengard P., Levine M.S. Dopamine enhancement of NMDA currents in dissociated medium-sized striatal neurons: role of D1 receptors and DARPP-32. J Neurophysiol 2002, 88:3010-3020.
34. Fonnum F. Glutamate: a neurotransmitter in mammalian brain. J Neurochem 1984, 42:1-11.
35. Gabbott P.L., Warner T.A., Jays P.R., Salway P., Busby S.J. Prefrontal cortex in the rat: projections to subcortical autonomic, motor, and limbic centers. J Comp Neurol 2005, 492:145-177.
36. Goldman-Rakic P.S., Selemon L.D. Topography of corticostriatal projections in nonhuman primates and implications for functional parcelletion of the neostriatum. Cerebral Cortex 1986, 447-466. Plenum Press, New York. E.G. Jones, A. Peters (Eds.).
37. Goto Y., Grace A.A. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 2005, 8:805-812.
38. Granon S., Passetti F., Thomas K.L., Dalley J.W., Everitt B.J., Robbins T.W. Enhanced and impaired attentional performance after infusion of D1 dopaminergic receptor agents into rat prefrontal cortex. J Neurosci 2000, 20:1208-1215.
39. Graybiel A.M. The basal ganglia. Trends Neurosci 1995, 18:60-62.
40. Greco B., Lopez S., van der Putten H., Flor P.J., Amalric M. Metabotropic glutamate 7 receptor subtype modulates motor symptoms in rodent models of Parkinson's disease. J Pharmacol Exp Ther 2010, 332:1064-1071.
41. Haber S.N., Fudge J.L., McFarland N.R. Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 2000, 20:2369-2382.
42. Haluk D.M., Floresco S.B. Ventral striatal dopamine modulation of different forms of behavioral flexibility. Neuropsychopharmacology 2009, 34:2041-2052.
43. Hersch S.M., Ciliax B.J., Gutekunst C.A., Rees H.D., Heilman C.J., Yung K.K., Bolam J.P., Ince E., Yi H., Levey A.I. Electron microscopic analysis of D1 and D2 dopamine receptor proteins in the dorsal striatum and their synaptic relationships with motor corticostriatal afferents. J Neurosci 1995, 15:5222-5237.
44. Honey G.D., Suckling J., Zelaya F., Long C., Routledge C., Jackson S., Ng V., Fletcher P.C., Williams S.C., Brown J., Bullmore E.T. Dopaminergic drug effects on physiological connectivity in a human cortico-striato-thalamic system. Brain 2003, 126:1767-1781.
45. Kiyatkin E.A., Rebec G.V. Dopaminergic modulation of glutamate-induced excitations of neurons in the neostriatum and nucleus accumbens of awake, unrestrained rats. J Neurophysiol 1996, 75:142-153.
46. Kolb B. Functions of the frontal cortex of the rat: a comparative review. Brain Res 1984, 320:65-98.
47. Kreipke C.W., Walker P.D. NMDA receptor blockade attenuates locomotion elicited by intrastriatal dopamine D1-receptor stimulation. Synapse 2004, 53:28-35.
48. Lawrence A.D., Sahakian B.J., Hodges J.R., Rosser A.E., Lange K.W., Robbins T.W. Executive and mnemonic functions in early Huntington's disease. Brain 1996, 119(Pt 5):1633-1645.
49. Lee F.J., Xue S., Pei L., Vukusic B., Chery N., Wang Y., Wang Y.T., Niznik H.B., Yu X.M., Liu F. Dual regulation of NMDA receptor functions by direct protein-protein interactions with the dopamine D1 receptor. Cell 2002, 111:219-230.
50. Lehmann J., Schneider J., McPherson S., Murphy D.E., Bernard P., Tsai C., Bennett D.A., Pastor G., Steel D.J., Boehm C., et al. CPP, a selective N-methyl-d-aspartate (NMDA)-type receptor antagonist: characterization in vitro and in vivo. J Pharmacol Exp Ther 1987, 240:737-746.
51. Levine M.S., Altemus K.L., Cepeda C., Cromwell H.C., Crawford C., Ariano M.A., Drago J., Sibley D.R., Westphal H. Modulatory actions of dopamine on NMDA receptor-mediated responses are reduced in D1A-deficient mutant mice. J Neurosci 1996, 16:5870-5882.
52. Lewis S.J., Dove A., Robbins T.W., Barker R.A., Owen A.M. Cognitive impairments in early Parkinson's disease are accompanied by reductions in activity in frontostriatal neural circuitry. J Neurosci 2003, 23:6351-6356.
53. Lopez S., Turle-Lorenzo N., Acher F., De Leonibus E., Mele A., Amalric M. Targeting group III metabotropic glutamate receptors produces complex behavioral effects in rodent models of Parkinson's disease. J Neurosci 2007, 27:6701-6711.
54. McPherson R.J., Marshall J.F. Intrastriatal AP5 differentially affects behaviors induced by local infusions of D1 vs. D2 dopamine agonists. Brain Res 1996, 739:19-25.
55. Mirjana C., Baviera M., Invernizzi R.W., Balducci C. The serotonin 5-HT2A receptors antagonist M100907 prevents impairment in attentional performance by NMDA receptor blockade in the rat prefrontal cortex. Neuropsychopharmacology 2004, 29:1637-1647.
56. Missale C., Nash S.R., Robinson S.W., Jaber M., Caron M.G. Dopamine receptors: from structure to function. Physiol Rev 1998, 78:189-225.
57. Monchi O., Petrides M., Mejia-Constain B., Strafella A.P. Cortical activity in Parkinson's disease during executive processing depends on striatal involvement. Brain 2007, 130:233-244.
58. Muir J.L., Everitt B.J., Robbins T.W. The cerebral cortex of the rat and visual attentional function: dissociable effects of mediofrontal, cingulate, anterior dorsolateral, and parietal cortex lesions on a five-choice serial reaction time task. Cereb Cortex 1996, 6:470-481.
59. Nagano-Saito A., Leyton M., Monchi O., Goldberg Y.K., He Y., Dagher A. Dopamine depletion impairs frontostriatal functional connectivity during a set-shifting task. J Neurosci 2008, 28:3697-3706.
60. Nakamura K., Kurasawa M., Shirane M. Impulsivity and AMPA receptors: aniracetam ameliorates impulsive behavior induced by a blockade of AMPA receptors in rats. Brain Res 2000, 862:266-269.
61. O'Donnell P. Dopamine gating of forebrain neural ensembles. Eur J Neurosci 2003, 17:429-435.
62. O'Donnell P., Grace A.A. Phencyclidine interferes with the hippocampal gating of nucleus accumbens neuronal activity in vivo. Neuroscience 1998, 87:823-830.
63. Owen A.M., James M., Leigh P.N., Summers B.A., Marsden C.D., Quinn N.P., Lange K.W., Robbins T.W. Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 1992, 115(Pt 6):1727-1751.
64. Passetti F., Chudasama Y., Robbins T.W. The frontal cortex of the rat and visual attentional performance: dissociable functions of distinct medial prefrontal subregions. Cereb Cortex 2002, 12:1254-1268.
65. Pattij T., Janssen M.C., Vanderschuren L.J., Schoffelmeer A.N., van Gaalen M.M. Involvement of dopamine D1 and D2 receptors in the nucleus accumbens core and shell in inhibitory response control. Psychopharmacology (Berl) 2007, 191:587-598.
66. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1982, Academic Press, Sidney.
67. Pennartz C.M., Groenewegen H.J., Lopes da Silva F.H. The nucleus accumbens as a complex of functionally distinct neuronal ensembles: an integration of behavioural, electrophysiological and anatomical data. Prog Neurobiol 1994, 42:719-761.
68. Pezze M.A., Dalley J.W., Robbins T.W. Differential roles of dopamine D1 and D2 receptors in the nucleus accumbens in attentional performance on the five-choice serial reaction time task. Neuropsychopharmacology 2007, 32:273-283.
69. Ragozzino M.E. The effects of dopamine D(1) receptor blockade in the prelimbic-infralimbic areas on behavioral flexibility. Learn Mem 2002, 9:18-28.
70. Redgrave P., Gurney K. The short-latency dopamine signal: a role in discovering novel actions?. Nat Rev Neurosci 2006, 7:967-975.
71. Reep R.L., Cheatwood J.L., Corwin J.V. The associative striatum: organization of cortical projections to the dorsocentral striatum in rats. J Comp Neurol 2003, 467:271-292.
72. Robbins T.W. The 5-choice serial reaction time task: behavioural pharmacology and functional neurochemistry. Psychopharmacology (Berl) 2002, 163:362-380.
73. Robbins T.W., Granon S., Muir J.L., Durantou F., Harrison A., Everitt B.J. Neural systems underlying arousal and attention. Implications for drug abuse. Ann N Y Acad Sci 1998, 846:222-237.
74. Roberts A.C., De Salvia M.A., Wilkinson L.S., Collins P., Muir J.L., Everitt B.J., Robbins T.W. 6-Hydroxydopamine lesions of the prefrontal cortex in monkeys enhance performance on an analog of the Wisconsin Card Sort Test: possible interactions with subcortical dopamine. J Neurosci 1994, 14:2531-2544.
75. Rogers R.D., Baunez C., Everitt B.J., Robbins T.W. Lesions of the medial and lateral striatum in the rat produce differential deficits in attentional performance. Behav Neurosci 2001, 115:799-811.
76. Sadikot A.F., Parent A., Smith Y., Bolam J.P. Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a light and electron microscopic study of the thalamostriatal projection in relation to striatal heterogeneity. J Comp Neurol 1992, 320:228-242.
77. Schultz W., Dayan P., Montague P.R. A neural substrate of prediction and reward. Science 1997, 275:1593-1599.
78. Scott L., Kruse M.S., Forssberg H., Brismar H., Greengard P., Aperia A. Selective up-regulation of dopamine D1 receptors in dendritic spines by NMDA receptor activation. Proc Natl Acad Sci U S A 2002, 99:1661-1664.
79. Smith Y., Bevan M.D., Shink E., Bolam J.P. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 1998, 86:353-387.
80. Smith-Roe S.L., Kelley A.E. Coincident activation of NMDA and dopamine D1 receptors within the nucleus accumbens core is required for appetitive instrumental learning. J Neurosci 2000, 20:7737-7742.
81. Sprengelmeyer R., Lange H., Homberg V. The pattern of attentional deficits in Huntington's disease. Brain 1995, 118(Pt 1):145-152.
82. Taverna S., Canciani B., Pennartz C.M. Dopamine D1-receptors modulate lateral inhibition between principal cells of the nucleus accumbens. J Neurophysiol 2005, 93:1816-1819.
83. van Schouwenburg M.R., den Ouden H.E., Cools R. The human basal ganglia modulate frontal-posterior connectivity during attention shifting. J Neurosci 2010, 30:9910-9918.
84. Vertes R.P. Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 2004, 51:32-58.
85. West A.R., Grace A.A. Opposite influences of endogenous dopamine D1 and D2 receptor activation on activity states and electrophysiological properties of striatal neurons: studies combining in vivo intracellular recordings and reverse microdialysis. J Neurosci 2002, 22:294-304.
86. Williams D., Tijssen M., Van Bruggen G., Bosch A., Insola A., Di Lazzaro V., Mazzone P., Oliviero A., Quartarone A., Speelman H., Brown P. Dopamine-dependent changes in the functional connectivity between basal ganglia and cerebral cortex in humans. Brain 2002, 125:1558-1569.
87. Zweifel L.S., Parker J.G., Lobb C.J., Rainwater A., Wall V.Z., Fadok J.P., Darvas M., Kim M.J., Mizumori S.J., Paladini C.A., Phillips P.E., Palmiter R.D. Disruption of NMDAR-dependent burst firing by dopamine neurons provides selective assessment of phasic dopamine-dependent behavior. Proc Natl Acad Sci U S A 2009, 106:7281-7288.