Extrastriatal D2-like receptors modulate basal ganglia pathways in normal and parkinsonian monkeys

Journal of Neurophysiology

Volumn 107, Issue 5, 2012, Pages 1500-1512

  Hadipour Niktarash, Arash ^a,c   Rommelfanger, Karen S ^a   Masilamoni, Gunasingh J ^a   Smith, Yoland ^a,b   Wichmann, Thomas ^a,b  

^a EMORY UNIVERSITY   (United States)

^b EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF CHICAGO MEDICAL CENTER   (United States)

Author keywords

Dopamine; Globus pallidus; Parkinsonism; Substantia nigra

Indexed keywords

1,2,3,6 TETRAHYDRO 1 METHYL 4 PHENYLPYRIDINE; DOPAMINE 2 LIKE RECEPTOR; DOPAMINE 2 RECEPTOR; QUINPIROLE; SULPIRIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTROPHYSIOLOGY; EXPERIMENTAL MONKEY; EXTERNAL SEGMENT OF THE GLOBUS PALLIDUS; GABAERGIC SYSTEM; GLOBUS PALLIDUS; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN VIVO STUDY; INTERNAL SEGMENT OF THE GLOBUS PALLIDUS; NEUROMODULATION; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; SUBSTANTIA NIGRA PARS RETICULATA;

ANIMALS; BASAL GANGLIA; CORPUS STRIATUM; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; MACACA MULATTA; NEURAL PATHWAYS; PARKINSONIAN DISORDERS; RECEPTORS, DOPAMINE D2;

EID: 84857286244     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00348.2011     Document Type: Article

References (86)

1. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders. Trends Neurosci 12: 366-375, 1989.
2. Aldridge JW, Gilman S. The temporal structure of spike trains in the primate basal ganglia: afferent regulation of bursting demonstrated with precentral cerebral cortical ablation. Brain Res 543: 123-138, 1991.
3. Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13: 266-271, 1990.
4. Ariano MA, Wang J, Noblett KL, Larson ER, Sibley DR. Cellular distribution of the rat D4 dopamine receptor protein in the CNS using antireceptor antisera. Brain Res 752: 26-34, 1997.
5. Arsenault MY, Parent A, Seguela P, Descarries L. Distribution and morphological characteristics of dopamine-immunoreactive neurons in the midbrain of the squirrel monkey (Saimiri sciureus). J Comp Neurol 267: 489-506, 1988.
6. Baron MS, Wichmann T, Ma D, DeLong MR. Effects of transient focal inactivation of the basal ganglia in parkinsonian primates. J Neurosci 22: 592-599, 2002.
7. Betarbet R, Greenamyre JT. Regulation of dopamine receptor and neuropeptide expression in the basal ganglia of monkeys treated with MPTP. Exp Neurol 189: 393-403, 2004.
8. Bezard E, Dovero S, Prunier C, Ravenscroft P, Chalon S, Guilloteau D, Crossman AR, Bioulac B, Brotchie JM, Gross CE. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J Neurosci 21: 6853-6861, 2001.
9. Bjorklund A, Lindvall O. Dopamine in dendrites of substantia nigra neurons: suggestions for a role in dendritic terminals. Brain Res 83: 531-537, 1975.
10. Brown P, Oliviero A, Mazzone P, Insola A, Tonali P, Di Lazzaro V. Dopamine dependency of oscillations between subthalamic nucleus and pallidum in Parkinson's disease. J Neurosci 21: 1033-1038, 2001.
11. Camps M, Cortes R, Gueye B, Probst A, Palacios JM. Dopamine receptors in human brain: autoradiographic distribution of D2 sites. Neuroscience 28: 275-290, 1989.
12. Camps M, Kelly PH, Palacios JM. Autoradiographic localization of dopamine D 1 and D 2 receptors in the brain of several mammalian species. J Neural Transm Gen Sect 80: 105-127, 1990.
13. Chefer SI, Kimes AS, Matochik JA, Horti AG, Kurian V, Shumway D, Domino EF, London ED, Mukhin AG. Estimation of D2-like receptor occupancy by dopamine in the putamen of hemiparkinsonian monkeys. Neuropsychopharmacology 33: 270-278, 2008.
14. Cheramy A, Leviel V, Glowinski J. Dendritic release of dopamine in the substantia nigra. Nature 289: 537-542, 1981.
15. Cooper AJ, Stanford IM. Dopamine D2 receptor mediated presynaptic inhibition of striatopallidal GABAA IPSCs in vitro. Neuropharmacology 41: 62-71, 2001.
16. Cooper AJ, Stanford IM. Electrophysiological and morphological characteristics of three subtypes of rat globus pallidus neurone in vitro. J Physiol 527: 291-304, 2000.
17. Cragg SJ, Greenfield SA. Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum. J Neurosci 17: 5738-5746, 1997.
18. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13: 281-285, 1990.
19. Deng P, Zhang Y, Xu ZC. Involvement of Ih in dopamine modulation of tonic firing in striatal cholinergic interneurons. J Neurosci 27: 3148-3156, 2007.
20. Floran B, Floran L, Sierra A, Aceves J. D2 receptor-mediated inhibition of GABA release by endogenous dopamine in the rat globus pallidus. Neurosci Lett 237: 1-4, 1997.
21. Galvan A, Hu X, Smith Y, Wichmann T. Localization and function of GABA transporters in the globus pallidus of parkinsonian monkeys. Exp Neurol 223: 505-515, 2010.
22. Galvan A, Hu X, Smith Y, Wichmann T. Localization and pharmacological modulation of GABA-B receptors in the globus pallidus of parkinsonian monkeys. Exp Neurol 229: 429-439, 2011.
23. Galvan A, Villalba RM, West SM, Maidment NT, Ackerson LC, Smith Y, Wichmann T. GABAergic modulation of the activity of globus pallidus neurons in primates: in vivo analysis of the functions of GABA receptors and GABA transporters. J Neurophysiol 94: 990-1000, 2005.
24. Garber JC, Barbee RW, Bielitzki JT, Clayton LA, Donovan JC, Hendriksen CFM, Kohn DF, Lipman NS, Locke PA, Melcher J, Quimby FW, Turner PV, Wood GA, Würbel H. Guide for the Care and Use of Laboratory Animals (8th ed.). Washington, DC: National Academies Press, 2010.
25. Gatev P, Darbin O, Wichmann T. Oscillations in the basal ganglia under normal conditions and in movement disorders. Mov Disord 21: 1566-1577, 2006.
26. Geffen LB, Jessell TM, Cuello AC, Iversen LL. Release of dopamine from dendrites in rat substantia nigra. Nature 260: 258-260, 1976.
27. Gnanalingham KK, Smith LA, Hunter AJ, Jenner P, Marsden CD. Alterations in striatal and extrastriatal D-1 and D-2 dopamine receptors in the MPTP-treated common marmoset: an autoradiographic study. Synapse 14: 184-194, 1993.
28. Gurevich EV, Joyce JN. Distribution of dopamine D3 receptor expressing neurons in the human forebrain: comparison with D2 receptor expressing neurons. Neuropsychopharmacology 20: 60-80, 1999.
29. Hammond C, Bergman H, Brown P. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 30: 357-364, 2007.
30. Hernandez A, Ibanez-Sandoval O, Sierra A, Valdiosera R, Tapia D, Anaya V, Galarraga E, Bargas J, Aceves J. Control of the subthalamic innervation of the rat globus pallidus by D2/3 and D4 dopamine receptors. J Neurophysiol 96: 2877-2888, 2006.
31. Herrero MT, Augood SJ, Asensi H, Hirsch EC, Agid Y, Obeso JA, Emson PC. Effects of L-DOPA-therapy on dopamine D2 receptor mRNA expression in the striatum of MPTP-intoxicated parkinsonian monkeys. Brain Res Mol Brain Res 42: 149-155, 1996.
32. Hoover BR, Marshall JF. Molecular, chemical, and anatomical characterization of globus pallidus dopamine D2 receptor mRNA-containing neurons. Synapse 52: 100-113, 2004.
33. Hurley MJ, Jolkkonen J, Stubbs CM, Jenner P, Marsden CD. Dopamine D3 receptors in the basal ganglia of the common marmoset and following MPTP and L-DOPA treatment. Brain Res 709: 259-264, 1996.
34. Ibanez-Sandoval O, Carrillo-Reid L, Galarraga E, Tapia D, Mendoza E, Gomora JC, Aceves J, Bargas J. Bursting in substantia nigra pars reticulata neurons in vitro: possible relevance for Parkinson disease. J Neurophysiol 98: 2311-2323, 2007.
35. Ibanez-Sandoval O, Hernandez A, Floran B, Galarraga E, Tapia D, Valdiosera R, Erlij D, Aceves J, Bargas J. Control of the subthalamic innervation of substantia nigra pars reticulata by D-1 and D-2 dopamine receptors. J Neurophysiol 95: 1800-1811, 2006.
36. Jan C, Francois C, Tande D, Yelnik J, Tremblay L, Agid Y, Hirsch E. Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients. Eur J Neurosci 12: 4525-4535, 2000.
37. Jiang ZG, Pessia M, North RA. Dopamine and baclofen inhibit the hyperpolarization-activated cation current in rat ventral tegmental neurones. J Physiol 462: 753-764, 1993.
38. Kawaguchi Y, Wilson CJ, Emson PC. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J Neurosci 10: 3421-3438, 1990.
39. Keja JA, Stoof JC, Kits KS. Dopamine D2 receptor stimulation differentially affects voltage-activated calcium channels in rat pituitary melanotropic cells. J Physiol 450: 409-435, 1992.
40. Khan ZU, Gutierrez A, Martin R, Penafiel A, Rivera A, De La Calle A. Differential regional and cellular distribution of dopamine D2-like receptors: an immunocytochemical study of subtype-specific antibodies in rat and human brain. J Comp Neurol 402: 353-371, 1998.
41. Kita H, Nambu A, Kaneda K, Tachibana Y, Takada M. Role of ionotropic glutamatergic and GABAergic inputs on the firing activity of neurons in the external pallidum in awake monkeys. J Neurophysiol 92: 3069-3084, 2004.
42. Kliem MA, Maidment NT, Ackerson LC, Chen S, Smith Y, Wichmann T. Activation of nigral and pallidal dopamine D1-like receptors modulates basal ganglia outflow in monkeys. J Neurophysiol 98: 1489-1500, 2007.
43. Kliem MA, Pare JF, Khan ZU, Wichmann T, Smith Y. Ultrastructural localization and function of dopamine D1-like receptors in the substantia nigra pars reticulata and the internal segment of the globus pallidus of parkinsonian monkeys. Eur J Neurosci 31: 836-851, 2010.
44. Kliem MA, Wichmann T. A method to record changes in local neuronal discharge in response to infusion of small drug quantities in awake monkeys. J Neurosci Methods 138: 45-49, 2004.
45. Legendy CR, Salcman M. Bursts and recurrences of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53: 926-939, 1985.
46. Lei W, Jiao Y, Del Mar N, Reiner A. Evidence for differential cortical input to direct pathway versus indirect pathway striatal projection neurons in rats. J Neurosci 24: 8289-8299, 2004.
47. Levesque M, Parent A. The striatofugal fiber system in primates: a reevaluation of its organization based on single-axon tracing studies. Proc Natl Acad Sci USA 102: 11888-11893, 2005.
48. Levey AI, Hersch SM, Rye DB, Sunahara RK, Niznik HB, Kitt CA, Price DL, Maggio R, Brann MR, Ciliax BJ. Localization of D1 and D2 dopamine receptors in brain with subtype-specific antibodies. Proc Natl Acad Sci USA 90: 8861-8865, 1993.
49. Liang L, DeLong MR, Papa SM. Inversion of dopamine responses in striatal medium spiny neurons and involuntary movements. J Neurosci 28: 7537-7547, 2008.
50. Lledo PM, Legendre P, Israel JM, Vincent JD. Dopamine inhibits two characterized voltage-dependent calcium currents in identified rat lactotroph cells. Endocrinology 127: 990-1001, 1990.
51. Macey TA, Gurevich VV, Neve KA. Preferential Interaction between the dopamine D2 receptor and Arrestin2 in neostriatal neurons. Mol Pharmacol 66: 1635-1642, 2004.
52. Marshall JF, Henry BL, Billings LM, Hoover BR. The role of the globus pallidus D2 subfamily of dopamine receptors in pallidal immediate early gene expression. Neuroscience 105: 365-378, 2001.
53. Masilamoni G, Votaw J, Howell L, Villalba RM, Goodman M, Voll RJ, Stehouwer J, Wichmann T, Smith Y. 18F-FECNT: validation as PET dopamine transporter ligand in parkinsonism. Exp Neurol 226: 265-273, 2010.
54. Mauger C, Sivan B, Brockhaus M, Fuchs S, Civelli O, Monsma F Jr. Development and characterization of antibodies directed against the mouse D4 dopamine receptor. Eur J Neurosci 10: 529-537, 1998.
55. Mengual E, Pickel VM. Ultrastructural immunocytochemical localization of the dopamine D2 receptor and tyrosine hydroxylase in the rat ventral pallidum. Synapse 43: 151-162, 2002.
56. Millan MJ, Maiofiss L, Cussac D, Audinot V, Boutin JA, Newman-Tancredi A. Differential actions of antiparkinson agents at multiple classes of monoaminergic receptor. I. A multivariate analysis of the binding profiles of 14 drugs at 21 native and cloned human receptor subtypes. J Pharmacol Exp Ther 303: 791-804, 2002.
57. Morissette M, Goulet M, Calon F, Falardeau P, Blanchet PJ, Bedard PJ, Di Paolo T. Changes of D1 and D2 dopamine receptor mRNA in the brains of monkeys lesioned with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine: correction with chronic administration of L-3,4-dihydroxyphenylalanine. Mol Pharmacol 50: 1073-1079, 1996.
58. Mrzljak L, Bergson C, Pappy M, Huff R, Levenson R, Goldman-Rakic PS. Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 381: 245-248, 1996.
59. Murray AM, Ryoo HL, Gurevich E, Joyce JN. Localization of dopamine D3 receptors to mesolimbic and D2 receptors to mesostriatal regions of human forebrain. Proc Natl Acad Sci USA 91: 11271-11275, 1994.
60. Nakanishi H, Hori N, Kastuda N. Neostriatal evoked inhibition and effects of dopamine on globus pallidal neurons in rat slice preparations. Brain Res 358: 282-286, 1985.
61. Nambu A, Llinas R. Electrophysiology of globus pallidus neurons in vitro. J Neurophysiol 72: 1127-1139, 1994.
62. Parent A, Lavoie B, Smith Y, Bedard P. The dopaminergic nigropallidal projection in primates: distinct cellular origin and relative sparing in MPTPtreated monkeys. Adv Neurol 53: 111-116, 1990.
63. Peters A, Palay SL, Webster HF. The Fine Structure of the Nervous System-Neurons and Their Supporting Cells. New York: Oxford University Press, 1991.
64. Pifl C, Bertel O, Hornykiewicz O. Extrastriatal dopamine in symptomatic and asymptomatic Rhesus monkeys treated with 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP). Neurochem Int 17: 263-270, 1990.
65. Plenz D, Kitai S. A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400: 677-682, 1999.
66. Querejeta E, Delgado A, Valdiosera R, Erlij D, Aceves J. Intrapallidal D2 dopamine receptors control globus pallidus neuron activity in the rat. Neurosci Lett 300: 79-82, 2001.
67. Quik M, Police S, He L, Di Monte DA, Langston JW. Expression of D3 receptor messenger RNA and binding sites in monkey striatum and substantia nigra after nigrostriatal degeneration: effect of levodopa treatment. Neuroscience 98: 263-273, 2000.
68. Richfield EK, Young AB, Penney JB. Comparative distribution of dopamine D-1 and D-2 receptors in the basal ganglia of turtles, pigeons, rats, cats, and monkeys. J Comp Neurol 262: 446-463, 1987.
69. Rommelfanger KS, Wichmann T. Extrastriatal dopaminergic circuits of the Basal Ganglia. Front Neuroanat 4: 139, 2010.
70. Ruskin DN, Bergstrom DA, Tierney PL, Walters JR. Correlated multisecond oscillations in firing rate in the basal ganglia: modulation by dopamine and the subthalamic nucleus. Neuroscience 117: 427-438, 2003.
71. Seeman P, Van Tol HH. Dopamine receptor pharmacology. Trends Pharmacol Sci 15: 264-270, 1994.
72. Shin RM, Masuda M, Miura M, Sano H, Shirasawa T, Song WJ, Kobayashi K, Aosaki T. Dopamine D4 receptor-induced postsynaptic inhibition of GABAergic currents in mouse globus pallidus neurons. J Neurosci 23: 11662-11672, 2003.
73. Smith Y, Bevan MD, Shink E, Bolam JP. Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience 86: 353-387, 1998.
74. Smith Y, Kieval JZ. Anatomy of the dopamine system in the basal ganglia. Trends Neurosci 23: S28-S33, 2000.
75. Smith Y, Lavoie B, Dumas J, Parent A. Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey. Brain Res 482: 381-386, 1989.
76. Smith Y, Villalba R. Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov Disord 23, Suppl 3: S534-S547, 2008.
77. Soares J, Kliem MA, Betarbet R, Greenamyre JT, Yamamoto B, Wichmann T. Role of external pallidal segment in primate parkinsonism: comparison of the effects of MPTP-induced parkinsonism and lesions of the external pallidal segment. J Neurosci 24: 6417-6426, 2004.
78. Terman D, Rubin JE, Yew AC, Wilson CJ. Activity patterns in a model for the subthalamopallidal network of the basal ganglia. J Neurosci 22: 2963-2976, 2002.
79. Wang H, Pickel VM. Dopamine D2 receptors are present in prefrontal cortical afferents and their targets in patches of the rat caudate-putamen nucleus. J Comp Neurol 442: 392-404, 2002.
80. Waszczak BL, Martin LP, Finlay HE, Zahr N, Stellar JR. Effects of individual and concurrent stimulation of striatal D1 and D2 dopamine receptors on electrophysiological and behavioral output from rat basal ganglia. J Pharmacol Exp Ther 300: 850-861, 2002.
81. Watanabe K, Kita T, Kita H. Presynaptic actions of D2-like receptors in the rat cortico-striato-globus pallidus disynaptic connection in vitro. J Neurophysiol 101: 665-671, 2009.
82. Whone AL, Moore RY, Piccini PP, Brooks DJ. Plasticity of the nigropallidal pathway in Parkinson's disease. Ann Neurol 53: 206-213, 2003.
83. Wichmann T, Bergman H, DeLong MR. The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of parkinsonism. J Neurophysiol 72: 521-530, 1994.
84. Wichmann T, Soares J. Neuronal firing before and after burst discharges in the monkey basal ganglia is predictably patterned in the normal state and altered in parkinsonism. J Neurophysiol 95: 2120-2133, 2006.
85. Yung KK, Bolam JP, Smith AD, Hersch SM, Ciliax BJ, Levey AI. Immunocytochemical localization of D1 and D2 dopamine receptors in the basal ganglia of the rat: light and electron microscopy. Neuroscience 65: 709-730, 1995.
86. Zhou FW, Jin Y, Matta SG, Xu M, Zhou FM. An ultra-short dopamine pathway regulates basal ganglia output. J Neurosci 29: 10424-10435, 2009.