Physiology of the normal and dopamine-depleted basal ganglia: Insights into levodopa pharmacotherapy

Movement Disorders

Volumn 23, Issue SUPPL. 3, 2008, Pages

  Grace, Anthony A ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Dopamine; Long term potentiation; Nucleus accumbens; Parkinson's disease; Tonic phasic

Indexed keywords

DOPAMINE; DOPAMINE RECEPTOR STIMULATING AGENT; LEVODOPA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR;

ARTICLE; BRAIN FUNCTION; CELL ACTIVITY; CELL INTERACTION; CELL LOSS; CELL MEMBRANE DEPOLARIZATION; CELL NUCLEUS; CELL POPULATION; COGNITIVE DEFECT; DOPAMINE BRAIN LEVEL; DOPAMINE RELEASE; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; DRUG EFFECT; DRUG EFFICACY; DRUG MECHANISM; DRUG SAFETY; DYSKINESIA; EXTRAPYRAMIDAL SYNDROME; GABAERGIC TRANSMISSION; HIPPOCAMPUS; HUMAN; LIMBIC SYSTEM; LONG TERM POTENTIATION; MENTAL TASK; MESOLIMBIC DOPAMINERGIC SYSTEM; MOTONEURON; MOTOR CORTEX; MOTOR DYSFUNCTION; NERVE CELL PLASTICITY; NEUROMODULATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEUS ACCUMBENS; PARKINSON DISEASE; POSTSYNAPTIC POTENTIAL; PREFRONTAL CORTEX; PRIORITY JOURNAL; REFRACTORY PERIOD; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

ANTIPARKINSON AGENTS; BASAL GANGLIA; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; HUMANS; LEVODOPA; NEURONS; NUCLEUS ACCUMBENS; PARKINSON DISEASE; RECEPTORS, DOPAMINE; SYNAPSES; SYNAPTIC TRANSMISSION;

EID: 53149111568     PISSN: 08853185     EISSN: 15318257     Source Type: Journal    
DOI: 10.1002/mds.22020     Document Type: Article

References (90)

1. Jellinger K. Overview of morphological changes in Parkinson's disease. Adv Neurol 1987;45:1-18.
2. Cotzias GC, Van Woert MH, Schiffer LM. Aromatic amino acids and modification of Parkinsonism. N Engl J Med 1967;276:374-379.
3. McGeer PL, McGeer EG. Neurotransmitter synthetic enzymes. Prog Neurobiol 1973;2:69-117.
4. Molinoff PB, Axelrod J. Biochemistry of catecholamines. Annu Rev Biochem 1971;40:465-500.
5. Hornykiewicz O. The mechanisms of action of L-dopa in Parkinson's disease. Life Sci 1974;15:1249-1259.
6. Marsden CD, Parkes JD. Success and problems of long-term levodopa therapy in Parkinson's disease. Lancet 1977;1:345-349.
7. Olanow CW. The scientific basis for the current treatment of Parkinson's disease. Annu Rev Med 2004;55:41-60.
8. Obeso JA, Olanow CW, Nutt JG. Levodopa motor complications in Parkinson's disease. Trends Neurosci 2000;23(Suppl 10):S2-S7.
9. Anden NE, Fuxe 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.
10. Doucet G, Descarries L, Garcia S. Quantification of the dopamine innervation in adult rat neostriatum. Neuroscience 1986;19: 427-445.
11. Fallon JH. Collateralization of monoamine neurons: mesotelencephalic dopamine projections to caudate, septum, and frontal cortex. J Neurosci 1981;1:1361-1368.
12. Loughlin SE, Fallon JH. Substantia nigra and ventral tegmental area projections to cortex: topography and collateralization. Neuroscience 1984;11:425-435.
13. Swanson LW. The projections of the ventral tegmental area and adjacent regions: a combined fluorescent retrograde tracer and immunofluorescence study in the rat. Brain Res Bull 1982; 9:321-353.
14. Grace AA, Bunney BS. Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. I. Identification and characterization. Neuroscience 1983;10:301-315.
15. Grace AA, Onn SP. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J Neurosci 1989;9:3463-3481.
16. Grace AA, Bunney BS. Opposing effects of striatonigral feedback pathways on midbrain dopamine cell activity. Brain Res 1985;333:271-284.
17. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: burst firing. J Neurosci 1984;4:2877-2890.
18. Lodge DJ, Grace AA. The laterodorsal tegmentum is essential for burst firing of ventral tegmental area dopamine neurons. Proc Natl Acad Sci USA 2006;103:5167-5172.
19. Floresco SB, West AR, Ash B, Moore H, Grace AA. Afferent modulation of dopamine neuron firing differentially regulates tonic and phasic dopamine transmission. Nat Neurosci 2003;6:968-973.
20. Grace AA, Bunney BS. The control of firing pattern in nigral dopamine neurons: single spike firing. J Neurosci 1984;4:2866-2876.
21. Grace AA. Dopamine. In: Davis KL, Charney D, Coyle JT, Nemeroff C, editors. Neuropsychopharmacology: the fifth generation of progress. New York: Lippincott Williams & Wilkins; 2002. p 119-132.
22. Grace AA, Bunney BS. Induction of depolarization block in midbrain dopamine neurons by repeated administration of haloperidol: analysis using in vivo intracellular recording. J Pharmacol Exp Ther 1986;238:1092-1100.
23. Hollerman JR, Grace AA. The effects of dopamine-depleting brain lesions on the electrophysiological activity of rat substantia nigra dopamine neurons. Brain Res 1990;533:203-212.
24. Bunney BS, Grace AA. Acute and chronic haloperidol treatment: comparison of effects on nigral dopaminergic cell activity. Life Sci 1978;23:1715-1727.
25. Harden DG, Grace AA. Activation of dopamine cell firing by repeated L-dopa administration to dopamine-depleted rats: its potential role in mediating the therapeutic response to L-dopa treatment. J Neurosci 1995;15:6157-6166.
26. Hollerman JR, Grace AA. Acute haloperidol administration induces depolarization block of nigral dopamine neurons in rats after partial dopamine lesions. Neurosci Lett 1989;96:82-88.
27. Hollerman JR, Abercrombie ED, Grace AA. Electrophysiological, biochemical, and behavioral studies of acute haloperidol-induced depolarization block of nigral dopamine neurons. Neuroscience 1992;47:589-601.
28. Nisenbaum ES, Stricker EM, Zigmond MJ, Berger TW. Spontaneous activity of type II but not type I striatal neurons is correlated with recovery of behavioral function after dopamine-depleting brain lesions. Brain Res 1988;473:389-393.
29. Nisenbaum ES, Stricker EM, Zigmond MJ, Berger TW. Long-term effects of dopamine-depleting brain lesions on spontaneous activity of type II striatal neurons: relation to behavioral recovery. Brain Res 1986;398:221-230.
30. Calabresi P, Centonze D, Bernardi G. Electrophysiology of dopamine in normal and denervated striatal neurons. Trends Neurosci 2000;23(Suppl 10):S57-S63.
31. Calabresi P, Mercuri NB, Sancesario G, Bernardi G. Electrophysiology of dopamine-denervated striatal neurons. Implications for Parkinson's disease. Brain 1993;116(Part 2):433-452.
32. Grace AA. Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 1991;41:1-24.
33. Abercrombie ED, Keefe KA, DiFrischia DS, Zigmond MJ. Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens, and medial frontal cortex. J Neurochem 1989;52:1655-1658.
34. Church WH, Justice JB Jr, Neill DB. Detecting behaviorally relevant changes in extracellular dopamine with microdialysis. Brain Res 1987;412:397-399.
35. Sharp T, Zetterstrom T, Ungerstedt U. An in vivo study of dopamine release and metabolism in rat brain regions using intracerebral dialysis. J Neurochem 1986;47:113-122.
36. Robinson TE, Whishaw IQ. Normalization of extracellular dopamine in striatum following recovery from a partial unilateral 6-OHDA lesion of the substantia nigra: a microdialysis study in freely moving rats. Brain Res 1988;450:209-224.
37. Grace AA. In vivo and in vitro intracellular recordings from rat midbrain dopamine neurons. Ann NY Acad Sci 1988;537:51-76.
38. Schultz W. The phasic reward signal of primate dopamine neurons. Adv Pharmacol 1998;42:686-690.
39. Mercuri NB, Stratta F, Calabresi P, Bernardi G. A voltage-clamp analysis of NMDA-induced responses on dopaminergic neurons of the rat substantia nigra zona compacta and ventral tegmental area. Brain Res 1992;593:51-56.
40. Seutin V, Verbanck P, Massotte L, Dresse A. Evidence for the presence of N-methyl-D-aspartate receptors in the ventral tegmental area of the rat: an electrophysiological in vitro study. Brain Res 1990;514:147-150.
41. Wang T, French ED. L-Glutamate excitation of A10 dopamine neurons is preferentially mediated by activation of NMDA receptors: extra- and intracellular electrophysiological studies in brain slices. Brain Res 1993;627:299-306.
42. Groenewegen HJ, Berendse HW. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J Comp Neurol 1990;294:607-622.
43. Kita H, Kitai ST. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 1987;260:435-452.
44. Ricardo JA. Efferent connections of the subthalamic region in the rat. I. The subthalamic nucleus of Luys. Brain Res 1980;202:257-271.
45. Smith ID, Grace AA. Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse 1992;12: 287-303.
46. Clements JR, Toth DD, Highfield DA, Grant SJ. Glutamate-like immunoreactivity is present within cholinergic neurons of the laterodorsal tegmental and pedunculopontine nuclei. Adv Exp Med Biol 1991;295:127-142.
47. Oakman SA, Faris PL, Kerr PE, Cozzari C, Hartman BK. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J Neurosci 1995;15:5859-5869.
48. Lodge DJ, Grace AA. The hippocampus modulates dopamine neuron responsivity by regulating the intensity of phasic neuron activation. Neuropsychopharmacology 2006;31:1356-1361.
49. Karreman M, Westerink BH, Moghaddam B. Excitatory amino acid receptors in the ventral tegmental area regulate dopamine release in the ventral striatum. J Neurochem 1996;67:601-607.
50. Chergui K, Charlety PJ, Akaoka H, et al. Tonic activation of NMDA receptors causes spontaneous burst discharge of rat midbrain dopamine neurons in vivo. Eur I Neurosci 1993;5:137-144.
51. Overton P, Clark D. Iontophoretically administered drugs acting at the N-methyl-D-aspartate receptor modulate burst firing in A9 dopamine neurons in the rat. Synapse 1992;10:131-140.
52. 2+ of NMDA responses in spinal cord neurones. Nature 1984; 309:261-263.
53. Floresco SB, Grace AA. Gating of hippocampal-evoked activity in prefrontal cortical neurons by inputs from the mediodorsal thalamus and ventral tegmental area. J Neurosci 2003;23:3930-3943.
54. Lisman JE, Grace AA. The hippocampal-VTA loop: controlling the entry of information into long-term memory. Neuron 2005;46:703-713.
55. May LJ, Kuhr WG, Wightman RM. Differentiation of dopamine overflow and uptake processes in the extracellular fluid of the rat caudate nucleus with fast-scan in vivo voltammetry. J Neurochem 1988;51:1060-1069.
56. Koepp MJ, Gunn RN, Lawrence AD, et al. Evidence for striatal dopamine release during a video game. Nature 1998;393:266-268.
57. Charara A, Grace AA. Dopamine receptor subtypes selectively modulate excitatory afferents from the hippocampus and amygdala to rat nucleus accumbens neurons. Neuropsychopharmacology 2003;28:1412-1421.
58. Goto Y, Grace AA. Dopaminergic modulation of limbic and cortical drive of nucleus accumbens in goal-directed behavior. Nat Neurosci 2005;8:805-812.
59. Goto Y, Grace AA. Dopamine-dependent interactions between limbic and prefrontal cortical synaptic plasticity in the nucleus accumbens: disruption by cocaine sensitization. Neuron 2005;47:255-266.
60. Owen AM, James M, Leigh PN, et al. Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain 1992; 115 (Part 6):1727-1751.
61. Morrison CE, Borod JC, Brin MF, Halbig TD, Olanow CW. Effects of levodopa on cognitive functioning in moderate-to-severe Parkinson's disease (MSPD). J Neural Transm 2004;111: 1333-1341.
62. Kalivas PW, Stewart J. Dopamine transmission in the initiation and expression of drug- and stress-induced sensitization of motor activity. Brain Res Brain Res Rev 1991;16:223-244.
63. Mehta MA, Manes FF, Magnolfi G, Sahakian BJ, Robbins TW. Impaired set-shifting and dissociable effects on tests of spatial working memory following the dopamine D2 receptor antagonist sulpiride in human volunteers. Psychopharmacology 2004;176: 331-342.
64. Cools R, Clark L, Robbins TW. Differential responses in human striatum and prefrontal cortex to changes in object and rule relevance. J Neurosci 2004;24:1129-1135.
65. Chudasama Y, Robbins TW. Dissociable contributions of the orbitofrontal and infralimbic cortex to pavlovian autoshaping and discrimination reversal learning: further evidence for the functional heterogeneity of the rodent frontal cortex. J Neurosci 2003;23:8771-8780.
66. Clark L, Cools R, Robbins TW. The neuropsychology of ventral prefrontal cortex: decision-making and reversal learning. Brain Cogn 2004;55:41-53.
67. Divac I, Rosvold HE, Szwarcbart MK. Behavioral effects of selective ablation of the caudate nucleus. J Comp Physiol Psychol 1967;63:184-190.
68. Taghzouti K, Louilot A, Herman JP, Le Moal M, Simon H. Alternation behavior, spatial discrimination, and reversal disturbances following 6-hydroxydopamine lesions in the nucleus accumbens of the rat. Behav Neural Biol 1985;44:354-363.
69. Heimer L, Albeid GF, de Olmos JS, et al. The accumbens: beyond the core-shell dichotomy. J Neuropsychiatry Clin Neurosci 1997;9:354-381.
70. Mogenson GJ, Jones DL, Yim CY. From motivation to action: functional interface between the limbic system and the motor system. Prog Neurobiol 1980;14:69-97.
71. Farley IJ, Price KS, Hornykiewicz O. Dopamine in the limbic regions of the human brain: normal and abnormal. Adv Biochem Psychopharmacol 1977;16:57-64.
72. Kish SJ, Shannak K, Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. N Engl J Med 1988;318:876-880.
73. Cools R, Lewis SJG, Clark L, Barker RA, Robbins TW. L-Dopa disrupts activity in the nucleus accumbens during reversal learning in Parkinson's disease. Neuropsychopharmacology 2007;32:199-190.
74. Cools R, Barker RA, Sahakian BJ, Robbins TW. Mechanisms of cognitive set flexibility in Parkinson's disease. Brain 2001;124 (Part 12):2503-2512.
75. Alexander GE, Crutcher MD, DeLong MR. Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, "prefrontal" and "limbic" functions. Prog Brain Res 1990;85: 119-146.
76. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 1986;9:357-381.
77. Gerfen CR, Engber TM, Mahan LC, et al. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striato-pallidal neurons. [see comment]. Science 1990;250:1429-1432.
78. Albin RL, Young AB, Penney JB. The functional anatomy of basal ganglia disorders [see comments]. Trends Neurosci 1989;12: 366-375.
79. DeLong MR. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 1990;13:281-285.
80. Onn SP, West AR, Grace AA. Dopamine-mediated regulation of striatal neuronal and network interactions. Trends Neurosci 2000;23(Suppl 10):S48-S56.
81. West AR, Grace AA. 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.
82. 2+ conductance. J Neurosci 1997;17:3334-3342.
83. Nelson LR, Ellison G. Enhanced stereotypies after repeated injections but not continuous amphetamines. Neuropharmacology 1978; 17:1081-1084.
84. Post RM. Intermittent versus continuous stimulation: effect of time interval on the development of sensitization or tolerance. Life Sci 1980;26:1275-1282.
85. Fischman MW, Schuster CR, Javaid J, Hatano Y, Davis J. Acute tolerance development to the cardiovascular and subjective effects of cocaine. J Pharmacol Exp Ther 1985;235:677-682.
86. Grace AA. The tonic/phasic model of dopamine system regulation: its relevance for understanding how stimulant abuse can alter basal ganglia function. Drug Alcohol Depend 1995;37:111-129.
87. Olanow CW, Obeso JA. Pulsatile stimulation of dopamine receptors and levodopa-induced motor complications in Parkinson's disease: implications for the early use of COMT inhibitors. Neurology 2000;55(11,Suppl 4):S72-S77; discussion S78-S81.
88. Stocchi F, Ruggieri S, Vacca L, Olanow CW. Prospective randomized trial of lisuride infusion versus oral levodopa in PD Patients. Brain 2002;125:2058-2066.
89. Stocchi F, Vacca L, Ruggieri S, Olanow CW. Infusion of levodopa methyl ester in patients with advanced PD: a clinical and pharmacokinetic study. Arch Neurol 2005;62:905-910.
90. Olanow CW, Obeso JA, Stocchi F. Continuous dopamine receptor stimulation in the treatment of Parkinson's disease: scientific rationale and clinical implications. Lancet Neurol 2006;5:677-687.