Functional domains in dorsal striatum of the nonhuman primate are defined by the dynamic behavior of dopamine

Journal of Neuroscience

Volumn 22, Issue 13, 2002, Pages 5705-5712

  Cragg, Stephanie J ^a   Hille, Christopher J ^a,b   Greenfield, Susan A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b Neurol Ctr Excellence Drug Discov   (United Kingdom)

Author keywords

Basal ganglia; Caudate; Cocaine; Corticostriatal; Dopamine transporter; Dopamine uptake; Marmoset; Mesostriatal; Nigrostriatal; Parkinson's disease; Primate; Putamen; Striatonigral; Synaptic depression; Ventral striatum; Voltammetry

Indexed keywords

COCAINE; DESIPRAMINE; DOPAMINE; DOPAMINE TRANSPORTER; PSYCHOSTIMULANT AGENT; VANOXERINE;

ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CAUDATE NUCLEUS; COCAINE DEPENDENCE; CONTROLLED STUDY; CYCLIC POTENTIOMETRY; DEGENERATIVE DISEASE; DOPAMINERGIC SYSTEM; DRUG DEPENDENCE; MALE; MARMOSET; NEUROLOGIC DISEASE; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; PARKINSON DISEASE; PRIMATE; PRIORITY JOURNAL; PUTAMEN;

EID: 0036663022     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-13-05705.2002     Document Type: Article

References (72)

1. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, Shinsky N, Verdugo JM, Armanini M, Ryan A, Hynes M, Phillips H, Sulzer D, Rosenthal A (2000) Mice lacking α-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25:239-252.
2. Alexander GE, DeLong MR (1985) Microstimulation of the primate neostriatum. II. Somatotropic organization of striatal microexcitable zones and their relation to neuronal response properties. J Neurophysiol 53:1417-1430.
3. Antonini A, Vontobel P, Psylla M, Gunther I, Maguire PR, Missimer J, Leenders KL (1995) Complementary positron emission tomographic studies of the striatal dopaminergic system in Parkinson's disease. Arch Neurol 52:1183-1190.
4. 2 receptors: Time course and functional characteristics in vivo. J Neurosci 21:9134-9141.
5. Bjorklund A, Lindvall O (1984) Dopamine-containing systems in the CNS. In: Handbook of Chemical Neuroanatomy (Bjorklund A, Hokfelt T, eds), pp 55-122. New York: Elsevier.
6. Blanchard V, Raisman-Vozari R, Vyas S, Michel PP, Javoy-Agid F, Uhl G, Agid Y (1994) Differential expression of tyrosine hydroxylase and membrane dopamine transporter genes in subpopulations of dopaminergic neurons of the rat mesencephalon. Mol Brain Res 22:29-40.
7. Bradberry CW, Barrett-Larimore RL, Jatlow P, Rubino SR (2000) Impact of self-administered cocaine and cocaine cues on extracellular dopamine in mesolimbic and sensorimotor striatum in rhesus monkeys. J Neurosci 20:3874-3883.
8. Bunney BS, Walters JR, Roth RH, Aghajanian GK (1973) Dopaminergic neurons: Effect of antipsychotic drugs and amphetamine on single cell activity. J Pharmacol Exp Ther 185:560-571.
9. 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.
10. Cass WA, Gerhardt GA, Mayfield RD, Curella P, Zahniser NR (1992) Differences in dopamine clearance and diffusion in rat striatum and nucleus accumbens following systemic cocaine administration. J Neurochem 59:259-266.
11. Cragg SJ, Greenfield SA (1997) Differential autoreceptor control of somatodendritic and axon terminal dopamine release in substantia nigra, ventral tegmental area, and striatum. J Neurosci 17:5738-5746.
12. Cragg SJ, Hille CJ, Greenfield SA (2000) Dopamine release and uptake dynamics within nonhuman primate striatum in vitro. J Neurosci 20:8209-8217.
13. Crutcher MD, DeLong MR (1984) Single cell studies of the primate putamen. I. Functional organisation. Exp Brain Res 53:233-243.
14. 3H]mazindol autoradiography. J Comp Neurol 304:419-434.
15. Elsworth JD, Deutch AY, Redmond DE, Sladek JR, Roth RH (1987) Effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) on catecholamines and metabolites in primate brain and CSF. Brain Res 415:293-299.
16. Gerfen CR, Baimbridge KG, Thibault J (1987) The neostriatal mosaic. III. Biochemical and developmental dissociation of patch-matrix mesostriatal systems. J Neurosci 7:3935-3944.
17. Gimenez-Amaya JM, McFarland NR, las-Heras S, Haber SN (1995) Organization of thalamic projections to the ventral striatum in the primate. J Comp Neurol 354:127-149.
18. Giros B, Jaber M, Jones SR, Wightman RM, Caron MG (1996) Hyperlocomotion and indifference to cocaine and amphetamine in mice lacking the dopamine transporter. Nature 379:606-612.
19. Grace AA, Bunney BS (1983) Intracellular and extracellular electrophysiology of nigral dopaminergic neurons. I. Identification and characterisation. Neuroscience 10:301-315.
20. Grace AA, Bunney BS (1984a) The control of firing pattern in nigral dopamine neurons: Single spike firing. J Neurosci 4:2866-2876.
21. Grace AA, Bunney BS (1984b) The control of firing pattern in nigral dopamine neurons: Burst firing. J Neurosci 4:2877-2890.
22. Haber SN, McFarland NR (1999) The concept of the ventral striatum in nonhuman primates. Ann NY Acad Sci 877:43-48.
23. Haber SN, Ryoo H, Cox C, Lu W (1995) Subsets of midbrain dopaminergic neurons in monkeys are distinguished by different levels of mRNA for the dopamine transporter: Comparison with the mRNA for the D2 receptor, tyrosine hydroxylase and calbindin immunoreactivity. J Comp Neurol 362:400-410.
24. Haber SN, Fudge JL, McFarland NR (2000) Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci 20:2369-2382.
25. Harvey DC, Lacan G, Melegan WP (2000) Regional heterogeneity of dopaminergic deficits in vervet monkey striatum and substantia nigra after methamphetamine exposure. Exp Brain Res 133:349-358.
26. Hazrati LN, Parent A (1992) The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res 592:213-227.
27. Hornykiewicz O (1966) Dopamine (3-hydroxytyramine) and brain function. Pharmacol Rev 18:925-964.
28. Horvitz JC (2000) Mesolimbocortical and nigrostriatal dopamine responses to salient non-reward events. Neuroscience 96:651-656.
29. Hurd YL, Pristupa ZB, Herman MM, Niznik HB, Kleinman JE (1994) The DA transporter and DA D2 receptor mRNAs are differentially expressed in limbic- and motor-related subpopulations of human mesencephalic neurons. Neuroscience 63:357-362.
30. Jenner P, Olanow CW (1996) Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 47:S161-S170.
31. Jones SR, Garris PA, Kilts CD, Wightman RM (1995) Comparison of dopamine uptake in the basolateral amygdaloid nucleus, caudateputamen and nucleus accumbens of the rat. J Neurochem 64:2581-2589.
32. Kaufman MJ, Madras BK (1991) Severe depletion of cocaine recognition sites associated with the dopamine transporter in Parkinson's-diseased striatum. Synapse 9:43-49.
33. 125I]RTI-55. Synapse 12:99-111.
34. Kawagoe KT, Garris PA, Wiedemann DJ, Wightman RM (1992) Regulation of transient dopamine concentration gradients in the microenvironment surrounding nerve terminals in the rat striatum. Neuroscience 51:55-64.
35. Kennedy RT, Jones SR, Wightman RM (1992) Dynamic observation of dopamine autoreceptor effects in rat striatal slices. J Neurochem 59:449-455.
36. Kish SJ, Shannak K, Hornykiewicz O (1988) Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease: Pathophysiologic and clinical implications N Engl J Med 318:876-880.
37. Kuczenski R, Segal DS (1992) Differential effects of amphetamine and dopamine uptake blockers (cocaine, nomifensine) on caudate and accumbens dialysate dopamine and 3-methoxytyramine. J Pharmacol Exp Ther 262:1085-1094.
38. Kunzle H (1975) Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia: An autoradiographic study in Macaca fascicularis. Brain Res 88:195-209.
39. Kunzle H (1977) Projections from the primary somatosensory cortex to basal ganglia and thalamus in the monkey. Exp Brain Res 30:481-492.
40. Limberger N, Trout SJ, Kruk ZL, Starke K (1991) "Real-time" measurement of endogenous DA release during short trains of pulses in slices of rat neostriatum and nucleus accumbens: Role of autoinhibition. Naunyn Schmiedebergs Arch Pharmacol 344:623-629.
41. Liss B, Franz O, Sewing S, Bruns R, Neuhoff H, Roeper J (2001) Tuning pacemaker frequency of individual dopaminergic neurons by Kv4.3L and KChip3.1 transcription. EMBO J 20:5715-5724.
42. Lynd-Balta E, Haber SN (1994a) Primate striatonigral projections: A comparison of the sensorimotor-related striatum and the ventral striatum. J Comp Neurol 345:562-578.
43. Lynd-Balta E, Haber SN (1994b) The organization of midbrain projections to the striatum in the primate: Sensorimotor-related striatum versus ventral striatum. Neuroscience 59:625-640.
44. Madras BK, Gracz LM, Fahey MA, Elmaleh D, Meltzer PC, Liang AY, Stopa EG, Babich J, Fischman AJ (1998) Altropane, a SPECT or PET imaging probe for dopamine neurons. III. Human dopamine transporter in postmortem normal and Parkinson's diseased brain. Synapse 29:116-127.
45. 3H]GBR 12935 binding to dopamine uptake sites: Subcellular localization and reduction in Parkinson's disease and progressive supranuclear palsy. Eur J Pharmacol 156:331-340.
46. McFarland NR, Haber SN (2000) Convergent inputs from thalamic motor nuclei and frontal cortical areas to the dorsal striatum in the primate. J Neurosci 20:3798-3813.
47. Meir A, Ginsburg S, Butkevich A, Kachalsky SG, Kaiserman I, Ahdut R, Demirgoren S, Rahamimoff R (1999) Ion channels in presynaptic nerve terminals and control of transmitter release. Physiol Rev 79:1019-1088.
48. Miller GW, Staley JK, Heilman CJ, Perez JT, Mash DC, Rye DB, Levey AI (1997) Immunochemical analysis of dopamine transporter protein in Parkinson's disease. Ann Neurol 41:530-539.
49. Moratalla R, Quinn B, DeLanney LE, Irwin I, Langston JW, Graybiel AM (1992) Differential vulnerability of primate caudate-putamen and striosome-matrix dopamine systems to the neurotoxic effects of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc Natl Acad Sci USA 89:3859-3863.
50. Nirenberg MJ, Chan J, Pohorille A, Vaughan RA, Uhl GR, Kuhar MJ, Pickel VM (1997) The dopamine transporter: Comparative ultrastructure of dopaminergic axons in limbic and motor compartments of the nucleus accumbens. J Neurosci 17:6899-6907.
51. Olanow CW, Tatton WG (1999) Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci 22:123-144.
52. Parent A, Mackey A, De Bellefeuille L (1983) The subcortical afferents to caudate nucleus and putamen in primate: A fluorescence retrograde double labeling study. Neuroscience 10:1137-1150.
53. Rice ME, Cragg SJ, Greenfield SA (1997) Characteristics of electrically evoked somatodendritic dopamine release in substantia nigra and ventral tegmental area in vitro. J Neurophysiol 77:853-862.
54. Ross SB (1991) Synaptic concentration of dopamine in the mouse striatum in relationship to the kinetic properties of the dopamine receptors and uptake mechanism. J Neurochem 56:22-29.
55. Russchen FT, Bakst I, Amaral DG, Price JL (1985) The amygdalostriatal projections in the monkey: An anterograde tracing study. Brain Res 329:241-257.
56. Sanghera MK, Manaye KF, Liang C-L, Iacopino AM, Bannon MJ, German DC (1994) Low dopamine transporter mRNA levels in midbrain regions containing calbindin. NeuroReport 5:1641-1644.
57. 3H]cocaine binding associated with dopamine uptake sites in the rat striatum and human putamen decrease after dopaminergic denervation and in Parkinson's disease. Naunyn Schmiedebergs Arch Pharmacol 329:227-235.
58. Schultz W (1984) Primate dopamine cell activity in relation to behavioural acts. Clin Neuropharmacol 7:48-49.
59. Schultz W (1986) Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. J Neurophysiol 56:1439-1461.
60. Schultz W, Ruffieux A, Aebischer P (1983) The activity of pars compacta neurons of the monkey substantia nigra in relation to motor activation. Exp Brain Res 51:377-387.
61. Seeman P, Niznik HB (1990) Dopamine receptors and transporters in Parkinson's disease and schizophrenia. FASEB J 4:2737-2744.
62. Selemon LD, Goldman-Rakic PS (1985) Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey. J Neurosci 5:776-794.
63. Sesack SR, Hawrylak VA, Matus C, Guido MA, Levey AI (1998) Dopamine axon varicosities in the prelimbic division of the rat prefrontal cortex exhibit sparse immunoreactivity for the dopamine transporter. J Neurosci 18:2687-2708.
64. Shimada S, Kitayama S, Walther D, Uhl G (1992) Dopamine transporter mRNA: Dense expression in ventral midbrain neurons. Mol Brain Res 13:359-362.
65. Smith Y, Parent A (1986) Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18:347-371.
66. Stephan H, Baron G, Schwerdtfeger WK (1980) The Brain of the Common Marmoset (Callithrix Jacchus): A Stereotaxic Atlas. New York: Springer.
67. Szabo J (1980) Organization of the ascending striatal afferents in monkeys. J Comp Neurol 189:307-321.
68. Thomson AM (2000) Molecular frequency filters at central synapses. Prog Neurobiol 62:159-196.
69. Wightman RM, Zimmerman JB (1990) Control of dopamine extracellular concentration in rat striatum by impulse flow and uptake. Brain Res Brain Res Rev 15:135-144.
70. Wightman RM, Amatore C, Engstrom RC, Hale PD, Kristensen EW, Kuhr WG, May LJ (1988) Real-time characterization of dopamine overflow and uptake in the rat striatum. Neuroscience 25:513-523.
71. Wolfart J, Neuhoff H, Franz O, Roeper J (2001) Differential expression of the small-conductance, calcium-activated potassium channel SK3 is critical for pacemaker control in dopaminergic midbrain neurons. J Neurosci 21:3443-3456.
72. Wu Q, Reith ME, Kuhar MJ, Carroll FI, Garris PA (2001) Preferential increases in nucleus accumbens dopamine after systemic cocaine administration are caused by unique characteristics of dopamine neurotransmission. J Neurosci 21:6338-6347.