1932
0
  1. Home
  2. A-Z Publications
  3. Annual Review of Neuroscience
  4. Volume 37, 2014
  5. Article

Annual Review of Neuroscience

Volume 37, 2014

Reassessing Models of Basal Ganglia Function and Dysfunction

Abstract

The basal ganglia are a series of interconnected subcortical nuclei. The function and dysfunction of these nuclei have been studied intensively in motor control, but more recently our knowledge of these functions has broadened to include prominent roles in cognition and affective control. This review summarizes historical models of basal ganglia function, as well as findings supporting or conflicting with these models, while emphasizing recent work in animals and humans directly testing the hypotheses generated by these models.

Keyword(s): dopamine, Parkinson's disease, striatum
Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-071013-013916
2014-07-08
2024-04-16
Loading full text...

Full text loading...

/deliver/fulltext/neuro/37/1/annurev-neuro-071013-013916.html?itemId=/content/journals/10.1146/annurev-neuro-071013-013916&mimeType=html&fmt=ahah

Literature Cited

  1. Albin RL, Young AB, Penney JB. 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci. 12:366–75 [Google Scholar]
  2. Albin RL, Young AB, Penney JB, Handelin B, Balfour R. et al. 1990. Abnormalities of striatal projection neurons and N-methyl-d-aspartate receptors in presymptomatic Huntington's disease. N. Engl. J. Med. 322:1293–98 [Google Scholar]
  3. Alexander GE, DeLong MR, Strick PL. 1986. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 9:357–81 [Google Scholar]
  4. Andre VM, Cepeda C, Cummings DM, Jocoy EL, Fisher YE. et al. 2010. Dopamine modulation of excitatory currents in the striatum is dictated by the expression of D1 or D2 receptors and modified by endocannabinoids. Eur. J. Neurosci. 31:14–28 [Google Scholar]
  5. Aylward EH, Sparks BF, Field KM, Yallapragada V, Shpritz BD. et al. 2004. Onset and rate of striatal atrophy in preclinical Huntington disease. Neurology 63:66–72 [Google Scholar]
  6. Bateup HS, Santini E, Shen W, Birnbaum S, Valjent E. et al. 2010. Distinct subclasses of medium spiny neurons differentially regulate striatal motor behaviors. Proc. Natl. Acad. Sci. USA 107:14845–50 [Google Scholar]
  7. Benarroch EE. 2013. Pedunculopontine nucleus: functional organization and clinical implications. Neurology 80:1148–55 [Google Scholar]
  8. Benazzouz A, Breit S, Koudsie A, Pollak P, Krack P, Benabid AL. 2002. Intraoperative microrecordings of the subthalamic nucleus in Parkinson's disease. Mov. Disord. 17:Suppl. 3S145–49 [Google Scholar]
  9. Berendse HW, Groenewegen HJ. 1990. Organization of the thalamostriatal projections in the rat, with special emphasis on the ventral striatum. J. Comp. Neurol. 299:187–228 [Google Scholar]
  10. Bergman H, Wichmann T, DeLong MR. 1990. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436–38 [Google Scholar]
  11. Bergman H, Wichmann T, Karmon B, DeLong MR. 1994. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 72:507–20 [Google Scholar]
  12. Berman BD, Starr PA, Marks WJ Jr, Ostrem JL. 2009. Induction of bradykinesia with pallidal deep brain stimulation in patients with cranial-cervical dystonia. Stereotact. Funct. Neurosurg. 87:37–44 [Google Scholar]
  13. Bevan MD, Booth PA, Eaton SA, Bolam JP. 1998. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J. Neurosci. 18:9438–52 [Google Scholar]
  14. Carpenter MB, Carleton SC, Keller JT, Conte P. 1981. Connections of the subthalamic nucleus in the monkey. Brain Res. 224:1–29 [Google Scholar]
  15. Chen CC, Kühn AA, Hoffmann KT, Kupsch A, Schneider GH. et al. 2006. Oscillatory pallidal local field potential activity correlates with involuntary EMG in dystonia. Neurology 66:418–20 [Google Scholar]
  16. Cools R. 2006. Dopaminergic modulation of cognitive function-implications for l-DOPA treatment in Parkinson's disease. Neurosci. Biobehav. Rev. 30:1–23 [Google Scholar]
  17. Cubo E, Shannon KM, Penn RD, Kroin JS. 2000. Internal globus pallidotomy in dystonia secondary to Huntington's disease. Mov. Disord. 15:1248–51 [Google Scholar]
  18. Cui G, Jun SB, Jin X, Pham MD, Vogel SS. et al. 2013. Concurrent activation of striatal direct and indirect pathways during action initiation. Nature 494:238–42 [Google Scholar]
  19. de Hemptinne C, Ryapolova-Webb ES, Air EL, Garcia PA, Miller KJ. et al. 2013. Exaggerated phase-amplitude coupling in the primary motor cortex in Parkinson disease. Proc. Natl. Acad. Sci. USA 110:4780–85 [Google Scholar]
  20. DeLong MR. 1983. The neurophysiologic basis of abnormal movements in basal ganglia disorders. Neurobehav. Toxicol. Teratol. 5:611–16 [Google Scholar]
  21. DeLong MR. 1990. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13:281–85 [Google Scholar]
  22. Deng YP, Albin RL, Penney JB, Young AB, Anderson KD, Reiner A. 2004. Differential loss of striatal projection systems in Huntington's disease: a quantitative immunohistochemical study. J. Chem. Neuroanat. 27:143–64 [Google Scholar]
  23. Deschênes M, Bourassa J, Doan VD, Parent A. 1996. A single-cell study of the axonal projections arising from the posterior intralaminar thalamic nuclei in the rat. Eur. J. Neurosci. 8:329–43 [Google Scholar]
  24. Desmurget M, Turner RS. 2008. Testing basal ganglia motor functions through reversible inactivations in the posterior internal globus pallidus. J. Neurophysiol. 99:1057–76 [Google Scholar]
  25. Drago J, Padungchaichot P, Wong JY, Lawrence AJ, McManus JF. et al. 1998. Targeted expression of a toxin gene to D1 dopamine receptor neurons by Cre-mediated site-specific recombination. J. Neurosci. 18:9845–57 [Google Scholar]
  26. Durieux PF, Bearzatto B, Guiducci S, Buch T, Waisman A. et al. 2009. D2R striatopallidal neurons inhibit both locomotor and drug reward processes. Nat. Neurosci. 12:393–95 [Google Scholar]
  27. Durieux PF, Schiffmann SN, de Kerchove d'Exaerde A. 2012. Differential regulation of motor control and response to dopaminergic drugs by D1R and D2R neurons in distinct dorsal striatum subregions. EMBO J. 31:640–53 [Google Scholar]
  28. Edley SM, Graybiel AM. 1983. The afferent and efferent connections of the feline nucleus tegmenti pedunculopontinus, pars compacta. J. Comp. Neurol. 217:187–215 [Google Scholar]
  29. Elena Erro M, Lanciego JL, Gimenez-Amaya JM. 2002. Re-examination of the thalamostriatal projections in the rat with retrograde tracers. Neurosci. Res. 42:45–55 [Google Scholar]
  30. Ellens DJ, Leventhal DK. 2013. Review: electrophysiology of basal ganglia and cortex in models of Parkinson disease. J. Parkinsons Dis. 3:241–54 [Google Scholar]
  31. Eusebio A, Brown P. 2009. Synchronisation in the beta frequency-band—the bad boy of parkinsonism or an innocent bystander?. Exp. Neurol. 217:1–3 [Google Scholar]
  32. Eusebio A, Pogosyan A, Wang S, Averbeck B, Gaynor LD. et al. 2009. Resonance in subthalamo-cortical circuits in Parkinson's disease. Brain 132:2139–50 [Google Scholar]
  33. Fan D, Rossi MA, Yin HH. 2012. Mechanisms of action selection and timing in substantia nigra neurons. J. Neurosci. 32:5534–48 [Google Scholar]
  34. Ferrante RJ, Kowall NW, Richardson EP Jr. 1991. Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: a combined study using the section-Golgi method and calbindin D28k immunocytochemistry. J. Neurosci. 11:3877–87 [Google Scholar]
  35. Filion M, Tremblay L. 1991. Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res. 547:142–51 [Google Scholar]
  36. Filion M, Tremblay L, Bédard PJ. 1991. Effects of dopamine agonists on the spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res. 547:152–61 [Google Scholar]
  37. Freeze BS, Kravitz AV, Hammack N, Berke JD, Kreitzer AC. 2013. Control of basal ganglia output by direct and indirect pathway projection neurons. J. Neurosci. 33:18531–39 [Google Scholar]
  38. Gerfen CR, Engber TM, Mahan LC, Susel Z, Chase TN. et al. 1990. D1 and D2 dopamine receptor-regulated gene expression of striatonigral and striatopallidal neurons. Science 250:1429–32 [Google Scholar]
  39. Gradinaru V, Mogri M, Thompson KR, Henderson JM, Deisseroth K. 2009. Optical deconstruction of parkinsonian neural circuitry. Science 324:354–59 [Google Scholar]
  40. Graybiel AM. 2008. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci. 31:359–87 [Google Scholar]
  41. Groenewegen HJ, Berendse HW. 1990. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J. Comp. Neurol. 294:607–22 [Google Scholar]
  42. Gulley JM, Kosobud AE, Rebec GV. 2002. Behavior-related modulation of substantia nigra pars reticulata neurons in rats performing a conditioned reinforcement task. Neuroscience 111:337–49 [Google Scholar]
  43. Gulley JM, Kuwajima M, Mayhill E, Rebec GV. 1999. Behavior-related changes in the activity of substantia nigra pars reticulata neurons in freely moving rats. Brain Res. 845:68–76 [Google Scholar]
  44. Guridi J, Herrero MT, Luquin R, Guillen J, Obeso JA. 1994. Subthalamotomy improves MPTP-induced parkinsonism in monkeys. Stereotact. Funct. Neurosurg. 62:98–102 [Google Scholar]
  45. Hahn PJ, Russo GS, Hashimoto T, Miocinovic S, Xu W. et al. 2008. Pallidal burst activity during therapeutic deep brain stimulation. Exp. Neurol. 211:243–51 [Google Scholar]
  46. Halliday GM, McRitchie DA, Macdonald V, Double KL, Trent RJ, McCusker E. 1998. Regional specificity of brain atrophy in Huntington's disease. Exp. Neurol. 154:663–72 [Google Scholar]
  47. Heimer G, Rivlin-Etzion M, Bar-Gad I, Goldberg JA, Haber SN, Bergman H. 2006. Dopamine replacement therapy does not restore the full spectrum of normal pallidal activity in the 1-methyl-4-phenyl-1,2,3,6-tetra-hydropyridine primate model of Parkinsonism. J. Neurosci. 26:8101–14 [Google Scholar]
  48. Hikida T, Kimura K, Wada N, Funabiki K, Nakanishi S. 2010. Distinct roles of synaptic transmission in direct and indirect striatal pathways to reward and aversive behavior. Neuron 66:896–907 [Google Scholar]
  49. Hikosaka O. 1991. Basal ganglia—possible role in motor coordination and learning. Curr. Opin. Neurobiol. 1:638–43 [Google Scholar]
  50. Hikosaka O. 1998. Neural systems for control of voluntary action—a hypothesis. Adv. Biophys. 35:81–102 [Google Scholar]
  51. Hikosaka O. 2007. GABAergic output of the basal ganglia. Prog. Brain Res. 160:209–26 [Google Scholar]
  52. Hikosaka O, Sakamoto M, Usui S. 1989. Functional properties of monkey caudate neurons. III. Activities related to expectation of target and reward. J. Neurophysiol. 61:814–32 [Google Scholar]
  53. Hikosaka O, Wurtz RH. 1983. Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J. Neurophysiol. 49:1230–53 [Google Scholar]
  54. Hollerman JR, Tremblay L, Schultz W. 1998. Influence of reward expectation on behavior-related neuronal activity in primate striatum. J. Neurophysiol. 80:947–63 [Google Scholar]
  55. Hutchison WD, Allan RJ, Opitz H, Levy R, Dostrovsky JO. et al. 1998. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease. Ann. Neurol. 44:622–28 [Google Scholar]
  56. Irwin DJ, White MT, Toledo JB, Xie SX, Robinson JL. et al. 2012. Neuropathologic substrates of Parkinson disease dementia. Ann. Neurol. 72:587–98 [Google Scholar]
  57. Isomura Y, Takekawa T, Harukuni R, Handa T, Aizawa H. et al. 2013. Reward-modulated motor information in identified striatum neurons. J. Neurosci. 33:10209–20 [Google Scholar]
  58. Jaeger D, Kita H. 2011. Functional connectivity and integrative properties of globus pallidus neurons. Neuroscience 198:44–53 [Google Scholar]
  59. Jernigan TL, Salmon DP, Butters N, Hesselink JR. 1991. Cerebral structure on MRI, Part II: Specific changes in Alzheimer's and Huntington's diseases. Biol. Psychiatry 29:68–81 [Google Scholar]
  60. Jessell TM, Emson PC, Paxinos G, Cuello AC. 1978. Topographic projections of substance P and GABA pathways in the striato- and pallido-nigral system: a biochemical and immunohistochemical study. Brain Res. 152:487–98 [Google Scholar]
  61. Jin X, Costa RM. 2010. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466:457–62 [Google Scholar]
  62. Jin X, Tecuapetla F, Costa RM. 2014. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat. Neurosci. 17:423–30 [Google Scholar]
  63. Jones EG, Leavitt RY. 1974. Retrograde axonal transport and the demonstration of non-specific projections to the cerebral cortex and striatum from thalamic intralaminar nuclei in the rat, cat and monkey. J. Comp. Neurol. 154:349–77 [Google Scholar]
  64. Kang GA, Heath S, Rothlind J, Starr PA. 2011. Long-term follow-up of pallidal deep brain stimulation in two cases of Huntington's disease. J. Neurol. Neurosurg. Psychiatry 82:272–77 [Google Scholar]
  65. Kawagoe R, Takikawa Y, Hikosaka O. 1998. Expectation of reward modulates cognitive signals in the basal ganglia. Nat. Neurosci. 1:411–16 [Google Scholar]
  66. Kimchi EY, Laubach M. 2009. Dynamic encoding of action selection by the medial striatum. J. Neurosci. 29:3148–59 [Google Scholar]
  67. Kita H, Kita T. 2001. Number, origins, and chemical types of rat pallidostriatal projection neurons. J. Comp. Neurol. 437:438–48 [Google Scholar]
  68. Kita H, Kitai ST. 1987. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. Comp. Neurol. 260:435–52 [Google Scholar]
  69. Kitai ST, Deniau JM. 1981. Cortical inputs to the subthalamus: intracellular analysis. Brain Res. 214:411–15 [Google Scholar]
  70. Kravitz AV, Freeze BS, Parker PRL, Kay K, Thwin MT. et al. 2010. Regulation of parkinsonian motor behaviours by optogenetic control of basal ganglia circuitry. Nature 466:622–26 [Google Scholar]
  71. Langston JW, Ballard P, Tetrud JW, Irwin I. 1983. Chronic Parkinsonism in humans due to a product of meperidine-analog synthesis. Science 219:979–80 [Google Scholar]
  72. Leventhal DK, Gage GJ, Schmidt R, Pettibone JR, Case AC, Berke JD. 2012. Basal ganglia beta oscillations accompany cue utilization. Neuron 73:523–36 [Google Scholar]
  73. Levy R, Dostrovsky JO, Lang AE, Sime E, Hutchison WD, Lozano AM. 2001a. Effects of apomorphine on subthalamic nucleus and globus pallidus internus neurons in patients with Parkinson's disease. J. Neurophysiol. 86:249–60 [Google Scholar]
  74. Levy R, Lang AE, Dostrovsky JO, Pahapill P, Romas J. et al. 2001b. Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 124:2105–18 [Google Scholar]
  75. Liang L, DeLong MR, Papa SM. 2008. Inversion of dopamine responses in striatal medium spiny neurons and involuntary movements. J. Neurosci. 28:7537–47 [Google Scholar]
  76. Litvak V, Jha A, Eusebio A, Oostenveld R, Foltynie T. et al. 2011. Resting oscillatory cortico-subthalamic connectivity in patients with Parkinson's disease. Brain 134:359–74 [Google Scholar]
  77. Lozano AM, Lang AE, Levy R, Hutchison W, Dostrovsky J. 2000. Neuronal recordings in Parkinson's disease patients with dyskinesias induced by apomorphine. Ann. Neurol. 47:S141–46 [Google Scholar]
  78. Mailly P, Aliane V, Groenewegen HJ, Haber SN, Deniau JM. 2013. The rat prefrontostriatal system analyzed in 3D: evidence for multiple interacting functional units. J. Neurosci. 33:5718–27 [Google Scholar]
  79. Mallet N, Ballion B, Le Moine C, Gonon F. 2006. Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J. Neurosci. 26:3875–84 [Google Scholar]
  80. Mallet N, Micklem BR, Henny P, Brown MT, Williams C. et al. 2012. Dichotomous organization of the external globus pallidus. Neuron 74:1075–86 [Google Scholar]
  81. McCairn KW, Turner RS. 2009. Deep brain stimulation of the globus pallidus internus in the parkinsonian primate: local entrainment and suppression of low-frequency oscillations. J. Neurophysiol. 101:1941–60 [Google Scholar]
  82. McFarland NR, Haber SN. 2000. Convergent inputs from thalamic motor nuclei and frontal cortical areas to the dorsal striatum in the primate. J. Neurosci. 20:3798–813 [Google Scholar]
  83. McFarland NR, Haber SN. 2001. Organization of thalamostriatal terminals from the ventral motor nuclei in the macaque. J. Comp. Neurol. 429:321–36 [Google Scholar]
  84. Mink JW. 1996. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50:381–425 [Google Scholar]
  85. Mink JW. 2001. Neurobiology of basal ganglia circuits in Tourette syndrome: faulty inhibition of unwanted motor patterns?. Adv. Neurol. 85:113–22 [Google Scholar]
  86. Mink JW, Thach WT. 1993. Basal ganglia intrinsic circuits and their role in behavior. Curr. Opin. Neurobiol. 3:950–57 [Google Scholar]
  87. Monakow KH, Akert K, Künzle H. 1978. Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Exp. Brain Res. 33:395–403 [Google Scholar]
  88. Moro E, Lang AE, Strafella AP, Poon YY, Arango PM. et al. 2004. Bilateral globus pallidus stimulation for Huntington's disease. Ann. Neurol. 56:290–94 [Google Scholar]
  89. Nambu A, Takada M, Inase M, Tokuno H. 1996. Dual somatotopical representations in the primate subthalamic nucleus: evidence for ordered but reversed body-map transformations from the primary motor cortex and the supplementary motor area. J. Neurosci. 16:2671–83 [Google Scholar]
  90. Nambu A, Tokuno H, Hamada I, Kita H, Imanishi M. et al. 2000. Excitatory cortical inputs to pallidal neurons via the subthalamic nucleus in the monkey. J. Neurophysiol. 84:289–300 [Google Scholar]
  91. Nambu A, Tokuno H, Takada M. 2002. Functional significance of the cortico-subthalamo-pallidal ‘hyperdirect’ pathway. Neurosci. Res. 43:111–17 [Google Scholar]
  92. Papa SM, Desimone R, Fiorani M, Oldfield EH. 1999. Internal globus pallidus discharge is nearly suppressed during levodopa-induced dyskinesias. Ann. Neurol. 46:732–38 [Google Scholar]
  93. Parent A. 1976. Striatal afferent connections in the turtle (Chrysemys picta) as revealed by retrograde axonal transport of horseradish peroxidase. Brain Res. 108:25–36 [Google Scholar]
  94. Parent A, Hazrati LN. 1995. Functional anatomy of the basal ganglia. II. The place of subthalamic nucleus and external pallidum in basal ganglia circuitry. Brain Res. Brain Res. Rev. 20:128–54 [Google Scholar]
  95. Parent M, Parent A. 2004. The pallidofugal motor fiber system in primates. Park. Relat. Disord. 10:203–11 [Google Scholar]
  96. Paulsen JS. 2011. Cognitive impairment in Huntington disease: diagnosis and treatment. Curr. Neurol. Neurosci. Rep. 11:474–83 [Google Scholar]
  97. Penney JB Jr, Young AB. 1983. Speculations on the functional anatomy of basal ganglia disorders. Annu. Rev. Neurosci. 6:73–94 [Google Scholar]
  98. Planert H, Berger TK, Silberberg G. 2013. Membrane properties of striatal direct and indirect pathway neurons in mouse and rat slices and their modulation by dopamine. PloS ONE 8:e57054 [Google Scholar]
  99. Plenz D, Kital ST. 1999. A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677–82 [Google Scholar]
  100. Ragsdale CW Jr, Graybiel AM. 1991. Compartmental organization of the thalamostriatal connection in the cat. J. Comp. Neurol. 311:134–67 [Google Scholar]
  101. Raz A, Vaadia E, Bergman H. 2000. Firing patterns and correlations of spontaneous discharge of pallidal neurons in the normal and the tremulous 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine vervet model of parkinsonism. J. Neurosci. 20:8559–71 [Google Scholar]
  102. Redgrave P, Rodriguez M, Smith Y, Rodriguez-Oroz MC, Lehericy S. et al. 2010. Goal-directed and habitual control in the basal ganglia: implications for Parkinson's disease. Nat. Rev. Neurosci. 11:760–72 [Google Scholar]
  103. Reiner A, Albin RL, Anderson KD, D'Amato CJ, Penney JB, Young AB. 1988. Differential loss of striatal projection neurons in Huntington disease. Proc. Natl. Acad. Sci. USA 85:5733–37 [Google Scholar]
  104. Reiner A, Dragatsis I, Dietrich P. 2011. Genetics and neuropathology of Huntington's disease. Int. Rev. Neurobiol. 98:325–72 [Google Scholar]
  105. Reiner A, Medina L, Veenman CL. 1998. Structural and functional evolution of the basal ganglia in vertebrates. Brain Res. Brain Res. Rev. 28:235–85 [Google Scholar]
  106. Richardson RM, Freed CR, Shimamoto SA, Starr PA. 2011. Pallidal neuronal discharge in Parkinson's disease following intraputamenal fetal mesencephalic allograft. J. Neurol. Neurosurg. Psychiatry 82:266–71 [Google Scholar]
  107. Rosas HD, Goodman J, Chen YI, Jenkins BG, Kennedy DN. et al. 2001. Striatal volume loss in HD as measured by MRI and the influence of CAG repeat. Neurology 57:1025–28 [Google Scholar]
  108. Rosin B, Slovik M, Mitelman R, Rivlin-Etzion M, Haber SN. et al. 2011. Closed-loop deep brain stimulation is superior in ameliorating parkinsonism. Neuron 72:370–84 [Google Scholar]
  109. Rothblat DS, Schneider JS. 1993. Response of caudate neurons to stimulation of intrinsic and peripheral afferents in normal, symptomatic, and recovered MPTP-treated cats. J. Neurosci. 13:4372–78 [Google Scholar]
  110. Royce GJ. 1978. Cells of origin of subcortical afferents to the caudate nucleus: a horseradish peroxidase study in the cat. Brain Res. 153:465–75 [Google Scholar]
  111. Sadikot AF, Parent A, Smith Y, Bolam JP. 1992. 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. 320:228–42 [Google Scholar]
  112. Sano H, Chiken S, Hikida T, Kobayashi K, Nambu A. 2013. Signals through the striatopallidal indirect pathway stop movements by phasic excitation in the substantia nigra. J. Neurosci. 33:7583–94 [Google Scholar]
  113. Sano H, Yasoshima Y, Matsushita N, Kaneko T, Kohno K. et al. 2003. Conditional ablation of striatal neuronal types containing dopamine D2 receptor disturbs coordination of basal ganglia function. J. Neurosci. 23:9078–88 [Google Scholar]
  114. Sato F, Lavallée P, Lévesque M, Parent A. 2000a. Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J. Comp. Neurol. 417:17–31 [Google Scholar]
  115. Sato F, Parent M, Levesque M, Parent A. 2000b. Axonal branching pattern of neurons of the subthalamic nucleus in primates. J. Comp. Neurol. 424:142–52 [Google Scholar]
  116. Sato M, Itoh K, Mizuno N. 1979. Distribution of thalamo-caudate neurons in the cat as demonstrated by horseradish peroxidase. Exp. Brain Res. Exp. 34:143–53 [Google Scholar]
  117. Schiffmann SN, Vanderhaeghen JJ. 1993. Adenosine A2 receptors regulate the gene expression of striatopallidal and striatonigral neurons. J. Neurosci. 13:1080–87 [Google Scholar]
  118. Schmidt R, Leventhal DK, Mallet N, Chen F, Berke JD. 2013. Canceling actions involves a race between basal ganglia pathways. Nat. Neurosci. 16:1118–24 [Google Scholar]
  119. Schrock LE, Ostrem JL, Turner RS, Shimamoto SA, Starr PA. 2009. The subthalamic nucleus in primary dystonia: single-unit discharge characteristics. J. Neurophysiol. 102:3740–52 [Google Scholar]
  120. Shimamoto SA, Ryapolova-Webb ES, Ostrem JL, Galifianakis NB, Miller KJ, Starr PA. 2013. Subthalamic nucleus neurons are synchronized to primary motor cortex local field potentials in Parkinson's disease. J. Neurosci. 33:7220–33 [Google Scholar]
  121. Smith Y, Hazrati LN, Parent A. 1990. Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J. Comp. Neurol. 294:306–23 [Google Scholar]
  122. Smith Y, Kieval JZ. 2000. Anatomy of the dopamine system in the basal ganglia. Trends Neurosci. 23:S28–33 [Google Scholar]
  123. Smith Y, Parent A. 1986. Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18:347–71 [Google Scholar]
  124. Smith Y, Raju DV, Pare JF, Sidibe M. 2004. The thalamostriatal system: a highly specific network of the basal ganglia circuitry. Trends Neurosci. 27:520–27 [Google Scholar]
  125. Starr PA, Kang GA, Heath S, Shimamoto S, Turner RS. 2008. Pallidal neuronal discharge in Huntington's disease: support for selective loss of striatal cells originating the indirect pathway. Exp. Neurol. 211:227–33 [Google Scholar]
  126. Starr PA, Rau GM, Davis V, Marks WJ Jr, Ostrem JL. et al. 2005. Spontaneous pallidal neuronal activity in human dystonia: comparison with Parkinson's disease and normal macaque. J. Neurophysiol. 93:3165–76 [Google Scholar]
  127. Steigerwald F, Pötter M, Herzog J, Pinsker M, Kopper F. et al. 2008. Neuronal activity of the human subthalamic nucleus in the parkinsonian and nonparkinsonian state. J. Neurophysiol. 100:2515–24 [Google Scholar]
  128. Stephenson-Jones M, Ericsson J, Robertson B, Grillner S. 2012. Evolution of the basal ganglia: dual-output pathways conserved throughout vertebrate phylogeny. J. Comp. Neurol. 520:2957–73 [Google Scholar]
  129. Stuber GD, Hnasko TS, Britt JP, Edwards RH, Bonci A. 2010. Dopaminergic terminals in the nucleus accumbens but not the dorsal striatum corelease glutamate. J. Neurosci. 30:8229–33 [Google Scholar]
  130. Tabrizi SJ, Scahill RI, Owen G, Durr A, Leavitt BR. et al. 2013. Predictors of phenotypic progression and disease onset in premanifest and early-stage Huntington's disease in the TRACK-HD study: analysis of 36-month observational data. Lancet Neurol. 12:637–49 [Google Scholar]
  131. Tachibana Y, Iwamuro H, Kita H, Takada M, Nambu A. 2011. Subthalamo-pallidal interactions underlying parkinsonian neuronal oscillations in the primate basal ganglia. Eur. J. Neurosci. 34:1470–84 [Google Scholar]
  132. Tai LH, Lee AM, Benavidez N, Bonci A, Wilbrecht L. 2012. Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value. Nat. Neurosci. 15:1281–89 [Google Scholar]
  133. Tang JK, Moro E, Lozano AM, Lang AE, Hutchison WD. et al. 2005. Firing rates of pallidal neurons are similar in Huntington's and Parkinson's disease patients. Exp. Brain Res. 166:230–36 [Google Scholar]
  134. Tippett LJ, Waldvogel HJ, Thomas SJ, Hogg VM, van Roon-Mom W. et al. 2007. Striosomes and mood dysfunction in Huntington's disease. Brain 130:206–21 [Google Scholar]
  135. Tritsch NX, Ding JB, Sabatini BL. 2012. Dopaminergic neurons inhibit striatal output through non-canonical release of GABA. Nature 490:262–66 [Google Scholar]
  136. Vitek JL, Chockkan V, Zhang JY, Kaneoke Y, Evatt M. et al. 1999. Neuronal activity in the basal ganglia in patients with generalized dystonia and hemiballismus. Ann. Neurol. 46:22–35 [Google Scholar]
  137. Vitek JL, Zhang J, Hashimoto T, Russo GS, Baker KB. 2012. External pallidal stimulation improves parkinsonian motor signs and modulates neuronal activity throughout the basal ganglia thalamic network. Exp. Neurol. 233:581–86 [Google Scholar]
  138. Wall NR, De La Parra M, Callaway EM, Kreitzer AC. 2013. Differential innervation of direct- and indirect-pathway striatal projection neurons. Neuron 79:347–60 [Google Scholar]
  139. Weinberger M, Hutchison WD, Alavi M, Hodaie M, Lozano AM. et al. 2012. Oscillatory activity in the globus pallidus internus: comparison between Parkinson's disease and dystonia. Clin. Neurophysiol. 123:358–68 [Google Scholar]
  140. Wichmann T, Bergman H, DeLong MR. 1994. 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. 72:521–30 [Google Scholar]
  141. Wichmann T, Bergman H, Starr PA, Subramanian T, Watts RL, DeLong MR. 1999. Comparison of MPTP-induced changes in spontaneous neuronal discharge in the internal pallidal segment and in the substantia nigra pars reticulata in primates. Exp. Brain Res. 125:397–409 [Google Scholar]
/content/journals/10.1146/annurev-neuro-071013-013916
Loading
Reassessing Models of Basal Ganglia Function and Dysfunction
Annual Review of Neuroscience 37, 117 (2014); https://doi.org/10.1146/annurev-neuro-071013-013916
/content/journals/10.1146/annurev-neuro-071013-013916
/content/journals/10.1146/annurev-neuro-071013-013916
Loading

Data & Media loading...

  • Article Type: Review Article

Most Cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error