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Abstract

Deciding what to do and when to move is vital to our survival. Clinical and fundamental studies have identified basal ganglia circuits as critical for this process. The main input nucleus of the basal ganglia, the striatum, receives inputs from frontal, sensory, and motor cortices and interconnected thalamic areas that provide information about potential goals, context, and actions and directly or indirectly modulates basal ganglia outputs. The striatum also receives dopaminergic inputs that can signal reward prediction errors and also behavioral transitions and movement initiation. Here we review studies and models of how direct and indirect pathways can modulate basal ganglia outputs to facilitate movement initiation, and we discuss the role of cortical and dopaminergic inputs to the striatum in determining what to do and if and when to do it. Complex but exciting scenarios emerge that shed new light on how basal ganglia circuits modulate self-paced movement initiation.

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2019-07-08
2024-10-13
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Literature Cited

  1. Albin RL, Young AB, Penney JB 1995. The functional anatomy of disorders of the basal ganglia. Trends Neurosci 18:263–64
    [Google Scholar]
  2. Alcacer C, Andreoli L, Sebastianutto I, Jakobsson J, Fieblinger T, Cenci MA 2017. Chemogenetic stimulation of striatal projection neurons modulates responses to Parkinson's disease therapy. J. Clin. Investig. 127:2720–34
    [Google Scholar]
  3. Alexander GE, Crutcher MD. 1990. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:7266–71
    [Google Scholar]
  4. Arber S, Costa RM. 2018. Connecting neuronal circuits for movement. Science 360:63961403–4
    [Google Scholar]
  5. Aron AR, Poldrack RA. 2006. Cortical and subcortical contributions to stop signal response inhibition: role of the subthalamic nucleus. J. Neurosci. 26:92424–33
    [Google Scholar]
  6. Barbera G, Liang B, Zhang L, Gerfen CR, Culurciello E et al. 2016. Spatially compact neural clusters in the dorsal striatum encode locomotion relevant information. Neuron 92:1202–13
    [Google Scholar]
  7. Barter JW, Li S, Lu D, Bartholomew RA, Rossi MA et al. 2015. Beyond reward prediction errors: the role of dopamine in movement kinematics. Front. Integr. Neurosci. 9:39
    [Google Scholar]
  8. Berardelli A, Rothwell JC, Thompson PD, Hallett M 2001. Pathophysiology of bradykinesia in Parkinson's disease. Brain 124:Pt. 112131–46
    [Google Scholar]
  9. Berke JD. 2018. What does dopamine mean. ? Nat. Neurosci. 21:6787–93
    [Google Scholar]
  10. Berke JD, Okatan M, Skurski J, Eichenbaum HB 2004. Oscillatory entrainment of striatal neurons in freely moving rats. Neuron 43:6883–96
    [Google Scholar]
  11. Bevan MD, Booth PAC, Eaton SA, Bolam JP 1998. Selective innervation of neostriatal interneurons by a subclass of neuron in the globus pallidus of the rat. J. Neurosci. 18:229438–52
    [Google Scholar]
  12. Björklund A, Dunnett SB. 2007. Dopamine neuron systems in the brain: an update. Trends Neurosci 30:5194–202
    [Google Scholar]
  13. Blackwell KT, Czubayko U, Plenz D 2003. Quantitative estimate of synaptic inputs to striatal neurons during up and down states in vitro. J. Neurosci. 23:279123–32
    [Google Scholar]
  14. Bonanni L, Thomas A, Onofrj M 2010. Paradoxical kinesia in parkinsonian patients surviving earthquake. Mov. Disord. 25:91302–4
    [Google Scholar]
  15. Bromberg-Martin ES, Matsumoto M, Hikosaka O 2010. Dopamine in motivational control: rewarding, aversive, and alerting. Neuron 68:5815–34
    [Google Scholar]
  16. Buford JA, Davidson AG. 2004. Movement-related and preparatory activity in the reticulospinal system of the monkey. Exp. Brain Res. 159:3284–300
    [Google Scholar]
  17. Caggiano V, Leiras R, Goñi-Erro H, Masini D, Bellardita C et al. 2018. Midbrain circuits that set locomotor speed and gait selection. Nature 553:7689455–60
    [Google Scholar]
  18. Capelli P, Pivetta C, Esposito MS, Arber S 2017. Locomotor speed control circuits in the caudal brainstem. Nature 551:7680373–77
    [Google Scholar]
  19. Carli M, Evenden JL, Robbins TW 1985. Depletion of unilateral striatal dopamine impairs initiation of contralateral actions and not sensory attention. Nature 313:6004679–82
    [Google Scholar]
  20. Carlsson A, Lindqvist M, Magnusson T, Waldeck B 1958. On the presence of 3-hydroxytyramine in brain. Science 127:3296471
    [Google Scholar]
  21. Coddington LT, Dudman JT. 2018. The timing of action determines reward prediction signals in identified midbrain dopamine neurons. Nat. Neurosci. 21:111563–73
    [Google Scholar]
  22. Collins AGE, Frank MJ. 2014. Opponent actor learning (OpAL): modeling interactive effects of striatal dopamine on reinforcement learning and choice incentive. Psychol. Rev. 121:3337–66
    [Google Scholar]
  23. Corbett D, Wise RA. 1980. Intracranial self-stimulation in relation to the ascending dopaminergic systems of the midbrain: a moveable electrode mapping study. Brain Res 185:11–15
    [Google Scholar]
  24. Costa RM, Cohen D, Nicolelis MA 2004. Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr. Biol. 14:131124–34
    [Google Scholar]
  25. Costa RM, Lin S-C, Sotnikova TD, Cyr M, Gainetdinov RR et al. 2006. Rapid alterations in corticostriatal ensemble coordination during acute dopamine-dependent motor dysfunction. Neuron 52:2359–69
    [Google Scholar]
  26. Cruz AV, Mallet N, Magill PJ, Brown P, Averbeck BB 2009. Effects of dopamine depletion on network entropy in the external globus pallidus. J. Neurophysiol. 102:21092–102
    [Google Scholar]
  27. 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 494:7436238–42
    [Google Scholar]
  28. Czubayko U, Plenz D. 2002. Fast synaptic transmission between striatal spiny projection neurons. PNAS 99:2415764–69
    [Google Scholar]
  29. da Silva JA, Tecuapetla F, Paixão V, Costa RM 2018. Dopamine neuron activity before action initiation gates and invigorates future movements. Nature 554:7691244–48
    [Google Scholar]
  30. Dahlström A, Fuxe K. 1964. Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. Suppl. 62:Suppl. 2321–55
    [Google Scholar]
  31. DeLong M, Wichmann T. 2009. Update on models of basal ganglia function and dysfunction. Parkinsonism Relat. Disord. 15:Suppl. 3S237–40
    [Google Scholar]
  32. Díaz-Hernández E, Contreras-López R, Sánchez-Fuentes A, Rodríguez-Sibrían L, Ramírez-Jarquín JO, Tecuapetla F 2018. The thalamostriatal projections contribute to the initiation and execution of a sequence of movements. Neuron 100:3739–52.e5
    [Google Scholar]
  33. Ding J, Peterson JD, Surmeier DJ 2008. Corticostriatal and thalamostriatal synapses have distinctive properties. J. Neurosci. 28:256483–92
    [Google Scholar]
  34. Dobbs LK, Kaplan AR, Lemos JC, Matsui A, Rubinstein M, Alvarez VA 2016. Dopamine regulation of lateral inhibition between striatal neurons gates the stimulant actions of cocaine. Neuron 90:51100–1113
    [Google Scholar]
  35. Dodson PD, Dreyer JK, Jennings KA, Syed ECJ, Wade-Martins R et al. 2016. Representation of spontaneous movement by dopaminergic neurons is cell-type selective and disrupted in parkinsonism. PNAS 113:15E2180–88
    [Google Scholar]
  36. Donaldson I, Marsden CD, Schneider S, Bhatia K 2012. Marsden's Book of Movement Disorders Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  37. Dudman JT, Krakauer JW. 2016. The basal ganglia: from motor commands to the control of vigor. Curr. Opin. Neurobiol. 37:158–66
    [Google Scholar]
  38. Esposito MS, Capelli P, Arber S 2014. Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature 508:7496351–56
    [Google Scholar]
  39. Fife KH, Gutierrez-Reed NA, Zell V, Bailly J, Lewis CM et al. 2017. Causal role for the subthalamic nucleus in interrupting behavior. eLife 6:e27689
    [Google Scholar]
  40. Foix C, Nicolesco J. 1925. Les Noyaux Gris Centraux et La Région Mésencéphalo-Sous-Optique: Suivi d'un Appendice Sur l'Anatomie Pathologique de La Maladie de Parkinson: Anatomie Cérébrale Paris: Masson
    [Google Scholar]
  41. 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 250:49861429–32
    [Google Scholar]
  42. Gerfen CR, Surmeier DJ. 2011. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci. 34:441–66
    [Google Scholar]
  43. Gittis AH, Berke JD, Bevan MD, Chan CS, Mallet N et al. 2014. New roles for the external globus pallidus in basal ganglia circuits and behavior. J. Neurosci. 34:4615178–83
    [Google Scholar]
  44. Goldberg JA, Boraud T, Maraton S, Haber SN, Vaadia E, Bergman H 2002. Enhanced synchrony among primary motor cortex neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine primate model of Parkinson's disease. J. Neurosci. 22:114639–53
    [Google Scholar]
  45. Gremel CM, Costa RM. 2013. Orbitofrontal and striatal circuits dynamically encode the shift between goal-directed and habitual actions. Nat Commun 4:2264
    [Google Scholar]
  46. Grillner S, Robertson B, Stephenson-Jones M 2013. The evolutionary origin of the vertebrate basal ganglia and its role in action selection. J. Physiol. 591:225425–31
    [Google Scholar]
  47. Guo Q, Wang D, He X, Feng Q, Lin R et al. 2015. Whole-brain mapping of inputs to projection neurons and cholinergic interneurons in the dorsal striatum. PLOS ONE 10:4e0123381
    [Google Scholar]
  48. Guo ZV, Inagaki HK, Daie K, Druckmann S, Gerfen CR, Svoboda K 2017. Maintenance of persistent activity in a frontal thalamocortical loop. Nature 545:181–86
    [Google Scholar]
  49. Haber SN, Calzavara R. 2009. The cortico-basal ganglia integrative network: the role of the thalamus. Brain Res. Bull. 78:2–369–74
    [Google Scholar]
  50. Hamid AA, Pettibone JR, Mabrouk OS, Hetrick VL, Schmidt R et al. 2016. Mesolimbic dopamine signals the value of work. Nat. Neurosci. 19:1117–26
    [Google Scholar]
  51. Hammond C, Bergman H, Brown P 2007. Pathological synchronization in Parkinson's disease: networks, models and treatments. Trends Neurosci 30:7357–64
    [Google Scholar]
  52. Hassler R. 1938. The pathology of paralysis agitans and post-encephalitic Parkinson's. J. Psychol. Neurol. 48:387–476
    [Google Scholar]
  53. Hernádi I, Grabenhorst F, Schultz W 2015. Planning activity for internally generated reward goals in monkey amygdala neurons. Nat. Neurosci. 18:3461–69
    [Google Scholar]
  54. Hikosaka O, Takikawa Y, Kawagoe R 2000. Role of the basal ganglia in the control of purposive saccadic eye movements. Physiol. Rev. 80:3953–78
    [Google Scholar]
  55. Hintiryan H, Foster NN, Bowman I, Bay M, Song MY et al. 2016. The mouse cortico-striatal projectome. Nat. Neurosci. 19:81100–14
    [Google Scholar]
  56. Hooks BM, Papale AE, Paletzki RF, Feroze MW, Eastwood BS et al. 2018. Topographic precision in sensory and motor corticostriatal projections varies across cell type and cortical area. Nat. Commun. 9:13549
    [Google Scholar]
  57. Hornykiewicz O. 1963. [The tropical localization and content of noradrenalin and dopamine (3-hydroxytyramine) in the substantia nigra of normal persons and patients with Parkinson's disease]. Wien. Klin. Wochenschr. 75:309–12 (In German)
    [Google Scholar]
  58. Howe MW, Dombeck DA. 2016. Rapid signalling in distinct dopaminergic axons during locomotion and reward. Nature 535:7613505–10
    [Google Scholar]
  59. Huerta-Ocampo I, Mena-Segovia J, Bolam JP 2014. Convergence of cortical and thalamic input to direct and indirect pathway medium spiny neurons in the striatum. Brain Struct. Funct. 219:51787–800
    [Google Scholar]
  60. Hunnicutt BJ, Jongbloets BC, Birdsong WT, Gertz KJ, Zhong H, Mao T 2016. A comprehensive excitatory input map of the striatum reveals novel functional organization. eLife 5:e19103
    [Google Scholar]
  61. Isomura Y, Takekawa T, Harukuni R, Handa T, Aizawa H et al. 2013. Reward-modulated motor information in identified striatum neurons. J. Neurosci. 33:2510209–20
    [Google Scholar]
  62. Jankovic J. 2008. Parkinson's disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry 79:4368–76
    [Google Scholar]
  63. Jiang H, Kim HF. 2018. Anatomical inputs from the sensory and value structures to the tail of the rat striatum. Front. Neuroanat. 12:30
    [Google Scholar]
  64. Jin X, Costa RM. 2010. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature 466:7305457–62
    [Google Scholar]
  65. Jin X, Tecuapetla F, Costa RM 2014. Basal ganglia subcircuits distinctively encode the parsing and concatenation of action sequences. Nat. Neurosci. 17:3423–30
    [Google Scholar]
  66. Jog MS, Kubota Y, Connolly CI, Hillegaart V, Graybiel AM 1999. Building neural representations of habits. Science 286:54451745–49
    [Google Scholar]
  67. 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. 154:4349–377
    [Google Scholar]
  68. Kamin LJ. 1969. Selective association and conditioning. Fundamental Issues in Associative Learning NJ Mackintosh, WK Honig 42–64 Halifax, NS: Dalhousie Univ. Press
    [Google Scholar]
  69. Kato S, Fukabori R, Nishizawa K, Okada K, Yoshioka N et al. 2018. Action selection and flexible switching controlled by the intralaminar thalamic neurons. Cell Rep 22:92370–82
    [Google Scholar]
  70. Kaufman MT, Churchland MM, Ryu SI, Shenoy KV 2014. Cortical activity in the null space: permitting preparation without movement. Nat. Neurosci. 17:3440–48
    [Google Scholar]
  71. Kelley AE, Domesick VB, Nauta WJH 1982. The amygdalostriatal projection in the rat—an anatomical study by anterograde and retrograde tracing methods. Neuroscience 7:3615–30
    [Google Scholar]
  72. Kim KM, Baratta MV, Yang A, Lee D, Boyden ES, Fiorillo CD 2012. Optogenetic mimicry of the transient activation of dopamine neurons by natural reward is sufficient for operant reinforcement. PLOS ONE 7:4e33612
    [Google Scholar]
  73. Klaus A, Martins GJ, Paixao VB, Zhou P, Paninski L, Costa RM 2017. The spatiotemporal organization of the striatum encodes action space. Neuron 95:51171–80.e7
    [Google Scholar]
  74. Klaus A, Plenz D. 2016. A low-correlation resting state of the striatum during cortical avalanches and its role in movement suppression. PLOS Biol 14:12e1002582
    [Google Scholar]
  75. Koós T, Tepper JM. 1999. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 2:5467–72
    [Google Scholar]
  76. 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 466:7306622–26
    [Google Scholar]
  77. Lau B, Monteiro T, Paton JJ 2017. The many worlds hypothesis of dopamine prediction error: implications of a parallel circuit architecture in the basal ganglia. Curr. Opin. Neurobiol. 46:241–47
    [Google Scholar]
  78. Lein ES, Hawrylycz MJ, Ao N, Ayres M, Bensinger A et al. 2007. Genome-wide atlas of gene expression in the adult mouse brain. Nature 445:7124168–76
    [Google Scholar]
  79. Lemon RN. 2008. Descending pathways in motor control. Annu. Rev. Neurosci. 31:195–218
    [Google Scholar]
  80. Li N, Chen T-W, Guo ZV, Gerfen CR, Svoboda K 2015. A motor cortex circuit for motor planning and movement. Nature 519:754151–56
    [Google Scholar]
  81. Li Y, Zeng J, Zhang J, Yue C, Zhong W et al. 2018. Hypothalamic circuits for predation and evasion. Neuron 97:4911–924.e5
    [Google Scholar]
  82. London TD, Licholai JA, Szczot I, Ali MA, LeBlanc KH et al. 2018. Coordinated ramping of dorsal striatal pathways preceding food approach and consumption. J. Neurosci. 38:3547–58
    [Google Scholar]
  83. Maeda K, Kunimatsu J, Hikosaka O 2018. Amygdala activity for the modulation of goal-directed behavior in emotional contexts. PLOS Biol 16:6e2005339
    [Google Scholar]
  84. Majid DSA, Cai W, Corey-Bloom J, Aron AR 2013. Proactive selective response suppression is implemented via the basal ganglia. J. Neurosci. 33:3313259–69
    [Google Scholar]
  85. Mallet N, Micklem BR, Henny P, Brown MT, Williams C et al. 2012. Dichotomous organization of the external globus pallidus. Neuron 74:61075–86
    [Google Scholar]
  86. Mallet N, Schmidt R, Leventhal D, Chen F, Amer N et al. 2016. Arkypallidal cells send a stop signal to striatum. Neuron 89:2308–16
    [Google Scholar]
  87. Markowitz JE, Gillis WF, Beron CC, Neufeld SQ, Robertson K et al. 2018. The striatum organizes 3D behavior via moment-to-moment action selection. Cell 174:144–58.e17
    [Google Scholar]
  88. Mastro KJ, Zitelli KT, Willard AM, Leblanc KH, Kravitz AV, Gittis AH 2017. Cell-specific pallidal intervention induces long-lasting motor recovery in dopamine-depleted mice. Nat. Neurosci. 20:6815–23
    [Google Scholar]
  89. Matsumoto M, Hikosaka O. 2009. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature 459:7248837–41
    [Google Scholar]
  90. Mazzoni P, Hristova A, Krakauer JW 2007. Why don't we move faster? Parkinson's disease, movement vigor, and implicit motivation. J. Neurosci. 27:277105–16
    [Google Scholar]
  91. Menegas W, Akiti K, Amo R, Uchida N, Watabe-Uchida M 2018. Dopamine neurons projecting to the posterior striatum reinforce avoidance of threatening stimuli. Nat. Neurosci. 21:1421–30
    [Google Scholar]
  92. Menegas W, Babayan BM, Uchida N, Watabe-Uchida M 2017. Opposite initialization to novel cues in dopamine signaling in ventral and posterior striatum in mice. Elife 6:e21886
    [Google Scholar]
  93. Minamimoto T, Hori Y, Kimura M 2005. Complementary process to response bias in the centromedian nucleus of the thalamus. Science 308:57291798–801
    [Google Scholar]
  94. Mink JW. 1996. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50:4381–425
    [Google Scholar]
  95. Mirenowicz J, Schultz W. 1994. Importance of unpredictability for reward responses in primate dopamine neurons. J. Neurophysiol. 72:21024–27
    [Google Scholar]
  96. Montague PR, Dayan P, Sejnowski TJ 1996. A framework for mesencephalic dopamine systems based on predictive Hebbian learning. J. Neurosci. 16:51936–47
    [Google Scholar]
  97. Nisenbaum ES, Wilson CJ. 1995. Potassium currents responsible for inward and outward rectification in rat neostriatal spiny projection neurons. J. Neurosci. 15:64449–63
    [Google Scholar]
  98. Niv Y, Daw ND, Dayan P 2005. How fast to work: response vigor, motivation and tonic dopamine. Adv. Neural Inf. Process. Syst. 18:1019–26
    [Google Scholar]
  99. Nomoto K, Schultz W, Watanabe T, Sakagami M 2010. Temporally extended dopamine responses to perceptually demanding reward-predictive stimuli. J. Neurosci. 30:3210692–702
    [Google Scholar]
  100. Nonomura S, Nishizawa K, Sakai Y, Kawaguchi Y, Kato S et al. 2018. Monitoring and updating of action selection for goal-directed behavior through the striatal direct and indirect pathways. Neuron 99:61302–14.e5
    [Google Scholar]
  101. O'Hare JK, Ade KK, Sukharnikova T, Van Hooser SD, Palmeri ML et al. 2016. Pathway-specific striatal substrates for habitual behavior. Neuron 89:3472–79
    [Google Scholar]
  102. Oldenburg IA, Sabatini BL. 2015. Antagonistic but not symmetric regulation of primary motor cortex by basal ganglia direct and indirect pathways. Neuron 86:51174–81
    [Google Scholar]
  103. Pan WX, Mao T, Dudman JT 2010. Inputs to the dorsal striatum of the mouse reflect the parallel circuit architecture of the forebrain. Front. Neuroanat. 4:147
    [Google Scholar]
  104. Panigrahi B, Martin KA, Li Y, Graves AR, Vollmer A et al. 2015. Dopamine is required for the neural representation and control of movement vigor. Cell 162:61418–30
    [Google Scholar]
  105. Parker JG, Marshall JD, Ahanonu B, Wu Y-W, Kim TH et al. 2018. Diametric neural ensemble dynamics in parkinsonian and dyskinetic states. Nature 557:7704177–82
    [Google Scholar]
  106. Parker NF, Cameron CM, Taliaferro JP, Lee J, Choi JY et al. 2016. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target. Nat. Neurosci. 19:6845–54
    [Google Scholar]
  107. Parker PRL, Lalive AL, Kreitzer AC 2016. Pathway-specific remodeling of thalamostriatal synapses in Parkinsonian mice. Neuron 89:4734–40
    [Google Scholar]
  108. Parkinson J. 2002. An essay on the shaking palsy. J. Neuropsychiatry Clin. Neurosci. 14:2223–36
    [Google Scholar]
  109. Phillips PEM, Stuber GD, Heien MLAV, Wightman RM, Carelli RM 2003. Subsecond dopamine release promotes cocaine seeking. Nature 422:6932614–18
    [Google Scholar]
  110. Pidoux M, Mahon S, Deniau J-M, Charpier S 2011. Integration and propagation of somatosensory responses in the corticostriatal pathway: an intracellular study in vivo. J. Physiol. 589:2263–81
    [Google Scholar]
  111. 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 8:3e57054
    [Google Scholar]
  112. Plotkin JL, Day M, Surmeier DJ 2011. Synaptically driven state transitions in distal dendrites of striatal spiny neurons. Nat. Neurosci. 14:7881–88
    [Google Scholar]
  113. Poulin J-F, Caronia G, Hofer C, Cui Q, Helm B et al. 2018. Mapping projections of molecularly defined dopamine neuron subtypes using intersectional genetic approaches. Nat. Neurosci. 21:91260
    [Google Scholar]
  114. Redgrave P, Prescott TJ, Gurney K 1999. The basal ganglia: a vertebrate solution to the selection problem. ? Neuroscience 89:41009–23
    [Google Scholar]
  115. Reig R, Silberberg G. 2014. Multisensory integration in the mouse striatum. Neuron 83:51200–12
    [Google Scholar]
  116. Reiner A, Hart NM, Lei W, Deng Y 2010. Corticostriatal projection neurons—dichotomous types and dichotomous functions. Front. Neuroanat. 4:142
    [Google Scholar]
  117. Rescorla RA, Wagner A. 1972. A theory of Pavlovian conditioning: variations in the effectiveness of reinforcement and nonreinforcement. Classical Conditioning II: Current Research and Theory AH Black, WF Prokasy 64–99 New York: Appleton-Century-Crofts
    [Google Scholar]
  118. Romo R, Scarnati E, Schultz W 1992. Role of primate basal ganglia and frontal cortex in the internal generation of movements. II. Movement-related activity in the anterior striatum. Exp. Brain Res. 91:3385–95
    [Google Scholar]
  119. Romo R, Schultz W. 1992. Role of primate basal ganglia and frontal cortex in the internal generation of movements. III. Neuronal activity in the supplementary motor area. Exp. Brain Res. 91:3396–407
    [Google Scholar]
  120. Rubinstein TC, Giladi N, Hausdorff JM 2002. The power of cueing to circumvent dopamine deficits: a review of physical therapy treatment of gait disturbances in Parkinson's disease. Mov. Disord. 17:61148–60
    [Google Scholar]
  121. Rueda-Orozco PE, Robbe D. 2015. The striatum multiplexes contextual and kinematic information to constrain motor habits execution. Nat. Neurosci. 18:3453–60
    [Google Scholar]
  122. Salamone JD, Steinpreis RE, McCullough LD, Smith P, Grebel D, Mahan K 1991. Haloperidol and nucleus accumbens dopamine depletion suppress lever pressing for food but increase free food consumption in a novel food choice procedure. Psychopharmacology 104:4515–21
    [Google Scholar]
  123. Sales-Carbonell C, Taouali W, Khalki L, Pasquet MO, Petit LF et al. 2018. No discrete start/stop signals in the dorsal striatum of mice performing a learned action. Curr. Biol. 28:193044–55.e5
    [Google Scholar]
  124. Samejima K, Ueda Y, Doya K, Kimura M 2005. Representation of action-specific reward values in the striatum. Science 310:57521337–40
    [Google Scholar]
  125. Saunders A, Huang KW, Sabatini BL 2016. Globus pallidus externus neurons expressing parvalbumin interconnect the subthalamic nucleus and striatal interneurons. PLOS ONE 11:2e0149798
    [Google Scholar]
  126. Saunders A, Oldenburg IA, Berezovskii VK, Johnson CA, Kingery ND et al. 2015. A direct GABAergic output from the basal ganglia to frontal cortex. Nature 521:755085–89
    [Google Scholar]
  127. Saunders BT, Richard JM, Margolis EB, Janak PH 2018. Dopamine neurons create Pavlovian conditioned stimuli with circuit-defined motivational properties. Nat. Neurosci. 21:81072–83
    [Google Scholar]
  128. Schlesinger I, Erikh I, Yarnitsky D 2007. Paradoxical kinesia at war. Mov. Disord. 22:162394–97
    [Google Scholar]
  129. Schmidt R, Leventhal DK, Mallet N, Chen F, Berke JD 2013. Canceling actions involves a race between basal ganglia pathways. Nat. Neurosci. 16:81118–24
    [Google Scholar]
  130. Schultz W. 1986. Responses of midbrain dopamine neurons to behavioral trigger stimuli in the monkey. J. Neurophysiol. 56:51439–61
    [Google Scholar]
  131. Schultz W. 2007. Multiple dopamine functions at different time courses. Annu. Rev. Neurosci. 30:259–88
    [Google Scholar]
  132. Schultz W. 2010. Dopamine signals for reward value and risk: basic and recent data. Behav. Brain Funct. 6:24
    [Google Scholar]
  133. Schultz W. 2016. Dopamine reward prediction error coding. Dialogues Clin. Neurosci. 18:123–32
    [Google Scholar]
  134. Schultz W, Dayan P, Montague PR 1997. A neural substrate of prediction and reward. Science 275:53061593–99
    [Google Scholar]
  135. Schultz W, Romo R. 1990. Dopamine neurons of the monkey midbrain: contingencies of responses to stimuli eliciting immediate behavioral reactions. J. Neurophysiol. 63:3607–24
    [Google Scholar]
  136. Schultz W, Romo R. 1992. Role of primate basal ganglia and frontal cortex in the internal generation of movements. I. Preparatory activity in the anterior striatum. Exp. Brain Res. 91:3363–84
    [Google Scholar]
  137. Seo M, Lee E, Averbeck BB 2012. Action selection and action value in frontal-striatal circuits. Neuron 74:5947–60
    [Google Scholar]
  138. Shepherd GMG. 2013. Corticostriatal connectivity and its role in disease. Nat. Rev. Neurosci. 14:4278–91
    [Google Scholar]
  139. Shin JH, Kim D, Jung MW 2018. Differential coding of reward and movement information in the dorsomedial striatal direct and indirect pathways. Nat. Commun. 9:1404
    [Google Scholar]
  140. Sippy T, Lapray D, Crochet S, Petersen CCH 2015. Cell-type-specific sensorimotor processing in striatal projection neurons during goal-directed behavior. Neuron 88:2298–305
    [Google Scholar]
  141. Smith Y, Galvan A, Ellender TJ, Doig N, Villalba RM et al. 2014. The thalamostriatal system in normal and diseased states. Front. Syst. Neurosci. 8:5
    [Google Scholar]
  142. Smith Y, Surmeier DJ, Redgrave P, Kimura M 2011. Thalamic contributions to basal ganglia-related behavioral switching and reinforcement. J. Neurosci. 31:4516102–6
    [Google Scholar]
  143. Snijders AH, van Kesteren M, Bloem BR 2012. Cycling is less affected than walking in freezers of gait. J. Neurol. Neurosurg. Psychiatry 83:5575–76
    [Google Scholar]
  144. Sotnikova TD, Beaulieu J-M, Barak LS, Wetsel WC, Caron MG, Gainetdinov RR 2005. Dopamine-independent locomotor actions of amphetamines in a novel acute mouse model of Parkinson disease. PLOS Biol 3:8e271
    [Google Scholar]
  145. Stalnaker TA, Berg B, Aujla N, Schoenbaum G 2016. Cholinergic interneurons use orbitofrontal input to track beliefs about current state. J. Neurosci. 36:236242–57
    [Google Scholar]
  146. Stauffer WR, Lak A, Yang A, Borel M, Paulsen O et al. 2016. Dopamine neuron-specific optogenetic stimulation in rhesus macaques. Cell 166:61564–71.e6
    [Google Scholar]
  147. Surmeier DJ, Ding J, Day M, Wang Z, Shen W 2007. D1 and D2 dopamine-receptor modulation of striatal glutamatergic signaling in striatal medium spiny neurons. Trends Neurosci 30:5228–35
    [Google Scholar]
  148. Sutton RS, Barto AG. 1981. Toward a modern theory of adaptive networks: expectation and prediction. Psychol. Rev. 88:2135–70
    [Google Scholar]
  149. Svoboda K, Li N. 2018. Neural mechanisms of movement planning: motor cortex and beyond. Curr. Opin. Neurobiol. 49:33–41
    [Google Scholar]
  150. Syed ECJ, Grima LL, Magill PJ, Bogacz R, Brown P, Walton ME 2015. Action initiation shapes mesolimbic dopamine encoding of future rewards. Nat. Neurosci. 19:34–36
    [Google Scholar]
  151. Tai L-H, Lee AM, Benavidez N, Bonci A, Wilbrecht L 2012. Transient stimulation of distinct subpopulations of striatal neurons mimics changes in action value. Nat. Neurosci. 15:91281–89
    [Google Scholar]
  152. Thompson JA, Felsen G. 2013. Activity in mouse pedunculopontine tegmental nucleus reflects action and outcome in a decision-making task. J. Neurophysiol. 110:122817–29
    [Google Scholar]
  153. Tecuapetla F, Jin X, Lima SQ, Costa RM 2016. Complementary contributions of striatal projection pathways to action initiation and execution. Cell 166:3703–15
    [Google Scholar]
  154. Tecuapetla F, Matias S, Dugue GP, Mainen ZF, Costa RM 2014. Balanced activity in basal ganglia projection pathways is critical for contraversive movements. Nat. Commun. 5:4315
    [Google Scholar]
  155. Thura D, Cisek P. 2017. The basal ganglia do not select reach targets but control the urgency of commitment. Neuron 95:51160–70.e5
    [Google Scholar]
  156. Tsai H-C, Zhang F, Adamantidis A, Stuber GD, Bonci A et al. 2009. Phasic firing in dopaminergic neurons is sufficient for behavioral conditioning. Science 324:59301080–84
    [Google Scholar]
  157. Tunstall MJ, Oorschot DE, Kean A, Wickens JR 2002. Inhibitory interactions between spiny projection neurons in the rat striatum. J. Neurophysiol. 88:31263–69
    [Google Scholar]
  158. Turner RS, Desmurget M. 2010. Basal ganglia contributions to motor control: a vigorous tutor. Curr. Opin. Neurobiol. 20:6704–16
    [Google Scholar]
  159. Waelti P, Dickinson A, Schultz W 2001. Dopamine responses comply with basic assumptions of formal learning theory. Nature 412:684243–48
    [Google Scholar]
  160. Wall NR, De La Parra M, Callaway EM, Kreitzer AC 2013. Differential innervation of direct- and indirect-pathway striatal projection neurons. Neuron 79:2347–60
    [Google Scholar]
  161. Wassum KM, Ostlund SB, Maidment NT 2012. Phasic mesolimbic dopamine signaling precedes and predicts performance of a self-initiated action sequence task. Biol. Psychiatry 71:10846–54
    [Google Scholar]
  162. Watabe-Uchida M, Eshel N, Uchida N 2017. Neural circuitry of reward prediction error. Annu. Rev. Neurosci. 40:373–94
    [Google Scholar]
  163. Wickens JR, Horvitz JC, Costa RM, Killcross S 2007. Dopaminergic mechanisms in actions and habits. J. Neurosci. 27:318181–83
    [Google Scholar]
  164. Wilson CJ. 1995. The contribution of cortical neurons to the firing pattern of striatal spiny neurons. Models of Information Processing in Basal Ganglia, Vol. 1 JC Houk, JL Davis, DG Beiser 29–31 Cambridge, MA: MIT Press
    [Google Scholar]
  165. Witten IB, Steinberg EE, Lee SY, Davidson TJ, Zalocusky KA et al. 2011. Recombinase-driver rat lines: tools, techniques, and optogenetic application to dopamine-mediated reinforcement. Neuron 72:5721–33
    [Google Scholar]
  166. Wong AL, Lindquist MA, Haith AM, Krakauer JW 2015. Explicit knowledge enhances motor vigor and performance: motivation versus practice in sequence tasks. J. Neurophysiol. 114:1219–32
    [Google Scholar]
  167. Xiao C, Cho JR, Zhou C, Treweek JB, Chan K et al. 2016. Cholinergic mesopontine signals govern locomotion and reward through dissociable midbrain pathways. Neuron 90:2333–47
    [Google Scholar]
  168. Yin HH, Mulcare SP, Hilário MR, Clouse E, Holloway T et al. 2009. Dynamic reorganization of striatal circuits during the acquisition and consolidation of a skill. Nat. Neurosci. 12:3333–41
    [Google Scholar]
  169. Yohn SE, Errante EE, Rosenbloom-Snow A, Somerville M, Rowland M et al. 2016. Blockade of uptake for dopamine, but not norepinephrine or 5-HT, increases selection of high effort instrumental activity: implications for treatment of effort-related motivational symptoms in psychopathology. Neuropharmacology 109:270–80
    [Google Scholar]
  170. Yttri EA, Dudman JT. 2016. Opponent and bidirectional control of movement velocity in the basal ganglia. Nature 533:7603402–6
    [Google Scholar]
  171. Zheng T, Wilson CJ. 2002. Corticostriatal combinatorics: the implications of corticostriatal axonal arborizations. J. Neurophysiol. 87:21007–17
    [Google Scholar]
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