1932

Abstract

Behavior is readily classified into patterns of movements with inferred common goals—actions. Goals may be discrete; movements are continuous. Through the careful study of isolated movements in laboratory settings, or via introspection, it has become clear that animals can exhibit exquisite graded specification to their movements. Moreover, graded control can be as fundamental to success as the selection of which action to perform under many naturalistic scenarios: a predator adjusting its speed to intercept moving prey, or a tool-user exerting the perfect amount of force to complete a delicate task. The basal ganglia are a collection of nuclei in vertebrates that extend from the forebrain (telencephalon) to the midbrain (mesencephalon), constituting a major descending extrapyramidal pathway for control over midbrain and brainstem premotor structures. Here we discuss how this pathway contributes to the continuous specification of movements that endows our voluntary actions with vigor and grace.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-070918-050452
2020-07-08
2024-07-16
Loading full text...

Full text loading...

/deliver/fulltext/neuro/43/1/annurev-neuro-070918-050452.html?itemId=/content/journals/10.1146/annurev-neuro-070918-050452&mimeType=html&fmt=ahah

Literature Cited

  1. Adesnik H, Scanziani M. 2010. Lateral competition for cortical space by layer-specific horizontal circuits. Nature 464:72921155–60
    [Google Scholar]
  2. Albin RL, Young AB, Penney JB 1989. The functional anatomy of basal ganglia disorders. Trends Neurosci 12:10366–75
    [Google Scholar]
  3. Aldridge JW, Anderson RJ, Murphy JT 1980. The role of the basal ganglia in controlling a movement initiated by a visually presented cue. Brain Res 192:13–16
    [Google Scholar]
  4. Alexander GE. 1987. Selective neuronal discharge in monkey putamen reflects intended direction of planned limb movements. Exp. Brain Res. 67:3623–34
    [Google Scholar]
  5. Alexander GE, Crutcher MD. 1990a. Preparation for movement: neural representations of intended direction in three motor areas of the monkey. J. Neurophysiol. 64:1133–50
    [Google Scholar]
  6. Alexander GE, Crutcher MD. 1990b. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci 13:7266–71
    [Google Scholar]
  7. Alexander GE, Crutcher MD. 1990c. Neural representations of the target (goal) of visually guided arm movements in three motor areas of the monkey. J. Neurophysiol. 64:1164–78
    [Google Scholar]
  8. 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]
  9. Ambroggi F, Ishikawa A, Fields HL, Nicola SM 2008. Basolateral amygdala neurons facilitate reward-seeking behavior by exciting nucleus accumbens neurons. Neuron 59:4648–61
    [Google Scholar]
  10. Anderson ME, Horak FB. 1985. Influence of the globus pallidus on arm movements in monkeys. III. Timing of movement-related information. J. Neurophysiol. 54:2433–48
    [Google Scholar]
  11. Anderson ME, Turner RS. 1991a. Activity of neurons in cerebellar-receiving and pallidal-receiving areas of the thalamus of the behaving monkey. J. Neurophysiol. 66:3879–93
    [Google Scholar]
  12. Anderson ME, Turner RS. 1991b. A quantitative analysis of pallidal discharge during targeted reaching movement in the monkey. Exp. Brain Res. 86:623–32
    [Google Scholar]
  13. Appell PP, Behan M. 1990. Sources of subcortical GABAergic projections to the superior colliculus in the cat. J. Comp. Neurol. 302:1143–58
    [Google Scholar]
  14. Assous M, Tepper JM. 2019. Excitatory extrinsic afferents to striatal interneurons and interactions with striatal microcircuitry. Eur. J. Neurosci. 49:5593–603
    [Google Scholar]
  15. Averbeck BB, Latham PE, Pouget A 2006. Neural correlations, population coding and computation. Nat. Rev. Neurosci. 7:5358–66
    [Google Scholar]
  16. Averbeck BB, Lehman J, Jacobson M, Haber SN 2014. Estimates of projection overlap and zones of convergence within frontal-striatal circuits. J. Neurosci. 34:299497–505
    [Google Scholar]
  17. Baraduc P, Thobois S, Gan J, Broussolle E, Desmurget M 2013. A common optimization principle for motor execution in healthy subjects and parkinsonian patients. J. Neurosci. 33:2665–77
    [Google Scholar]
  18. 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]
  19. Barter JW, Li S, Sukharnikova T, Rossi MA, Bartholomew RA, Yin HH 2015. Basal ganglia outputs map instantaneous position coordinates during behavior. J. Neurosci. 35:62703–16
    [Google Scholar]
  20. Basso MA, Sommer MA. 2011. Exploring the role of the substantia nigra pars reticulata in eye movements. Neuroscience 198:205–12
    [Google Scholar]
  21. Basso MA, Wurtz RH. 2002. Neuronal activity in substantia nigra pars reticulata during target selection. J. Neurosci. 22:51883–94
    [Google Scholar]
  22. Bayer HM, Handel A, Glimcher PW 2004. Eye position and memory saccade related responses in substantia nigra pars reticulata. Exp. Brain Res. 154:4428–41
    [Google Scholar]
  23. Bocarsly ME, Jiang W-C, Wang C, Dudman JT, Ji N, Aponte Y 2015. Minimally invasive microendoscopy system for in vivo functional imaging of deep nuclei in the mouse brain. Biomed. Opt. Express 6:114546–56
    [Google Scholar]
  24. Bodor ÁL, Giber K, Rovó Z, Ulbert I, Acsády L 2008. Structural correlates of efficient GABAergic transmission in the basal ganglia-thalamus pathway. J. Neurosci. 28:123090–102
    [Google Scholar]
  25. Bohn DA. 1986. Constant-Q graphic equalizers. J. Audio Eng. Soc. 34:9611–26
    [Google Scholar]
  26. Bosch-Bouju C, Hyland BI, Parr-Brownlie LC 2013. Motor thalamus integration of cortical, cerebellar and basal ganglia information: implications for normal and parkinsonian conditions. Front. Comput. Neurosci. 7:163
    [Google Scholar]
  27. Bosch-Bouju C, Smither RA, Hyland BI, Parr-Brownlie LC 2014. Reduced reach-related modulation of motor thalamus neural activity in a rat model of Parkinson's disease. J. Neurosci. 34:4815836–50
    [Google Scholar]
  28. Bostan AC, Strick PL. 2010. The cerebellum and basal ganglia are interconnected. Neuropsychol. Rev. 20:3261–70
    [Google Scholar]
  29. Brazhnik E, McCoy AJ, Novikov N, Hatch CE, Walters JR 2016. Ventral medial thalamic nucleus promotes synchronization of increased high beta oscillatory activity in the basal ganglia-thalamocortical network of the hemiparkinsonian rat. J. Neurosci. 36:4196–208
    [Google Scholar]
  30. Brown J, Martin KA, Dudman JT 2016. Behavioral evidence for feedback gain control by the inhibitory microcircuit of the substantia nigra. bioRxiv 090209. https://doi.org/10.1101/090209
    [Crossref]
  31. Brown J, Pan W-X, Dudman JT 2014. The inhibitory microcircuit of the substantia nigra provides feedback gain control of the basal ganglia output. eLife 3:e02397
    [Google Scholar]
  32. Brown VJ, Robbins TW. 1989. Elementary processes of response selection mediated by distinct regions of the striatum. J. Neurosci. 9:113760–65
    [Google Scholar]
  33. Buchwald NA, Hull CD, Levine MS 1979. Basal ganglionic neuronal activity and behavioral set. Appl. Neurophysiol. 42:1–2109–12
    [Google Scholar]
  34. Burke DA, Rotstein HG, Alvarez VA 2017. Striatal local circuitry: a new framework for lateral inhibition. Neuron 96:2267–84
    [Google Scholar]
  35. Chevalier G, Deniau JM. 1990. Disinhibition as a basic process in the expression of striatal functions. Trends Neurosci 13:7277–80
    [Google Scholar]
  36. Chevalier G, Deniau JM, Thierry AM, Feger J 1981. The nigro-tectal pathway. An electrophysiological reinvestigation in the rat. Brain Res 213:2253–63
    [Google Scholar]
  37. Chevalier G, Vacher S, Deniau JM, Desban M 1985. Disinhibition as a basic process in the expression of striatal functions. I. The striato-nigral influence on tecto-spinal/tecto-diencephalic neurons. Brain Res 334:2215–26
    [Google Scholar]
  38. Coddington LT, Dudman JT. 2019. Learning from action: reconsidering movement signaling in midbrain dopamine neuron activity. Neuron 104:163–77
    [Google Scholar]
  39. Coffey KR, Nader M, West MO 2016. Single body parts are processed by individual neurons in the mouse dorsolateral striatum. Brain Res 1636:200–7
    [Google Scholar]
  40. Collins AG, 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]
  41. Costa RM, Cohen D, Nicolelis MAL 2004. Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr. Biol. 14:131124–34
    [Google Scholar]
  42. Cui G, Jun SB, Jin X, Luo G, Pham MD et al. 2014. Deep brain optical measurements of cell type-specific neural activity in behaving mice. Nat. Protoc. 9:61213–28
    [Google Scholar]
  43. 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]
  44. Czubayko U, Plenz D. 2002. Fast synaptic transmission between striatal spiny projection neurons. PNAS 99:2415764–69
    [Google Scholar]
  45. DeLong M, Wichmann T. 2010. Changing views of basal ganglia circuits and circuit disorders. Clin. EEG Neurosci. 41:261–67
    [Google Scholar]
  46. DeLong MR. 1990. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:7281–85
    [Google Scholar]
  47. DeLong MR, Alexander GE, Georgopoulos AP, Crutcher MD, Mitchell SJ, Richardson RT 1984. Role of basal ganglia in limb movements. Hum. Neurobiol. 2:4235–44
    [Google Scholar]
  48. Deniau JM, Chevalier G. 1985. Disinhibition as a basic process in the expression of striatal functions. II. The striato-nigral influence on thalamocortical cells of the ventromedial thalamic nucleus. Brain Res 334:2227–33
    [Google Scholar]
  49. Deniau JM, Mailly P, Maurice N, Charpier S 2007. The pars reticulata of the substantia nigra: a window to basal ganglia output. Prog. Brain Res. 160:151–72
    [Google Scholar]
  50. Desmurget M, Turner RS. 2010. Motor sequences and the basal ganglia: kinematics, not habits. J. Neurosci. 30:227685–90
    [Google Scholar]
  51. 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 90:51100–13
    [Google Scholar]
  52. Dudman JT, Gerfen CR. 2015. The basal ganglia. The Rat Nervous System G Paxinos 391–440 New York: Elsevier
    [Google Scholar]
  53. Dudman JT, Krakauer JW. 2016. The basal ganglia: from motor commands to the control of vigor. Curr. Opin. Neurobiol. 37:158–66
    [Google Scholar]
  54. Edgerton JR, Jaeger D. 2014. Optogenetic activation of nigral inhibitory inputs to motor thalamus in the mouse reveals classic inhibition with little potential for rebound activation. Front. Cell. Neurosci. 8:36
    [Google Scholar]
  55. Evans DA, Stempel AV, Vale R, Ruehle S, Lefler Y, Branco T 2018. A synaptic threshold mechanism for computing escape decisions. Nature 558:7711590–94
    [Google Scholar]
  56. Fobbs WC, Bariselli S, Licholai JA, Miyazaki NL, Matikainen-Ankney BA et al. 2020. Continuous representations of speed by striatal medium spiny neurons. J. Neurosci. 40:81679–88
    [Google Scholar]
  57. Frank MJ. 2011. Computational models of motivated action selection in corticostriatal circuits. Curr. Opin. Neurobiol. 21:3381–86
    [Google Scholar]
  58. Gabbiani F, Krapp HG, Koch C, Laurent G 2002. Multiplicative computation in a visual neuron sensitive to looming. Nature 420:6913320–24
    [Google Scholar]
  59. Gage GJ, Stoetzner CR, Wiltschko AB, Berke JD 2010. Selective activation of striatal fast-spiking interneurons during choice execution. Neuron 67:466–79
    [Google Scholar]
  60. Gandhi NJ, Katnani HA. 2011. Motor functions of the superior colliculus. Annu. Rev. Neurosci. 34:205–31
    [Google Scholar]
  61. Gerfen C, Surmeier D. 2010. Dichotomous modulation of striatal direct and indirect pathway neurons by dopamine. Annu. Rev. Neurosci. 34:441–66
    [Google Scholar]
  62. Gittis AH, Nelson AB, Thwin MT, Palop JJ, Kreitzer AC 2010. Distinct roles of GABAergic interneurons in the regulation of striatal output pathways. J. Neurosci. 30:62223–34
    [Google Scholar]
  63. Goldberg JH, Farries MA, Fee MS 2012. Integration of cortical and pallidal inputs in the basal ganglia-recipient thalamus of singing birds. J. Neurophysiol. 108:51403–29
    [Google Scholar]
  64. Goldberg JH, Farries MA, Fee MS 2013. Basal ganglia output to the thalamus: still a paradox. Trends Neurosci 36:12695–705
    [Google Scholar]
  65. Goldberg JH, Fee MS. 2012. A cortical motor nucleus drives the basal ganglia-recipient thalamus in singing birds. Nat. Neurosci. 15:4620–27
    [Google Scholar]
  66. Graybiel AM. 1998. The basal ganglia and chunking of action repertoires. Neurobiol. Learn. Mem. 70:1–2119–36
    [Google Scholar]
  67. 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]
  68. Guo ZV, Inagaki HK, Daie K, Druckmann S, Gerfen CR, Svoboda K 2017. Maintenance of persistent activity in a frontal thalamocortical loop. Nature 545:7653181–86
    [Google Scholar]
  69. Haber SN. 2003. The primate basal ganglia: parallel and integrative networks. J. Chem. Neuroanat. 26:4317–30
    [Google Scholar]
  70. Handel A, Glimcher PW. 1999. Quantitative analysis of substantia nigra pars reticulata activity during a visually guided saccade task. J. Neurophysiol. 82:63458–75
    [Google Scholar]
  71. Hartline HK, Wagner HG, Ratliff F 1956. Inhibition in the eye of Limulus. J. Gen. Physiol. 39:5651–73
    [Google Scholar]
  72. Hemelt ME, Keller A. 2008. Superior colliculus control of vibrissa movements. J. Neurophysiol. 100:31245–54
    [Google Scholar]
  73. Higgs MH, Wilson CJ. 2016. Unitary synaptic connections among substantia nigra pars reticulata neurons. J. Neurophysiol. 115:62814–29
    [Google Scholar]
  74. 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]
  75. Hikosaka O, Wurtz RH. 1983a. Visual and oculomotor functions of monkey substantia nigra pars reticulata. I. Relation of visual and auditory responses to saccades. J. Neurophysiol. 49:51230–53
    [Google Scholar]
  76. Hikosaka O, Wurtz RH. 1983b. Visual and oculomotor functions of monkey substantia nigra pars reticulata. IV. Relation of substantia nigra to superior colliculus. J. Neurophysiol. 49:51285–301
    [Google Scholar]
  77. Hikosaka O, Wurtz RH. 1985. Modification of saccadic eye movements by GABA-related substances. II. Effects of muscimol in monkey substantia nigra pars reticulata. J. Neurophysiol. 53:1292–308
    [Google Scholar]
  78. Hikosaka O, Wurtz RH. 1986. Saccadic eye movements following injection of lidocaine into the superior colliculus. Exp. Brain Res. 61:3531–39
    [Google Scholar]
  79. Horak FB, Anderson ME. 1984a. Influence of globus pallidus on arm movements in monkeys. I. Effects of kainic acid-induced lesions. J. Neurophysiol. 52:2290–304
    [Google Scholar]
  80. Horak FB, Anderson ME. 1984b. Influence of globus pallidus on arm movements in monkeys. II. Effects of stimulation. J. Neurophysiol. 52:2305–22
    [Google Scholar]
  81. Hoy JL, Bishop HI, Niell CM 2019. Defined cell types in superior colliculus make distinct contributions to prey capture behavior in the mouse. Curr. Biol. 29:234130–38.e5
    [Google Scholar]
  82. Hughes HC, Reuter-Lorenz PA, Nozawa G, Fendrich R 1994. Visual-auditory interactions in sensorimotor processing: saccades versus manual responses. J. Exp. Psychol. Hum. Percept. Perform. 20:1131–53
    [Google Scholar]
  83. Humphries MD, Stewart RD, Gurney KN 2006. A physiologically plausible model of action selection and oscillatory activity in the basal ganglia. J. Neurosci. 26:5012921–42
    [Google Scholar]
  84. 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]
  85. Inase M, Buford JA, Anderson ME 1996. Changes in the control of arm position, movement, and thalamic discharge during local inactivation in the globus pallidus of the monkey. J. Neurophysiol. 75:31087–104
    [Google Scholar]
  86. 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]
  87. Jonas E, Kording KP. 2017. Could a neuroscientist understand a microprocessor. ? PLoS Comput. Biol. 13:1e1005268
    [Google Scholar]
  88. Kaneda K, Isa K, Yanagawa Y, Isa T 2008. Nigral inhibition of GABAergic neurons in mouse superior colliculus. J. Neurosci. 28:4311071–78
    [Google Scholar]
  89. Katnani HA, Gandhi NJ. 2012. The relative impact of microstimulation parameters on movement generation. J. Neurophysiol. 108:2528–38
    [Google Scholar]
  90. Kawagoe R, Takikawa Y, Hikosaka O 1998. Expectation of reward modulates cognitive signals in the basal ganglia. Nat. Neurosci. 1:5411–16
    [Google Scholar]
  91. Kawaguchi Y, Wilson CJ, Emson PC 1990. Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J. Neurosci. 10:103421–38
    [Google Scholar]
  92. Kim J, Kim Y, Nakajima R, Shin A, Jeong M et al. 2017. Inhibitory basal ganglia inputs induce excitatory motor signals in the thalamus. Neuron 95:51181–96.e8
    [Google Scholar]
  93. Kim N, Barter JW, Sukharnikova T, Yin HH 2014. Striatal firing rate reflects head movement velocity. Eur. J. Neurosci. 40:103481–90
    [Google Scholar]
  94. Kim N, Li HE, Hughes RN, Watson GDR, Gallegos D et al. 2019. A striatal interneuron circuit for continuous target pursuit. Nat. Commun. 10:2715
    [Google Scholar]
  95. Klaus A, Alves da Silva J, Costa RM 2019. What, if, and when to move: basal ganglia circuits and self-paced action initiation. Annu. Rev. Neurosci. 42:459–83
    [Google Scholar]
  96. 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. Erratum. 2017 Neuron 96:4949
    [Google Scholar]
  97. Koós T, Tepper JM. 1999. Inhibitory control of neostriatal projection neurons by GABAergic interneurons. Nat. Neurosci. 2:5467–72
    [Google Scholar]
  98. Koos T, Tepper JM, Wilson CJ 2004. Comparison of IPSCs evoked by spiny and fast-spiking neurons in the neostriatum. J. Neurosci. 24:367916–22
    [Google Scholar]
  99. Kornhuber HH. 1971. Motor functions of cerebellum and basal ganglia: the cerebellocortical saccadic (ballistic) clock, the cerebellonuclear hold regulator, and the basal ganglia ramp (voluntary speed smooth movement) generator. Kybernetik 8:4157–62
    [Google Scholar]
  100. 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]
  101. Kupferschmidt DA, Juczewski K, Cui G, Johnson KA, Lovinger DM 2017. Parallel, but dissociable, processing in discrete corticostriatal inputs encodes skill learning. Neuron 96:2476–89.e5
    [Google Scholar]
  102. Kuramoto E, Fujiyama F, Nakamura KC, Tanaka Y, Hioki H, Kaneko T 2011. Complementary distribution of glutamatergic cerebellar and GABAergic basal ganglia afferents to the rat motor thalamic nuclei. Eur. J. Neurosci. 33:195–109
    [Google Scholar]
  103. Kuramoto E, Furuta T, Nakamura KC, Unzai T, Hioki H, Kaneko T 2009. Two types of thalamocortical projections from the motor thalamic nuclei of the rat: a single neuron-tracing study using viral vectors. Cereb. Cortex 19:92065–77
    [Google Scholar]
  104. Kuramoto E, Ohno S, Furuta T, Unzai T, Tanaka YR et al. 2015. Ventral medial nucleus neurons send thalamocortical afferents more widely and more preferentially to layer 1 than neurons of the ventral anterior-ventral lateral nuclear complex in the rat. Cereb. Cortex 25:1221–35
    [Google Scholar]
  105. Larkum ME, Senn W, Lüscher H-R 2004. Top-down dendritic input increases the gain of layer 5 pyramidal neurons. Cereb. Cortex 14:101059–70
    [Google Scholar]
  106. Lee C, Rohrer WH, Sparks DL 1988. Population coding of saccadic eye movements by neurons in the superior colliculus. Nature 332:6162357–60
    [Google Scholar]
  107. Lee K, Holley SM, Shobe JL, Chong NC, Cepeda C et al. 2018. Parvalbumin interneurons modulate striatal output and enhance performance during associative learning. Neuron 93:61451–63.e4
    [Google Scholar]
  108. Liles SL. 1985. Activity of neurons in putamen during active and passive movements of wrist. J. Neurophysiol. 53:1217–36
    [Google Scholar]
  109. Mallet N, Le Moine C, Charpier S, Gonon F 2005. Feedforward inhibition of projection neurons by fast-spiking GABA interneurons in the rat striatum in vivo. J. Neurosci. 25:153857–69
    [Google Scholar]
  110. 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]
  111. May PJ. 2006. The mammalian superior colliculus: laminar structure and connections. Prog. Brain Res. 151:321–78
    [Google Scholar]
  112. McGinty VB, Lardeux S, Taha SA, Kim JJ, Nicola SM 2013. Invigoration of reward seeking by cue and proximity encoding in the nucleus accumbens. Neuron 78:5910–22
    [Google Scholar]
  113. Meng C, Zhou J, Papaneri A, Peddada T, Xu K, Cui G 2018. Spectrally resolved fiber photometry for multi-component analysis of brain circuits. Neuron 98:4707–17.e4
    [Google Scholar]
  114. Meng G, Liang Y, Sarsfield S, Jiang W-C, Lu R et al. 2019. High-throughput synapse-resolving two-photon fluorescence microendoscopy for deep-brain volumetric imaging in vivo. eLife 8:e40805
    [Google Scholar]
  115. Mink JW. 1996. The basal ganglia: focused selection and inhibition of competing motor programs. Prog. Neurobiol. 50:4381–425
    [Google Scholar]
  116. Mink JW, Thach WT. 1991a. Basal ganglia motor control. III. Pallidal ablation: normal reaction time, muscle cocontraction, and slow movement. J. Neurophysiol. 65:2330–51
    [Google Scholar]
  117. Mink JW, Thach WT. 1991b. Basal ganglia motor control. II. Late pallidal timing relative to movement onset and inconsistent pallidal coding of movement parameters. J. Neurophysiol. 65:2301–29
    [Google Scholar]
  118. Mink JW, Thach WT. 1991c. Basal ganglia motor control. I. Nonexclusive relation of pallidal discharge to five movement modes. J. Neurophysiol. 65:2273–300
    [Google Scholar]
  119. Mitchell SJ, Silver RA. 2003. Shunting inhibition modulates neuronal gain during synaptic excitation. Neuron 38:3433–45
    [Google Scholar]
  120. Munoz DP, Guitton D. 1986. Presaccadic burst discharges of tecto-reticulo-spinal neurons in the alert head-free and -fixed cat. Brain Res 398:1185–90
    [Google Scholar]
  121. Musall S, Kaufman MT, Juavinett AL, Gluf S, Churchland AK 2019. Single-trial neural dynamics are dominated by richly varied movements. Nat. Neurosci. 22:1677–1686
    [Google Scholar]
  122. Nakamura KC, Sharott A, Magill PJ 2012. Temporal coupling with cortex distinguishes spontaneous neuronal activities in identified basal ganglia-recipient and cerebellar-recipient zones of the motor thalamus. Cereb. Cortex 24:181–97
    [Google Scholar]
  123. Neafsey EJ, Hull CD, Buchwald NA 1978. Preparation for movement in the cat. II. Unit activity in the basal ganglia and thalamus. Electroencephalogr. Clin. Neurophysiol. 44:6714–23
    [Google Scholar]
  124. Nelson AB, Kreitzer AC. 2014. Reassessing models of basal ganglia function and dysfunction. Annu. Rev. Neurosci. 37:117–35
    [Google Scholar]
  125. Ohno S, Kuramoto E, Furuta T, Hioki H, Tanaka YR et al. 2012. A morphological analysis of thalamocortical axon fibers of rat posterior thalamic nuclei: a single neuron tracing study with viral vectors. Cereb. Cortex 22:122840–57
    [Google Scholar]
  126. Owen SF, Berke JD, Kreitzer AC 2018. Fast-spiking interneurons supply feedforward control of bursting, calcium, and plasticity for efficient learning. Cell 172:4683–95.e15
    [Google Scholar]
  127. Packard MG, McGaugh JL. 1996. Inactivation of hippocampus or caudate nucleus with lidocaine differentially affects expression of place and response learning. Neurobiol. Learn. Mem. 65:165–72
    [Google Scholar]
  128. 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]
  129. 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]
  130. Park J, Phillips JW, Martin KA, Hantman AW, Dudman JT 2019. Flexible routing of motor control signals through neocortical projection neuron classes. bioRxiv 772517. https://doi.org/10.1101/772517
    [Crossref]
  131. 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]
  132. Parr-Brownlie LC, Poloskey SL, Bergstrom DA, Walters JR 2009. Parafascicular thalamic nucleus activity in a rat model of Parkinson's disease. Exp. Neurol. 217:2269–81
    [Google Scholar]
  133. Paz JT, Chavez M, Saillet S, Deniau JM, Charpier S 2007. Activity of ventral medial thalamic neurons during absence seizures and modulation of cortical paroxysms by the nigrothalamic pathway. J. Neurosci. 27:4929–41
    [Google Scholar]
  134. Perrott DR, Saberi K, Brown K, Strybel TZ 1990. Auditory psychomotor coordination and visual search performance. Percept. Psychophys. 48:3214–26
    [Google Scholar]
  135. Person AL, Perkel DJ. 2005. Unitary IPSPs drive precise thalamic spiking in a circuit required for learning. Neuron 46:1129–40
    [Google Scholar]
  136. Philipp R, Hoffmann K-P. 2014. Arm movements induced by electrical microstimulation in the superior colliculus of the macaque monkey. J. Neurosci. 34:93350–63
    [Google Scholar]
  137. Phillips JW, Schulmann A, Hara E, Winnubst J, Liu C et al. 2019. A repeated molecular architecture across thalamic pathways. Nat. Neurosci. 22:1925–35
    [Google Scholar]
  138. Planert H, Szydlowski SN, Hjorth JJJ, Grillner S, Silberberg G 2010. Dynamics of synaptic transmission between fast-spiking interneurons and striatal projection neurons of the direct and indirect pathways. J. Neurosci. 30:93499–507
    [Google Scholar]
  139. Polack P-O, Friedman J, Golshani P 2013. Cellular mechanisms of brain state–dependent gain modulation in visual cortex. Nat. Neurosci. 16:91331–39
    [Google Scholar]
  140. Preston RJ, Bishop GA, Kitai ST 1980. Medium spiny neuron projection from the rat striatum: an intracellular horseradish peroxidase study. Brain Res 183:2253–63
    [Google Scholar]
  141. 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. 11:11760–72
    [Google Scholar]
  142. Roberts BM, White MG, Patton MH, Chen R, Mathur BN 2019. Ensemble encoding of action speed by striatal fast-spiking interneurons. Brain Struct. Funct. 224:72567–76
    [Google Scholar]
  143. Roseberry TK, Lee AM, Lalive AL, Wilbrecht L, Bonci A, Kreitzer AC 2016. Cell-type-specific control of brainstem locomotor circuits by basal ganglia. Cell 164:3526–37
    [Google Scholar]
  144. Rossi MA, Li HE, Lu D, Kim IH, Bartholomew RA et al. 2016. A GABAergic nigrotectal pathway for coordination of drinking behavior. Nat. Neurosci. 19:5742–48
    [Google Scholar]
  145. Rothman JS, Cathala L, Steuber V, Silver RA 2009. Synaptic depression enables neuronal gain control. Nature 457:72321015–18
    [Google Scholar]
  146. Rovó Z, Ulbert I, Acsády L 2012. Drivers of the primate thalamus. J. Neurosci. 32:4917894–908
    [Google Scholar]
  147. Royer S, Zemelman BV, Losonczy A, Kim J, Chance F et al. 2012. Control of timing, rate and bursts of hippocampal place cells by dendritic and somatic inhibition. Nat. Neurosci. 15:769–75
    [Google Scholar]
  148. Rubelowski JM, Menge M, Distler C, Rothermel M, Hoffmann K-P 2013. Connections of the superior colliculus to shoulder muscles of the rat: a dual tracing study. Front. Neuroanat. 7:17
    [Google Scholar]
  149. 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]
  150. 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]
  151. Salinas E, Thier P. 2000. Gain modulation: a major computational principle of the central nervous system. Neuron 27:115–21
    [Google Scholar]
  152. Sato M, Hikosaka O. 2002. Role of primate substantia nigra pars reticulata in reward-oriented saccadic eye movement. J. Neurosci. 22:62363–73
    [Google Scholar]
  153. Schultz W, Dayan P, Montague PR 1997. A neural substrate of prediction and reward. Science 275:53061593–99
    [Google Scholar]
  154. 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]
  155. Schwab BC, Kase D, Zimnik A, Rosenbaum R, Rubin JE, Turner RS 2019. Weak modulation of thalamic discharge by basal ganglia output in association with a reaching task. bioRxiv 546598. https://doi.org/10.1101/546598
    [Crossref]
  156. Schwarting RK, Huston JP. 1996. Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog. Neurobiol. 49:3215–66
    [Google Scholar]
  157. Semba K, Fibiger HC. 1992. Afferent connections of the laterodorsal and the pedunculopontine tegmental nuclei in the rat: a retro-and antero-grade transport and immunohistochemical study. J. Comp. Neurol. 323:3387–410
    [Google Scholar]
  158. Seo M, Lee E, Averbeck BB 2012. Action selection and action value in frontal-striatal circuits. Neuron 74:5947–60
    [Google Scholar]
  159. Shenoy KV, Sahani M, Churchland MM 2013. Cortical control of arm movements: a dynamical systems perspective. Annu. Rev. Neurosci. 36:337–59
    [Google Scholar]
  160. Sherman SM. 2016. Thalamus plays a central role in ongoing cortical functioning. Nat. Neurosci. 19:4533–41
    [Google Scholar]
  161. Shin S, Sommer MA. 2010. Activity of neurons in monkey globus pallidus during oculomotor behavior compared with that in substantia nigra pars reticulata. J. Neurophysiol. 103:41874–87
    [Google Scholar]
  162. Silberberg G, Bolam JP. 2015. Local and afferent synaptic pathways in the striatal microcircuitry. Curr. Opin. Neurobiol. 33:182–87
    [Google Scholar]
  163. Smalianchuk I, Jagadisan UK, Gandhi NJ 2018. Instantaneous midbrain control of saccade velocity. J. Neurosci. 38:4710156–67
    [Google Scholar]
  164. 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]
  165. Sober SJ, Sponberg S, Nemenman I, Ting LH 2018. Millisecond spike timing codes for motor control. Trends Neurosci 41:10644–48
    [Google Scholar]
  166. Somogyi P, Bolam JP, Smith AD 1981. Monosynaptic cortical input and local axon collaterals of identified striatonigral neurons. A light and electron microscopic study using the Golgi-peroxidase transport-degeneration procedure. J. Comp. Neurol. 195:4567–84
    [Google Scholar]
  167. Sparks DL. 1986. Translation of sensory signals into commands for control of saccadic eye movements: role of primate superior colliculus. Physiol. Rev. 66:1118–71
    [Google Scholar]
  168. Sparks DL, Mays LE. 1990. Signal transformations required for the generation of saccadic eye movements. Annu. Rev. Neurosci. 13:309–36
    [Google Scholar]
  169. Stanford TR, Freedman EG, Sparks DL 1996. Site and parameters of microstimulation: evidence for independent effects on the properties of saccades evoked from the primate superior colliculus. J. Neurophysiol. 76:53360–81
    [Google Scholar]
  170. Stringer C, Pachitariu M, Steinmetz N, Reddy CB, Carandini M, Harris KD 2019. Spontaneous behaviors drive multidimensional, brainwide activity. Science 364:6437eaav7893
    [Google Scholar]
  171. Stroud JP, Porter MA, Hennequin G, Vogels TP 2018. Motor primitives in space and time via targeted gain modulation in cortical networks. Nat. Neurosci 21:121774–83 Erratum. 2018 Nat. Neurosci 22:504
    [Google Scholar]
  172. Surmeier DJ, Plotkin J, Shen W 2009. Dopamine and synaptic plasticity in dorsal striatal circuits controlling action selection. Curr. Opin. Neurobiol. 19:6621–28
    [Google Scholar]
  173. 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. 15:91281–89
    [Google Scholar]
  174. Tanaka YH, Tanaka YR, Kondo M, Terada S-I, Kawaguchi Y, Matsuzaki M 2018. Thalamocortical axonal activity in motor cortex exhibits layer-specific dynamics during motor learning. Neuron 100:1244–58.e12
    [Google Scholar]
  175. Taverna S, van Dongen YC, Groenewegen HJ, Pennartz CMA 2004. Direct physiological evidence for synaptic connectivity between medium-sized spiny neurons in rat nucleus accumbens in situ. J. Neurophysiol 91:31111–21
    [Google Scholar]
  176. Tepper JM, Koós T, Wilson CJ 2004. GABAergic microcircuits in the neostriatum. Trends Neurosci 27:11662–69
    [Google Scholar]
  177. 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]
  178. Turner RS, Anderson ME. 1997. Pallidal discharge related to the kinematics of reaching movements in two dimensions. J. Neurophysiol. 77:31051–74
    [Google Scholar]
  179. Turner RS, Desmurget M. 2010. Basal ganglia contributions to motor control: a vigorous tutor. Curr. Opin. Neurobiol. 20:6704–16
    [Google Scholar]
  180. Van Opstal AJ, Hepp K, Suzuki Y, Henn V 1995. Influence of eye position on activity in monkey superior colliculus. J. Neurophysiol. 74:41593–610
    [Google Scholar]
  181. Wallace MT, Wilkinson LK, Stein BE 1996. Representation and integration of multiple sensory inputs in primate superior colliculus. J. Neurophysiol. 76:21246–66
    [Google Scholar]
  182. Wang L, Rangarajan KV, Gerfen CR, Krauzlis RJ 2018. Activation of striatal neurons causes a perceptual decision bias during visual change detection in mice. Neuron 97:61369–81.e5
    [Google Scholar]
  183. Werner W, Dannenberg S, Hoffmann K-P 1997. Arm-movement-related neurons in the primate superior colliculus and underlying reticular formation: comparison of neuronal activity with EMGs of muscles of the shoulder, arm and trunk during reaching. Exp. Brain Res. 115:2191–205
    [Google Scholar]
  184. West MO, Carelli RM, Pomerantz M, Cohen SM, Gardner JP et al. 1990. A region in the dorsolateral striatum of the rat exhibiting single-unit correlations with specific locomotor limb movements. J. Neurophysiol. 64:41233–46
    [Google Scholar]
  185. Westby GWM, Collinson C, Redgrave P, Dean P 1994. Opposing excitatory and inhibitory influences from the cerebellum and basal ganglia converge on the superior colliculus: an electrophysiological investigation in the rat. Eur. J. Neurosci. 6:81335–42
    [Google Scholar]
  186. Williams LE, Holtmaat A. 2019. Higher-order thalamocortical inputs gate synaptic long-term potentiation via disinhibition. Neuron 101:191–102.e4
    [Google Scholar]
  187. Wiltschko AB, Johnson MJ, Iurilli G, Peterson RE, Katon JM et al. 2015. Mapping sub-second structure in mouse behavior. Neuron 88:61121–35
    [Google Scholar]
  188. Winnubst J, Bas E, Ferreira TA, Wu Z, Economo MN et al. 2019. Reconstruction of 1,000 projection neurons reveals new cell types and organization of long-range connectivity in the mouse brain. Cell 179:1268–81.e13
    [Google Scholar]
  189. Wolf AB, Lintz MJ, Costabile JD, Thompson JA, Stubblefield EA, Felsen G 2015. An integrative role for the superior colliculus in selecting targets for movements. J. Neurophysiol. 114:42118–31
    [Google Scholar]
  190. Xu M, Li L, Pittenger C 2016. Ablation of fast-spiking interneurons in the dorsal striatum, recapitulating abnormalities seen post-mortem in Tourette syndrome, produces anxiety and elevated grooming. Neuroscience 324:321–29
    [Google Scholar]
  191. Yazebnik Y. 2012. Can a biologist fix a radio?—Or, what I learned while studying apoptosis. Cancer Cell 2:3179–82
    [Google Scholar]
  192. Yttri EA, Dudman JT. 2016. Opponent and bidirectional control of movement velocity in the basal ganglia. Nature 533:7603402–6
    [Google Scholar]
  193. Yttri EA, Dudman JT. 2018. A proposed circuit computation in basal ganglia: history‐dependent gain. Mov. Disord. 33:5704–16
    [Google Scholar]
  194. Zahn JR, Abel LA, Dell'Osso LF 1978. Audio-ocular response characteristics. Sens. Processes 2:132–37
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-070918-050452
Loading
/content/journals/10.1146/annurev-neuro-070918-050452
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
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