1932

Abstract

Locomotion is a universal motor behavior that is expressed as the output of many integrated brain functions. Locomotion is organized at several levels of the nervous system, with brainstem circuits acting as the gate between brain areas regulating innate, emotional, or motivational locomotion and executive spinal circuits. Here we review recent advances on brainstem circuits involved in controlling locomotion. We describe how delineated command circuits govern the start, speed, stop, and steering of locomotion. We also discuss how these pathways interface between executive circuits in the spinal cord and diverse brain areas important for context-specific selection of locomotion. A recurrent theme is the need to establish a functional connectome to and from brainstem command circuits. Finally, we point to unresolved issues concerning the integrated function of locomotor control.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-neuro-082321-025137
2022-07-08
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/neuro/45/1/annurev-neuro-082321-025137.html?itemId=/content/journals/10.1146/annurev-neuro-082321-025137&mimeType=html&fmt=ahah

Literature Cited

  1. Adam EM, Johns T, Sur M. 2020. Cortico-subthalamic projections send brief stop signals to halt visually-guided locomotion. bioRxiv 2020.02.05.936443. https://doi.org/10.1101/2020.02.05.936443
    [Crossref]
  2. Al-Mosawie A, Wilson JM, Brownstone RM 2007. Heterogeneity of V2-derived interneurons in the adult mouse spinal cord. Eur. J. Neurosci. 26:113003–15
    [Google Scholar]
  3. Allen LF, Inglis WL, Winn P. 1996. Is the cuneiform nucleus a critical component of the mesencephalic locomotor region? An examination of the effects of excitotoxic lesions of the cuneiform nucleus on spontaneous and nucleus accumbens induced locomotion. Brain Res. Bull. 41:4201–10
    [Google Scholar]
  4. Amemiya M, Yamaguchi T. 1984. Fictive locomotion of the forelimb evoked by stimulation of the mesencephalic locomotor region in the decerebrate cat. Neurosci. Lett. 50:1–391–96
    [Google Scholar]
  5. Assareh N, Sarrami M, Carrive P, McNally GP 2016. The organization of defensive behavior elicited by optogenetic excitation of rat lateral or ventrolateral periaqueductal gray. Behav. Neurosci. 130:4406–14
    [Google Scholar]
  6. Ausborn J, Shevtsova N, Caggiano V, Danner S, Rybak I. 2019. Computational modeling of brainstem circuits controlling locomotor frequency and gait. eLife 8:e43587
    [Google Scholar]
  7. Aziz TZ, Davies L, Stein J, France S. 1998. The role of descending basal ganglia connections to the brain stem in Parkinsonian akinesia. Br. J. Neurosurg. 12:3245–49
    [Google Scholar]
  8. Bellardita C, Kiehn O. 2015. Phenotypic characterization of speed-associated gait changes in mice reveals modular organization of locomotor networks. Curr. Biol. 25:111426–36
    [Google Scholar]
  9. Botta P, Fushiki A, Vicente A, Hammond L, Mosberger A et al. 2020. An amygdala circuit mediates experience-dependent momentary arrests during exploration. Cell 183:3605–619.e22
    [Google Scholar]
  10. Bouvier J, Caggiano V, Leiras R, Caldeira V, Bellardita C et al. 2015. Descending command neurons in the brainstem that halt locomotion. Cell 163:51191–203
    [Google Scholar]
  11. Branco T, Redgrave P. 2020. The neural basis of escape behavior in vertebrates. Annu. Rev. Neurosci. 43:417–39
    [Google Scholar]
  12. Bretzner F, Brownstone R. 2013. Lhx3-Chx10 reticulospinal neurons in locomotor circuits. J. Neurosci. 33:3714681–92
    [Google Scholar]
  13. Brocard F, Ryczko D, Fénelon K, Hatem R, Gonzales D et al. 2010. The transformation of a unilateral locomotor command into a symmetrical bilateral activation in the brainstem. J. Neurosci. 30:2523–33
    [Google Scholar]
  14. Brownstone R, Chopek J. 2018. Reticulospinal systems for tuning motor commands. Front. Neural Circuits 12:30
    [Google Scholar]
  15. Brudzynski SM, Houghton PE, Brownlee RD, Mogenson GJ. 1986. Involvement of neuronal cell bodies of the mesencephalic locomotor region in the initiation of locomotor activity of freely behaving rats. Brain Res. Bull. 16:3377–81
    [Google Scholar]
  16. Brudzynski SM, Mogenson GJ. 1985. Association of the mesencephalic locomotor region with locomotor activity induced by injections of amphetamine into the nucleus accumbens. Brain Res 334:177–84
    [Google Scholar]
  17. Brudzynski SM, Wang D. 1996. c-Fos immunohistochemical localization of neurons in the mesencephalic locomotor region in the rat brain. Neuroscience 75:3793–803
    [Google Scholar]
  18. Butt S, Kiehn O. 2003. Functional identification of interneurons responsible for left-right coordination of hindlimbs in mammals. Neuron 38:6953–63
    [Google Scholar]
  19. 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]
  20. Caldeira V, Dougherty KJ, Borgius L, Kiehn O. 2017. Spinal Hb9::Cre-derived excitatory interneurons contribute to rhythm generation in the mouse. Sci. Rep. 7:41369
    [Google Scholar]
  21. Capelli P, Pivetta C, Esposito MS, Arber S. 2017. Locomotor speed control circuits in the caudal brainstem. Nature 551:7680373–77
    [Google Scholar]
  22. Carvalho MM, Tanke N, Kropff E, Witter MP, Moser MB, Moser EI. 2020. A brainstem locomotor circuit drives the activity of speed cells in the medial entorhinal cortex. Cell Rep 32:10108123
    [Google Scholar]
  23. Ciocchi S, Herry C, Grenier F, Wolff S, Letzkus J et al. 2010. Encoding of conditioned fear in central amygdala inhibitory circuits. Nature 468:7321277–82
    [Google Scholar]
  24. Coles SK, Iles JF, Nicolopoulos-Stournaras S. 1989. The mesencephalic centre controlling locomotion in the rat. Neuroscience 28:1149–57
    [Google Scholar]
  25. Cregg JM, Leiras R, Montalant A, Wanken P, Wickersham IR, Kiehn O. 2020. Brainstem neurons that command mammalian locomotor asymmetries. Nat. Neurosci. 23:6730–40
    [Google Scholar]
  26. Crone SA, Quinlan KA, Zagoraiou L, Droho S, Restrepo CE et al. 2008. Genetic ablation of V2a ipsilateral interneurons disrupts left-right locomotor coordination in mammalian spinal cord. Neuron 60:170–83
    [Google Scholar]
  27. Dampney RAL, Furlong TM, Horiuchi J, Iigaya K. 2013. Role of dorsolateral periaqueductal grey in the coordinated regulation of cardiovascular and respiratory function. Auton. Neurosci. Basic Clin. 175:1–217–25
    [Google Scholar]
  28. Darmohray DM, Jacobs JR, Marques HG, Carey MR. 2019. Spatial and temporal locomotor learning in mouse cerebellum. Neuron 102:1217–31.e4
    [Google Scholar]
  29. Dautan D, Kovács A, Bayasgalan T, Diaz-Acevedo M, Pal B, Mena-Segovia J. 2021. Modulation of motor behavior by the mesencephalic locomotor region. Cell Rep 36:8109594
    [Google Scholar]
  30. Dean P, Mitchell IJ, Redgrave P 1988. Responses resembling defensive behaviour produced by microinjection of glutamate into superior colliculus of rats. Neuroscience 24:2501–10
    [Google Scholar]
  31. Dean P, Redgrave P, Sahibzada N, Tsuji K. 1986. Head and body movements produced by electrical stimulation of superior colliculus in rats: effects of interruption of crossed tectoreticulospinal pathway. Neuroscience 19:2367–80
    [Google Scholar]
  32. Dean P, Redgrave P, Westby GWM 1989. Event or emergency? Two response systems in the mammalian superior colliculus. Trends Neurosci 12:4137–47
    [Google Scholar]
  33. DeLong MR. 1990. Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:7281–85
    [Google Scholar]
  34. Deng H, Xiao X, Wang Z 2016. Periaqueductal gray neuronal activities underlie different aspects of defensive behaviors. J. Neurosci. 36:297580–88
    [Google Scholar]
  35. Dougherty K, Ha N. 2019. The rhythm section: an update on spinal interneurons setting the beat for mammalian locomotion. Curr. Opin. Physiol. 8:84–93
    [Google Scholar]
  36. Dougherty KJ, Zagoraiou L, Satoh D, Rozani I, Doobar S et al. 2013. Locomotor rhythm generation linked to the output of spinal Shox2 excitatory interneurons. Neuron 80:920–33
    [Google Scholar]
  37. Douglas J, Noga B, Dai X, Jordan L. 1993. The effects of intrathecal administration of excitatory amino acid agonists and antagonists on the initiation of locomotion in the adult cat. J. Neurosci. 13:3990–1000
    [Google Scholar]
  38. Drew T, Marigold D 2015. Taking the next step: cortical contributions to the control of locomotion. Curr. Opin. Neurobiol. 33:25–33
    [Google Scholar]
  39. Dubuc R, Brocard F, Antri M, Fénelon K, Gariépy J-F et al. 2008. Initiation of locomotion in lampreys. Brain Res. Rev. 57:1172–82
    [Google Scholar]
  40. Dyson K, Miron J, Drew T. 2014. Differential modulation of descending signals from the reticulospinal system during reaching and locomotion. J. Neurophysiol. 112:102505–28
    [Google Scholar]
  41. Edgley S, Jankowska E, Shefchyk S 1988. Evidence that mid-lumbar neurones in reflex pathways from group II afferents are involved in locomotion in the cat. J. Physiol. 403:157–71
    [Google Scholar]
  42. Eidelberg E, Walden JG, Nguyen LH 1981. Locomotor control in macaque monkeys. Brain 104:4647–63
    [Google Scholar]
  43. Eklöf Ljunggren E, Haupt S, Ausborn J, Ampatzis K, El Manira A. 2014. Optogenetic activation of excitatory premotor interneurons is sufficient to generate coordinated locomotor activity in larval zebrafish. J. Neurosci. 34:1134–39
    [Google Scholar]
  44. 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]
  45. Fadok JP, Krabbe S, Markovic M, Courtin J, Xu C et al. 2017. A competitive inhibitory circuit for selection of active and passive fear responses. Nature 542:763996–99
    [Google Scholar]
  46. Fagerstedt P, Orlovsky GN, Deliagina TG, Grillner S, Ullén F 2001. Lateral turns in the lamprey. II. Activity of reticulospinal neurons during the generation of fictive turns. J. Neurophysiol. 86:52257–65
    [Google Scholar]
  47. Ferreira-Pinto M, Kanodia H, Falasconi A, Sigrist M, Esposito M, Arber S. 2021. Functional diversity for body actions in the mesencephalic locomotor region. Cell 184:4564–78.e18
    [Google Scholar]
  48. Ferreira-Pinto MJ, Ruder L, Capelli P, Arber S 2018. Connecting circuits for supraspinal control of locomotion. Neuron 100:2361–74
    [Google Scholar]
  49. Ferris BD, Green J, Maimon G. 2018. Abolishment of spontaneous flight turns in visually responsive Drosophila. Curr. Biol. 28:2170–80.e5
    [Google Scholar]
  50. Fobbs W, Bariselli S, Licholai J, Miyazaki N, Matikainen-Ankney B et al. 2020. Continuous representations of speed by striatal medium spiny neurons. J. Neurosci. 40:81679–88
    [Google Scholar]
  51. Garcia-Rill E. 1986. The basal ganglia and the locomotor regions. Brain Res. Rev. 11:147–63
    [Google Scholar]
  52. Garcia-Rill E, Skinner RD, Fitzgerald JA. 1985. Chemical activation of the mesencephalic locomotor region. Brain Res 330:143–54
    [Google Scholar]
  53. Garcia-Rill E, Skinner RD, Gilmore SA. 1981. Pallidal projections to the mesencephalic locomotor region (MLR) in the cat. Am. J. Anat. 161:3311–21
    [Google Scholar]
  54. Goñi-Erro H, Leiras R, Kiehn O 2020. A subpopulation of glutamatergic pedunculopontine neurons transiently arrests movement. FENS Virtual Forum 2020:2292 (Abstr.)
    [Google Scholar]
  55. Goulding M. 2009. Circuits controlling vertebrate locomotion: moving in a new direction. Nat. Rev. Neurosci. 10:7507–18
    [Google Scholar]
  56. Grätsch S, Auclair F, Demers O, Auguste E, Hanna A et al. 2019. A brainstem neural substrate for stopping locomotion. J. Neurosci. 39:61044–57
    [Google Scholar]
  57. Grillner S. 2003. The motor infrastructure: from ion channels to neuronal networks. Nat. Rev. Neurosci. 4:7573–86
    [Google Scholar]
  58. Grillner S, El Manira A. 2020. Current principles of motor control, with special reference to vertebrate locomotion. Physiol. Rev. 100:1271–320
    [Google Scholar]
  59. Grillner S, Georgopoulos AP, Jordan L 1997. Neurons, Networks and Motor Behavior Cambridge, MA: MIT Press
  60. Grillner S, Jessell TM. 2009. Measured motion: searching for simplicity in spinal locomotor networks. Curr. Opin. Neurobiol. 19:6572–86
    [Google Scholar]
  61. Grillner S, Kozlov A, Dario P, Stefanini C, Menciassi A et al. 2007. Modeling a vertebrate motor system: pattern generation, steering and control of body orientation. Prog. Brain Res. 165:221–34
    [Google Scholar]
  62. Grillner S, Robertson B. 2015. The basal ganglia downstream control of brainstem motor centres—an evolutionarily conserved strategy. Curr. Opin. Neurobiol. 33:47–52
    [Google Scholar]
  63. Gruntman E, Benjamini Y, Golani I. 2007. Coordination of steering in a free-trotting quadruped. J. Comp. Physiol. A. Neuroethol. Sens. Neural. Behav. Physiol. 193:3331–45
    [Google Scholar]
  64. Guillaumin A, Serra G, Georges F, Wallén-Mackenzie Å. 2021. Experimental investigation into the role of the subthalamic nucleus (STN) in motor control using optogenetics in mice. Brain Res 1755:147226
    [Google Scholar]
  65. Hägglund M, Borgius L, Dougherty KJ, Kiehn O. 2010. Activation of groups of excitatory neurons in the mammalian spinal cord or hindbrain evokes locomotion. Nat. Neurosci. 13:246–52
    [Google Scholar]
  66. Harris-Warrick RM. 2011. Neuromodulation and flexibility in Central Pattern Generator networks. Curr. Opin. Neurobiol. 21:5685–92
    [Google Scholar]
  67. Herry C, Johansen J. 2014. Encoding of fear learning and memory in distributed neuronal circuits. Nat. Neurosci. 17:121644–54
    [Google Scholar]
  68. Huang KH, Ahrens MB, Dunn TW, Engert F. 2013. Spinal projection neurons control turning behaviors in zebrafish. Curr. Biol. 23:161566–73
    [Google Scholar]
  69. Inglis WL, Allen LF, Whitelaw RB, Latimer MP, Brace HM, Winn P. 1994. An investigation into the role of the pedunculopontine tegmental nucleus in the mediation of locomotion and orofacial stereotypy induced by d-amphetamine and apomorphine in the rat. Neuroscience 58:4817–33
    [Google Scholar]
  70. Isa K, Sooksawate T, Kobayashi K, Kobayashi K, Redgrave P, Isa T 2020. Dissecting the tectal output channels for orienting and defense responses. eNeuro 7:5ENEURO.0271–20.2020
    [Google Scholar]
  71. Isa T, Marquez-Legorreta E, Grillner S, Scott EK 2021. The tectum/superior colliculus as the vertebrate solution for spatial sensory integration and action. Curr. Biol. 31:11R741–62
    [Google Scholar]
  72. Jankowska E. 2008. Spinal interneuronal networks in the cat: elementary components. Brain Res. Rev. 57:146–55
    [Google Scholar]
  73. Jankowska E, Hammar I, Slawinska U, Maleszak K, Edgley S 2003. Neuronal basis of crossed actions from the reticular formation on feline hindlimb motoneurons. J. Neurosci. 23:51867–78
    [Google Scholar]
  74. Jordan L. 1998. Initiation of locomotion in mammals. Ann. N. Y. Acad. Sci. 860:83–93
    [Google Scholar]
  75. Jordan LM, Liu J, Hedlund PB, Akay T, Pearson KG 2008. Descending command systems for the initiation of locomotion in mammals. Brain Res. Rev. 57:1183–91
    [Google Scholar]
  76. Josset N, Roussel M, Lemieux M, Lafrance-Zoubga D, Rastqar A, Bretzner F 2018. Distinct contributions of mesencephalic locomotor region nuclei to locomotor control in the freely behaving mouse. Curr. Biol. 28:6884–901.e3
    [Google Scholar]
  77. Juvin L, Grätsch S, Trillaud-Doppia E, Gariépy J-F, Büschges A, Dubuc R 2016. A specific population of reticulospinal neurons controls the termination of locomotion. Cell Rep 15:112377–86
    [Google Scholar]
  78. Karachi C, Grabli D, Bernard FA, Tandé D, Wattiez N et al. 2010. Cholinergic mesencephalic neurons are involved in gait and postural disorders in Parkinson disease. J. Clin. Investig. 120:2745–54
    [Google Scholar]
  79. Kiehn O. 2006. Locomotor circuits in the mammalian spinal cord. Annu. Rev. Neurosci. 29:279–306
    [Google Scholar]
  80. Kiehn O. 2016. Decoding the organization of spinal circuits that control locomotion. Nat. Rev. Neurosci. 17:4224–38
    [Google Scholar]
  81. Kim LH, Sharma S, Sharples SA, Mayr KA, Kwok CHT, Whelan PJ. 2017. Integration of descending command systems for the generation of context-specific locomotor behaviors. Front. Neurosci. 11:581
    [Google Scholar]
  82. 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]
  83. 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]
  84. Kroeger D, Ferrari L, Petit G, Mahoney C, Fuller P et al. 2017. Cholinergic, glutamatergic, and GABAergic neurons of the pedunculopontine tegmental nucleus have distinct effects on sleep/wake behavior in mice. J. Neurosci. 37:51352–66
    [Google Scholar]
  85. Lanuza GM, Gosgnach S, Pierani A, Jessell TM, Goulding M. 2004. Genetic identification of spinal interneurons that coordinate left-right locomotor activity necessary for walking movements. Neuron 42:3375–86
    [Google Scholar]
  86. Lee A, Hoy J, Bonci A, Wilbrecht L, Stryker M, Niell C. 2014. Identification of a brainstem circuit regulating visual cortical state in parallel with locomotion. Neuron 83:2455–66
    [Google Scholar]
  87. Lemieux M, Bretzner F. 2019. Glutamatergic neurons of the gigantocellular reticular nucleus shape locomotor pattern and rhythm in the freely behaving mouse. PLOS Biol 17:4e2003880
    [Google Scholar]
  88. Li WC, Soffe SR, Wolf E, Roberts A 2006. Persistent responses to brief stimuli: feedback excitation among brainstem neurons. J. Neurosci. 26:154026–35
    [Google Scholar]
  89. Liu J, Jordan LM. 2005. Stimulation of the parapyramidal region of the neonatal rat brain stem produces locomotor-like activity involving spinal 5-HT7 and 5-HT2A receptors. J. Neurophysiol. 94:21392–404
    [Google Scholar]
  90. Lundfald L, Restrepo CE, Butt SJB, Peng CY, Droho S et al. 2007. Phenotype of V2-derived interneurons and their relationship to the axon guidance molecule EphA4 in the developing mouse spinal cord. Eur. J. Neurosci. 26:112989–3002
    [Google Scholar]
  91. Marlinsky VV, Voitenko LP. 1991. The effect of procaine injection into the medullary reticular formation on forelimb muscle activity evoked by mesencephalic locomotor region and vestibular stimulation in the decerebrated guinea-pig. Neuroscience 45:3753–59
    [Google Scholar]
  92. Masini D, Kiehn O. 2022. Targeted activation of midbrain neurons restores locomotor function in mouse models of parkinsonism. Nat. Commun 13:504
    [Google Scholar]
  93. Masullo L, Mariotti L, Alexandre N, Freire-Pritchett P, Boulanger J, Tripodi M. 2019. Genetically defined functional modules for spatial orienting in the mouse superior colliculus. Curr. Biol. 29:172892–904.e8
    [Google Scholar]
  94. Matsuyama K, Nakajima K, Mori F, Aoki M, Mori S. 2004. Lumbar commissural interneurons with reticulospinal inputs in the cat: morphology and discharge patterns during fictive locomotion. J. Comp. Neurol. 474:4546–61
    [Google Scholar]
  95. McClellan AD, Grillner S. 1984. Activation of “fictive swimming” by electrical microstimulation of brainstem locomotor regions in an in vitro preparation of the lamprey central nervous system. Brain Res 300:2357–61
    [Google Scholar]
  96. McElvain L, Chen Y, Moore J, Brigidi G, Bloodgood B et al. 2021. Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon. Neuron 109:101721–38.e4
    [Google Scholar]
  97. McLean D, Masino M, Koh I, Lindquist W, Fetcho J. 2008. Continuous shifts in the active set of spinal interneurons during changes in locomotor speed. Nat. Neurosci. 11:121419–29
    [Google Scholar]
  98. Mena-Segovia J, Bolam JP. 2017. Rethinking the pedunculopontine nucleus: from cellular organization to function. Neuron 94:17–18
    [Google Scholar]
  99. Milner KL, Mogenson GJ. 1988. Electrical and chemical activation of the mesencephalic and subthalamic locomotor regions in freely moving rats. Brain Res 452:1–2273–85
    [Google Scholar]
  100. Mori S, Nishimura H, Kurakami C, Yamamura T, Aoki M 1978. Controlled locomotion in the mesencephalic cat: distribution of facilitatory and inhibitory regions within pontine tegmentum. J. Neurophysiol. 41:61580–91
    [Google Scholar]
  101. Mori S, Sakamoto T, Ohta Y, Takakusaki K, Matsuyama K 1989. Site-specific postural and locomotor changes evoked in awake, freely moving intact cats by stimulating the brainstem. Brain Res 505:166–74
    [Google Scholar]
  102. Mullie Y, Arto I, Yahiaoui N, Drew T 2020. Contribution of the entopeduncular nucleus and the globus pallidus to the control of locomotion and visually guided gait modifications in the cat. Cereb. Cortex 30:95121–46
    [Google Scholar]
  103. Musienko PE, Zelenin PV, Lyalka VF, Gerasimenko YP, Orlovsky GN, Deliagina TG. 2012. Spinal and supraspinal control of the direction of stepping during locomotion. J. Neurosci. 32:4817442–53
    [Google Scholar]
  104. Nambu A. 2004. A new dynamic model of the cortico-basal ganglia loop. Prog. Brain Res. 143:461–66
    [Google Scholar]
  105. Noga BR, Kettler J, Jordan LM. 1988. Locomotion produced in mesencephalic cats by injections of putative transmitter substances and antagonists into the medial reticular formation and the pontomedullary locomotor strip. J. Neurosci. 8:62074–86
    [Google Scholar]
  106. Noga BR, Kriellaars DJ, Jordan LM. 1991. The effect of selective brainstem or spinal cord lesions on treadmill locomotion evoked by stimulation of the mesencephalic or pontomedullary locomotor regions. J. Neurosci. 11:61691–700
    [Google Scholar]
  107. Ohta Y, Grillner S. 1989. Monosynaptic excitatory amino acid transmission from the posterior rhombencephalic reticular nucleus to spinal neurons involved in the control of locomotion in lamprey. J. Neurophysiol. 62:51079–89
    [Google Scholar]
  108. Opris I, Dai X, Johnson DMG, Sanchez FJ, Villamil LM et al. 2019. Activation of brainstem neurons during mesencephalic locomotor region-evoked locomotion in the cat. Front. Syst. Neurosci. 13:69
    [Google Scholar]
  109. Packard MG, McGaugh JL. 1992. Double dissociation of fornix and caudate nucleus lesions on acquisition of two water maze tasks: further evidence for multiple memory systems. Behav. Neurosci. 106:3439–46
    [Google Scholar]
  110. Parolari L, Schneeberger M, Heintz N, Friedman J. 2021. Functional analysis of distinct populations of subthalamic nucleus neurons on Parkinson's disease and OCD-like behaviors in mice. Mol. Psychiatry 26:702946
    [Google Scholar]
  111. Quinlan K, Kiehn O 2007. Segmental, synaptic actions of commissural interneurons in the mouse spinal cord. J. Neurosci. 27:246521–30
    [Google Scholar]
  112. Rancic V, Gosgnach S. 2021. Recent insights into the rhythmogenic core of the locomotor CPG. Int. J. Mol. Sci. 22:31394
    [Google Scholar]
  113. Rayshubskiy A, Holtz S, D'Alessandro I, Li A, Vanderbeck Q et al. 2020. Neural circuit mechanisms for steering control in walking Drosophila. bioRxiv 2020.04.04.024703. https://doi.org/10.1101/2020.04.04.024703
    [Crossref]
  114. Rizzi G, Tan KR. 2019. Synergistic nigral output pathways shape movement. Cell Rep 27:72184–98.e4
    [Google Scholar]
  115. Robbe D. 2018. To move or to sense? Incorporating somatosensory representation into striatal functions. Curr. Opin. Neurobiol. 52:123–30
    [Google Scholar]
  116. Roberts A, Li WC, Soffe SR. 2010. How neurons generate behavior in a hatchling amphibian tadpole: an outline. Front. Behav. Neurosci. 4:16
    [Google Scholar]
  117. Rolland AS, Tandé D, Herrero MT, Luquin MR, Vazquez-Claverie M et al. 2009. Evidence for a dopaminergic innervation of the pedunculopontine nucleus in monkeys, and its drastic reduction after MPTP intoxication. J. Neurochem. 110:41321–29
    [Google Scholar]
  118. Roseberry T, Kreitzer A. 2017. Neural circuitry for behavioural arrest. Philos. Trans. R. Soc. Lond. B. Biol. Sci. 372:171820160197
    [Google Scholar]
  119. Roseberry TK, Lalive AL, Margolin BD, Kreitzer AC. 2019. Locomotor suppression by a monosynaptic amygdala to brainstem circuit. bioRxiv 724252. https://doi.org/10.1101/724252
    [Crossref]
  120. 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]
  121. Ruder L, Arber S. 2019. Brainstem circuits controlling action diversification. Annu. Rev. Neurosci. 42:485–504
    [Google Scholar]
  122. Ryczko D, Cone JJ, Alpert MH, Goetz L, Auclair F et al. 2016. A descending dopamine pathway conserved from basal vertebrates to mammals. PNAS 113:17E2440–49
    [Google Scholar]
  123. Ryczko D, Dubuc R. 2013. The multifunctional mesencephalic locomotor region. Curr. Pharm. Des. 19:244448–70
    [Google Scholar]
  124. Schepens B, Drew T. 2006. Descending signals from the pontomedullary reticular formation are bilateral, asymmetric, and gated during reaching movements in the cat. J. Neurophysiol. 96:52229–52
    [Google Scholar]
  125. Schmidt BJ, Jordan LM. 2000. The role of serotonin in reflex modulation and locomotor rhythm production in the mammalian spinal cord. Brain Res. Bull. 53:5689–710
    [Google Scholar]
  126. Schwarz M, Sontag KH, Wand P. 1984. Sensory-motor processing in substantia nigra pars reticulata in conscious cats. J. Physiol. 347:1129–47
    [Google Scholar]
  127. Schweizer N, Pupe S, Arvidsson E, Nordenankar K, Smith-Anttila C et al. 2014. Limiting glutamate transmission in a Vglut2-expressing subpopulation of the subthalamic nucleus is sufficient to cause hyperlocomotion. PNAS 111:217837–42
    [Google Scholar]
  128. Schwenkgrub J, Harrell ER, Bathellier B, Bouvier J. 2020. Deep imaging in the brainstem reveals functional heterogeneity in V2a neurons controlling locomotion. Sci. Adv. 6:49eabc6309
    [Google Scholar]
  129. Shefchyk SJ, Jell RM, Jordan LM. 1984. Reversible cooling of the brainstem reveals areas required for mesencephalic locomotor region evoked treadmill locomotion. Exp. Brain Res. 56:2257–62
    [Google Scholar]
  130. Shefchyk SJ, Jordan LM. 1985. Excitatory and inhibitory postsynaptic potentials in α-motoneurons produced during fictive locomotion by stimulation of the mesencephalic locomotor region. J. Neurophysiol. 53:61345–55
    [Google Scholar]
  131. Shi LH, Luo F, Woodward DJ, Chang JY. 2004. Neural responses in multiple basal ganglia regions during spontaneous and treadmill locomotion task in rats. Exp. Brain Res. 157:3303–14
    [Google Scholar]
  132. Shik ML, Severin FV, Orlovskii˘ GN. 1966. Control of walking and running by means of electric stimulation of the midbrain. Biofizika 11:4659–66
    [Google Scholar]
  133. Sirota MG, Di Prisco GV, Dubuc R. 2000. Stimulation of the mesencephalic locomotor region elicits controlled swimming in semi-intact lampreys. Eur. J. Neurosci. 12:114081–92
    [Google Scholar]
  134. Sirota MG, Shik ML. 1973. [Locomotion of the cat on stimulation of the mesencephalon]. Fiziol. Zhurnal SSSR Im. I.M. Sechenova. 59:91314–21 In Russian )
    [Google Scholar]
  135. Skinner RD, Garcia-Rill E. 1984. The mesencephalic locomotor region (MLR) in the rat. Brain Res 323:2385–89
    [Google Scholar]
  136. Song J, Pallucchi I, Ausborn J, Ampatzis K, Bertuzzi M et al. 2020. Multiple rhythm-generating circuits act in tandem with pacemaker properties to control the start and speed of locomotion. Neuron 105:61048–61.e4
    [Google Scholar]
  137. Svoboda K, Li N. 2018. Neural mechanisms of movement planning: motor cortex and beyond. Curr. Opin. Neurobiol. 49:33–41
    [Google Scholar]
  138. Szokol K, Glover J, Perreault M. 2011. Organization of functional synaptic connections between medullary reticulospinal neurons and lumbar descending commissural interneurons in the neonatal mouse. J. Neurosci. 31:124731–42
    [Google Scholar]
  139. Takakusaki K, Chiba R, Nozu T, Okumura T. 2016. Brainstem control of locomotion and muscle tone with special reference to the role of the mesopontine tegmentum and medullary reticulospinal systems. J. Neural Transm. 123:7695–729
    [Google Scholar]
  140. Takakusaki K, Habaguchi T, Ohtinata-Sugimoto J, Saitoh K, Sakamoto T 2003. Basal ganglia efferents to the brainstem centers controlling postural muscle tone and locomotion: a new concept for understanding motor disorders in basal ganglia dysfunction. Neuroscience 119:1293–308
    [Google Scholar]
  141. Takakusaki K, Oohinata-Sugimoto J, Saitoh K, Habaguchi T 2004. Role of basal ganglia-brainstem systems in the control of postural muscle tone and locomotion. Prog. Brain Res. 143:231–37
    [Google Scholar]
  142. Talpalar A, Bouvier J, Borgius L, Fortin G, Pierani A, Kiehn O 2013. Dual-mode operation of neuronal networks involved in left-right alternation. Nature 500:746085–88
    [Google Scholar]
  143. 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. 5:14315
    [Google Scholar]
  144. Thiele TR, Donovan JC, Baier H. 2014. Descending control of swim posture by a midbrain nucleus in zebrafish. Neuron 83:3679–91
    [Google Scholar]
  145. Tovote P, Esposito MS, Botta P, Chaudun F, Fadok JP et al. 2016. Midbrain circuits for defensive behaviour. Nature 534:7606206–12
    [Google Scholar]
  146. Tovote P, Fadok JP, Lüthi A. 2015. Neuronal circuits for fear and anxiety. Nat. Rev. Neurosci. 16:6317–31
    [Google Scholar]
  147. Usseglio G, Gatier E, Heuzé A, Hérent C, Bouvier J. 2020. Control of orienting movements and locomotion by projection-defined subsets of brainstem V2a neurons. Curr. Biol. 30:234665–4681.e6
    [Google Scholar]
  148. van der Zouwen CI, Boutin J, Fougère M, Flaive A, Vivancos M et al. 2021. Freely behaving mice can brake and turn during optogenetic stimulation of the mesencephalic locomotor region. Front. Neural Circuits 15:639900
    [Google Scholar]
  149. Virmani T, Urbano FJ, Bisagno V, Garcia-Rill E. 2019. The pedunculopontine nucleus: from posture and locomotion to neuroepigenetics. AIMS Neurosci 6:4219–30
    [Google Scholar]
  150. Warren RA, Zhang Q, Hoffman JR, Li EY, Hong YK et al. 2021. A rapid whisker-based decision underlying skilled locomotion in mice. eLife 10:e63596
    [Google Scholar]
  151. Watson G, Hughes R, Petter E, Fallon I, Kim N et al. 2021. Thalamic projections to the subthalamic nucleus contribute to movement initiation and rescue of parkinsonian symptoms. Sci. Adv. 7:6eabe9192
    [Google Scholar]
  152. Wessel J, Aron A. 2017. On the globality of motor suppression: unexpected events and their influence on behavior and cognition. Neuron 93:2259–80
    [Google Scholar]
  153. Winn P. 2006. How best to consider the structure and function of the pedunculopontine tegmental nucleus: evidence from animal studies. J. Neurol. Sci. 248:1–2234–50
    [Google Scholar]
  154. 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]
  155. Zingg B, Chou X, Zhang Z, Mesik L, Liang F et al. 2017. AAV-mediated anterograde transsynaptic tagging: mapping corticocollicular input-defined neural pathways for defense behaviors. Neuron 93:133–47
    [Google Scholar]
/content/journals/10.1146/annurev-neuro-082321-025137
Loading
/content/journals/10.1146/annurev-neuro-082321-025137
Loading

Data & Media loading...

  • 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