Login Register Cart 0
Generic placeholder image

Current Neuropharmacology

Editor-in-Chief

ISSN (Print): 1570-159X
ISSN (Online): 1875-6190

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

The Basal Ganglia and Mesencephalic Locomotor Region Connectivity Matrix

Author(s): Nicolás A. Morgenstern and Maria S. Esposito*

Volume 22, Issue 9, 2024

Published on: 09 August, 2023

Page: [1454 - 1472] Pages: 19

DOI: 10.2174/1570159X21666230809112840

Price: $65

Abstract

Although classically considered a relay station for basal ganglia (BG) output, the anatomy, connectivity, and function of the mesencephalic locomotor region (MLR) were redefined during the last two decades. In striking opposition to what was initially thought, MLR and BG are actually reciprocally and intimately interconnected. New viral-based, optogenetic, and mapping technologies revealed that cholinergic, glutamatergic, and GABAergic neurons coexist in this structure, which, in addition to extending descending projections, send long-range ascending fibers to the BG. These MLR projections to the BG convey motor and non-motor information to specific synaptic targets throughout different nuclei. Moreover, MLR efferent fibers originate from precise neuronal subpopulations located in particular MLR subregions, defining independent anatomo-functional subcircuits involved in particular aspects of animal behavior such as fast locomotion, explorative locomotion, posture, forelimb- related movements, speed, reinforcement, among others. In this review, we revised the literature produced during the last decade linking MLR and BG. We conclude that the classic framework considering the MLR as a homogeneous output structure passively receiving input from the BG needs to be revisited. We propose instead that the multiple subcircuits embedded in this region should be taken as independent entities that convey relevant and specific ascending information to the BG and, thus, actively participate in the execution and tuning of behavior.

« Previous Next »
Graphical Abstract

[1]
Shik, M.L.; Severin, F.V. Orlovskiĭ G.N. Control of walking and running by means of electric stimulation of the midbrain. Biofizika, 1966, 11(4), 659-666.
[PMID: 6000625]
[2]
Mori, S.; Sakamoto, T.; Ohta, Y.; Takakusaki, K.; Matsuyama, K. Site-specific postural and locomotor changes evoked in awake, freely moving intact cats by stimulating the brainstem. Brain Res., 1989, 505(1), 66-74.
[http://dx.doi.org/10.1016/0006-8993(89)90116-9] [PMID: 2611678]
[3]
Eidelberg, E.; Walden, J.G.; Nguyen, L.H. Locomotor control in macaque monkeys. Brain, 1981, 104(4), 647-663.
[http://dx.doi.org/10.1093/brain/104.4.647-a] [PMID: 7326562]
[4]
McClellan, A.D.; Grillner, S. Activation of ‘fictive swimming’ by electrical microstimulation of brainstem locomotor regions in an in vitro preparation of the lamprey central nervous system. Brain Res., 1984, 300(2), 357-361.
[http://dx.doi.org/10.1016/0006-8993(84)90846-1] [PMID: 6733478]
[5]
Garcia-Rill, E.; Skinner, R.D.; Fitzgerald, J.A. Chemical activation of the mesecephalic locomotor region. Brain Res., 1985, 330(1), 43-54.
[http://dx.doi.org/10.1016/0006-8993(85)90006-X] [PMID: 3986540]
[6]
Masdeu, J.C.; Alampur, U.; Cavaliere, R.; Tavoulareas, G. Astasia and gait failure with damage of the pontomesencephalic locomotor region. Ann. Neurol., 1994, 35(5), 619-621.
[http://dx.doi.org/10.1002/ana.410350517] [PMID: 8179307]
[7]
Dubuc, R.; Brocard, F.; Antri, M.; Fénelon, K.; Gariépy, J.F.; Smetana, R.; Ménard, A.; Le Ray, D.; Viana Di Prisco, G.; Pearlstein, É.; Sirota, M.G.; Derjean, D.; St-Pierre, M.; Zielinski, B.; Auclair, F.; Veilleux, D. Initiation of locomotion in lampreys. Brain Res. Brain Res. Rev., 2008, 57(1), 172-182.
[http://dx.doi.org/10.1016/j.brainresrev.2007.07.016] [PMID: 17916380]
[8]
Roseberry, T.K.; Lee, A.M.; Lalive, A.L.; Wilbrecht, L.; Bonci, A.; Kreitzer, A.C. Cell-type-specific control of brainstem locomotor circuits by basal ganglia. Cell, 2016, 164(3), 526-537.
[http://dx.doi.org/10.1016/j.cell.2015.12.037] [PMID: 26824660]
[9]
Grillner, S.; Robertson, B. The basal ganglia over 500 million years. Curr. Biol., 2016, 26(20), R1088-R1100.
[http://dx.doi.org/10.1016/j.cub.2016.06.041]
[10]
Garcia-Rill, E.; Houser, C.R.; Skinner, R.D.; Smith, W.; Woodward, D.J. Locomotion-inducing sites in the vicinity of the pedunculopontine nucleus. Brain Res. Bull., 1987, 18(6), 731-738.
[http://dx.doi.org/10.1016/0361-9230(87)90208-5] [PMID: 3304544]
[11]
Mena-Segovia, J.; Bolam, J.P.; Magill, P.J. Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Trends Neurosci., 2004, 27(10), 585-588.
[http://dx.doi.org/10.1016/j.tins.2004.07.009] [PMID: 15374668]
[12]
Winn, P. How best to consider the structure and function of the pedunculopontine tegmental nucleus: Evidence from animal studies. J. Neurol. Sci., 2006, 248(1-2), 234-250.
[http://dx.doi.org/10.1016/j.jns.2006.05.036] [PMID: 16765383]
[13]
Ryczko, D.; Grätsch, S.; Auclair, F.; Dubé, C.; Bergeron, S.; Alpert, M.H.; Cone, J.J.; Roitman, M.F.; Alford, S.; Dubuc, R. Forebrain dopamine neurons project down to a brainstem region controlling locomotion. Proc. Natl. Acad. Sci. USA, 2013, 110(34), E3235-E3242.
[http://dx.doi.org/10.1073/pnas.1301125110] [PMID: 23918379]
[14]
Takakusaki, K.; Chiba, R.; Nozu, T.; Okumura, T. Brainstem control of locomotion and muscle tone with special reference to the role of the mesopontine tegmentum and medullary reticulospinal systems. J. Neural Transm., 2016, 123(7), 695-729.
[http://dx.doi.org/10.1007/s00702-015-1475-4]
[15]
Noga, B.R.; Whelan, P.J. The mesencephalic locomotor region: Beyond locomotor control. Front. Neural Circuits, 2022, 16, 884785.
[http://dx.doi.org/10.3389/fncir.2022.884785] [PMID: 35615623]
[16]
Grillner, S.; Robertson, B. The basal ganglia downstream control of brainstem motor centres—an evolutionarily conserved strategy. Curr. Opin. Neurobiol., 2015, 33, 47-52.
[http://dx.doi.org/10.1016/j.conb.2015.01.019] [PMID: 25682058]
[17]
Caggiano, V.; Leiras, R.; Goñi-Erro, H.; Masini, D.; Bellardita, C.; Bouvier, J.; Caldeira, V.; Fisone, G.; Kiehn, O. Midbrain circuits that set locomotor speed and gait selection. Nature, 2018, 553(7689), 455-460.
[http://dx.doi.org/10.1038/nature25448] [PMID: 29342142]
[18]
Huerta-Ocampo, I.; Dautan, D.; Gut, N.K.; Khan, B.; Mena-Segovia, J. Whole-brain mapping of monosynaptic inputs to midbrain cholinergic neurons. Sci. Rep., 2021, 11(1), 9055.
[http://dx.doi.org/10.1038/s41598-021-88374-6] [PMID: 33907215]
[19]
Dautan, D.; Kovács, A.; Bayasgalan, T.; Diaz-Acevedo, M.A.; Pal, B.; Mena-Segovia, J. Modulation of motor behavior by the mesencephalic locomotor region. Cell Rep., 2021, 36(8), 109594.
[http://dx.doi.org/10.1016/j.celrep.2021.109594] [PMID: 34433068]
[20]
Dautan, D.; Huerta-Ocampo, I.; Witten, I.B.; Deisseroth, K.; Bolam, J.P.; Gerdjikov, T.; Mena-Segovia, J. A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J. Neurosci., 2014, 34(13), 4509-4518.
[http://dx.doi.org/10.1523/JNEUROSCI.5071-13.2014] [PMID: 24671996]
[21]
Xiao, C.; Cho, J.R.; Zhou, C.; Treweek, J.B.; Chan, K.; McKinney, S.L.; Yang, B.; Gradinaru, V. Cholinergic mesopontine signals govern locomotion and reward through dissociable midbrain pathways. Neuron, 2016, 90(2), 333-347.
[http://dx.doi.org/10.1016/j.neuron.2016.03.028] [PMID: 27100197]
[22]
Kroeger, D.; Ferrari, L.L.; Petit, G.; Mahoney, C.E.; Fuller, P.M.; Arrigoni, E.; Scammell, T.E. Cholinergic, glutamatergic, and GABAergic neurons of the pedunculopontine tegmental nucleus have distinct effects on sleep/wake behavior in mice. J. Neurosci., 2017, 37(5), 1352-1366.
[http://dx.doi.org/10.1523/JNEUROSCI.1405-16.2016] [PMID: 28039375]
[23]
Assous, M.; Dautan, D.; Tepper, J.M.; Mena-Segovia, J. Pedunculopontine glutamatergic neurons provide a novel source of feedforward inhibition in the striatum by selectively targeting interneurons. J. Neurosci., 2019, 39(24), 4727-4737.
[http://dx.doi.org/10.1523/JNEUROSCI.2913-18.2019] [PMID: 30952811]
[24]
Dautan, D.; Huerta-Ocampo, I.; Gut, N.K.; Valencia, M.; Kondabolu, K.; Kim, Y.; Gerdjikov, T.V.; Mena-Segovia, J. Cholinergic midbrain afferents modulate striatal circuits and shape encoding of action strategies. Nat. Commun., 2020, 11(1), 1739.
[http://dx.doi.org/10.1038/s41467-020-15514-3] [PMID: 32269213]
[25]
Ferreira-Pinto, M.J.; Kanodia, H.; Falasconi, A.; Sigrist, M.; Esposito, M.S.; Arber, S. Functional diversity for body actions in the mesencephalic locomotor region. Cell, 2021, 184(17), 4564-4578.e18.
[http://dx.doi.org/10.1016/j.cell.2021.07.002] [PMID: 34302739]
[26]
Lee, J.; Wang, W.; Sabatini, B.L. Anatomically segregated basal ganglia pathways allow parallel behavioral modulation. Nat. Neurosci., 2020, 23(11), 1388-1398.
[http://dx.doi.org/10.1038/s41593-020-00712-5] [PMID: 32989293]
[27]
Arber, S.; Costa, R.M. Networking brainstem and basal ganglia circuits for movement. Nat. Rev. Neurosci., 2022, 23(6), 342-360.
[http://dx.doi.org/10.1038/s41583-022-00581-w] [PMID: 35422525]
[28]
Garcia-Rill, E.; Kinjo, N.; Atsuta, Y.; Ishikawa, Y.; Webber, M.; Skinner, R.D. Posterior midbrain-induced locomotion. Brain Res. Bull., 1990, 24(3), 499-508.
[http://dx.doi.org/10.1016/0361-9230(90)90103-7] [PMID: 1970947]
[29]
Rye, D.B.; Saper, C.B.; Lee, H.J.; Wainer, B.H. Pedunculopontine tegmental nucleus of the rat: Cytoarchitecture, cytochemistry, and some extrapyramidal connections of the mesopontine tegmentum. J. Comp. Neurol., 1987, 259(4), 483-528.
[http://dx.doi.org/10.1002/cne.902590403] [PMID: 2885347]
[30]
Grofova, I.; Zhou, M. Nigral innervation of cholinergic and glutamatergic cells in the rat mesopontine tegmentum: Light and electron microscopic anterograde tracing and immunohistochemical studies. J. Comp. Neurol., 1998, 395(3), 359-379.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19980808)395:3<359:AID-CNE7>3.0.CO;2-1] [PMID: 9596529]
[31]
Mink, J.W. A model for waste processing? Pergamorr. Prog. Neurobiol., 1996, 50, 26.
[32]
Steriade, M.; Paré, D.; Parent, A.; Smith, Y. Projections of cholinergic and non-cholinergic neurons of the brainstem core to relay and associational thalamic nuclei in the cat and macaque monkey. Neuroscience, 1988, 25(1), 47-67.
[http://dx.doi.org/10.1016/0306-4522(88)90006-1] [PMID: 3393286]
[33]
Lee, H.J.; Rye, D.B.; Hallanger, A.E.; Levey, A.I.; Wainer, B.H. Cholinergic vs. noncholinergic efferents from the mesopontine tegmentum to the extrapyramidal motor system nuclei. J. Comp. Neurol., 1988, 275(4), 469-492.
[http://dx.doi.org/10.1002/cne.902750402] [PMID: 2461392]
[34]
Skinner, R.D.; Garcia-Rill, E. The mesencephalic locomotor region (MLR) in the rat. Brain Res., 1984, 323(2), 385-389.
[http://dx.doi.org/10.1016/0006-8993(84)90319-6] [PMID: 6525525]
[35]
Peng, Y.; Schöneberg, N.; Esposito, M.S.; Geiger, J.R.P.; Sharott, A.; Tovote, P. Current approaches to characterize micro- and macroscale circuit mechanisms of Parkinson’s disease in rodent models. Exp. Neurol., 2022, 351(351), 114008.
[http://dx.doi.org/10.1016/j.expneurol.2022.114008] [PMID: 35149118]
[36]
Clements, J.R.; Grant, S. Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci. Lett., 1990, 120(1), 70-73.
[http://dx.doi.org/10.1016/0304-3940(90)90170-E] [PMID: 2293096]
[37]
Ford, B.; Holmes, C.J.; Mainville, L.; Jones, B.E. GABAergic neurons in the rat pontomesencephalic tegmentum: Codistribution with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J. Comp. Neurol., 1995, 363(2), 177-196.
[http://dx.doi.org/10.1002/cne.903630203] [PMID: 8642069]
[38]
Jones, B.E. Immunohistochemical study of choline acetyltransferase-immunoreactive processes and cells innervating the pontomedullary reticular formation in the rat. J. Comp. Neurol., 1990, 295(3), 485-514.
[http://dx.doi.org/10.1002/cne.902950311] [PMID: 2351765]
[39]
Martinez-Gonzalez, C.; Bolam, J.P.; Mena-Segovia, J. Topographical organization of the pedunculopontine nucleus. Front. Neuroanat., 2011, 5, 22.
[http://dx.doi.org/10.3389/fnana.2011.00022] [PMID: 21503154]
[40]
Wang, H.L.; Morales, M. Pedunculopontine and laterodorsal tegmental nuclei contain distinct populations of cholinergic, glutamatergic and GABAergic neurons in the rat. Eur. J. Neurosci., 2009, 29(2), 340-358.
[http://dx.doi.org/10.1111/j.1460-9568.2008.06576.x] [PMID: 19200238]
[41]
Sébille, S.B.; Rolland, A.S.; Faillot, M.; Perez-Garcia, F.; Colomb-Clerc, A.; Lau, B.; Dumas, S.; Vidal, S.F.; Welter, M.L.; Francois, C.; Bardinet, E.; Karachi, C. Normal and pathological neuronal distribution of the human mesencephalic locomotor region. Mov. Disord., 2019, 34(2), 218-227.
[http://dx.doi.org/10.1002/mds.27578] [PMID: 30485555]
[42]
Lee, A.M.; Hoy, J.L.; Bonci, A.; Wilbrecht, L.; Stryker, M.P.; Niell, C.M. Identification of a brainstem circuit regulating visual cortical state in parallel with locomotion. Neuron, 2014, 83(2), 455-466.
[http://dx.doi.org/10.1016/j.neuron.2014.06.031] [PMID: 25033185]
[43]
Capelli, P.; Pivetta, C.; Soledad Esposito, M.; Arber, S. Locomotor speed control circuits in the caudal brainstem. Nature, 2017, 551(7680), 373-377.
[http://dx.doi.org/10.1038/nature24064] [PMID: 29059682]
[44]
Josset, N.; Roussel, M.; Lemieux, M.; Lafrance-Zoubga, D.; Rastqar, A.; Bretzner, F. Distinct Contributions of Mesencephalic Locomotor Region Nuclei to Locomotor Control in the Freely Behaving Mouse. Curr. Biol., 2018, 28(6), 884-901.e3.
[http://dx.doi.org/10.1016/j.cub.2018.02.007] [PMID: 29526593]
[45]
Gut, N.K.; Yilmaz, D.; Kondabolu, K. Selective inhibition of goal-directed actions in the mesencephalic locomotor region. bioRxiv, 2022, 2022.01.18.476772.
[46]
van der Zouwen, C.I.; Boutin, J.; Fougère, M.; Flaive, A.; Vivancos, M.; Santuz, A.; Akay, T.; Sarret, P.; Ryczko, D. Freely Behaving Mice Can Brake and Turn During Optogenetic Stimulation of the Mesencephalic Locomotor Region. Front. Neural Circuits, 2021, 15, 639900.
[http://dx.doi.org/10.3389/fncir.2021.639900] [PMID: 33897379]
[47]
Carvalho, M.M.; Tanke, N.; Kropff, E.; Witter, M.P.; Moser, M.B.; Moser, E.I. A Brainstem Locomotor Circuit Drives the Activity of Speed Cells in the Medial Entorhinal Cortex. Cell Rep., 2020, 32(10), 108123.
[http://dx.doi.org/10.1016/j.celrep.2020.108123] [PMID: 32905779]
[48]
Masini, D.; Kiehn, O. Targeted activation of midbrain neurons restores locomotor function in mouse models of parkinsonism. Nat. Commun., 2022, 13(1), 504.
[http://dx.doi.org/10.1038/s41467-022-28075-4] [PMID: 35082287]
[49]
Wolff, S.B.E.; Ölveczky, B.P. The promise and perils of causal circuit manipulations. Curr. Opin. Neurobiol., 2018, 49, 84-94.
[http://dx.doi.org/10.1016/j.conb.2018.01.004] [PMID: 29414070]
[50]
Roš, H.; Magill, P.J.; Moss, J.; Bolam, J.P.; Mena-Segovia, J. Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience, 2010, 170(1), 78-91.
[http://dx.doi.org/10.1016/j.neuroscience.2010.06.068] [PMID: 20603194]
[51]
Boucetta, S.; Cissé, Y.; Mainville, L.; Morales, M.; Jones, B.E. Discharge profiles across the sleep-waking cycle of identified cholinergic, GABAergic, and glutamatergic neurons in the pontomesencephalic tegmentum of the rat. J. Neurosci., 2014, 34(13), 4708-4727.
[http://dx.doi.org/10.1523/JNEUROSCI.2617-13.2014] [PMID: 24672016]
[52]
Petzold, A.; Valencia, M.; Pál, B.; Mena-Segovia, J. Decoding brain state transitions in the pedunculopontine nucleus: cooperative phasic and tonic mechanisms. Front. Neural Circuits, 2015, 9, 68.
[http://dx.doi.org/10.3389/fncir.2015.00068] [PMID: 26582977]
[53]
Martinez-Gonzalez, C.; Wang, H.L.; Micklem, B.R.; Bolam, J.P.; Mena-Segovia, J. Subpopulations of cholinergic, GABAergic and glutamatergic neurons in the pedunculopontine nucleus contain calcium-binding proteins and are heterogeneously distributed. Eur. J. Neurosci., 2012, 35(5), 723-734.
[http://dx.doi.org/10.1111/j.1460-9568.2012.08002.x] [PMID: 22356461]
[54]
Martinez-Gonzalez, C.; van Andel, J.; Bolam, J.P.; Mena-Segovia, J. Divergent motor projections from the pedunculopontine nucleus are differentially regulated in Parkinsonism. Brain Struct. Funct., 2013, 219(4), 1451-1462.
[http://dx.doi.org/10.1007/s00429-013-0579-6] [PMID: 23708060]
[55]
Mena-Segovia, J. Structural and functional considerations of the cholinergic brainstem. J. Neural Transm., 2016, 123(7), 731-736.
[http://dx.doi.org/10.1007/s00702-016-1530-9]
[56]
Mena-Segovia, J.; Sims, H.M.; Magill, P.J.; Bolam, J.P. Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J. Physiol., 2008, 586(12), 2947-2960.
[http://dx.doi.org/10.1113/jphysiol.2008.153874] [PMID: 18440991]
[57]
Mena-Segovia, J.; Micklem, B.R.; Nair-Roberts, R.G.; Ungless, M.A.; Bolam, J.P. GABAergic neuron distribution in the pedunculopontine nucleus defines functional subterritories. J. Comp. Neurol., 2009, 515(4), 397-408.
[http://dx.doi.org/10.1002/cne.22065] [PMID: 19459217]
[58]
Brown, R.E.; Basheer, R.; McKenna, J.T.; Strecker, R.E.; McCarley, R.W. Control of sleep and wakefulness. Physiol. Rev., 2012, 92(3), 1087-1187.
[http://dx.doi.org/10.1152/physrev.00032.2011] [PMID: 22811426]
[59]
Fuller, P.M.; Saper, C.B.; Lu, J. The pontine REM switch: past and present. J. Physiol., 2007, 584(3), 735-741.
[http://dx.doi.org/10.1113/jphysiol.2007.140160] [PMID: 17884926]
[60]
Garcia-Rill, E.; Kezunovic, N.; Hyde, J.; Simon, C.; Beck, P.; Urbano, F.J. Coherence and frequency in the reticular activating system (RAS). Sleep Med Rev, 2013, 17(3), 227-38.
[http://dx.doi.org/10.1016/j.smrv.2012.06.002]
[61]
Jones, B.E. Arousal and sleep circuits. Neuropsychopharmacology, 2020, 45(1), 6-20.
[http://dx.doi.org/10.1038/s41386-019-0444-2]
[62]
Van Dort, C.J.; Zachs, D.P.; Kenny, J.D.; Zheng, S.; Goldblum, R.R.; Gelwan, N.A.; Ramos, D.M.; Nolan, M.A.; Wang, K.; Weng, F.J.; Lin, Y.; Wilson, M.A.; Brown, E.N. Optogenetic activation of cholinergic neurons in the PPT or LDT induces REM sleep. Proc. Natl. Acad. Sci. USA, 2015, 112(2), 584-589.
[http://dx.doi.org/10.1073/pnas.1423136112] [PMID: 25548191]
[63]
Pernía-Andrade, A.J.; Wenger, N.; Esposito, M.S.; Tovote, P. Circuits for State-Dependent Modulation of Locomotion. Front. Hum. Neurosci., 2021, 15, 745689.
[http://dx.doi.org/10.3389/fnhum.2021.745689] [PMID: 34858153]
[64]
Keating, G.L.; Winn, P. Examination of the role of the pedunculopontine tegmental nucleus in radial maze tasks with or without a delay. Neuroscience, 2002, 112(3), 687-696.
[http://dx.doi.org/10.1016/S0306-4522(02)00108-2] [PMID: 12074910]
[65]
Alderson, H.L.; Latimer, M.P.; Blaha, C.D.; Phillips, A.G.; Winn, P. An examination of d-amphetamine self-administration in pedunculopontine tegmental nucleus-lesioned rats. Neuroscience, 2004, 125(2), 349-358.
[http://dx.doi.org/10.1016/j.neuroscience.2004.02.015] [PMID: 15062978]
[66]
Wilson, D.I.G.; MacLaren, D.A.A.; Winn, P. Bar pressing for food: differential consequences of lesions to the anterior versus posterior pedunculopontine. Eur. J. Neurosci., 2009, 30(3), 504-513.
[http://dx.doi.org/10.1111/j.1460-9568.2009.06836.x] [PMID: 19614747]
[67]
MacLaren, D.A.A.; Wilson, D.I.G.; Winn, P. Updating of action-outcome associations is prevented by inactivation of the posterior pedunculopontine tegmental nucleus. Neurobiol. Learn. Mem., 2013, 102, 28-33.
[http://dx.doi.org/10.1016/j.nlm.2013.03.002] [PMID: 23567109]
[68]
Okada, K.; Toyama, K.; Inoue, Y.; Isa, T.; Kobayashi, Y. Different pedunculopontine tegmental neurons signal predicted and actual task rewards. J. Neurosci., 2009, 29(15), 4858-4870.
[http://dx.doi.org/10.1523/JNEUROSCI.4415-08.2009] [PMID: 19369554]
[69]
Hong, S.; Hikosaka, O. Pedunculopontine tegmental nucleus neurons provide reward, sensorimotor, and alerting signals to midbrain dopamine neurons. Neuroscience, 2014, 282, 139-155.
[http://dx.doi.org/10.1016/j.neuroscience.2014.07.002] [PMID: 25058502]
[70]
Norton, A.B.W.; Jo, Y.S.; Clark, E.W.; Taylor, C.A.; Mizumori, S.J.Y. Independent neural coding of reward and movement by pedunculopontine tegmental nucleus neurons in freely navigating rats. Eur. J. Neurosci., 2011, 33(10), 1885-1896.
[http://dx.doi.org/10.1111/j.1460-9568.2011.07649.x] [PMID: 21395868]
[71]
Thompson, J.A.; Felsen, G. Activity in mouse pedunculopontine tegmental nucleus reflects action and outcome in a decision-making task. J. Neurophysiol., 2013, 110(12), 2817-2829.
[http://dx.doi.org/10.1152/jn.00464.2013] [PMID: 24089397]
[72]
Thompson, J.A.; Costabile, J.D.; Felsen, G. Mesencephalic representations of recent experience influence decision making. eLife, 2016, 5, e16572.
[http://dx.doi.org/10.7554/eLife.16572] [PMID: 27454033]
[73]
Ruan, Y.; Li, K.Y.; Zheng, R.; Yan, Y.Q.; Wang, Z.X.; Chen, Y.; Liu, Y.; Tian, J.; Zhu, L.Y.; Lou, H.F.; Yu, Y.Q.; Pu, J.L.; Zhang, B.R. Cholinergic neurons in the pedunculopontine nucleus guide reversal learning by signaling the changing reward contingency. Cell Rep., 2022, 38(9), 110437.
[http://dx.doi.org/10.1016/j.celrep.2022.110437] [PMID: 35235804]
[74]
Inagaki, H.K.; Chen, S.; Ridder, M.C.; Sah, P.; Li, N.; Yang, Z.; Hasanbegovic, H.; Gao, Z.; Gerfen, C.R.; Svoboda, K. A midbrain-thalamus-cortex circuit reorganizes cortical dynamics to initiate movement. Cell, 2022, 185(6), 1065-1081.e23.
[http://dx.doi.org/10.1016/j.cell.2022.02.006] [PMID: 35245431]
[75]
Alexander, G.E.; Crutcher, M.D. Functional Architectures of Basal Ganglia Circuits. Trends Neurosci., 1990, 13(7), 266-271.
[http://dx.doi.org/10.1016/0166-2236(90)90107-L] [PMID: 1695401]
[76]
Gerfen, C.R.; Surmeier, D.J. Modulation of striatal projection systems by dopamine. Annu. Rev. Neurosci., 2011, 34(1), 441-466.
[http://dx.doi.org/10.1146/annurev-neuro-061010-113641] [PMID: 21469956]
[77]
Klaus, A.; Alves da Silva, J.; Costa, R.M. What, If, and When to Move: Basal Ganglia Circuits and Self-Paced Action Initiation. Annu. Rev. Neurosci., 2019, 42(1), 459-483.
[http://dx.doi.org/10.1146/annurev-neuro-072116-031033] [PMID: 31018098]
[78]
Alexander, G.E.; DeLong, M.R.; Strick, P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci., 1986, 9(1), 357-381.
[http://dx.doi.org/10.1146/annurev.ne.09.030186.002041] [PMID: 3085570]
[79]
Kemp, J.M.; Powell, T.P. The structure of the caudate nucleus of the cat: light and electron microscopy. Philos. Trans. R. Soc. Lond. B Biol. Sci., 1971, 262(845), 383-401.
[http://dx.doi.org/10.1098/rstb.1971.0102] [PMID: 4107495]
[80]
McElvain, L.E.; Chen, Y.; Moore, J.D.; Brigidi, G.S.; Bloodgood, B.L.; Lim, B.K.; Costa, R.M.; Kleinfeld, D. Specific populations of basal ganglia output neurons target distinct brain stem areas while collateralizing throughout the diencephalon. Neuron, 2021, 109(10), 1721-1738.e4.
[http://dx.doi.org/10.1016/j.neuron.2021.03.017] [PMID: 33823137]
[81]
Rommelfanger, K.S.; Wichmann, T. Extrastriatal dopaminergic circuits of the basal ganglia. Front. Neuroanat., 2010, 4, 139.
[http://dx.doi.org/10.3389/fnana.2010.00139] [PMID: 21103009]
[82]
Gerfen, C.R.; Wilson, C.J. Chapter II The Basal Ganglia. In: Handbook of Chemical Neuroanatomy; , 1996; 12, pp. 371-468.
[http://dx.doi.org/10.1016/S0924-8196(96)80004-2]
[83]
Assous, M.; Tepper, J.M. Excitatory extrinsic afferents to striatal interneurons and interactions with striatal microcircuitry. Eur. J. Neurosci., 2019, 49(5), 593-603.
[http://dx.doi.org/10.1111/ejn.13881] [PMID: 29480942]
[84]
Graybiel, A.M. Habits, rituals, and the evaluative brain. Annu. Rev. Neurosci., 2008, 31(1), 359-387.
[http://dx.doi.org/10.1146/annurev.neuro.29.051605.112851] [PMID: 18558860]
[85]
Hintiryan, H.; Foster, N.N.; Bowman, I.; Bay, M.; Song, M.Y.; Gou, L.; Yamashita, S.; Bienkowski, M.S.; Zingg, B.; Zhu, M.; Yang, X.W.; Shih, J.C.; Toga, A.W.; Dong, H.W. The mouse cortico-striatal projectome. Nat. Neurosci., 2016, 19(8), 1100-1114.
[http://dx.doi.org/10.1038/nn.4332] [PMID: 27322419]
[86]
Klug, J.R.; Engelhardt, M.D.; Cadman, C.N.; Li, H.; Smith, J.B.; Ayala, S.; Williams, E.W.; Hoffman, H.; Jin, X. Differential inputs to striatal cholinergic and parvalbumin interneurons imply functional distinctions. eLife, 2018, 7, e35657.
[http://dx.doi.org/10.7554/eLife.35657] [PMID: 29714166]
[87]
Morgenstern, N.A.; Isidro, A.F.; Israely, I.; Costa, R.M. Pyramidal tract neurons drive amplification of excitatory inputs to striatum through cholinergic interneurons. Sci. Adv., 2022, 8(6), eabh4315.
[http://dx.doi.org/10.1126/sciadv.abh4315] [PMID: 35138902]
[88]
Tanimura, A.; Du, Y.; Kondapalli, J.; Wokosin, D.L.; Surmeier, D.J. Cholinergic interneurons amplify thalamostriatal excitation of striatal indirect pathway neurons in Parkinson’s disease models. Neuron, 2019, 101(3), 444-458.e6.
[http://dx.doi.org/10.1016/j.neuron.2018.12.004] [PMID: 30658860]
[89]
Threlfell, S.; Lalic, T.; Platt, N.J.; Jennings, K.A.; Deisseroth, K.; Cragg, S.J. Striatal dopamine release is triggered by synchronized activity in cholinergic interneurons. Neuron, 2012, 75(1), 58-64.
[http://dx.doi.org/10.1016/j.neuron.2012.04.038] [PMID: 22794260]
[90]
Jin, X.; Costa, R.M. Start/stop signals emerge in nigrostriatal circuits during sequence learning. Nature, 2010, 466(7305), 457-462.
[http://dx.doi.org/10.1038/nature09263] [PMID: 20651684]
[91]
Freeze, B.S.; Kravitz, A.V.; Hammack, N.; Berke, J.D.; Kreitzer, A.C. Control of basal ganglia output by direct and indirect pathway projection neurons. J. Neurosci., 2013, 33(47), 18531-18539.
[http://dx.doi.org/10.1523/JNEUROSCI.1278-13.2013] [PMID: 24259575]
[92]
Graybiel, A.M.; Aosaki, T.; Flaherty, A.W.; Kimura, M. The basal ganglia and adaptive motor control. Science, 1994, 265(5180), 1826-1831.
[http://dx.doi.org/10.1126/science.8091209]
[93]
Yin, H.H.; Knowlton, B.J. The role of the basal ganglia in habit formation. Nat. Rev. Neurosci., 2006, 7(6), 464-476.
[http://dx.doi.org/10.1038/nrn1919] [PMID: 16715055]
[94]
Zhai, S.; Shen, W.; Graves, S.M.; Surmeier, D.J. Dopaminergic modulation of striatal function and Parkinson’s disease. J. Neural Transm., 2019, 126(4), 411-422.
[http://dx.doi.org/10.1007/s00702-019-01997-y]
[95]
Wang, Z.; Kai, L.; Day, M.; Ronesi, J.; Yin, H.H.; Ding, J.; Tkatch, T.; Lovinger, D.M.; Surmeier, D.J. Dopaminergic control of corticostriatal long-term synaptic depression in medium spiny neurons is mediated by cholinergic interneurons. Neuron, 2006, 50(3), 443-452.
[http://dx.doi.org/10.1016/j.neuron.2006.04.010] [PMID: 16675398]
[96]
Lerner, T.N.; Shilyansky, C.; Davidson, T.J.; Evans, K.E.; Beier, K.T.; Zalocusky, K.A.; Crow, A.K.; Malenka, R.C.; Luo, L.; Tomer, R.; Deisseroth, K. Intact-brain analyses reveal distinct information carried by SNc dopamine subcircuits. Cell, 2015, 162(3), 635-647.
[http://dx.doi.org/10.1016/j.cell.2015.07.014] [PMID: 26232229]
[97]
Matsumoto, M.; Hikosaka, O. Two types of dopamine neuron distinctly convey positive and negative motivational signals. Nature, 2009, 459(7248), 837-841.
[http://dx.doi.org/10.1038/nature08028] [PMID: 19448610]
[98]
Panigrahi, B.; Martin, K.A.; Li, Y.; Graves, A.R.; Vollmer, A.; Olson, L.; Mensh, B.D.; Karpova, A.Y.; Dudman, J.T. Dopamine is required for the neural representation and control of movement vigor. Cell, 2015, 162(6), 1418-1430.
[http://dx.doi.org/10.1016/j.cell.2015.08.014] [PMID: 26359992]
[99]
Howe, M.W.; Dombeck, D.A. Rapid signalling in distinct dopaminergic axons during locomotion and reward. Nature, 2016, 535(7613), 505-510.
[http://dx.doi.org/10.1038/nature18942] [PMID: 27398617]
[100]
da Silva, J.A.; Tecuapetla, F.; Paixão, V.; Costa, R.M. Dopamine neuron activity before action initiation gates and invigorates future movements. Nature, 2018, 554(7691), 244-248.
[http://dx.doi.org/10.1038/nature25457] [PMID: 29420469]
[101]
Parker, N.F.; Cameron, C.M.; Taliaferro, J.P.; Lee, J.; Choi, J.Y.; Davidson, T.J.; Daw, N.D.; Witten, I.B. Reward and choice encoding in terminals of midbrain dopamine neurons depends on striatal target. Nat. Neurosci., 2016, 19(6), 845-854.
[http://dx.doi.org/10.1038/nn.4287] [PMID: 27110917]
[102]
Hernández-López, S.; Góngora-Alfaro, J.; Martínez-Fong, D.; Aceves, J. A cholinergic input to the substantia nigra pars compacta increases striatal dopamine metabolism measured by in vivo voltammetry. Brain Res., 1992, 598(1-2), 114-120.
[http://dx.doi.org/10.1016/0006-8993(92)90174-8] [PMID: 1486473]
[103]
Futami, T.; Takakusaki, K.; Kitai, S.T. Glutamatergic and cholinergic inputs from the pedunculopontine tegmental nucleus to dopamine neurons in the substantia nigra pars compacta. Neurosci. Res., 1995, 21(4), 331-342.
[http://dx.doi.org/10.1016/0168-0102(94)00869-H] [PMID: 7777224]
[104]
Scarnati, E.; Campana, E.; Pacitti, C. Pedunculopontine-evoked excitation of substantia nigra neurons in the rat. Brain Res., 1984, 304(2), 351-361.
[http://dx.doi.org/10.1016/0006-8993(84)90339-1] [PMID: 6744046]
[105]
Scarnati, E.; Proia, A.; Campana, E.; Pacitti, C. A microiontophoretic study on the nature of the putative synaptic neurotransmitter involved in the pedunculopontine-substantia nigra pars compacta excitatory pathway of the rat. Exp. Brain Res., 1986, 62(3), 470-478.
[http://dx.doi.org/10.1007/BF00236025] [PMID: 2873047]
[106]
Bolam, J.P.; Francis, C.M.; Henderson, Z. Cholinergic input to dopaminergic neurons in the substantia nigra: A double immunocytochemical study. Neuroscience, 1991, 41(2-3), 483-494.
[http://dx.doi.org/10.1016/0306-4522(91)90343-M] [PMID: 1678502]
[107]
Matsubayashi, H.; Amano, T.; Seki, T.; Sasa, M.; Sakai, N. Electrophysiological characterization of nicotine-induced excitation of dopaminergic neurons in the rat substantia nigra. J. Pharmacol. Sci., 2003, 93(2), 143-148.
[http://dx.doi.org/10.1254/jphs.93.143] [PMID: 14578581]
[108]
Watabe-Uchida, M.; Zhu, L.; Ogawa, S.K.; Vamanrao, A.; Uchida, N. Whole-brain mapping of direct inputs to midbrain dopamine neurons. Neuron, 2012, 74(5), 858-873.
[http://dx.doi.org/10.1016/j.neuron.2012.03.017] [PMID: 22681690]
[109]
Pan, W.X.; Hyland, B.I. Pedunculopontine tegmental nucleus controls conditioned responses of midbrain dopamine neurons in behaving rats. J. Neurosci., 2005, 25(19), 4725-4732.
[http://dx.doi.org/10.1523/JNEUROSCI.0277-05.2005] [PMID: 15888648]
[110]
Hassan, A.; Benarroch, E.E. Heterogeneity of the midbrain dopamine system. Neurology, 2015, 85(20), 1795-1805.
[http://dx.doi.org/10.1212/WNL.0000000000002137] [PMID: 26475693]
[111]
Di Loreto, S.; Florio, T.; Scarnati, E. Evidence that non-NMDA receptors are involved in the excitatory pathway from the pedunculopontine region to nigrostriatal dopaminergic neurons. Exp. Brain Res., 1992, 89(1), 79-86.
[http://dx.doi.org/10.1007/BF00229003] [PMID: 1351000]
[112]
Galtieri, D.J.; Estep, C.M.; Wokosin, D.L.; Traynelis, S.; Surmeier, D.J. Pedunculopontine glutamatergic neurons control spike patterning in substantia nigra dopaminergic neurons. eLife, 2017, 6, e30352.
[http://dx.doi.org/10.7554/eLife.30352] [PMID: 28980939]
[113]
Rolland, A.S.; Tandé, D.; Herrero, M.T.; Luquin, M.R.; Vazquez-Claverie, M.; Karachi, C.; Hirsch, E.C.; François, C. Evidence for a dopaminergic innervation of the pedunculopontine nucleus in monkeys, and its drastic reduction after MPTP intoxication. J. Neurochem., 2009, 110(4), 1321-1329.
[http://dx.doi.org/10.1111/j.1471-4159.2009.06220.x] [PMID: 19527435]
[114]
Ryczko, D.; Cone, J.J.; Alpert, M.H.; Goetz, L.; Auclair, F.; Dubé, C.; Parent, M.; Roitman, M.F.; Alford, S.; Dubuc, R. A descending dopamine pathway conserved from basal vertebrates to mammals. Proc. Natl. Acad. Sci. USA, 2016, 113(17), E2440-E2449.
[http://dx.doi.org/10.1073/pnas.1600684113] [PMID: 27071118]
[115]
Bevan, M.D.; Bolam, J.P. Cholinergic, GABAergic, and glutamate-enriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J. Neurosci., 1995, 15(11), 7105-7120.
[http://dx.doi.org/10.1523/JNEUROSCI.15-11-07105.1995] [PMID: 7472465]
[116]
Kita, T.; Kita, H. Cholinergic and non-cholinergic mesopontine tegmental neurons projecting to the subthalamic nucleus in the rat. Eur. J. Neurosci., 2011, 33(3), 433-443.
[http://dx.doi.org/10.1111/j.1460-9568.2010.07537.x] [PMID: 21198985]
[117]
Hammond, C.; Rouzaire-Dubois, B.; Féger, J.; Jackson, A.; Crossman, A.R. Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat. Neuroscience, 1983, 9(1), 41-52.
[http://dx.doi.org/10.1016/0306-4522(83)90045-3] [PMID: 6308507]
[118]
Esposito, M.S.; Capelli, P.; Arber, S. Brainstem nucleus MdV mediates skilled forelimb motor tasks. Nature, 2014, 508(7496), 351-356.
[http://dx.doi.org/10.1038/nature13023] [PMID: 24487621]
[119]
Bouvier, J.; Caggiano, V.; Leiras, R.; Caldeira, V.; Bellardita, C.; Balueva, K.; Fuchs, A.; Kiehn, O. Descending command neurons in the brainstem that halt locomotion. Cell, 2015, 163(5), 1191-1203.
[http://dx.doi.org/10.1016/j.cell.2015.10.074] [PMID: 26590422]
[120]
Cregg, J.M.; Leiras, R.; Montalant, A.; Wanken, P.; Wickersham, I.R.; Kiehn, O. Brainstem neurons that command mammalian locomotor asymmetries. Nat. Neurosci., 2020, 23(6), 730-740.
[http://dx.doi.org/10.1038/s41593-020-0633-7] [PMID: 32393896]
[121]
Ruder, L.; Schina, R.; Kanodia, H.; Valencia-Garcia, S.; Pivetta, C.; Arber, S. A functional map for diverse forelimb actions within brainstem circuitry. Nature, 2021, 590(7846), 445-450.
[http://dx.doi.org/10.1038/s41586-020-03080-z] [PMID: 33408409]
[122]
Usseglio, G.; Gatier, E.; Heuzé, A.; Hérent, C.; Bouvier, J. Control of orienting movements and locomotion by projection-defined subsets of brainstem V2a neurons. Curr. Biol., 2020, 30(23), 4665-4681.e6.
[http://dx.doi.org/10.1016/j.cub.2020.09.014] [PMID: 33007251]
[123]
Hou, X.H.; Hyun, M.; Taranda, J.; Huang, K.W.; Todd, E.; Feng, D.; Atwater, E.; Croney, D.; Zeidel, M.L.; Osten, P.; Sabatini, B.L. Central control circuit for context-dependent micturition. Cell, 2016, 167(1), 73-86.e12.
[http://dx.doi.org/10.1016/j.cell.2016.08.073] [PMID: 27662084]
[124]
Crapse, T.B.; Sommer, M.A. Corollary discharge across the animal kingdom. Nat. Rev. Neurosci., 2008, 9(8), 587-600.
[http://dx.doi.org/10.1038/nrn2457] [PMID: 18641666]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy