Recent advances in understanding the role of the basal ganglia

Kristina Simonyan, Kristina Simonyan

Abstract

The basal ganglia are a complex subcortical structure that is principally involved in the selection and implementation of purposeful actions in response to external and internal cues. The basal ganglia set the pattern for facilitation of voluntary movements and simultaneous inhibition of competing or interfering movements. In addition, the basal ganglia are involved in the control of a wide variety of non-motor behaviors, spanning emotions, language, decision making, procedural learning, and working memory. This review presents a comparative overview of classic and contemporary models of basal ganglia organization and functional importance, including their increased integration with cortical and cerebellar structures.

Keywords: basal ganglia; extrinsic network; intrinsic network; somatotopy.

Conflict of interest statement

No competing interests were disclosed.No competing interests were disclosed.No competing interests were disclosed.

Figures

Figure 1.
Figure 1.
Schematic representation of basal ganglia intrinsic and extrinsic connectivity according to (A) the classical model and (B) the contemporary model. Modified and adapted with permission from Simonyanet al. .
Figure 2.
Figure 2.
Somatotopical representations within the motor cortex, basal ganglia, and thalamus (A) Lateral and medial view of the monkey brain showing the somatotopic representation of body regions. Light-gray shading indicates primary motor cortex, and dark-gray shading indicates premotor cortex. Adapted with permission from Fadigaet al. . (B, C) Dorsoventral views of the basal ganglia subdivisions (B) (putamen, external segment of the globus pallidus [GPe], internal segment of the globus pallidus [GPi], substantia nigra pars reticulata [SNr], and substantia nigra pars compacta [SNc]) and thalamus (C) depicting somatotopic body representations. Adapted with permission from Nambu .
Figure 3.. Schematic representation of major basal…
Figure 3.. Schematic representation of major basal ganglia loops: the motor, associative, and limbic.
The representation is organized according to (A) the parallel-projecting hypothesis – and (B) information convergence across the loops. Adapted from Percheron and Filion .

References

    1. Redgrave P, Prescott TJ, Gurney K: The basal ganglia: a vertebrate solution to the selection problem? Neuroscience. 1999;89(4):1009–23. 10.1016/S0306-4522(98)00319-4
    1. Mink JW: The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol. 1996;50(4):381–425. 10.1016/S0301-0082(96)00042-1
    1. Albin RL, Young AB, Penney JB: The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989;12(10):366–75. 10.1016/0166-2236(89)90074-X
    1. Wu Y, Richard S, Parent A: The organization of the striatal output system: a single-cell juxtacellular labeling study in the rat. Neurosci Res. 2000;38(1):49–62. 10.1016/S0168-0102(00)00140-1
    1. Matamales M, Bertran-Gonzalez J, Salomon L, et al. : Striatal medium-sized spiny neurons: identification by nuclear staining and study of neuronal subpopulations in BAC transgenic mice. PLoS One. 2009;4(3):e4770. 10.1371/journal.pone.0004770
    1. Cazorla M, de Carvalho FD, Chohan MO, et al. : Dopamine D2 receptors regulate the anatomical and functional balance of basal ganglia circuitry. Neuron. 2014;81(1):153–64. 10.1016/j.neuron.2013.10.041

    2. F1000 Recommendation

    1. Simonyan K, Cho H, Hamzehei Sichani A, et al. : The direct basal ganglia pathway is hyperfunctional in focal dystonia. Brain. 2017;140(12):3179–90. 10.1093/brain/awx263

    2. F1000 Recommendation

    1. Nambu A, Tokuno H, Takada M: Functional significance of the cortico-subthalamo-pallidal 'hyperdirect' pathway. Neurosci Res. 2002;43(2):111–7. 10.1016/S0168-0102(02)00027-5
    1. Coizet V, Graham JH, Moss J, et al. : Short-latency visual input to the subthalamic nucleus is provided by the midbrain superior colliculus. J Neurosci. 2009;29(17):5701–9. 10.1523/JNEUROSCI.0247-09.2009
    1. Lanciego JL, Gonzalo N, Castle M, et al. : Thalamic innervation of striatal and subthalamic neurons projecting to the rat entopeduncular nucleus. Eur J Neurosci. 2004;19(5):1267–77. 10.1111/j.1460-9568.2004.03244.x
    1. Smith Y, Bevan MD, Shink E, et al. : Microcircuitry of the direct and indirect pathways of the basal ganglia. Neuroscience. 1998;86(2):353–87. 10.1016/S0306-4522(98)00004-9
    1. Kita H, Tokuno H, Nambu A: Monkey globus pallidus external segment neurons projecting to the neostriatum. Neuroreport. 1999;10(7):1467–72. 10.1097/00001756-199905140-00014
    1. Mallet N, Micklem BR, Henny P, et al. : Dichotomous organization of the external globus pallidus. Neuron. 2012;74(6):1075–86. 10.1016/j.neuron.2012.04.027

    2. F1000 Recommendation

    1. Mastro KJ, Bouchard RS, Holt HA, et al. : Transgenic mouse lines subdivide external segment of the globus pallidus (GPe) neurons and reveal distinct GPe output pathways. J Neurosci. 2014;34(6):2087–99. 10.1523/JNEUROSCI.4646-13.2014

    2. F1000 Recommendation

    1. Gittis AH, Berke JD, Bevan MD, et al. : New roles for the external globus pallidus in basal ganglia circuits and behavior. J Neurosci. 2014;34(46):15178–83. 10.1523/JNEUROSCI.3252-14.2014

    2. F1000 Recommendation

    1. Grabli D, McCairn K, Hirsch EC, et al. : Behavioural disorders induced by external globus pallidus dysfunction in primates: I. Behavioural study. Brain. 2004;127(Pt 9):2039–54. 10.1093/brain/awh220
    1. François C, Grabli D, McCairn K, et al. : Behavioural disorders induced by external globus pallidus dysfunction in primates II. Anatomical study. Brain. 2004;127(Pt 9):2055–70. 10.1093/brain/awh239
    1. Betarbet R, Turner R, Chockkan V, et al. : Dopaminergic neurons intrinsic to the primate striatum. J Neurosci. 1997;17(17):6761–8. 10.1523/JNEUROSCI.17-17-06761.1997
    1. Cossette M, Lecomte F, Parent A: Morphology and distribution of dopaminergic neurons intrinsic to the human striatum. J Chem Neuroanat. 2005;29(1):1–11. 10.1016/j.jchemneu.2004.08.007
    1. Lévesque M, Bédard A, Cossette M, et al. : Novel aspects of the chemical anatomy of the striatum and its efferents projections. J Chem Neuroanat. 2003;26(4):271–81. 10.1016/j.jchemneu.2003.07.001
    1. Xenias HS, Ibáñez-Sandoval O, Koós T, et al. : Are striatal tyrosine hydroxylase interneurons dopaminergic? J Neurosci. 2015;35(16):6584–99. 10.1523/JNEUROSCI.0195-15.2015

    2. F1000 Recommendation

    1. Künzle H: Bilateral projections from precentral motor cortex to the putamen and other parts of the basal ganglia. An autoradiographic study in Macaca fascicularis. Brain Res. 1975;88(2):195–209. 10.1016/0006-8993(75)90384-4
    1. Simonyan K, Jürgens U: Efferent subcortical projections of the laryngeal motorcortex in the rhesus monkey. Brain Res. 2003;974(1–2):43–59. 10.1016/S0006-8993(03)02548-4
    1. Gerardin E, Lehéricy S, Pochon JB, et al. : Foot, hand, face and eye representation in the human striatum. Cereb Cortex. 2003;13(2):162–9. 10.1093/cercor/13.2.162
    1. Maillard L, Ishii K, Bushara K, et al. : Mapping the basal ganglia: fMRI evidence for somatotopic representation of face, hand, and foot. Neurology. 2000;55(3):377–83. 10.1212/WNL.55.3.377
    1. Romanelli P, Esposito V, Schaal DW, et al. : Somatotopy in the basal ganglia: experimental and clinical evidence for segregated sensorimotor channels. Brain Res Brain Res Rev. 2005;48(1):112–28. 10.1016/j.brainresrev.2004.09.008
    1. Nambu A, Kaneda K, Tokuno H, et al. : Organization of corticostriatal motor inputs in monkey putamen. J Neurophysiol. 2002;88(4):1830–42. 10.1152/jn.2002.88.4.1830
    1. Nambu A: Somatotopic organization of the primate Basal Ganglia. Front Neuroanat. 2011;5:26. 10.3389/fnana.2011.00026
    1. DeLong MR, Crutcher MD, Georgopoulos AP: Relations between movement and single cell discharge in the substantia nigra of the behaving monkey. J Neurosci. 1983;3(8):1599–606. 10.1523/JNEUROSCI.03-08-01599.1983
    1. Kitano H, Tanibuchi I, Jinnai K: The distribution of neurons in the substantia nigra pars reticulata with input from the motor, premotor and prefrontal areas of the cerebral cortex in monkeys. Brain Res. 1998;784(1–2):228–38. 10.1016/S0006-8993(97)01332-2
    1. Smith Y, Parent A: Differential connections of caudate nucleus and putamen in the squirrel monkey ( Saimiri sciureus). Neuroscience. 1986;18(2):347–71. 10.1016/0306-4522(86)90159-4
    1. Haber SN, Lynd E, Klein C, et al. : Topographic organization of the ventral striatal efferent projections in the rhesus monkey: an anterograde tracing study. J Comp Neurol. 1990;293(2):282–98. 10.1002/cne.902930210
    1. Carpenter MB, Peter P: Nigrostriatal and nigrothalamic fibers in the rhesus monkey. J Comp Neurol. 1972;144(1):93–115. 10.1002/cne.901440105
    1. Childs JA, Gale K: Neurochemical evidence for a nigrotegmental GAbAergic projection. Brain Res. 1983;258(1):109–14. 10.1016/0006-8993(83)91233-7
    1. Thörner G, Lange H, Hopf A: [Morphometrical-statistical structure analysis of human striatum, pallidus and subthalamic nucleus. II. Globus pallidus]. J Hirnforsch. 1975;16(5):401–13.
    1. Ungerstedt U: Stereotaxic mapping of the monoamine pathways in the rat brain. Acta Physiol Scand Suppl. 1971;367:1–48. 10.1111/j.1365-201X.1971.tb10998.x
    1. Haber SN, Fudge JL, McFarland NR: Striatonigrostriatal pathways in primates form an ascending spiral from the shell to the dorsolateral striatum. J Neurosci. 2000;20(6):2369–82. 10.1523/JNEUROSCI.20-06-02369.2000
    1. Lynd-Balta E, Haber SN: The organization of midbrain projections to the striatum in the primate: sensorimotor-related striatum versus ventral striatum. Neuroscience. 1994;59(3):625–40. 10.1016/0306-4522(94)90182-1
    1. Hedreen JC, Struble RG, Whitehouse PJ, et al. : Topography of the magnocellular basal forebrain system in human brain. J Neuropathol Exp Neurol. 1984;43(1):1–21. 10.1097/00005072-198401000-00001
    1. Wassef M, Berod A, Sotelo C: Dopaminergic dendrites in the pars reticulata of the rat substantia nigra and their striatal input. Combined immunocytochemical localization of tyrosine hydroxylase and anterograde degeneration. Neuroscience. 1981;6(11):2125–39. 10.1016/0306-4522(81)90003-8
    1. Lynd-Balta E, Haber SN: Primate striatonigral projections: a comparison of the sensorimotor-related striatum and the ventral striatum. J Comp Neurol. 1994;345(4):562–78. 10.1002/cne.903450407
    1. Somogyi P, Bolam JP, Smith AD: 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. 1981;195(4):567–84. 10.1002/cne.901950403
    1. Franois C, Yelnik J, Tand D, et al. : Dopaminergic cell group A8 in the monkey: anatomical organization and projections to the striatum. J Comp Neurol. 1999;414(3):334–47. 10.1002/(SICI)1096-9861(19991122)414:3<334::AID-CNE4>;2-X
    1. Joel D, Niv Y, Ruppin E: Actor-critic models of the basal ganglia: new anatomical and computational perspectives. Neural Netw. 2002;15(4–6):535–47. 10.1016/S0893-6080(02)00047-3
    1. McGeorge AJ, Faull RL: The organization of the projection from the cerebral cortex to the striatum in the rat. Neuroscience. 1989;29(3):503–37. 10.1016/0306-4522(89)90128-0
    1. Rock C, Zurita H, Wilson C, et al. : An inhibitory corticostriatal pathway. eLife. 2016;5: pii: e15890. 10.7554/eLife.15890

    2. F1000 Recommendation

    1. Melzer S, Gil M, Koser DE, et al. : Distinct Corticostriatal GABAergic Neurons Modulate Striatal Output Neurons and Motor Activity. Cell Rep. 2017;19(5):1045–55. 10.1016/j.celrep.2017.04.024

    2. F1000 Recommendation

    1. Saunders A, Oldenburg IA, Berezovskii VK, et al. : A direct GABAergic output from the basal ganglia to frontal cortex. Nature. 2015;521(7550):85–9. 10.1038/nature14179

    2. F1000 Recommendation

    1. Fadiga L, Fogassi, L, Gallese, V, et al. : Visuomotor neurons: ambiguity of the discharge or 'motor' perception? Int J Psychophysiol. 2000;35(2–3):165–77. 10.1016/S0167-8760(99)00051-3
    1. Allen GI, Tsukahara N: Cerebrocerebellar communication systems. Physiol Rev. 1974;54(4):957–1006. 10.1152/physrev.1974.54.4.957
    1. Allen GI, Gilbert PF, Yin TC: Convergence of cerebral inputs onto dentate neurons in monkey. Exp Brain Res. 1978;32(2):151–70. 10.1007/BF00239724
    1. Asanuma C, Thach WT, Jones EG: Distribution of cerebellar terminations and their relation to other afferent terminations in the ventral lateral thalamic region of the monkey. Brain Res Rev. 1983;286(3):237–65. 10.1016/0165-0173(83)90015-2
    1. Evarts EV, Thach WT: Motor mechanisms of the CNS: cerebrocerebellar interrelations. Annu Rev Physiol. 1969;31:451–98. 10.1146/annurev.ph.31.030169.002315
    1. Kemp JM, Powell TP: The connexions of the striatum and globus pallidus: synthesis and speculation. Philos Trans R Soc Lond B Biol Sci. 1971;262(845):441–57. 10.1098/rstb.1971.0106
    1. Alexander GE, DeLong MR, Strick PL: Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci. 1986;9:357–81. 10.1146/annurev.ne.09.030186.002041
    1. Wiesendanger E, Clarke S, Kraftsik R, et al. : Topography of cortico-striatal connections in man: anatomical evidence for parallel organization. Eur J Neurosci. 2004;20(7):1915–22. 10.1111/j.1460-9568.2004.03640.x
    1. McHaffie JG, Stanford TR, Stein BE, et al. : Subcortical loops through the basal ganglia. Trends Neurosci. 2005;28(8):401–7. 10.1016/j.tins.2005.06.006
    1. Draganski B, Kherif F, Klöppel S, et al. : Evidence for segregated and integrative connectivity patterns in the human Basal Ganglia. J. Neurosci. 2008;28(28):7143–52. 10.1523/JNEUROSCI.1486-08.2008

    2. F1000 Recommendation

    1. Percheron G, Filion M: Parallel processing in the basal ganglia: up to a point. Trends Neurosci. 1991;14(2):55–9. 10.1016/0166-2236(91)90020-U
    1. Lynch JC, Hoover JE, Strick PL: Input to the primate frontal eye field from the substantia nigra, superior colliculus, and dentate nucleus demonstrated by transneuronal transport. Exp Brain Res. 1994;100(1):181–6. 10.1007/BF00227293
    1. Middleton FA, Strick PL: The temporal lobe is a target of output from the basal ganglia. Proc Natl Acad Sci U S A. 1996;93(16):8683–7. 10.1073/pnas.93.16.8683
    1. Middleton FA, Strick PL: Dentate output channels: motor and cognitive components. Prog Brain Res. 1997;114:553–66. 10.1016/S0079-6123(08)63386-5
    1. Middleton FA, Strick PL: Cerebellar output: motor and cognitive channels. Trends Cogn Sci. 1998;2(9):348–54. 10.1016/S1364-6613(98)01220-0
    1. Zemanick MC, Strick PL, Dix RD: Direction of transneuronal transport of herpes simplex virus 1 in the primate motor system is strain-dependent. Proc Natl Acad Sci U S A. 1991;88(18):8048–51. 10.1073/pnas.88.18.8048
    1. Hoover JE, Strick PL: Multiple output channels in the basal ganglia. Science. 1993;259(5096):819–21. 10.1126/science.7679223
    1. Hoover JE, Strick PL: The organization of cerebellar and basal ganglia outputs to primary motor cortex as revealed by retrograde transneuronal transport of herpes simplex virus type 1. J Neurosci. 1999;19(4):1446–63. 10.1523/JNEUROSCI.19-04-01446.1999
    1. Middleton FA, Strick PL: Anatomical evidence for cerebellar and basal ganglia involvement in higher cognitive function. Science. 1994;266(5184):458–61. 10.1126/science.7939688
    1. Middleton FA, Strick PL: Basal ganglia and cerebellar loops: motor and cognitive circuits. Brain Res Brain Res Rev. 2000;31(2–3):236–50. 10.1016/S0165-0173(99)00040-5
    1. Doya K: Complementary roles of basal ganglia and cerebellum in learning and motor control. Curr Opin Neurobiol. 2000;10(6):732–9. 10.1016/S0959-4388(00)00153-7
    1. Bostan AC, Dum RP, Strick PL: Cerebellar networks with the cerebral cortex and basal ganglia. Trends Cogn Sci. 2013;17(5):241–54. 10.1016/j.tics.2013.03.003

    2. F1000 Recommendation

    1. Hoshi E, Tremblay L, Féger J, et al. : The cerebellum communicates with the basal ganglia. Nat Neurosci. 2005;8(11):1491–3. 10.1038/nn1544

    2. F1000 Recommendation

    1. Bostan AC, Strick PL: The cerebellum and basal ganglia are interconnected. Neuropsychol Rev. 2010;20(3):261–70. 10.1007/s11065-010-9143-9
    1. Bostan AC, Dum RP, Strick PL: The basal ganglia communicate with the cerebellum. Proc Natl Acad Sci U S A. 2010;107(18):8452–6. 10.1073/pnas.1000496107
    1. Ichinohe N, Mori F, Shoumura K: A di-synaptic projection from the lateral cerebellar nucleus to the laterodorsal part of the striatum via the central lateral nucleus of the thalamus in the rat. Brain Res. 2000;880(1–2):191–7. 10.1016/S0006-8993(00)02744-X
    1. Jwair S, Coulon P, Ruigrok TJ: Disynaptic Subthalamic Input to the Posterior Cerebellum in Rat. Front Neuroanat. 2017;11:13. 10.3389/fnana.2017.00013
    1. Bostan AC, Strick PL: The basal ganglia and the cerebellum: nodes in an integrated network. Nat Rev Neurosci. 2018;19(6):338–50. 10.1038/s41583-018-0002-7

    2. F1000 Recommendation

Source: PubMed

Sponsors et collaborateurs

Les conditions médicales

Interventions en matière de drogue

3
S'abonner