Brain Structure and Function

, Volume 221, Issue 9, pp 4291–4317 | Cite as

Chemical anatomy of pallidal afferents in primates

  • Lara Eid
  • Martin ParentEmail author


Neurons of the globus pallidus receive massive inputs from the striatum and the subthalamic nucleus, but their activity, as well as those of their striatal and subthalamic inputs, are modulated by brainstem afferents. These include serotonin (5-HT) projections from the dorsal raphe nucleus, cholinergic (ACh) inputs from the pedunculopontine tegmental nucleus, and dopamine (DA) afferents from the substantia nigra pars compacta. This review summarizes our recent findings on the distribution, quantitative and ultrastructural aspects of pallidal 5-HT, ACh and DA innervations. These results have led to the elaboration of a new model of the pallidal neuron based on a precise knowledge of the hierarchy and chemical features of the various synaptic inputs. The dense 5-HT, ACh and DA innervations disclosed in the associative and limbic pallidal territories suggest that these brainstem inputs contribute principally to the planification of motor behaviors and the regulation of attention and mood. Although 5-HT, ACh and DA inputs were found to modulate pallidal neurons and their afferents mainly through asynaptic (volume) transmission, genuine synaptic contacts occur between these chemospecific axon varicosities and pallidal dendrites, revealing that these brainstem projections have a direct access to pallidal neurons, in addition to their indirect input through the striatum and subthalamic nucleus. Altogether, these findings reveal that the brainstem 5-HT, ACh and DA pallidal afferents act in concert with the more robust GABAergic inhibitory striatopallidal and glutamatergic excitatory subthalamopallidal inputs. We hypothesize that a fragile equilibrium between forebrain and brainstem pallidal afferents plays a key role in the functional organization of the primate basal ganglia, in both health and disease.


Basal ganglia Serotonin Acetylcholine Dopamine Monkey Globus pallidus 



This study was supported by research grants from the Canadian Institutes of Health Research (CIHR MOP-115008) and the Natural Sciences and Engineering Research Council of Canada (NSERC 386396-2010). L.E. was the recipient of a doctoral fellowship from the Fonds de recherche du Québec en santé (FRQS 14D 29441). We thank Marie-Josée Wallman for her technical assistance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

429_2016_1216_MOESM1_ESM.docx (24 kb)
Supplementary material 1 (DOCX 23 kb)


  1. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12(10):366–375PubMedCrossRefGoogle Scholar
  2. Alexander GE, DeLong MR, Strick PL (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu Rev Neurosci 9:357–381PubMedCrossRefGoogle Scholar
  3. Armonda RA, Carpenter MB (1991) Distribution of cholinergic pallidal neurons in the squirrel monkey (Saimiri sciureus) based upon choline acetyltransferase. Journal für Hirnforschung 32(3):357–367PubMedGoogle Scholar
  4. Azmitia EC, Gannon PJ (1986) The primate serotonergic system: a review of human and animal studies and a report on Macaca fascicularis. Adv Neurol 43:407–468PubMedGoogle Scholar
  5. Baker K, Halliday G, Törk I (1990) Cytoarchitecture of the human dorsal raphe nucleus. J Comp Neurol 301(2):147–161PubMedCrossRefGoogle Scholar
  6. Baxter MG, Chiba AA (1999) Cognitive functions of the basal forebrain. Curr Opin Neurobiol 9(2):178–183PubMedCrossRefGoogle Scholar
  7. Beaudet A, Sotelo C (1981) Synaptic remodeling of serotonin axon terminals in rat agranular cerebellum. Brain Res 206(2):305–329PubMedCrossRefGoogle Scholar
  8. Beckstead RM (1983) A pallidostriatal projection in the cat and monkey. Brain Res Bull 11(6):629–632PubMedCrossRefGoogle Scholar
  9. Bédard C, Wallman MJ, Pourcher E, Gould PV, Parent A, Parent M (2011) Serotonin and dopamine striatal innervation in Parkinson’s disease and Huntington’s chorea. Parkinson Relat Disord 17(8):593–598CrossRefGoogle Scholar
  10. Benazzouz A, Mamad O, Abedi P, Bouali-Benazzouz R, Chetrit J (2014) Involvement of dopamine loss in extrastriatal basal ganglia nuclei in the pathophysiology of Parkinson’s disease. Front Aging Neurosci 6(87):1–5Google Scholar
  11. Benhamou L, Bronfeld M, Bar-Gad I, Cohen D (2012) Globus Pallidus external segment neuron classification in freely moving rats: a comparison to primates. PLoS One 7(9):e45421PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bernard V, Norm E, Bloch B (1992) Phenotypical characterization of the rat striatal neurons expressing muscarinic receptor genes. J Neurosci 12(9):3591–3600PubMedGoogle Scholar
  13. Bevan MD, Clarke NP, Bolam JP (1997) Synaptic integration of functionally diverse pallidal information in the entopeduncular nucleus and subthalamic nucleus in the rat. J Neurosci 17(1):308–324PubMedGoogle Scholar
  14. Björklund A, Dunnett SB (2007) Dopamine neuron systems in the brain: an update. Trends Neurosci 30(5):194–202PubMedCrossRefGoogle Scholar
  15. Bobillier P, Seguin S, Petitjean F, Salvert D, Touret M, Jouvet M (1976) The raphe nuclei of the cat brain stem: a topographical atlas of their efferent projections as revealed by autoradiography. Brain Res 113(3):449–486PubMedCrossRefGoogle Scholar
  16. Bogenpohl J, Galvan A, Hu X, Wichmann T, Smith Y (2013) Metabotropic glutamate receptor 4 in the basal ganglia of parkinsonian monkeys: ultrastructural localization and electrophysiological effects of activation in the striatopallidal complex. Neuropharmacology 66:242–252PubMedCrossRefGoogle Scholar
  17. Bohnen NI, Albin RL (2011) The cholinergic system and Parkinson disease. Behav Brain Res 221(2):564–573PubMedCrossRefGoogle Scholar
  18. Bolam JP, Smith Y (1992) The striatum and the globus pallidus send convergent synaptic inputs onto single cells in the entopeduncular nucleus of the rat: a double anterograde labelling study combined with postembedding immunocytochemistry for GABA. J Comp Neurol 321(3):456–476PubMedCrossRefGoogle Scholar
  19. Boraud T, Bezard E, Guehl D, Bioulac B, Gross C (1998) Effects of l-DOPA on neuronal activity of the globus pallidus externalis (GPe) and globus pallidus internalis (GPi) in the MPTP-treated monkey. Brain Res 787(1):157–160PubMedCrossRefGoogle Scholar
  20. Braak H, del Tredici K, Rüb U, de Vos RAI, Steur ENHJ, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24(2):197–211PubMedCrossRefGoogle Scholar
  21. Bryant CE, Rupniak NM, Iversen SD (1988) Effects of different environmental enrichment devices on cage stereotypies and autoaggression in captive cynomolgus monkeys. J Med Primatol 17(5):257–269PubMedGoogle Scholar
  22. Burdach K (1822) Vom Baue und Leben des Gehirns, vol 2. Dyk, LeipzigGoogle Scholar
  23. Canteras NS, Shammah-Lagnado SJ, Silva BA, Ricardo JA (1990) Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res 513(1):43–59PubMedCrossRefGoogle Scholar
  24. Carpenter MB, Strominger NL (1967) Efferent fibers of the subthalamic nucleus in the monkey. A comparison of the efferent projections of the subthalamic nucleus, substantia nigra and globus pallidus. Am J Anat 121(1):41–72PubMedCrossRefGoogle Scholar
  25. Carpenter MB 3rd, Batton RR, Carleton SC, Keller JT (1981) Interconnections and organization of pallidal and subthalamic nucleus neurons in the monkey. J Comp Neurol 197(4):579–603PubMedCrossRefGoogle Scholar
  26. Carta M, Carlsson T, Kirik D, Bjorklund A (2007) Dopamine released from 5-HT terminals is the cause of l-DOPA-induced dyskinesia in parkinsonian rats. Brain 130(7):1819–1833PubMedCrossRefGoogle Scholar
  27. Castro ME, Pascual J, Romón T, Berciano J, Figols J, Pazos A (1998) 5-HT1B receptor binding in degenerative movement disorders. Brain Res 790:323–328PubMedCrossRefGoogle Scholar
  28. Celio MR (1986) Parvalbumin in most gamma-aminobutyric acid-containing neurons of the rat cerebral cortex. Science 231(4741):995–997PubMedCrossRefGoogle Scholar
  29. Chan-Palay V (1977) Indoleamine neurons and their processes in the normal rat brain and in chronic diet-induced thiamine deficiency demonstrated by uptake of 3H-serotonin. J Comp Neurol 176(4):467–493PubMedCrossRefGoogle Scholar
  30. Charara A, Parent A (1994) Brainstem dopaminergic, cholinergic and serotoninergic afferents to the pallidum in the squirrel monkey. Brain Res 640:155–170PubMedCrossRefGoogle Scholar
  31. Charara A, Heilman TC, Levey AI, Smith Y (2000) Pre- and postsynaptic localization of GABA(B) receptors in the basal ganglia in monkeys. Neuroscience 95(1):127–140PubMedCrossRefGoogle Scholar
  32. Charara A, Galvan A, Kuwajima M, Hall RA, Smith Y (2004) An electron microscope immunocytochemical study of GABAB R2 receptors in the monkey basal ganglia: a comparative analysis with GABAB R1 receptor distribution. J Comp Neurol 476(1):65–79PubMedCrossRefGoogle Scholar
  33. Charara A, Pare JF, Levey AI, Smith Y (2005) Synaptic and extrasynaptic GABA-A and GABA-B receptors in the globus pallidus: an electron microscopic immunogold analysis in monkeys. Neuroscience 131(4):917–933PubMedCrossRefGoogle Scholar
  34. Cools A, van den Bercken J, Horstink M, van Spaendonck K, Berger H (1981) The basal ganglia and the programming of behaviour. Trends Neurosci 4:124–125CrossRefGoogle Scholar
  35. Cooper AJ, Stanford IM (2002) Calbindin D-28k positive projection neurons and calretinin positive interneurones of the rat globus pallidus. Brain Res 929(2):243–251PubMedCrossRefGoogle Scholar
  36. Cortés R, Probst A, Palacios JM (1984) Quantitative light microscopic autoradiographic localization of cholinergic muscarinic receptors in the human brain: brainstem. Neuroscience 12(4):1003–1026PubMedCrossRefGoogle Scholar
  37. Cortés R, Probst A, Palacios JM (1987) Quantitative light microscopic autoradiographic localization of cholinergic muscarinic receptors in the human brain: forebrain. Neuroscience 20(1):65–107PubMedCrossRefGoogle Scholar
  38. Cossette M, Lévesque M, Parent A (1999) Extrastriatal dopaminergic innervation of human basal ganglia. Neurosci Res 34(1):51–54PubMedCrossRefGoogle Scholar
  39. Dautan D, Huerta-Ocampo I, Witten IB, Deisseroth K, Bolam JP, Gerdjikov T, Mena-Segovia J (2014) A major external source of cholinergic innervation of the striatum and nucleus accumbens originates in the brainstem. J Neurosci 34(13):4509–4518PubMedPubMedCentralCrossRefGoogle Scholar
  40. Davids E, Zhang K, Tarazi FI, Baldessarini RJ (2003) Animal models of attention-deficit hyperactivity disorder. Brain Res Rev 42(1):1–21PubMedCrossRefGoogle Scholar
  41. Debeir T, Ginestet L, François C, Laurens S, Martel JC, Chopin P, Marien M, Colpaert F, Raisman-Vozari R (2005) Effect of intrastriatal 6-OHDA lesion on dopaminergic innervation of the rat cortex and globus pallidus. Exp Neurol 193(2):444–454PubMedCrossRefGoogle Scholar
  42. Delaville C, Navailles S, Benazzouz A (2012) Effects of noradrenaline and serotonin depletions on the neuronal activity of globus pallidus and substantia nigra pars reticulata in experimental parkinsonism. Neuroscience 202:424–433PubMedCrossRefGoogle Scholar
  43. DeLong MR (1971) Activity of pallidal neurons during movement. J Neurophysiol 34(3):414–427PubMedGoogle Scholar
  44. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13(7):281–285PubMedCrossRefGoogle Scholar
  45. DeLong MR, Wichmann T (2015) Basal ganglia circuits as targets for neuromodulation in Parkinson disease. JAMA Neurol 72(11):1354–1360PubMedCrossRefGoogle Scholar
  46. Descarries L (1998) The hypothesis of an ambient level of acetylcholine in the central nervous system. J Physiol 92(3–4):215–220Google Scholar
  47. Descarries L, Mechawar N (2008) Structural organization of monoamine and acetylcholine neuron systems in the rat CNS. In: Lajtha A, Vizi E (eds) Handbook of neurochemistry and molecular biology. Springer, New York, pp 1–20Google Scholar
  48. Descarries L, Gisiger V, Steriade M (1997) Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53(5):603–625PubMedCrossRefGoogle Scholar
  49. Descarries L, Riad M, Parent M (2010) Ultrastructure of the serotonin innervation in the mammalian central nervous system. In: Muller CP, Jacobs BL (eds) Handbook of behavioral neuroscience. Academic Press, London, pp 65–102Google Scholar
  50. Deschênes M, Bourassa J, Doan VD, Parent A (1996) A single-cell study of the axonal projections arising from the posterior intralaminar thalamic nuclei in the rat. Eur J Neurosci 8(2):329–343PubMedCrossRefGoogle Scholar
  51. DeVito JL, Anderson ME, Walsh KE (1980) A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta. Exp Brain Res 38(1):65–73PubMedCrossRefGoogle Scholar
  52. Di Giovanni G, Esposito E, Di Matteo V (2010) Role of serotonin in central dopamine dysfunction. CNS Neurosci Ther 16(3):179–194PubMedCrossRefGoogle Scholar
  53. Di Matteo V, Pierucci M, Esposito E, Crescimanno G, Benigno A, Di Giovanni G (2008) Serotonin modulation of the basal ganglia circuitry: therapeutic implication for Parkinson’s disease and other motor disorders. Prog Brain Res 172:423–463PubMedCrossRefGoogle Scholar
  54. DiFiglia M, Rafols JA (1988) Synaptic organization of the globus pallidus. J Electron Microsc Tech 10(3):247–263PubMedCrossRefGoogle Scholar
  55. DiFiglia M, Pasik P, Pasik T (1982) A Golgi and ultrastructural study of the monkey globus pallidus. J Comp Neurol 212(1):53–75PubMedCrossRefGoogle Scholar
  56. Dopeso-Reyes IG, Rico AJ, Roda E, Sierra S, Pignataro D, Lanz M, Sucunza D, Chang-Azancot L, Lanciego JL (2014) Calbindin content and differential vulnerability of midbrain efferent dopaminergic neurons in macaques. Front Neuroanat 8(146):1–12Google Scholar
  57. Eid L, Parent M (2015a) Cholinergic neurons intrinsic to the primate external pallidum. Synapse 69(8):416–419PubMedCrossRefGoogle Scholar
  58. Eid L, Parent M (2015b) Morphological evidence for dopamine interactions with pallidal neurons in primates. Front Neuroanat 9(111):1–14Google Scholar
  59. Eid L, Champigny MF, Parent A, Parent M (2013) Quantitative and ultrastructural study of serotonin innervation of the globus pallidus in squirrel monkeys. Eur J Neurosci 37(10):1659–1668PubMedCrossRefGoogle Scholar
  60. Eid L, Parent A, Parent M (2016) Asynaptic feature and heterogeneous distribution of the cholinergic innervation of the globus pallidus in primates. Brain Struct Funct 221(2):1139–1155PubMedCrossRefGoogle Scholar
  61. Everitt BJ, Sirkiä TE, Roberts AC, Jones GH, Robbins TW (1988) Distribution and some projections of cholinergic neurons in the brain of the common marmoset, Callithrix jacchus. J Comp Neurol 271(4):533–558PubMedCrossRefGoogle Scholar
  62. Fernández-Suárez D, Celorrio M, Lanciego JL, Franco R, Aymerich MS (2012) Loss of parvalbumin-positive neurons from the globus pallidus in animal models of Parkinson disease. J Neuropathol Exp Neurol 71(11):973–982PubMedCrossRefGoogle Scholar
  63. Filion M, Tremblay L (1991) Abnormal spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547(1):142–151PubMedGoogle Scholar
  64. Filion M, Tremblay L, Bédard PJ (1991) Effects of dopamine agonists on the spontaneous activity of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res 547(1):152–161PubMedGoogle Scholar
  65. Flaherty AW, Graybiel AM (1994) Input-output organization of the sensorimotor striatum in the squirrel monkey. J Neurosci 14(2):599–610PubMedGoogle Scholar
  66. Fortin M, Parent A (1994) Calretinin labels a specific neuronal subpopulation in primate globus pallidus. Neuroreport 5(16):2097–2100PubMedCrossRefGoogle Scholar
  67. Fox SH (2013) Non-dopaminergic treatments for motor control in Parkinson’s disease. Drugs 73(13):1405–1415PubMedCrossRefGoogle Scholar
  68. Fox CA, Andrade AN, Qui IJL, Rafols JA (1974) The primate globus pallidus: a Golgi and electron microscopic study. Journal für Hirnforschung 15(1):75–93PubMedGoogle Scholar
  69. François C, Percheron G, Yelnik J, Heyner S (1984) A Golgi analysis of the primate globus pallidus. I. Inconstant processes of large neurons, other neuronal types, and afferent axons. J Comp Neurol 227(2):182–199PubMedCrossRefGoogle Scholar
  70. François C, Yelnik J, Percheron G, Fénelon G (1994) Topographic distribution of the axonal endings from the sensorimotor and associative striatum in the macaque pallidum and substantia nigra. Exp Brain Res 102(2):305–318PubMedCrossRefGoogle Scholar
  71. François C, Grabli D, McCairn K, Jan Karachi C, Hirsch EC, Féger J, Tremblay L (2004) Behavioural disorders induced by external globus pallidus dysfunction in primates II. Anatomical study. Brain 127(9):2055–2070PubMedCrossRefGoogle Scholar
  72. Fuchs H, Hauber W (2004) Dopaminergic innervation of the rat globus pallidus characterized by microdialysis and immunohistochemistry. Exp Brain Res 154(1):66–75PubMedCrossRefGoogle Scholar
  73. Gagnon D, Parent M (2014) Distribution of VGLUT3 in highly collateralized axons from the rat dorsal raphe nucleus as revealed by single-neuron reconstructions. PLoS One 9(2):e87709PubMedPubMedCentralCrossRefGoogle Scholar
  74. Gagnon D, Gregoire L, Di Paolo T, Parent M (2015) Serotonin hyperinnervation of the striatum with high synaptic incidence in parkinsonian monkeys. Brain Struct Funct [Epub ahead of print] Google Scholar
  75. Galvan A, Floran B, Erlij D, Aceves J (2001) Intrapallidal dopamine restores motor deficits induced by 6-hydroxydopamine in the rat. J Neural Transm 108(2):153–166PubMedCrossRefGoogle Scholar
  76. Galvan A, Villalba RM, West SM, Maidment NT, Ackerson LC, Yol Smith Y, Smith Wichmann T (2005) GABAergic modulation of the activity of globus pallidus neurons in primates: in vivo analysis of the functions of GABA receptors and GABA transporters. J Neurophysiol 94(2):990–1000PubMedCrossRefGoogle Scholar
  77. Gash DM, Zhang Z, Ovadia A, Cass WA, Yi A, Simmerman L, Russell D, Martin D, Lapchak PA, Collins F, Hoffer BJ, Gerhardt GA (1996) Functional recovery in parkinsonian monkeys treated with GDNF. Nature 380:252–255PubMedCrossRefGoogle Scholar
  78. Gauthier J, Parent M, Lévesque M, Parent A (1999) The axonal arborization of single nigrostriatal neurons in rats. Brain Res 834:228–232PubMedCrossRefGoogle Scholar
  79. Gerfen CR, Bolam JP (2010) The neuroanatomical organization of the basal ganglia. In: Steiner H, Tseng KY (eds) Handbook of basal ganglia structure and function. Academic Press/Elsevier, London, pp 3–28CrossRefGoogle Scholar
  80. Giménez-Amaya JM, Graybiel AM (1990) Compartmental origins of the striatopallidal projection in the primate. Neuroscience 34(1):111–126PubMedCrossRefGoogle Scholar
  81. Grabli D, McCairn K, Hirsch EC, Agid Y, Féger J, François C, Tremblay L (2004) Behavioural disorders induced by external globus pallidus dysfunction in primates: I. Behavioural study. Brain 127(9):2039–2054PubMedCrossRefGoogle Scholar
  82. Grabli D, Karachi C, Folgoas E, Monfort M, Tande D, Clark S, Civelli O, Hirsch EC, Francois C (2013) Gait disorders in parkinsonian monkeys with pedunculopontine nucleus lesions: a tale of two systems. J Neurosci 33(29):11986–11993PubMedCrossRefGoogle Scholar
  83. Griffiths PD, Sambrook MA, Perry R, Crossman AR (1990) Changes in benzodiazepine and acetylcholine receptors in the globus pallidus in Parkinson’s disease. J Neurol Sci 100(1–2):131–136PubMedCrossRefGoogle Scholar
  84. Groenewegen HJ, van den Heuvel OA, Cath DC, Voorn P, Veltman DJ (2003) Does an imbalance between the dorsal and ventral striatopallidal systems play a role in Tourette’s syndrome? A neuronal circuit approach. Brain Dev 25(Suppl 1):S3–S14PubMedCrossRefGoogle Scholar
  85. Gurevich EV, Joyce JN (1999) Distribution of dopamine D3 receptor expressing neurons in the human forebrain: comparison with D2 receptor expressing neurons. Neuropsychopharmacology 20(1):60–80PubMedCrossRefGoogle Scholar
  86. Haber S, Elde R (1982) The distribution of enkephalin immunoreactive fibers and terminals in the monkey central nervous system: an immunohistochemical study. Neuroscience 7(5):1049–1095PubMedCrossRefGoogle Scholar
  87. Haber SN, Lynd E, Klein C, Groenewegen HJ (1990) Topographic organization of the ventral striatal efferent projections in the rhesus monkey: an anterograde tracing study. J Comp Neurol 293(2):282–298PubMedCrossRefGoogle Scholar
  88. Hadipour-Niktarash A, Rommelfanger KS, Masilamoni GJ, Smith Y, Wichmann T (2012) Extrastriatal D2-like receptors modulate basal ganglia pathways in normal and parkinsonian monkeys. J Neurophysiol 107(5):1500–1512PubMedCrossRefGoogle Scholar
  89. Hall H, Lundkvist C, Halldin C, Farde L, Pike VW, McCarron JA, Fletcher A, Cliffe IA, Barf T, Wikström H, Sedvall G (1997) Autoradiographic localization of 5-HT1A receptors in the post-mortem human brain using [3H]WAY-100635 and [11C]way-100635. Brain Res 745(1–2):96–108PubMedCrossRefGoogle Scholar
  90. Halliday GM, Blumbergs PC, Cotton RG, Blessing WW, Geffen LB (1990a) Loss of brainstem serotonin- and substance P-containing neurons in Parkinson’s disease. Brain Res 510(1):104–107PubMedCrossRefGoogle Scholar
  91. Halliday GM, Li YW, Blumbergs PC, Joh TH, Cotton RG, Howe PR, Blessing WW, Geffen LB (1990b) Neuropathology of immunohistochemically identified brainstem neurons in Parkinson’s disease. Ann Neurol 27(4):373–385PubMedCrossRefGoogle Scholar
  92. Hanson JE, Smith Y (1999) Group I metabotropic glutamate receptors at GABAergic synapses in monkeys. J Neurosci 19(15):6488–6496PubMedGoogle Scholar
  93. Hardman CD, Henderson JM, Finkelstein DI, Horne MK, Paxinos G, Halliday GM (2002) Comparison of the basal ganglia in rats, marmosets, macaques, baboons, and humans: volume and neuronal number for the output, internal relay, and striatal modulating nuclei. J Comp Neurol 445(3):238–255PubMedCrossRefGoogle Scholar
  94. Hasselmo ME (1995) Neuromodulation and cortical function: modeling the physiological basis of behavior. Behav Brain Res 67(1):1–27PubMedCrossRefGoogle Scholar
  95. Hauber W, Lutz S (1999) Dopamine D1 or D2 receptor blockade in the globus pallidus produces akinesia in the rat. Behav Brain Res 106:143–150PubMedCrossRefGoogle Scholar
  96. Hazrati LN, Parent A (1992a) Convergence of subthalamic and striatal efferents at pallidal level in primates: an anterograde double-labeling study with biocytin and PHA-L. Brain Res 569(2):336–340PubMedCrossRefGoogle Scholar
  97. Hazrati LN, Parent A (1992b) The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res 592:213–227PubMedCrossRefGoogle Scholar
  98. Hazrati LN, Parent A, Mitchell S, Haber SN (1990) Evidence for interconnections between the two segments of the globus pallidus in primates: a PHA-L anterograde tracing study. Brain Res 533(1):171–175PubMedCrossRefGoogle Scholar
  99. He L, Di Monte DA, Langston JW, Quik M (2000) Autoradiographic analysis of N-methyl-d-aspartate receptor binding in monkey brain: effects of 1-methyl-4-phenyl-1,2,3, 6-tetrahydropyridine and levodopa treatment. Neuroscience 99(4):697–704PubMedCrossRefGoogle Scholar
  100. Heckers S, Geula C, Mesulam MM (1992) Cholinergic innervation of the human thalamus: dual origin and differential nuclear distribution. J Comp Neurol 325(1):68–82PubMedCrossRefGoogle Scholar
  101. Hedreen JC (1999) Tyrosine hydroxylase-immunoreactive elements in the human globus pallidus and subthalamic nucleus. J Comp Neurol 409(3):400–410PubMedCrossRefGoogle Scholar
  102. Hedreen JC, DeLong MR (1991) Organization of striatopallidal, striatonigral, and nigrostriatal projections in the macaque. J Comp Neurol 304(4):569–595PubMedCrossRefGoogle Scholar
  103. Hikosaka O, Nakamura K, Sakai K, Nakahara H (2002) Central mechanisms of motor skill learning. Curr Opin Neurobiol 12(2):217–222PubMedCrossRefGoogle Scholar
  104. Hoover B, Marshall J (2002) Further characterization of preproenkephalin mRNA-containing cells in the rodent globus pallidus. Neuroscience 111(1):111–125PubMedCrossRefGoogle Scholar
  105. Hoyer D, Hannon JP, Martin GR (2002) Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71(4):533–554PubMedCrossRefGoogle Scholar
  106. Huot P, Fox SH (2013) The serotonergic system in motor and non-motor manifestations of Parkinson’s disease. Exp Brain Res 230(4):463–476PubMedCrossRefGoogle Scholar
  107. Huot P, Fox SH, Newman-Tancredi A, Brotchie JM (2011) Anatomically selective serotonergic type 1A and serotonergic type 2A therapies for Parkinson’s disease: an approach to reducing dyskinesia without exacerbating parkinsonism? J Pharmacol Exp Ther 339(1):2–8PubMedCrossRefGoogle Scholar
  108. Huot P, Johnston TH, Winkelmolen L, Fox SH, Brotchie JM (2012) 5-HT2A receptor levels increase in MPTP-lesioned macaques treated chronically with l-DOPA. Neurobiol Aging 33(1):194.e5–194.e15CrossRefGoogle Scholar
  109. Jan C, François C, Tandé D, Yelnik J, Tremblay L, Agid Y, Hirsch E (2000) Dopaminergic innervation of the pallidum in the normal state, in MPTP-treated monkeys and in parkinsonian patients. Eur J Neurosci 12(12):4525–4535PubMedGoogle Scholar
  110. Jin XT, Smith Y (2011) Localization and functions of kainate receptors in the basal ganglia. Adv Exp Med Biol 717:27–37PubMedCrossRefGoogle Scholar
  111. Kane-Jackson R, Smith Y (2003) Pre-synaptic kainate receptors in GABAergic and glutamatergic axon terminals in the monkey globus pallidus. Neuroscience 122(2):285–289PubMedCrossRefGoogle Scholar
  112. Karain B, Xu D, Bellone JA, Hartman RE, Shi WX (2015) Rat globus pallidus neurons: functional classification and effects of dopamine depletion. Synapse 69(1):41–51PubMedCrossRefGoogle Scholar
  113. Kayadjanian N, Rétaux S, Menétrey A, Besson MJ (1994) Stimulation by nicotine of the spontaneous release of [H]gamma-aminobutyric acid in the substantia nigra and in the globus pallidus of the rat. Brain Res 649(1–2):129–135PubMedCrossRefGoogle Scholar
  114. Kayadjanian N, Menétrey A, Besson MJ (1997) Activation of muscarinic receptors stimulates GABA release in the rat globus pallidus. Synapse 26(2):131–139PubMedCrossRefGoogle Scholar
  115. Kempf F, Brücke C, Kühn AA, Schneider GH, Kupsch A, Chen CC, Androulidakis AG, Wang S, Vandenberghe W, Nuttin B, Aziz T, Brown P (2007) Modulation by dopamine of human basal ganglia involvement in feedback control of movement. Curr Biol 17(15):R587–R589PubMedCrossRefGoogle Scholar
  116. Kim R, Nakano K, Jayaraman A, Carpenter MB (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the monkey. J Comp Neurol 169(3):263–290PubMedCrossRefGoogle Scholar
  117. Kincaid AE, Penney JB Jr, Young AB, Newman SW (1991) The globus pallidus receives a projection from the parafascicular nucleus in the rat. Brain Res 553(1):18–26PubMedCrossRefGoogle Scholar
  118. Kita H (2007) Globus pallidus external segment. Prog Brain Res 160:111–133PubMedCrossRefGoogle Scholar
  119. Kita H (2010) Organization of the globus pallidus. In: Steiner H, Tseng KY (eds) Handbook of basal ganglia structure and function. Academic Press Elsevier, London, pp 223–247Google Scholar
  120. Kita H, Kitai ST (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J Comp Neurol 260(3):435–452PubMedCrossRefGoogle Scholar
  121. Kita H, Tokuno H, Nambu A (1999) Monkey globus pallidus external segment neurons projecting to the neostriatum. Neuroreport 10(7):1467–1472PubMedCrossRefGoogle Scholar
  122. Kita H, Nambu A, Kaneda K, Tachibana Y, Takada M (2004) Role of ionotropic glutamatergic and GABAergic inputs on the firing activity of neurons in the external pallidum in awake monkeys. J Neurophysiol 92(5):3069–3084PubMedCrossRefGoogle Scholar
  123. Kita H, Chiken S, Tachibana Y, Nambu A (2007) Serotonin modulates pallidal neuronal activity in the awake monkey. J Neurosci 27(1):75–83PubMedCrossRefGoogle Scholar
  124. Kitai S, Kita H (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In: Carpenter MB, Jayaraman A (eds) The basal ganglia II. Plenum Press, New York, pp 357–373CrossRefGoogle Scholar
  125. Kliem MA, Maidment NT, Ackerson LC, Chen S, Smith Y, Wichmann T (2007) Activation of nigral and pallidal dopamine D1-like receptors modulates basal ganglia outflow in monkeys. J Neurophysiol 98(3):1489–1500PubMedCrossRefGoogle Scholar
  126. Kliem MA, Paré JF, Khan ZU, Wichmann T, Smith Y (2010) Ultrastructural localization and function of dopamine D1-like receptors in the substantia nigra pars reticulata and the internal segment of the globus pallidus of parkinsonian monkeys. Eur J Neurosci 31(5):836–851PubMedCrossRefPubMedCentralGoogle Scholar
  127. Kosinski CM, Standaert DG, Counihan TJ, Scherzer CR, Kerner JA, Daggett LP, Veliçelebi G, Penney JB, Young AB, Landwehrmeyer GB (1998) Expression of N-methyl-d-aspartate receptor subunit mRNAs in the human brain: striatum and globus pallidus. J Comp Neurol 390(1):63–74PubMedCrossRefGoogle Scholar
  128. Laurie DJ, Seeburg PH (1994) Ligand affinities at recombinant N-methyl-d-aspartate receptors depend on subunit composition. Eur J Pharmacol 268(3):335–345PubMedCrossRefGoogle Scholar
  129. Lavoie B, Parent A (1990) Immunohistochemical study of the serotoninergic innervation of the basal ganglia in the squirrel monkey. J Comp Neurol 299(1):1–16PubMedCrossRefGoogle Scholar
  130. Lavoie B, Parent A (1991) Serotoninergic innervation of the thalamus in the primate: an immunohistochemical study. J Comp Neurol 312(1):1–18PubMedCrossRefGoogle Scholar
  131. Lavoie B, Parent A (1994a) Pedunculopontine nucleus in the squirrel monkey: cholinergic and glutamatergic projections to the substantia nigra. J Comp Neurol 344(2):232–241PubMedCrossRefGoogle Scholar
  132. Lavoie B, Parent A (1994b) Pedunculopontine nucleus in the squirrel monkey: projections to the basal ganglia as revealed by anterograde tract-tracing methods. J Comp Neurol 344(2):210–231PubMedCrossRefGoogle Scholar
  133. Lavoie B, Smith Y, Parent A (1989) Dopaminergic innervation of the basal ganglia in the squirrel monkey as revealed by tyrosine hydroxylase immunohistochemistry. J Comp Neurol 289(1):36–52PubMedCrossRefGoogle Scholar
  134. Lee MS, Rinne JO, Marsden CD (2000) The pedunculopontine nucleus: its role in the genesis of movement disorders. Yonsei Med J 41(2):167–184PubMedCrossRefGoogle Scholar
  135. Lee M, Ryu YH, Cho WG, Kang YW, Lee SJ, Jeon TJ, Lyoo CH, Kim CH, Kim DG, Lee K, Choi TH, Choi JY (2015) Relationship between dopamine deficit and the expression of depressive behavior resulted from alteration of serotonin system. Synapse 69(9):453–460PubMedCrossRefGoogle Scholar
  136. Lénárd L, Karádi Z, Faludi B, Czurkó A, Niedetzky C, Vida I, Nishino H (1995) Glucose-sensitive neurons of the globus pallidus: I. Neurochemical characteristics. Brain Res Bull 37(2):149–155PubMedCrossRefGoogle Scholar
  137. Lindvall O, Björklund A (1979) Dopaminergic innervation of the globus pallidus by collaterals from the nigrostriatal pathway. Brain Res 172(1):169–173PubMedCrossRefGoogle Scholar
  138. Mallet N, Micklem BR, Henny P, Brown MT, Williams C, Bolam JP, Nakamura KC, Magill PJ (2012) Dichotomous organization of the external globus pallidus. Neuron 74(6):1075–1086PubMedCrossRefPubMedCentralGoogle Scholar
  139. Marsden CD (1980) The enigma of the basal ganglia and movement. Trends Neurosci 3:284–287CrossRefGoogle Scholar
  140. Marsden CD (1981) The basal ganglia and the programming of behaviour: motor activity and the outputs of the basal ganglia. Trends Neurosci 4:124–125CrossRefGoogle Scholar
  141. Martinez-Gonzalez C, Bolam JP, Mena-Segovia J (2011) Topographical organization of the pedunculopontine nucleus. Front Neuroanat 5(22):1–10Google Scholar
  142. Martinez-Martin P, Chaudhuri KR, Rojo-Abuin JM, Rodriguez-Blazquez C, Alvarez-Sanchez M, Arakaki T, Bergareche-Yarza A, Chade A, Garretto N, Gershanik O, Kurtis MM, Martinez-Castrillo JC, Mendoza-Rodriguez A, Moore HP, Rodriguez-Violante M, Singer C, Tilley BC, Huang J, Stebbins GT, Goetz CG (2015) Assessing the non-motor symptoms of Parkinson’s disease: MDS-UPDRS and NMS Scale. Eur J Neurol 22(1):37–43PubMedCrossRefGoogle Scholar
  143. Mastro KJ, Bouchard RS, Holt HAK, Gittis AH (2014) Transgenic mouse lines subdivide external segment of the globus pallidus (GPe) neurons and reveal distinct GPe output pathways. J Neurosci 34(6):2087–2099PubMedPubMedCentralCrossRefGoogle Scholar
  144. Matsumoto N, Hanakawa T, Maki S, Graybiel AM, Kimura M (1999) Nigrostriatal dopamine system in learning to perform sequential motor tasks in a predictive manner. J Neurophysiol 82(2):978–998PubMedGoogle Scholar
  145. McCormick DA (1992) Neurotransmitter actions in the thalamus and cerebral cortex and their role in neuromodulation of thalamocortical activity. Prog Neurobiol 39(4):337–388PubMedCrossRefGoogle Scholar
  146. Mena-Segovia J, Bolam JP, Magill PJ (2004) Pedunculopontine nucleus and basal ganglia: distant relatives or part of the same family? Trends Neurosci 27(10):585–588PubMedCrossRefGoogle Scholar
  147. Mena-Segovia J, Sims HM, Magill PJ, Bolam JP (2008) Cholinergic brainstem neurons modulate cortical gamma activity during slow oscillations. J Physiol 586(12):2947–2960PubMedPubMedCentralCrossRefGoogle Scholar
  148. Mesulam MM, Mufson EJ (1984) Neural inputs into the nucleus basalis of the substantia innominata (Ch4) in the rhesus monkey. Brain 107:253–274PubMedCrossRefGoogle Scholar
  149. Mesulam MM, Mash D, Hersh L, Bothwell M, Geula C (1992) Cholinergic innervation of the human striatum, globus pallidus, subthalamic nucleus, substantia nigra, and red nucleus. J Comp Neurol 323(2):252–268PubMedCrossRefGoogle Scholar
  150. Milardi D, Gaeta M, Marino S, Arrigo A, Vaccarino G, Mormina E, Rizzo G, Milazzo C, Finocchio G, Baglieri A, Anastasi G, Quartarone A (2015) Basal ganglia network by constrained spherical deconvolution: a possible cortico-pallidal pathway? Mov Disord 30(3):342–349PubMedCrossRefGoogle Scholar
  151. Mineur YS, Obayemi A, Wigestrand MB, Fote GM, Calarco CA, Li AM, Picciotto MR (2013) Cholinergic signaling in the hippocampus regulates social stress resilience and anxiety- and depression-like behavior. Proc Natl Acad Sci 110(9):3573–3578PubMedPubMedCentralCrossRefGoogle Scholar
  152. Miyamoto Y, Fukuda T (2015) Immunohistochemical study on the neuronal diversity and three-dimensional organization of the mouse entopeduncular nucleus. Neurosci Res 94:37–49PubMedCrossRefGoogle Scholar
  153. Miyoshi R, Kito S, Shimoyama M (1989) Quantitative autoradiographic localization of the M1 and M2 subtypes of muscarinic acetylcholine receptors in the monkey brain. Jpn J Pharmacol 51(2):247–255PubMedCrossRefGoogle Scholar
  154. Moore RY, Halaris AE, Jones BE (1978) Serotonin neurons of the midbrain raphe: ascending projections. J Comp Neurol 180(3):417–438PubMedCrossRefGoogle Scholar
  155. Mostany R, Pazos A, Castro ME (2005) Autoradiographic characterisation of [35S]GTPgammaS binding stimulation mediated by 5-HT1B receptor in postmortem human brain. Neuropharmacology 48(1):25–33PubMedCrossRefGoogle Scholar
  156. Mounayar S, Boulet S, Tandé D, Jan C, Pessiglione M, Hirsch EC, Féger J, Savasta M, François C, Tremblay L (2007) A new model to study compensatory mechanisms in MPTP-treated monkeys exhibiting recovery. Brain 130(11):2898–2914PubMedCrossRefGoogle Scholar
  157. Mrzljak L, Bergson C, Pappy M, Huff R, Levenson R, Goldman-Rakic PS (1996) Localization of dopamine D4 receptors in GABAergic neurons of the primate brain. Nature 381(6579):245–248PubMedCrossRefGoogle Scholar
  158. Naito A, Kita H (1994) The cortico-pallidal projection in the rat: an anterograde tracing study with biotinylated dextran amine. Brain Res 653(1–2):251–257PubMedCrossRefGoogle Scholar
  159. Nambu A (2007) Globus pallidus internal segment. Prog Brain Res 160:135–150PubMedCrossRefGoogle Scholar
  160. Nauta WJ, Mehler WR (1966) Projections of the lentiform nucleus in the monkey. Brain Res 1(1):3–42PubMedCrossRefGoogle Scholar
  161. Nevalainen N, af Bjerkén S, Lundblad M, Gerhardt GA, Strömberg I (2011) Dopamine release from serotonergic nerve fibers is reduced in l-DOPA-induced dyskinesia. J Neurochem 118(1):12–23PubMedPubMedCentralCrossRefGoogle Scholar
  162. Nobin A, Björklund A (1973) Topography of the monoamine neuron systems in the human brain as revealed in fetuses. Acta Physiol Scand Suppl 388(Suppl.):1–40PubMedGoogle Scholar
  163. Novak MA, Kinsey JH, Jorgensen MJ, Hazen TJ (1998) Effects of puzzle feeders on pathological behavior in individually housed rhesus monkeys. Am J Primatol 46(3):213–227PubMedCrossRefGoogle Scholar
  164. Palkovits M, Brownstein M, Saavedra JM (1974) Serotonin content of the brain stem nuclei in the rat. Brain Res 80(2):237–249PubMedCrossRefGoogle Scholar
  165. Paquet M, Smith Y (1996) Differential localization of AMPA glutamate receptor subunits in the two segments of the globus pallidus and the substantia nigra pars reticulata in the squirrel monkey. Eur J Neurosci 8(1):229–233PubMedCrossRefGoogle Scholar
  166. Parent A (1990) Extrinsic connections of the basal ganglia. Trends Neurosci 13(7):254–258PubMedCrossRefGoogle Scholar
  167. Parent A, de Bellefeuille L (1983) The pallidointralaminar and pallidonigral projections in primate as studied by retrograde double-labeling method. Brain Res 278(1–2):11–27PubMedCrossRefGoogle Scholar
  168. Parent A, Hazrati L (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Rev 20:91–127PubMedCrossRefGoogle Scholar
  169. Parent A, Lavoie B (1993) The heterogeneity of the mesostriatal dopaminergic system as revealed in normal and parkinsonian monkeys. Adv Neurol 60:25–33PubMedGoogle Scholar
  170. Parent M, Parent A (2004) The pallidofugal motor fiber system in primates. Parkinson Relat Disord 10(4):203–211CrossRefGoogle Scholar
  171. Parent M, Parent A (2005) Single-axon tracing and three-dimensional reconstruction of centre médian-parafascicular thalamic neurons in primates. J Comp Neurol 481(1):127–144PubMedCrossRefGoogle Scholar
  172. Parent M, Parent A (2016) The primate basal ganglia connectome as revealed by single-axon tracing. In: Rockland KS (ed) Axons and brain architecture. Elsevier, Amsterdam, pp 27–37CrossRefGoogle Scholar
  173. Parent A, Smith Y (1987a) Differential dopaminergic innervation of the two pallidal segments in the squirrel monkey (Saimiri sciureus). Brain Res 426(2):397–400PubMedCrossRefGoogle Scholar
  174. Parent A, Smith Y (1987b) Organization of efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res 436(2):296–310PubMedCrossRefGoogle Scholar
  175. Parent A, Gravel S, Olivier A (1979) The extrapyramidal and limbic systems relationship at the globus pallidus level: A comparative histochemical study in rat, cat and monkey. In: Poirier LJ, Sourkes TL, Bédard PJ (eds) The extrapyramidal system, its disorders. Raven Press, New York, pp 1–11Google Scholar
  176. Parent A, Mackey A, de Bellefeuille L (1983) The subcortical afferents to caudate nucleus and putamen in primate: a fluorescence retrograde double labeling study. Neuroscience 10(4):1137–1150PubMedCrossRefGoogle Scholar
  177. Parent A, Lavoie B, Smith Y, Bédard P (1990) The dopaminergic nigropallidal projection in primates: distinct cellular origin and relative sparing in MPTP-treated monkeys. Adv Neurol 53:111–116PubMedGoogle Scholar
  178. Parent A, Charara A, Pinault D (1995) Single striatofugal axons arborizing in both pallidal segments and in the substantia nigra in primates. Brain Res 698(1–2):280–284PubMedCrossRefGoogle Scholar
  179. Parent M, Lévesque M, Parent A (1999) The pallidofugal projection system in primates: evidence for neurons branching ipsilaterally and contralaterally to the thalamus and brainstem. J Chem Neuroanat 16(3):153–165PubMedCrossRefGoogle Scholar
  180. Parent M, Lévesque M, Parent A (2001) Two types of projection neurons in the internal pallidum of primates: single-axon tracing and three-dimensional reconstruction. J Comp Neurol 439(2):162–175PubMedCrossRefGoogle Scholar
  181. Parent M, Wallman MJ, Gagnon D, Parent A (2011) Serotonin innervation of basal ganglia in monkeys and humans. J Chem Neuroanat 41(4):256–265PubMedCrossRefGoogle Scholar
  182. Pasik P, Pasik T, Holstein GR, Saavedra JP (1984a) Serotoninergic innervation of the monkey basal ganglia: an immunocytochemical, light and electron microscopic study. In: McKenzie JS, Kenn RE, Wilcock LN (eds) The basal ganglia: structure and function. Plenum Press, New York, pp 115–129CrossRefGoogle Scholar
  183. Pasik P, Pasik T, Pecci-Saavedra J, Holstein GR, Yahr MD (1984b) Serotonin in pallidal neuronal circuits: an immunocytochemical study in monkeys. Adv Neurol 40:63–76PubMedGoogle Scholar
  184. Pellicano C, Assogna F, Cravello L, Langella R, Caltagirone C, Spalletta G, Pontieri FE (2015) Neuropsychiatric and cognitive symptoms and body side of onset of parkinsonism in unmedicated Parkinson’s disease patients. Parkinson Relat Disord 21(9):11096–11100CrossRefGoogle Scholar
  185. Penney JB, Young AB (1983) Speculations on the functional anatomy of basal ganglia disorders. Annu Rev Neurosci 6:73–94PubMedCrossRefGoogle Scholar
  186. Percheron G, Yelnik J, Francois C (1984) A Golgi analysis of the primate globus pallidus. III. Spatial organization of the striato-pallidal complex. J Comp Neurol 227(2):214–227PubMedCrossRefGoogle Scholar
  187. Politis M, Wu K, Loane C, Brooks DJ, Kiferle L, Turkheimer FE, Bain P, Molloy S, Piccini P (2014) Serotonergic mechanisms responsible for levodopa-induced dyskinesias in Parkinson’s disease patients. J Clin Investig 124(3):1340–1349PubMedPubMedCentralCrossRefGoogle Scholar
  188. Porritt M, Stanic D, Finkelstein D, Batchelor P, Lockhart S, Hughes A, Kalnins R, Howells D (2005) Dopaminergic innervation of the human striatum in Parkinson’s disease. Mov Disord 20(7):810–818PubMedCrossRefGoogle Scholar
  189. Prensa L, Parent A (2001) The nigrostriatal pathway in the rat: a single-axon study of the relationship between dorsal and ventral tier nigral neurons and the striosome/matrix striatal compartments. J Neurosci 21(18):7247–7260PubMedGoogle Scholar
  190. Prensa L, Cossette M, Parent A (2000) Dopaminergic innervation of human basal ganglia. J Chem Neuroanat 20:207–213PubMedCrossRefGoogle Scholar
  191. Qamhawi Z, Towey D, Shah B, Pagano G, Seibyl J, Marek K, Borghammer P, Brooks DJ, Pavese N (2015) Clinical correlates of raphe serotonergic dysfunction in early Parkinson’s disease. Brain 138:2964–2973PubMedCrossRefGoogle Scholar
  192. Quik M, Polonskaya Y, Gillespie A, Jakowec M, Lloyd GK, Langston JW (2000) Localization of nicotinic receptor subunit mRNAs in monkey brain by in situ hybridization. J Comp Neurol 425(1):58–69PubMedCrossRefGoogle Scholar
  193. Reijnders JSAM, Ehrt U, Weber WEJ, Aarsland D, Leentjens AFG (2008) A systematic review of prevalence studies of depression in Parkinson’s disease. Mov Disord 23(2):183–189PubMedCrossRefGoogle Scholar
  194. Riahi G, Morissette M, Parent M, Di Paolo T (2011) Brain 5-HT2A receptors in MPTP monkeys and levodopa-induced dyskinesias. Eur J Neurosci 33(10):1823–1831PubMedCrossRefGoogle Scholar
  195. Riahi G, Morissette M, Samadi P, Parent M, Di Paolo T (2013) Basal ganglia serotonin 1B receptors in parkinsonian monkeys with l-DOPA-induced dyskinesia. Biochem Pharmacol 86(7):970–978PubMedCrossRefGoogle Scholar
  196. Richfield EK, Young AB, Penney JB (1987) Comparative distribution of dopamine D-1 and D-2 receptors in the basal ganglia of turtles, pigeons, rats, cats, and monkeys. J Comp Neurol 262(3):446–463PubMedCrossRefGoogle Scholar
  197. Rinvik E, Grofova I, Hammond C, Féger J, Deniau JM (1979) A study of the afferent connections to the subthalamic nucleus in the monkey and the cat using the HRP technique. In: Poirier LJ, Sourkes TL, Bédard PJ (eds) Advances in neurology. Raven Press, New York, pp 53–70Google Scholar
  198. Rodrigo J, Fernández P, Bentura ML, de Velasco JM, Serrano J, Uttenthal O, Martínez-Murillo R (1998) Distribution of catecholaminergic afferent fibres in the rat globus pallidus and their relations with cholinergic neurons. J Chem Neuroanat 15(1):1–20PubMedCrossRefGoogle Scholar
  199. Rommelfanger KS, Wichmann T (2010) Extrastriatal dopaminergic circuits of the basal ganglia. Front Neuroanat 4(139):1–17Google Scholar
  200. Roš H, Magill PJ, Moss J, Bolam JP, Mena-Segovia J (2010) Distinct types of non-cholinergic pedunculopontine neurons are differentially modulated during global brain states. Neuroscience 170(1):78–91PubMedPubMedCentralCrossRefGoogle Scholar
  201. Rouse ST, Marino MJ, Bradley SR, Awad H, Wittmann M, Conn PJ (2000) Distribution and roles of metabotropic glutamate receptors in the basal ganglia motor circuit: implications for treatment of Parkinson’s disease and related disorders. Pharmacol Ther 88(3):427–435PubMedCrossRefGoogle Scholar
  202. Royce GJ, Mourey RJ (1985) Efferent connections of the centromedian and parafascicular thalamic nuclei: an autoradiographic investigation in the cat. J Comp Neurol 235(3):277–300PubMedCrossRefGoogle Scholar
  203. Ruskin DN, Bergstrom DA, Baek D, Freeman LE, Walters JR (2001) Cocaine or selective block of dopamine transporters influences multisecond oscillations in firing rate in the globus pallidus. Neuropsychopharmacology 25(1):28–40PubMedCrossRefGoogle Scholar
  204. Rylander D, Parent M, O’Sullivan SS, Dovero S, Lees AJ, Bezard E, Descarries L, Cenci MA (2010) Maladaptive plasticity of serotonin axon terminals in levodopa-induced dyskinesia. Ann Neurol 68(5):619–628PubMedCrossRefGoogle Scholar
  205. Sadikot AF, Parent A, François C (1992) Efferent connections of the centromedian and parafascicular thalamic nuclei in the squirrel monkey: a PHA-L study of subcortical projections. J Comp Neurol 315(2):137–159PubMedCrossRefGoogle Scholar
  206. Saint-Cyr JA, Ungerleider LG, Desimone R (1990) Organization of visual cortical inputs to the striatum and subsequent outputs to the pallido-nigral complex in the monkey. J Comp Neurol 298(2):129–156PubMedCrossRefGoogle Scholar
  207. Sari Y (2004) Serotonin receptors: from protein to physiological function and behavior. Neurosci Biobehav Rev 28(6):565–582PubMedCrossRefGoogle Scholar
  208. Sarter M, Bruno JP, Givens B (2003) Attentional functions of cortical cholinergic inputs: what does it mean for learning and memory? Neurobiol Learn Mem 80(3):245–256PubMedCrossRefGoogle Scholar
  209. Sato F, Lavallée P, Lévesque M, Parent A (2000a) Single-axon tracing study of neurons of the external segment of the globus pallidus in primate. J Comp Neurol 417(1):17–31PubMedCrossRefGoogle Scholar
  210. Sato F, Parent M, Levesque M, Parent A (2000b) Axonal branching pattern of neurons of the subthalamic nucleus in primates. J Comp Neurol 424(1):142–152PubMedCrossRefGoogle Scholar
  211. Saunders A, Oldenburg IA, Berezovskii VK, Johnson CA, Kingery ND, Elliott HL, Xie T, Gerfen CR, Sabatini BL (2015) A direct GABAergic output from the basal ganglia to frontal cortex. Nature 521(7550):85–89PubMedPubMedCentralCrossRefGoogle Scholar
  212. Schneider JS, Dacko S (1991) Relative sparing of the dopaminergic innervation of the globus pallidus in monkeys made hemi-parkinsonian by intracarotid MPTP infusion. Brain Res 556(2):292–296PubMedCrossRefGoogle Scholar
  213. Schröder K, Hopf A, Lange H, Thörner G, Thörner G (1975) Morphometrisch-statistische strukturanalysen des striatum, pallidum un nucleus subthalamicus bei memschen. J Hirnforsch 16(4):222–250Google Scholar
  214. Schultz W, Apicella P, Scarnati E, Ljungberg T (1992) Neuronal activity in monkey ventral striatum related to the expectation of reward. J Neurosci 12(12):4595–4610PubMedGoogle Scholar
  215. Selemon LD, Goldman-Rakic PS (1990) Topographic intermingling of striatonigral and striatopallidal neurons in the rhesus monkey. J Comp Neurol 297(3):359–376PubMedCrossRefGoogle Scholar
  216. 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(3):387–410PubMedCrossRefGoogle Scholar
  217. Shabel SJ, Proulx CD, Trias A, Murphy RT, Malinow R (2012) Input to the lateral habenula from the basal ganglia is excitatory, aversive, and suppressed by serotonin. Neuron 74(3):475–481PubMedPubMedCentralCrossRefGoogle Scholar
  218. Shink E, Smith Y (1995) Differential synaptic innervation of neurons in the internal and external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey. J Comp Neurol 358(1):119–141PubMedCrossRefGoogle Scholar
  219. Shink E, Bevan MD, Bolam JP, Smith Y (1996) The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in the monkey. Neuroscience 73(2):335–357PubMedCrossRefGoogle Scholar
  220. Sidibé M, Bevan MD, Bolam JP, Smith Y (1997) Efferent connections of the internal globus pallidus in the squirrel monkey: I. Topography and synaptic organization of the pallidothalamic projection. J Comp Neurol 382(3):323–347PubMedCrossRefGoogle Scholar
  221. Smith Y, Bolam JP (1989) Neurons of the substantia nigra reticulata receive a dense GABA-containing input from the globus pallidus in the rat. Brain Res 493(1):160–167PubMedCrossRefGoogle Scholar
  222. Smith Y, Bolam JP (1990) The output neurones and the dopaminergic neurones of the substantia nigra receive a GABA-containing input from the globus pallidus in the rat. J Comp Neurol 296(1):47–64PubMedCrossRefGoogle Scholar
  223. Smith Y, Bolam JP (1991) Convergence of synaptic inputs from the striatum and the globus pallidus onto identified nigrocollicular cells in the rat: a double anterograde labelling study. Neuroscience 44(1):45–73PubMedCrossRefGoogle Scholar
  224. Smith Y, Parent A (1986) Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18(2):347–371PubMedCrossRefGoogle Scholar
  225. Smith Y, Parent A (1988) Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res 453(1–2):353–356PubMedGoogle Scholar
  226. Smith Y, Villalba R (2008) Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov Disord 23(S3):S534–S547PubMedCrossRefGoogle Scholar
  227. Smith Y, Wichmann T (2014) The cortico-pallidal projection: an additional route for cortical regulation of the basal ganglia circuitry. Mov Disord 30(3):293–295PubMedPubMedCentralCrossRefGoogle Scholar
  228. Smith Y, Parent A, Seguela P, Descarries L (1987) Distribution of GABA-immunoreactive neurons in the basal ganglia of the squirrel monkey (Saimiri sciureus). J Comp Neurol 259(1):50–64PubMedCrossRefGoogle Scholar
  229. Smith Y, Lavoie B, Dumas J, Parent A (1989) Evidence for a distinct nigropallidal dopaminergic projection in the squirrel monkey. Brain Res 482(2):381–386PubMedCrossRefGoogle Scholar
  230. Smith Y, Wichmann T, DeLong MR (1994) Synaptic innervation of neurones in the internal pallidal segment by the subthalamic nucleus and the external pallidum in monkeys. J Comp Neurol 343(2):297–318PubMedCrossRefGoogle Scholar
  231. Smith Y, Charara A, Hanson JE, Paquet M, Levey AI (2000) GABA(B) and group I metabotropic glutamate receptors in the striatopallidal complex in primates. J Anat 196:555–576PubMedPubMedCentralCrossRefGoogle Scholar
  232. Smith R, Wu K, Hart T, Loane C, Brooks D, Björklund A, Odin P, Piccini P, Politis M (2015) The role of pallidal serotonergic function in Parkinson’s disease dyskinesias: a positron emission tomography study. Neurobiol Aging 36:1736–1742PubMedCrossRefGoogle Scholar
  233. Stanford IM, Kantaria MA, Chahal HS, Loucif KC, Wilson CL (2005) 5-Hydroxytryptamine induced excitation and inhibition in the subthalamic nucleus: action at 5-HT(2C), 5-HT(4) and 5-HT(1A) receptors. Neuropharmacology 49(8):1228–1234PubMedCrossRefGoogle Scholar
  234. Sutoo D, Akiyama K, Yabe K, Kohno K (1994) Quantitative analysis of immunohistochemical distributions of cholinergic and catecholaminergic systems in the human brain. Neuroscience 58(1):227–234PubMedCrossRefGoogle Scholar
  235. Tremblay PL, Bedard MA, Langlois D, Blanchet PJ, Lemay M, Parent M (2010) Movement chunking during sequence learning is a dopamine-dependant process: a study conducted in Parkinson’s disease. Exp Brain Res 205(3):375–385PubMedCrossRefGoogle Scholar
  236. Tremblay L, Worbe Y, Thobois S, Sgambato-Faure V, Féger J (2015) Selective dysfunction of basal ganglia subterritories: from movement to behavioral disorders. Mov Disord 30(9):1155–1170PubMedCrossRefGoogle Scholar
  237. Varnäs K, Hall H, Bonaventure P, Sedvall G (2001) Autoradiographic mapping of 5-HT(1B) and 5-HT(1D) receptors in the post mortem human brain using [(3)H]GR 125743. Brain Res 915(1):47–57PubMedCrossRefGoogle Scholar
  238. Varnäs K, Halldin C, Hall H (2004) Autoradiographic distribution of serotonin transporters and receptor subtypes in human brain. Hum Brain Mapp 22(3):246–260PubMedCrossRefGoogle Scholar
  239. Varnäs K, Hurd YL, Hall H (2005) Regional expression of 5-HT1B receptor mRNA in the human brain. Synapse 56(1):21–28PubMedCrossRefGoogle Scholar
  240. Varnäs K, Nyberg S, Halldin C, Varrone A, Takano A, Karlsson P, Andersson J, McCarthy D, Smith M, Pierson ME, Söderström J, Farde L (2010) Quantitative analysis of [11C]AZ10419369 binding to 5-HT1B receptors in human brain. J Cereb Blood Flow Metab 31(1):113–123PubMedPubMedCentralCrossRefGoogle Scholar
  241. Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313(4):643–668PubMedCrossRefGoogle Scholar
  242. Vicente AM, Costa RM (2012) Looking at the trees in the central forest: a new pallidal–striatal cell type. Neuron 74(6):967–969PubMedCrossRefGoogle Scholar
  243. Vonsattel JP, Myers RH, Stevens TJ, Ferrante RJ, Bird ED, Richardson EP Jr (1985) Neuropathological classification of Huntington’s disease. J Neuropathol Exp Neurol 44(6):559–577PubMedCrossRefGoogle Scholar
  244. Waldvogel HJ, Kubota Y, Fritschy J, Mohler H, Faull RL (1999) Regional and cellular localisation of GABA(A) receptor subunits in the human basal ganglia: an autoradiographic and immunohistochemical study. J Comp Neurol 415(3):313–340PubMedCrossRefGoogle Scholar
  245. Waldvogel HJ, Billinton A, White JH, Emson PC, Faull RLM (2004) Comparative cellular distribution of GABAA and GABAB receptors in the human basal ganglia: immunohistochemical colocalization of the alpha-1 subunit of the GABAA receptor, and the GABABR1 and GABABR2 receptor subunits. J Comp Neurol 470(4):339–356PubMedCrossRefGoogle Scholar
  246. Wallman MJ, Gagnon D, Parent M (2011) Serotonin innervation of human basal ganglia. Eur J Neurosci 33(8):1519–1532PubMedCrossRefGoogle Scholar
  247. Whone AL, Moore RY, Piccini PP, Brooks DJ (2003) Plasticity of the nigropallidal pathway in Parkinson’s disease. Annals of Neurology 53(2):206–213PubMedCrossRefGoogle Scholar
  248. Willis T (1664) Cerebri anatome: Cui accessit nervorum descriptio et usus. Martyn & Allestry, LondonGoogle Scholar
  249. Woolf NJ, Butcher LL (1986) Cholinergic systems in the rat brain: III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia, and basal forebrain. Brain Res Bull 16(5):603–637PubMedCrossRefGoogle Scholar
  250. Yan Z, Flores-Hernandez J, Surmeier DJ (2001) Coordinated expression of muscarinic receptor messenger RNAs in striatal medium spiny neurons. Neuroscience 103(4):1017–1024PubMedCrossRefGoogle Scholar
  251. Yelnik J, Percheron G, François C (1984) A Golgi analysis of the primate globus pallidus. II. Quantitative morphology and spatial orientation of dendritic arborizations. J Comp Neurol 227(2):200–213PubMedCrossRefGoogle Scholar
  252. Yoshida A, Tanaka M (2016) Two types of neurons in the primate globus pallidus external segment play distinct roles in antisaccade generation. Cereb Cortex 26(3):1187–1199PubMedCrossRefGoogle Scholar
  253. Young AB, Dauth GW, Hollingsworth Z, Penney JB, Kaatz K, Gilman S (1990) Quisqualate- and NMDA-sensitive [3H]glutamate binding in primate brain. J Neurosci Res 27(4):512–521PubMedCrossRefGoogle Scholar
  254. Zeng BY, Iravani MM, Jackson MJ, Rose S, Parent A, Jenner P (2010) Morphological changes in serotoninergic neurites in the striatum and globus pallidus in levodopa primed MPTP treated common marmosets with dyskinesia. Neurobiol Dis 40(3):599–607PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2016

Authors and Affiliations

  1. 1.Department of Psychiatry and Neuroscience, Faculty of Medicine, Centre de recherche de l’Institut universitaire en santé mentale de Québec (CRIUSMQ)Université LavalQuebecCanada

Personalised recommendations