The subthalamic nucleus and the external pallidum: Two tightly interconnected structures that control the output of the basal ganglia in the monkey

Neuroscience

Volumn 73, Issue 2, 1996, Pages 335-357

  Shink, E ^b   Bevan, M D ^a   Bolam, J P ^a   Smith, Y ^b  

^a MRC Anat Neuropharmacology Unit   (United Kingdom)

^b NONE

Author keywords

basal ganglia; pallidosubthalamic pathway; pallidum; post embedding immunocytochemistry; subthalamopallidal pathway; tract tracing method

Indexed keywords

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; CONTROLLED STUDY; ELECTRON MICROSCOPY; GLOBUS PALLIDUS; HISTOCHEMISTRY; IMMUNOCYTOCHEMISTRY; MALE; MONKEY; NERVE CELL NETWORK; NONHUMAN; PRIORITY JOURNAL; SUBTHALAMIC NUCLEUS;

EID: 0030014312     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/0306-4522(96)00022-X     Document Type: Article

References (77)

1. Alexander G. E., DeLong M. R. and Strick P. L. (1986) Parallel organization of functionally segregated circuits linking basal ganglia and cortex. A. Rev. Neurosci. 9, 357-381.
2. Alexander G. E. and Crutcher M. D. (1990) Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. 13, 266-271.
3. Aziz T. Z., Peggs D., Sambrook M. A. and Crossman A. R. (1991) Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinsonism in the primate. Mov. Disorders 6, 288-292.
4. Bergman H. and DeLong M. R. (1989) Electro-physiological studies of the connections of the subthalamic nucleus and globus pallidus in behaving monkeys. Soc. Neurosci. 15, 902.
5. Bergman H., Wichmann T. and DeLong M. R. (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249, 1436-1438.
6. Bevan M. D., Bolam J. P. and Crossman A. R. (1994) Convergent synaptic input from the neostriatum and the subthalamus onto identified nigrothalamic neurons in the rat. Eur. J. Neurosci. 6, 320-334.
7. Bevan M. D., Crossman A. R. and Bolam J. P. (1994) Neurons projecting from the entopeduncular nucleus to the thalamus receive convergent synaptic inputs from the subthalamic nucleus and the neostriatum in the rat. Brain Res. 659, 99-109.
8. Bolam J. P. and 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 post-embedding immunocytochemistry for GABA. J. comp. Neurol. 321, 456-476.
9. Brandt H. M. and Apkarian A. V. (1992) Biotin-dextran: a sensitive anterograde tracer for neuroanatomic studies in rat and monkey. J. Neurosci. Meth. 45, 35-40.
10. Brotchie P., Iansek R. and Horne M. K. (1991) Motor function of the monkey globus pallidus. 1. Neuronal discharge and parameters of movement. Brain 114, 1667-1683.
11. Carpenter M. B., Batton R. R. III, Carleton S. C. and Keller J. T. (1981) Interconnections and organization of pallidal and subthalamic nucleus neurons in the monkey. J. comp. Neurol. 197, 579-603.
12. Chang H. T., Wilson C. J. and Kitai S. T. (1981) Single neostriatal efferent axons to the globus pallidus: a light and electron microscopic study. Science 213, 915-918.
13. Dale N., Ottersen O. P., Roberts A. and Storm-Mathisen J. (1986) Inhibitory neurones of a motor pattern generator in Xenopus revealed by antibodies to glycine. Nature 324, 255-257.
14. DeLong M. R. (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 13, 281-285.
15. DeVito J. L. and Anderson M. E. (1982) An autoradiographic study of efferent connections of the globus pallidus in Macaca mulatta. Expl Brain Res. 46, 107-117.
16. DeVito J. L., Anderson M. E. and Walsh K. E. (1980) A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta. Expl Brain Res. 38, 65-73.
17. Emmers R. and Akert K. (1963) A Stereotaxic Atlas of the Brain of the Squirrel Monkey (Saimiri sciureus). University of Wisconsin Press, Madison.
18. Féger J. and Robledo P. (1991) The effects of activation or inhibition of the subthalamic nucleus on the metabolic and electrophysiological activities within the pallidal complex and substantia nigra in the rat. Eur. J. Neurosci. 3, 947-952.
19. Fink-Jensen A. and Mikkelsen J. D. (1991) A direct projection from the entopeduncular nucleus to the globus pallidus. A PHA-L anterograde tracing study in the rat. Brain Res. 542, 175-179.
20. Flaherty A. W. and Graybiel A. M. (1993) Output architecture of the primate putamen. J. Neurosci. 13, 3222-3237.
21. Fujimoto K. and Kita H. (1992) Responses of rat substantia nigra pars reticulata units to cortical stimulation. Neurosci. Lett. 142, 105-109.
22. Georgopoulos A. P., DeLong M. R. and Crutcher M. D. (1983) Relations between parameters of step-tracking movements and single cell discharge in the globus pallidus and subthalamic nucleus of the behaving monkey. J. Neurosci. 3, 1586-1598.
23. Gerfen C. R. (1985) The neostriatal mosaic: I. Compartmental organization of projections from the striatum to the substantia nigra in the rat. J. comp. Neurol. 236, 454-476.
24. Gerfen C. R. and Sawchenko P. E. (1984) An anterograde neuroanatomical tracing method that shows the detailed morphology of neurons, their axons and terminals: immunohistochemical localization of an axonally transported plant lectin, Phaseolus vulgaris-leucoagglutinin (PHA-L). Brain Res. 290, 219-238.
25. Groenewegen H. J., Berendse H. W. and Haber S. N. (1993) Organization of the output of the ventral striatopallidal system in the rat: ventral pallidal efferents. Neuroscience 57, 113-142.
26. Haber S. N., Lyn-Balta E. and Mitchell S. J. (1993) The organization of the descending ventral pallidal projections in the monkey. J. comp. Neurol. 329, 111-128.
27. Hamada I. and DeLong M. R. (1992) Excitotoxic acid lesions of the primate subthalamic nucleus result in reduced pallidal neuronal activity during active holding. J. Neurophysiol. 68, 1859-1866.
28. Hazrati L.-N. and Parent A. (1992) The striatopallidal projection displays a high degree of anatomical specificity in the primate. Brain Res. 592, 213-227.
29. Hazrati L.-N. and Parent A. (1992) Convergence of subthalamic and striatal efferents at pallidal level in primates: an anterograde double-labeling study with biocytin and PHA-L. Brain Res. 569, 336-340.
30. Hazrati L.-N., Parent A., Mitchell S. and Haber S. N. (1990) Evidence for interconnections between the two segments of the globus pallidus in primates: a PHA-L anterograde tracing study. Brain Res. 533, 171-175.
31. Hodgson A. J., Penke B., Erdei A., Chubb I. W. and Somogyi P. (1985) Antisera to γ-aminobutyric acid. I. Production and characterization using a new model system. J. Histochem. Cytochem. 33, 229-239.
32. Kawaguchi Y., Wilson C. J. and Emson P. C. (1990) Projection subtypes of rat neostriatal matrix cells revealed by intracellular injection of biocytin. J. Neurosci. 10, 3421-3438.
33. Kim R., Nakano K., Jayaraman A. and Carpenter M. B. (1976) Projections of the globus pallidus and adjacent structures: an autoradiographic study in the moneky. J. comp. Neurol. 169, 263-290.
34. Kincaid A. E., Newman S. W., Young A. B. and Penney J. B. (1990) Evidence for a projection from the globus pallidus to the entopeduncular nucleus in the rat. Neurosci. Lett. 128, 121-125.
35. Kisvarday Z. F. and Eysel U. T. (1992) Cellular organization of reciprocal patchy networks in layer III of cat visual cortex (area 17). Neuroscience 46, 275-286.
36. Kita H. (1993) Physiology of two disynaptic pathways from the sensorimotor cortex to the basal ganglia output nuclei. In The Basal Ganglia IV - New Ideas and Data on Structure and Function (eds Percheron G., McKenzie J. S. and Féger J.), pp. 263-276. Plenum, New York.
37. Kita H., Chang H. T. and Kitai S. T. (1983) The morphology of intracellularly labeled rat subthalamic neurons: a light microscopic analysis. J. comp. Neurol. 215, 245-257.
38. Kita H. and Kitai S. T. (1987) Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. comp. Neurol. 260, 435-452.
39. Kita H. and Kitai S. T. (1994) The morphology of globus pallidus projection neurons in the rat: an intracellular staining study. Brain Res. 636, 308-319.
40. Kitai S. T. and Kita H. (1987) Dual striatonigral inhibitory actions. In Proceedings of the International Conference Neural Mechanisms of Disorders of Movement, p. 21. Manchester, U.K.
41. Kitai S. T. and Kita H. (1987) Anatomy and physiology of the subthalamic nucleus: a driving force of the basal ganglia. In The Basal Ganglia II - Structure and Function: Current Concepts (eds Carpenter M. B. and Jayaraman A.), pp. 357-373. Plenum, New York.
42. Mink J. W. and Thach W. T. (1991) Basal ganglia motor control. III. Pallidal ablation: normal reaction time, muscle cocontraction, and slow movement. J. Neurophysiol. 65, 330-351.
43. Mink J. W. and Thach W. T. (1993) Basal ganglia intrinsic circuits and their role in behavior. Curr. Opin. Neurobiol. 3, 950-957.
44. Mitchell S. J., Richardson R. T., Baker F. H. and DeLong M. R. (1987) The primate globus pallidus: neuronal activity related to direction of movement. Expl Brain Res. 68, 491-505.
45. Nauta H. J. W. and Cole M. (1978) Efferent projections of the subthalamic nucleus: an autoradiographic study in monkey and cat. J. comp. Neurol. 180, 1-16.
46. Nini A., Feingold A., Slovin H. and Bergman H. (1995) Neurons in the globus pallidus do not show correlated activity in the normal monkey, but phase-locked oscillations appear in the MPTP model of parkinsonism. J. Neurophysiol. 74, 1800-1805.
47. Parent A. (1990) Extrinsic connections of the basal ganglia. Trends Neurosci. 13, 254-258.
48. Parent A. and Hazrati L.-N. (1993) Anatomical aspects of information processing in primate basal ganglia. Trends Neurosci. 16, 111-116.
49. Parent A. and Smith Y. (1987) Organization of the efferent projections of the subthalamic nucleus in the squirrel monkey as revealed by retrograde labeling methods. Brain Res. 436, 296-310.
50. Parent A., Smith Y., Filion M. and Dumas J. (1989) Distinct afferents to internal and external pallidal segments in the squirrel monkey. Neurosci. Lett. 96, 140-144.
51. Phend K. D., Weinberg R. J. and Rustioni A. (1992) Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J. Histochem. Cytochem. 40, 1011-1020.
52. Rajakumar N., Elisevich K. and Flumerfelt B. A. (1993) Biotinylated dextran: a versatile anterograde and retrograde neuronal tracer. Brain Res. 607, 47-53.
53. Reiner A., Veenman C. L. and Honig M. G. (1993) Anterograde tracing using biotinylated dextran amine. Neurosci. Protocols 93-050-14-01.
54. Reynolds E. S. (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J. Cell Biol. 17, 208-212.
55. Rinvik E. and Ottersen O. P. (1993) Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: an electron microscopic, immunogold analysis in the cat. J. chem. Neuroanat. 6, 19-30.
56. Rouzaire-Dubois B., Hammond C., Yelnik J. and Féger J. (1984) Anatomy and neurophysiology of subthalamic efferent neurons. In The Basal Ganglia, Structure and Function (eds Kemm R. E. and Wilcock L. N.), pp. 205-234. Plenum, New York.
57. Shink E. and Smith Y. (1995) Differential synaptic innervation of neurones in the internal and the external segments of the globus pallidus by the GABA- and glutamate-containing terminals in the squirrel monkey. J. comp. Neurol. 358, 119-141.
58. Smith Y. and Bolam J. P. (1989) Neurons of the substantia nigra reticulata receive a dense GABA-containing input from the globus pallidus in the rat. Brain Res. 493, 160-167.
59. Smith Y. and Bolam J. P. (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, 47-64.
60. Smith Y. and Bolam J. P. (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, 45-73.
61. Smith Y., Bolam J. P. and von Krosigk M. (1990) Topographical and synaptic organization of the GABA-containing pallidosubthalamic projection in the rat. Eur. J. Neurosci. 2, 500-511.
62. Smith Y., Hazrati L.-N. and Parent A. (1990) Efferent projections of the subthalamic nucleus in the squirrel monkey as studied by the PHA-L anterograde tracing method. J. comp. Neurol. 294, 306-323.
63. Smith Y. and Parent A. (1986) Differential connections of caudate nucleus and putamen in the squirrel monkey (Saimiri sciureus). Neuroscience 18, 347-371.
64. Smith Y., Parent A. and Dumas J. (1988) Organization of efferent connections of the two pallidal segments in primate as revealed by PHA-L anterograde tracing method. Soc. Neurosci. 14, 719.
65. Smith Y., Shink E., Bevan M. D. and Bolam J. P. (1995) The subthalamic nucleus and the external pallidum: two tightly interconnected structures that control the output of the basal ganglia in primates. Brain Res. Ass. Abstr. 12, 89.
66. Smith Y., Sidibé M. and Shink E. (1994) A light and electron microscopic analysis of the interconnections between the two pallidal segments and the subthalamic nucleus in the squirrel monkey. Soc. Neurosci. 20, 332.
67. Smith Y., Wichmann T. and DeLong M. R. (1993) The external pallidum and the subthalamic nucleus send convergent synaptic inputs onto single neurones in the internal pallidal segment in monkey: anatomical organization and functional significance. In The Basal Ganglia IV: New Ideas and Data on Structure and Function (eds Percheron G., McKenzie J. S. and Féger J.), pp. 51-62. Plenum, New York.
68. Smith Y., Wichmann T. and DeLong M. R. (1994b) Synaptic innervation of neurones in the internal pallidal segment by the subthalamic nucleus and the external pallidum in monkeys. J. comp. Neurol. 343, 297-318.
69. Somogyi P. and Hodgson A. J. (1985) Antisera to γ-aminobutyric acid. III. Demonstration of GABA in Golgi-impregnated neurons and in conventional electron microscopic sections of cat striate cortex. J. Histochem. Cytochem. 33, 249-257.
70. Somogyi P., Hodgson A. J., Chubb I. W., Penke B. and Erdei A. (1985) Antisera to γ-aminobutyric acid. II. Immunocytochemical application to the central nervous system. J. Histochem. Cytochem. 33, 240-248.
71. Staines W. A. (1988) PHA-L studies of the efferent connections of the rat globus pallidus. Soc. Neurosci. Abstr. 16, 427.
72. Veenman C. L., Reiner A. and Honig M. G. (1992) Biotinylated dextran amine as an anterograde tracer for single-and double-labeling studies. J. Neurosci. Meth. 41, 239-254.
73. Von Krosigk M., Smith Y., Bolam J. P. and Smith A. D. (1992) Synaptic organization of GABAergic inputs from the striatum and the globus pallidus onto neurons in the substantia nigra and retrorubral field which project to the medullary reticular formation. Neuroscience 50, 531-549.
74. Von Monakow K. H., Akert K. and Künzle H. (1978) Projections of the precentral motor cortex and other cortical areas of the frontal lobe to the subthalamic nucleus in the monkey. Expl Brain Res. 33, 395-403.
75. Wichmann T., Bergman H. and DeLong M. R. (1994) The primate subthalamic nucleus. I. Functional properties in intact animals. J. Neurophysiol. 72, 494-506.
76. Wichmann T., Bergman H. and DeLong M. R. (1994) The primate subthalamic nucleus. III. Changes in motor behavior and neuronal activity in the internal pallidum induced by subthalamic inactivation in the MPTP model of Parkinsonism. J. Neurophysiol. 72, 521-530.
77. Wilson C. J. and Phelan K. D. (1982) Dual topographic representation of neostriatum in the globus pallidus of rats. Brain Res. 243, 354-359.