Glutamate-enriched cholinergic synaptic terminals in the entopeduncular nucleus and subthalamic nucleus of the rat

Neuroscience

Volumn 81, Issue 2, 1997, Pages 371-385

  Clarke, N P ^a   Bevan, M D ^a   Cozzari, C ^b   Hartman, B K ^c   Bolam, J P ^a  

^a MRC Anat Neuropharmacology Unit   (United Kingdom)

^b CNR   (Italy)

^c UNIVERSITY OF MINNESOTA   (United States)

Author keywords

Acetylcholine; Basal ganglia; Choline acetyltransferase; GABA; Glutamate

Indexed keywords

4 AMINOBUTYRIC ACID; AVIDIN; BIOTIN; GLUTAMIC ACID; PEROXIDASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; ELECTRON MICROSCOPY; ENTOPEDUNCULAR NUCLEUS; ENZYME ACTIVITY; GABAERGIC TRANSMISSION; IMMUNOCYTOCHEMISTRY; IMMUNOGOLD STAINING; IMMUNOREACTIVITY; NONHUMAN; PRIORITY JOURNAL; RAT; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

ANIMALS; BASAL GANGLIA; CHOLINERGIC FIBERS; GLUTAMIC ACID; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, ELECTRON; PRESYNAPTIC TERMINALS; RATS; RATS, SPRAGUE-DAWLEY; THALAMIC NUCLEI;

EID: 0031559963     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0306-4522(97)00247-9     Document Type: Article

References (88)

1. Abdullah L. H., Ordronneau P., Petrusz P. Molecular requirements for hapten binding to antibodies against glutamate and aspartate. Neuroscience. 51:1992;729-738.
2. Aziz T. Z., Peggs D., Sambrook M. A., Crossman A. R. Lesion of the subthalamic nucleus for the alleviation of 1-methyl-4-phenyl-1,2,3,6,-tetrahydropridine (MPTP)-induced parkinsonism in the primate. Movement Disord. 6:1991;288-292.
3. Baron M. S., Vitek J. L., Bakay R. A. E., Green J., Kaneoke Y., Hashimoto T., Turner R. S., Woodard J. L., Cole S. A., McDonald W. M., DeLong M. R. Treatment of advanced Parkinson's Disease by posterior GPi Pallidotomy: 1-Year results of a pilot study. Ann. Neurol. 40:1996;355-366.
4. Bartfai T., Iverfeldt K., Fisone G., Serfozo P. Regulation of release of coexisting transmitters. A. Rev. Pharmac. 28:1988;285-310.
5. Beaulieu C., Somogyi P. Enrichment of cholinergic synaptic terminals on GABAergic neurons and coexistence of immunoreactive GABA and choline acetyltransferase in the same synaptic terminals in the striate cortex of the cat. J. comp. Neurol. 304:1991;666-680.
6. Benazzouz A., Gross C., Féger J., Boraud T., Bioulac B. Reversal of rigidity and improvement in motor performance by subthalamic high-frequency stimulation in MPTP-treated monkeys. Eur. J. Neurosci. 5:1993;382-389.
7. Bergman H., Wichmann T., DeLong M. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science. 249:1990;1436-1438.
8. 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. 15:1995;7105-7120.
9. Bevan M. D., Bolam J. P., Crossman A. R. Convergent synaptic input from the neostriatum and the subthalamus onto identified nigrothalamic neurons in the rat. Eur. J. Neurosci. 6:1994;320-334.
10. Bevan M. D., Clarke N. P., Bolam J. P. Synaptic integration of functionally diverse pallidal information in the entopeduncular nucleus and subthalamic nucleus of the rat. J. Neurosci. 17:1997;308-324.
11. Bevan M. D., Crossman A. R., Bolam J. P. 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. 659:1994;99-109.
12. Bevan M. D., Francis C. M., Bolam J. P. The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: Convergence with GABA-positive terminals. J. comp. Neurol. 361:1995;491-511.
13. Blomqvist A., Ericson A.-C., Craig A. D., Broman J. Evidence for glutamate as a neurotransmitter in spinothalamic tract terminals in the posterior region of owl monkeys. Expl Brain Res. 108:1996;33-44.
14. Bolam J. P. (1992) Preparation of CNS tissue for light and electron microscopy. In Experimental Neuroanatomy - A Practical Approach (ed. Bolam J. P.), pp. 1-29. Oxford University Press, Oxford.
15. Bolam J. P., Smith Y. The striatum and the globus pallidus send convergent synaptic inputs onto single cells in the entopeduncular nucleus of the rat: a double anterograde labeling study combined with post-embedding immunocytochemistry for GABA. J. comp. Neurol. 321:1992;456-476.
16. Bolam J. P., Smith Y., Ingham C. A., von Krosigk M. and Smith A. D. (1993) Convergence of synaptic terminals from the striatum and the globus pallidus onto single neurones in the substantia nigra and the entopeduncular nucleus. In Chemical Signalling in the Basal Ganglia (eds Arbuthnott G. W. and Emson P. C.), Vol. 99, pp. 73-88. Elsevier Science Publishers, Oxford.
17. Brotchie J. M., Mitchell I. J., Sambrook M. A., Crossman A. R. Alleviation of parkinsonism by antagonism of excitatory amino acid transmission in the medial segment of the globus pallidus in rat and primate. Movement Disord. 6:1991;133-138.
18. Canteras N. S., Shammah-Lagnado S. J., Silva B. A., Ricardo J. A. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res. 513:1990;43-59.
19. Charara A., Parent A. Brainstem dopaminergic, cholinergic and serotoninergic afferents to the pallidum in the squirrel monkey. Brain Res. 640:1994;155-170.
20. Chedotal A., Umbriaco D., Descarries L., Hartman B. K., Hamel E. Light and electron microscopic immunocytochemical analysis of the neurovascular relationships of choline acetyltransferase and vasoactive intestinal polypeptide nerve terminals in the rat cerebral cortex. J. comp. Neurol. 343:1994;57-71.
21. Clarke N. P., Bevan M. D., Cozzari C., Hartman B. K., Bolam J. P. Glutamate-enriched cholinergic terminals in the basal ganglia. Soc. Neurosci. Abstr. 22:1996;893.
22. Clarke N. P. and Bolam J. P. (1997) Co-localization of neurotransmitters in the basal ganglia. Br. J. Pharmac. 120, 281 P.
23. Clarke N. P., Bolam J. P., Bevan M. D. Glutamate-enriched inputs from the mesopontine tegmentum to the entopeduncular nucleus in the rat. Eur. J. Neurosci. 8:1996;1363-1376.
24. Clements J. R., Grant S. Glutamate-like immunoreactivity in neurons of the laterodorsal tegmental and pedunculopontine nuclei in the rat. Neurosci. Lett. 120:1990;70-73.
25. Clements J. R., Grant S. R. Glutamate and acetylcholine are co-localized in the lateral dorsal tegmental and pedunculopontine nuclei. Soc. Neurosci. Abstr. 16:1990;1189.
26. Clements J. R., Toth D. D., Highfield D. A., Grant S. J. Glutamate-like immunoreactivity is present within cholinergic neurons of the laterodorsal tegmental and pedunculopontine nuclei. Adv. exp. med. Biol. 295:1991;127-142.
27. Cozzari C., Howard J., Hartman B. Analysis of epitopes on choline acetyltransferase (ChAT) using monoclonal antibodies (Mabs). Soc. Neurosci. Abstr. 16:1990;200.
28. DeLong M. R. Activity of pallidal neurons during movement. J. Neurophysiol. 34:1971;414-427.
29. DeLong M. R. The pathophysiology of parkinsonism. Brain Res. Ass. Abstr. 12:1995;64.
30. DeVito J. L., Anderson M. E., Walsh K. E. A horseradish peroxidase study of afferent connections of the globus pallidus in Macaca mulatta. Expl Brain Res. 38:1980;65-73.
31. Docherty M., Bradford H. F., Wu J.-Y. Co-release of glutamate and aspartate from cholinergic and GABAergic synaptosomes. Nature. 330:1987;64-66.
32. Ericson A.-M., Blomqvist A., Craig A. D., Ottersen O. P., Broman J. Evidence for glutamate as neurotransmitter in trigemino- and spinothalamic tract terminals in the nucleus submedius of cats. Eur. J. Neurosci. 7:1995;305-317.
33. Filion M., Tremblay L. Abnormal spontaneous activity of of globus pallidus neurons in monkeys with MPTP-induced parkinsonism. Brain Res. 547:1991;142-151.
34. Ford B., Holmes C. J., Mainville L., Jones B. E. GABAergic neurons in the rat pontomesencephalic tegmentum: Codistribuiton with cholinergic and other tegmental neurons projecting to the posterior lateral hypothalamus. J. comp. Neurol. 363:1995;177-196.
35. Freund T. F. GABAergic septohippocampal neurons contain parvalbumin. Brain Res. 478:1989;375-381.
36. Garcia-Rill E. The pedunculopontine nucleus. Prog. Neurobiol. 36:1991;363-389.
37. Gonya-Magee T., Anderson M. E. An electrophysiological characterization of projections from the pedunculopontine area to entopeduncular nucleus and globus pallidus in the cat. Expl Brain Res. 49:1983;269-279.
38. Graybiel A. M. Direct and indirect preoculomotor pathways of the brainstem: An autoradiographic study of the pontine reticular formation in the cat. J. comp. Neurol. 175:1977;37-78.
39. Groenewegen H. J., Berendse H. W. Connections of the subthalamic nucleus with ventral striatopallidal parts of the basal ganglia in the rat. J. comp. Neurol. 294:1990;607-622.
40. Hepler J. R., Toomim C. S., McCarthy K. D., Conti F., Battaglia G., Rustioni A., Petrusz P. Characterization of antisera to glutamate and aspartate. J. Histochem. Cytochem. 36:1988;13-22.
41. Hodgson A. J., Penke B., Erdei A., Chubb I. W., Somogyi P. Antisera to γ-aminobutyric acid. I Production and characterization using a new model system. J. Histochem. Cytochem. 33:1985;229-239.
42. Israel M., Lesbats B., Bruner J. Glutamate and acetylcholine release from cholinergic nerve terminals, a calcium control of the specificity of the release mechanism. Neurochem. Int. 22:1993;53-58.
43. Jackson A., Crossman A. R. Nucleus tegmenti pedunculopontinus: Efferent connections with special reference to the basal ganglia, studied in the rat by anterograde and retrograde transport of horseradish peroxidase. Neuroscience. 10:1983;725-765.
44. Ji Z., Aas J.-E., Laake J., Walberg F., Ottersen O. P. An electron microscopic, immunogold analysis of glutamate and glutamine in terminals of rat spinocerebellar fibers. J. comp. Neurol. 307:1991;296-310.
45. Johnson N. L. Some simple tests of mixtures with symmetrical components. Communications in Statistics. 1:1973;17-25.
46. Jones B. E. Relationship of GABAergic to cholinergic neurons within the laterodorsal and pedunculopontine tegmental nuclei. Soc. Neurosci. Abstr. 16:1990;300.
47. Jones B. E. The organization of central cholinergic systems and their functional importance in sleep-waking states. Prog. Brain Res. 98:1993;61-71.
48. Kharazia V. N., Weinberg R. J. Glutamate in thalamic fibers terminating in layer IV of primary sensory cortex. J. Neurosci. 14:1994;6021-6032.
49. Kita H., Kitai S. T. Efferent projections of the subthalamic nucleus in the rat: light and electron microscopic analysis with the PHA-L method. J. comp. Neurol. 260:1987;435-452.
50. Kita H., Kitai S. T. Intracellular study of rat globus pallidus neurons - membrane properties and responses to neostriatal, subthalamic and nigral stimulation. Brain Res. 564:1991;296-305.
51. Kondoh T., Blount J. P., McDaniels E. P., Ebner T. J., Low W. C., Maxwell R. F. Posteroventral pallidotomy for the treatment of dystonia. Soc. Neurosci. Abstr. 20:1994;1257.
52. Kosaka T., Tauchi M., Dahl J. L. Cholinergic neurons containing GABA-like and/or glutamic acid decarboxylase-like immunoreactivities in various brain regions of the rat. Expl Brain Res. 70:1988;605-617.
53. Lavoie B., Parent A. Pedunculopontine nucleus in the squirrel monkey: distribution of cholinergic and monoaminergic neurons in the mesopontine tegmentum with evidence for the presence of glutamate in cholinergic neurons. J. comp. Neurol. 344:1994;190-209.
54. Lavoie B., Parent A. Pedunculopontine nucleus in the squirrel monkey: projections to the basal ganglia as revealed by anterograde tract-tracing methods. J. comp. Neurol. 344:1994;210-231.
55. Lee H. J., Rye D. B., Hallenger 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. 275:1988;469-492.
56. Llewellyn-Smith I. J., Phend K. D., Minson J. B., Pilowsky P. M., Chalmers J. P. Glutamate-immunoreactive synapses on retrogradely-labelled sympathetic preganglionic neurons in rat thoracic spinal cord. Brain Res. 581:1992;67-80.
57. Lozano A. M., Lang A. E., Galvez-Jimenez N., Miyasaki J., Duff J., Hutchinson W. D., Dostrovsky J. O. Effect of GPi pallidotomy on motor function in Parkinson's disease. Lancet. 346:1995;1383-1387.
58. Mesulam M.-M., Mash D., Hersh L., Bothwell M., Geula C. Cholinergic innervation of the human striatum, globus pallidus, subthalamic nucleus, substantia nigra and red nucleus. J. comp. Neurol. 323:1992;252-268.
59. Mink J. W., Thach W. T. Basal ganglia motor control. I. Nonexclusive relation of pallidal discharge to five movement modes. J. Neurophysiol. 65:1991;273-300.
60. Mrini A., Moukhles H., Jacomy H., Bosler O., Doucet G. Efficient immunodetection of various protein antigens in glutaraldehyde-fixed brain tissue. J. Histochem. Cytochem. 43:1995;1285-1291.
61. Nakanishi H., Kita H., Kitai S. T. Intracellular study of rat substantia nigra pars reticulata neurons in an in vitro slice preparation: electrical membrane properties and response characteristics to subthalamic stimulation. Brain Res. 437:1987;35-44.
62. Nakanishi H., Kita H., Kitai S. T. Intracellular study of rat entopeduncular nucleus neurons in an in vitro slice preparation: response to subthalamic stimulation. Brain Res. 549:1991;285-291.
63. Oakman S. A., Faris P. L., Kerr P. E., Cozzari C., Hartman B. K. Distribution of pontomesencephalic cholinergic neurons projecting to substantia nigra differs significantly from those projecting to ventral tegmental area. J. Neurosci. 15:1995;5859-5869.
64. Ottersen O. P. Quantitative electron microscopic immunocytochemistry of neuroactive amino acids. Anat. Embryol. 180:1989;1-15.
65. Park M. R., Falls W. M., Kitai S. T. An intracellular HRP study of the rat globus pallidus. I. Responses and light microscopic analysis. J. comp. Neurol. 211:1982;284-294.
66. Petrusz P., Van Eyck S. L., Weinberg R. J., Rustioni A. Antibodies to glutamate and aspartate recognize non-endogenous ligands for excitatory amino acid receptors. Brain Res. 529:1990;339-344.
67. Phend K. D., Weinberg R. J., Rustioni A. Techniques to optimize post-embedding single and double staining for amino acid neurotransmitters. J. Histochem. Cytochem. 40:1992;1011-1020.
68. Rinvik E., Ottersen O. P. Terminals of subthalamonigral fibres are enriched with glutamate-like immunoreactivity: an electron microscopic, immunogold analysis in the cat. J. chem. Neuroanat. 6:1993;19-30.
69. 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. 259:1987;483-528.
70. Saper C. B., Loewy A. D. Projections of the pedunculopontine tegmental nucleus in the rat: evidence for additional extrapyramidal circuitry. Brain Res. 252:1982;367-372.
71. Scarnati E., Di Loreto S., Proia A., Gallie G. The functional role of the peduculopontine nucleus in the regulation of the electrical activity of entopenduncular neurons in the rat. Archs ital. Biol. 126:1988;145-163.
72. Shink E., Smith Y. 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. 358:1995;119-141.
73. Shupliakov O., Brodin L., Cullheim S., Ottersen O. P., Storm-Mathisen J. Immunogold quantification of glutamate in two types of excitatory synapse with different firing patterns. J. Neurosci. 12:1992;3789-3803.
74. Smith Y., Bolam J. P., von Krosigk M. Topographical and synaptic organisation of the GABA-containing pallidosubthalamic projection in the rat. Eur. J. Neurosci. 2:1990;500-511.
75. Smith Y., Parent A. Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res. 453:1988;353-356.
76. Smith Y., Wichmann T., Delong M. R. Synaptic innervation of neurones in the internal pallidal segment by the subthalamic nucleus and the external pallidum in monkeys. J. comp. Neurol. 343:1994;297-318.
77. Somogyi P., Halasy K., Somogyi J., Storm-Mathisen J., Ottersen O. P. Quantification of immunogold labelling reveals enrichment of glutamate in mossy and parallel fibre terminals in cat cerebellum. Neuroscience. 19:1986;145-150.
78. Somogyi P., Hodgson A. J. 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. 33:1985;249-257.
79. Somogyi P., Hodgson A. J., Chubb I. W., Penke B., Erdei A. Antisera to γ-aminobutyric acid. II Immunocytochemical application to the central nervous system. J. Histochem. Cytochem. 33:1985;240-248.
80. Spann B. M., Grofova I. Origin of ascending and spinal pathways from the nucleus tegmenti pedunculopontinus in the rat. J. comp. Neurol. 283:1989;13-27.
81. Spann B. M., Grofova I. Cholinergic and non-cholinergic neurons in the pedunculopontine tegmental nucleus. Anat. Embryol. 186:1992;215-227.
82. Steininger T. L., Rye D. B., Wainer B. H. Afferent projections to the cholinergic pedunculopontine tegmental nucleus and adjacent midbrain extrapyramidal area in the albino rat. 1. Retrograde tracing studies. J. comp. Neurol. 321:1992;515-543.
83. Umbriaco D., Watkins K. C., Descarries L., Cozzari C., Hartman B. K. Ultrastructural and morphometric features of the acetylcholine innervation in adult rat parietal cortex: an electron microscopic study in serial sections. J. comp. Neurol. 348:1994;351-373.
84. Valtschanoff J. G., Phend K. D., Bernardi P. S., Weinberg R. J., Rustioni A. Amino acid immunocytochemistry of primary afferent terminals in the rat dorsal horn. J. comp. Neurol. 346:1994;237-252.
85. Van den Pol A. N. Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. J. Neurosci. 11:1991;2087-2101.
86. Wainer B. H., Levey A. I., Mufson E. J., Mesulam M.-M. Cholinergic systems in mammalian brain identified with antibodies against choline acetyltransferase. Neurochem. Int. 6:1984;163-182.
87. Woolf N. J. Cholinergic systems in mammalian brain and spinal cord. Prog. Neurobiol. 37:1991;475-524.
88. Woolf N. J., Butcher L. L. Cholinergic systems in the rat brain. III. Projections from the pontomesencephalic tegmentum to the thalamus, tectum, basal ganglia and basal forebrain. Brain Res. Bull. 16:1986;603-637.