The switch of subthalamic neurons from an irregular to a bursting pattern does not solely depend on their GABAergic inputs in the anesthetic-free rat

Journal of Neuroscience

Volumn 22, Issue 19, 2002, Pages 8665-8675

  Urbain, Nadia ^a   Rentéro, Nicolas ^a   Gervasoni, Damien ^b   Renaud, Bernard ^a   Chouvet, Guy ^a  

^a UNIVERSITÉ LYON 1   (France)

^b DUKE UNIVERSITY MEDICAL CENTER   (United States)

Author keywords

Bicuculline; Bursts of spikes; Extracellular single unit recordings; Firing pattern; GABA; Gabazine; Microiontophoresis; Nonanesthetized animal; Sleep wake cycle; Subthalamic nucleus

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID RECEPTOR; 4 AMINOBUTYRIC ACID RECEPTOR STIMULATING AGENT; ANESTHETIC AGENT;

ALERTNESS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BASAL GANGLION; BRAIN FUNCTION; CONTROLLED STUDY; GABAERGIC TRANSMISSION; GLOBUS PALLIDUS; HORMONE RECEPTOR INTERACTION; IN VITRO STUDY; IN VIVO STUDY; LIGAND BINDING; MALE; MICROIONTOPHORESIS; MOTOR DYSFUNCTION; NERVE CELL; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SLOW WAVE SLEEP; SUBTHALAMIC NUCLEUS; WAKEFULNESS;

EID: 0036813078     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-19-08665.2002     Document Type: Article

References (110)

1. Afsharpour S (1985) Topographical projections of the cerebral cortex to the subthalamic nucleus. J Comp Neurol 236:14-28.
2. Akaoka H, Charléty P, Saunier CF, Buda M, Chouvet G (1992) Inhibition of nigral dopamine neurons by systemic and local apomorphine: Possible contribution of dendritic autoreceptors. Neuroscience 49:879-891.
3. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-374.
4. Albin RL, Young AB, Penney JB (1995) The functional anatomy of disorders of the basal ganglia. Trends Neurosci 18:63-64.
5. Ashby P, Kim YJ, Kumar R, Lang AE, Lozano AM (1999) Neurophysiological effects of stimulation trough electrodes in the human subthalamic nucleus. Brain 122:1919-1931.
6. Ashby P, Paradiso G, Saint-Cyr JA, Chen R, Lang AE, Lozano AE (2001) Potentials recorded at the scalp by stimulation near the human subthalamic nucleus. Clin Neurophysiol 112:431-437.
7. Baufreton J, Garret M, Dovero S, Dufy B, Bioulac B, Taupignon A (2001) Activation of GABAA receptors in subthalamic neurons in vitro: Properties of native receptors and inhibition mechanisms. J Neurophysiol 86:75-85.
8. Bell K, Churchill L, Kalivas PW (1995) GABAergic projection from the ventral pallidum and globus pallidus to the subthalamic nucleus. Synapse 20:10-18.
9. Benabid AL, Pollak P, Gross C, Hoffman D, Benazzouz A, Gao DM, Laurent A, Gentil M, Perret J (1994) Acute and long-term effects of subthalamic nucleus stimulation in Parkinson's disease. Stereotact Funct Neurosurg 62:76-84.
10. Benazzouz A, Gross C, Féger J, Boraud T, Bioulac B (1993) Reversal of rigidity and improvement in motor performance by subthalamic highfrequency stimulation in MPTP-treated monkeys. Eur J Neurosci 5:382-389.
11. Benazzouz A, Piallat B, Pollak P, Benabid AL (1995) Responses of substantia nigra pars reticulata and globus pallidus complex to high frequency stimulation of the subthalamic nucleus in rats: Electrophysiological data. Neurosci Lett 189:77-80.
12. Benazzouz A, Boraud T, Féger J, Burbaud P, Bioulac B, Gross C (1996) Alleviation of experimental hemiparkinsonism by high-frequency stimulation of the subthalamic nucleus in primates: A comparison with L-dopa treatment. Mov Disord 11:627-632.
13. Benazzouz A, Gao DM, Ni GZ, Piallat B, Boualli-Benazzouz R, Benabid AL (2000) Effect of hih-frequency stimulation of the subthalamic nucleus on the neuronal activities of the substantia nigra pars reticulata and ventrolateral nucleus of the thalamus in the rat. Neuroscience 99:289-295.
14. Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436-1438.
15. Bergman H, Wichmann T, Karmon B, DeLong MR (1994) The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J Neurophysiol 72:507-520.
16. Bergman H, Raz A, Feingold A, Nini A, Nelken I, Hansel D, Benpazi H, Reches A (1998) Physiology of MPTP tremor. Mov Disord 13:29-34.
17. Beurrier C, Bézard E, Bioulac B, Gross C (1997) Subthalamic stimulation elicits hemiballismus in normal monkey. NeuroReport 8:1625-1629.
18. Beurrier C, Congar P, Bioulac B, Hammond C (1999) Subthalamic nucleus neurons switch from single-spike activity to burst-firing mode. J Neurosci 19:599-609.
19. Bevan MD, Bolam JP (1995) Cholinergic, GABAergic, and glutamateenriched inputs from the mesopontine tegmentum to the subthalamic nucleus in the rat. J Neurosci 15:7105-7120.
20. Bevan MD, Wilson CJ (1999) Mechanisms underlying spontaneous oscillation and rhythmic firing in rat subthalamic neurons. J Neurosci 19:7617-7628.
21. Bevan MD, Francis CM, Bolam JP (1995) The glutamate-enriched cortical and thalamic input to neurons in the subthalamic nucleus of the rat: Convergence with GABA-positive terminals. J Comp Neurol 361:491-511.
22. 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 17:308-324.
23. Bevan MD, Wilson CJ, Bolam JP, Magill PJ (2000) Equilibrium potential of GABA(A) current and implications for rebound burst firing in rat subthalamic neurons in vitro. J Neurophysiol 83:3169-3172.
24. Bevan MD, Magill PJ, Hallworth NE, Bolam JP, Wilson CJ (2002) Regulation of the timing and pattern of action potential generation in rat subthalamic neurons in vitro by GABA-A IPSPs. J Neurophysiol 87:1348-1362.
25. Booth PAC, Bolam JP, Ige AO, Disney GH, Marshall FH, White JH, Emson PC (2000) GABAB receptors in the rat brain: Cellular and subcellular distribution in the basal ganglia. Eur J Neurosci 12:133.
26. Burbaud P, Gross C, Bioulac B (1994) Effect of subthalamic high frequency stimulation on substantia nigra pars reticulata and globus pallidus neurons in normal rats. J Physiol (Paris) 88:359-361.
27. 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 513:43-59.
28. Charara A, Heilman TC, Levey AI, Smith Y (2000) Pre- and postsynaptic localization of GABA(B) receptors in the basal ganglia in monkeys. Neuroscience 95:127-140.
29. Cheruel F, Dormont JF, Farin D (1996) Activity of neurons of the subthalamic nucleus in relation to motor performance in the cat. Exp Brain Res 108:206-220.
30. Contreras D, Steriade M (1997a) Synchronization of low-frequency rhythms in corticothalamic networks. Neuroscience 76:11-24.
31. Contreras D, Steriade M (1997b) State-dependent fluctuations of lowfrequency rhythms in corticothalamic networks. Neuroscience 76:25-38.
32. Crossman AR, Sambrook MA, Jackson A (1980) Experimental hemiballismus in the baboon produced by injection of a gamma-aminobutyric acid antagonist into the basal ganglia. Neurosci Lett 20:369-372.
33. Crossman AR, Sambrook MA, Jackson A (1984) Experimental hemichorea/hemiballismus in the monkey. Studies on the intracerebral site of action in a drug-induced dyskinesia. Brain 107:579-596.
34. Darracq L, Gervasoni D, Soulière F, Lin JS, Fort P, Chouvet G, Luppi PH (1996) Effect of strychnine on rat locus coeruleus neurones during sleep and wakefulness. NeuroReport 8:351-355.
35. Debarbieux F, Brunton J, Charpak S (1998) Effect of bicuculline on thalamic activity: A direct blockade of IAHP in reticularis neurons. J Neurophysiol 79:2911-2918.
36. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
37. DeLong MR, Crutcher MD, Georgopoulos AP (1985) Primate globus pallidus and subthalamic nucleus: Functional organization. J Neurophysiol 53:530-543.
38. Féger J, Robledo P, Renwart N (1991) The subthalamic nucleus: New data, new questions. In: The Basal Ganglia III (Bernardi G, Carpentier MB, Di Chiara G, Morelli M, Stanzione P, eds), pp 99-108. New York: Plenum.
39. Féger J, Bevan M, Crossman AR (1994) The projections from the parafascicular thalamic nucleus to the subthalamic nucleus and the striatum arise from separate neuronal populations: A comparison with the corticostriatal and corticosubthalamic efferents in a retrograde fluorescent double-labelling study. Neuroscience 60:125-132.
40. Fujimoto K, Kita H (1993) Response characteristics of subthalamic neurons to the stimulation of the sensorimotor cortex in the rat. Brain Res 609:185-192.
41. Gervasoni D, Darracq L, Fort P, Soulière F, Chouvet G, Luppi PH (1998) Electrophysiological evidence that noradrenergic neurons of the rat locus coeruleus are tonically inhibited by GABA during sleep. Eur J Neurosci 10:964-970.
42. Gervasoni D, Peyron C, Rampon C, Barbagli B, Chouvet G, Urbain N, Fort P, Luppi PH (2000) Role and origin of the GABAergic innervation of dorsal raphe serotonergic neurons. J Neurosci 20:4217-4225.
43. Hamann M, Desarmenien M, Desaulles E, Bader MF, Feltz P (1988) Quantitative evaluation of the properties of a pyridazinyl GABA derivative (SR 95531) as a GABAA competitive antagonist. An electrophysiological approach. Brain Res 442:287-296.
44. Hammond C, Féger J, Bioulac B, Souteyrand JP (1979) Experimental hemiballism in the monkey produced by unilateral kainic acid lesion in corpus Luysii. Brain Res 171:577-580.
45. Hammond C, Rouzaire-Dubois B, Féger J, Jackson A, Crossman AR (1983) Anatomical and electrophysiological studies on the reciprocal projections between the subthalamic nucleus and nucleus tegmenti pedunculopontinus in the rat. Neuroscience 9:41-52.
46. Hassani OK, Mouroux M, Féger J (1996) Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus. Neuroscience 72:105-115.
47. Hashimoto T, Elder CM, DeLong MR, Vitek JL (2001) Responses of pallidal neurons to electrical stimulation of the subthalamic nucleus in experimental parkinsonism. Soc Neurosci Abstr 27:1994.
48. Heaulme M, Chambo JP, Leyris R, Molimard JC, Wermuth CG, Bizière K (1986) Biochemical characterization of the interaction of three pyridazinyl-GABA derivatives with the GABAA receptor site. Brain Res 384:224-231.
49. Hollerman JR, Grace AA (1992) Subthalamic nucleus cell firing in the 6-OHDA-treated rat: Basal activity and response to haloperidol. Brain Res 590:291-299.
50. + currents. Neurosci Lett 231:13-16.
51. Kaneoke Y, Vitek JL (1996) Burst and oscillation as disparate neuronal properties. J Neurosci Methods 68:211-223.
52. Khawaled R, Bruening-Wright A, Adelman JP, Maylie J (1999) Bicuculline block of small-conductance calcium-activated potassium channels. Pflügers Arch 438:314-321.
53. Kita H (1994) Parvalbumin-immunopositive neurons in rat globus pallidus: A light and electron microscopic study. Brain Res 657:31-41.
54. Kita H, Chang HT, Kitai ST (1983) Pallidal inputs to subthalamus: Intracellular analysis. Brain Res 264:255-265.
55. Kitai ST, Deniau JM (1981) Cortical inputs to the subthalamus: Intracellular analysis. Brain Res 214:411-415.
56. Kitai ST, 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 (Carpenter MB, Jayavaman A, eds), pp 357-373. New York: Plenum.
57. Kreiss DS, Anderson LA, Walters JR (1996) Apomorphine and dopamine D-1 receptor agonists increase the firing rates of subthalamic nucleus neurons. Neuroscience 72:863-876.
58. Kreiss DS, Mastropietro CW, Rawji SS, Walters JR (1997) The response of subthalamic nucleus neurons to dopamine receptor stimulation in a rodent model of Parkinson's disease. J Neurosci 17:6807-6819.
59. Legendy CR, Salcman M (1985) Bursts and recurrence of bursts in the spike trains of spontaneously active striate cortex neurons. J Neurophysiol 53:926-939.
60. Levy R, Hutchison WD, Lozano AM, Dostrovsky JO (2000) Highfrequency synchronization of neuronal activity in the subthalamic nucleus of parkinsonian patients with limb tremor. J Neurosci 20:7766-7775.
61. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Broussolle E, Perret JE, Benabid AL (1995a) Bilateral subthalamic nucleus stimulation for severe Parkinson's disease. Mov Disord 10:672-674.
62. Limousin P, Pollak P, Benazzouz A, Hoffmann D, Le Bas JF, Broussolle E, Perret JE, Benabid AL (1995b) Effect on parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 345:91-95.
63. Magariñoz-Ascone CM, Figueiras-Mendez R, Riva-Meana C, Cordoba-Fernandez A (2000) Subthalamic neuron activity related to tremor and movement in Parkinson's disease. Eur J Neurosci 12:2597-2607.
64. Magill PJ, Bolam JP, Bevan MD (2000) Relationship of activity in the subthalamic nucleus-globus pallidus network to cortical electroencephalogram. J Neurosci 20:820-833.
65. Magill PJ, Bolam JP, Bevan MD (2001) Dopamine regulates the impact of the cerebral cortex on the subthalamic nucleus-globus pallidus network. Neuroscience 106:313-330.
66. Matsumura M, Kojima J, Gardiner TW, Hikosaka O (1992) Visual and oculomotor functions of monkey subthalamic nucleus. J Neurophysiol 67:1615-1632.
67. McCormick DA, Bal T (1997) Sleep and arousal: Thalamocortical mechanisms. Annu Rev Neurosci 20:185-215.
68. 2+ transients in rat cerebellar granule cells through non-GABA(A) receptor associated mechanisms. Neurosci Lett 265:95-98.
69. Michaud JC, Mienville JM, Chambon JP, Bizière K (1986) Interactions between three pyridazinyl-GABA derivatives and central GABA and glycine receptors in the rat, an in vivo microiontophoretic study. Neuropharmacology 25:1197-1203.
70. Mienville JM, Vicini S (1987) A pyridazinyl derivative of gammaaminobutyric acid (GABA), SR 95531, is a potent antagonist of Clchannel opening regulated by GABAA receptors. Neuropharmacology 26:779-783.
71. Miller JJ, McLennan (1974) The action of bicuculline upon acetylcholineinduced excitations of central neurones. Neuropharmacology 13:785-787.
72. Mink JW, Thach WT (1993) Basal ganglia intrinsic circuits and their role in behavior. Curr Opin Neurobiol 3:950-957.
73. Moriizumi T, Hattori T (1992) Separate neuronal populations of the rat globus pallidus projecting to the subthalamic nucleus, auditory cortex and pedunculopontine tegmental area. Neuroscience 46:701-710.
74. Mouroux M, Féger J (1993) Evidence that the parafascicular projection to the subthalamic nucleus is glutamatergic. NeuroReport 4:613-615.
75. Mouroux M, Hassani OK, Féger J (1995) Electrophysiological study of the excitatory parafascicular projection to the subthalamic nucleus and evidence for ipsi- and contralateral controls. Neuroscience 67:399-407.
76. Mouroux M, Hassani OK, Féger J (1997) Electrophysiological and Fos immunohistochemical evidence for the excitatory nature of the parafascicular projection to the globus pallidus. Neuroscience 81:387-397.
77. Nakanishi, Kita H, Kitai ST (1987) Electrical membrane properties of rat subthalamic neurons in an in vitro slice preparation. Brain Res 437:35-44.
78. Nakao N, Ogura M, Nakai K, Itakura T (1998) Intrastriatal mesencephalic grafts affect neuronal activity in basal ganglia nuclei and their target structures in a rat model of Parkinson's disease. J Neurosci 18:1806-1817.
79. B receptors in the rat subthalamic nucleus. Soc Neurosci Abstr 27:764.
80. Nowak LG, Bullier J (1998a) Axons, but not cell bodies, are activated by electrical stimulation in cortical grey matter. I. Evidence from chronaxie measurements. Exp Brain Res 118:477-488.
81. Nowak LG, Bullier J (1998b) Axons, but not cell bodies, are activated by electrical stimulation in cortical gray matter. II. Evidence from selective inactivation of cell bodies and axon initial segments. Exp Brain Res 118:489-500.
82. Overton PG, Greenfield SA (1995) Determinants of neuronal firing pattern in the guinea-pig subthalamic nucleus: An in vivo and in vitro comparison. J Neural Transm Park Dis Dement Sect 10:41-54.
83. Paxinos G, Watson W (1996) The Rat Brain in Stereotaxic Coordinates. Sydney: Academic.
84. Périer C, Agid Y, Hirsch EC, Féger J (2000) Ipsilateral and contralateral subthalamic activity after unilateral dopaminergic lesion. NeuroReport 11:3275-3278.
85. Plenz D, Kitai ST (1999) A basal ganglia pacemaker formed by the subthalamic nucleus and external globus pallidus. Nature 400:677-682.
86. Rodriguez MC, Guridi OJ, Alvarez L, Mewes K, Macias R, Vitek J, Delong MR, Obeso JA (1998) The subthalamic nucleus and tremor in Parkinson's disease. Mov Disord 13:111-118.
87. Rognan D, Boulanger T, Hoffmann R, Vercauteren DP, Andre JM, Durant F, Wermuth CG (1992) Structure and molecular modeling of GABAA receptor antagonists. J Med Chem 35:1969-1977.
88. Rouzaire-Dubois B, Hammond C, Hamon B, Féger J (1980) Pharmacological blockade of the globus pallidus-induced inhibitory response of subthalamic cells in the rat. Brain Res 200:321-329.
89. Ryan LJ, Clark KB (1992) Alteration of neuronal responses in the subthalamic nucleus following globus pallidus and neostriatal lesions in rats. Brain Res Bull 29:319-327.
90. Ryan LJ, Sanders DJ, Clark KB (1992) Auto- and cross-correlation analysis of subthalamic nucleus neuronal activity in neostriatal- and globus pallidal-lesioned rats. Brain Res 583:253-261.
91. Schwarzer C, Berresheim U, Pirker S, Wieselthaler A, Fuchs K, Sieghart W, Sperk G (2001) Distribution of the major gamma-aminobutyric acid (A) receptor subunits in the basal ganglia and associated limbic areas of the adult rat. J Comp Neurol 433:526-549.
92. Seutin V, Scuvée-Moreau J, Dresse A (1997) Evidence for a non-GABAergic action of quaternary salts of bicuculline on dopaminergic neurones. Neuropharmacology 36:1653-1657.
93. Shen KZ, Johnson SW (2001) Presynaptic GABAB receptors inhibit synaptic inputs to rat subthalamic neurons. Neuroscience 108:431-436.
94. Smith Y, Bolam JP, Von Krosigk M (1990) Topographical and synaptic organisation of the GABA-containing pallidosubthalamic projection in the rat. Eur J Neurosci 2:500-511.
95. Soulière F, Urbain N, Gervasoni D, Schmitt P, Guillemort C, Fort P, Renaud B, Luppi PH, Chouvet G (2000) Single-unit and polygraphic recordings associated with systemic or local pharmacology: A multipurpose stereotaxic approach for the awake, anaesthetic-free, and head-restrained rat. J Neurosci Res 61:88-100.
96. Steriade M (1993) Central core modulation of spontaneous oscillations and sensory transmission in thalamocortical systems. Curr Opin Neurobiol 3:619-625.
97. Steriade M, McCormick DA, Sejnowski TJ (1993) Thalamocortical oscillations in the sleeping and aroused brain. Science 262:679-685.
98. Stone TW (1985) Microiontophoresis and Pressure Ejection. New York: Wiley.
99. Svenneby G, Roberts E (1973) Bicuculline and N-methylbicuculline: Competitive inhibitors of brain acetylcholinesterase. J Neurochem 21:1025-1026.
100. Urbain N, Gervasoni D, Soulière F, Lobo L, Rentéro N, Windels F, Astier B, Savasta M, Fort P, Renaud B, Luppi PH, Chouvet G (2000) Unrelated course of subthalamic nucleus and globus pallidus neuronal activities across vigilance states in the rat. Eur J Neurosci 12:3361-3374.
101. Van der Kooy D, Kolb B (1985) Non-cholinergic globus pallidus cells that project to the cortex but not to the subthalamic nucleus in rat. Neurosci Lett 57:113-118.
102. Van der Kooy D, Hattori T, Shannak K, Hornikiewicz O (1981) The pallido-subthalamic projection in rat: Anatomical and biochemical studies. Brain Res 204:253-268.
103. Vila M, Périer C, Féger J, Yelnik J, Faucheux B, Ruberg M, RaismanVozri R, Agid Y, Hirsch EC (2000) Evolution of changes in neuronal activity in the subthalamic nucleus of rats with unilateral lesion of the substantia nigra assessed by metabolic and electrophysiological measurements. Eur J Neurosci 12:337-344.
104. Wichmann T, Bergman H, DeLong MR (1994a) The primate subthalamic nucleus. I. Functional properties in intact animals. J Neurophysiol 72:494-506.
105. Wichmann T, Bergman H, DeLong MR (1994b) 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.
106. + current in rat subthalamic nucleus neurones. J Physiol (Lond) 527:493-506.
107. Windels F, Bruet N, Poupard A, Urbain N, Chouvet G, Feuerstein C, Savasta M (2000) Effects of high frequency stimulation of subthalamic nucleus on extracellular glutamate and GABA in substantia nigra and globus pallidus in the normal rat. Eur J Neurosci 12:4141-4146.
108. Wisden W, Laurie DJ, Monyer H, Seeburg PH (1992) The distribution of 13 GABAA receptor subunits mRNAs in the rat brain. I. Telencephalon, diencephalon, mesencephalon. J Neurosci 12:1040-1062.
109. Yu S, Ho IK (1990) Effects of GABA antagonists, SR 95531 and bicuculline, on GABAA receptor-regulated chloride flux in rat cortical synaptoneurosomes. Neurochem Res 15:905-910.
110. Zhang JH, Araki T, Sato M, Toyama M (1991) Distribution of GABAA-receptor alpha 1 subunit gene expression in the rat forebrain. Brain Res Mol Brain Res 11:239-247.