A continuous high frequency stimulation of the subthalamic nucleus determines a suppression of excitatory synaptic transmission in nigral dopaminergic neurons recorded in vitro

Experimental Neurology

Volumn 233, Issue 1, 2012, Pages 292-302

  Ledonne, Ada ^a,b   Mango, Dalila ^a,b   Bernardi, Giorgio ^a,b   Berretta, Nicola ^b   Mercuri, Nicola Biagio ^a,b  

^a UNIVERSITY OF ROME TOR VERGATA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

Author keywords

Deep brain stimulation; Dopamine; Parkinson's disease; Substantia nigra; Synaptic depression

Indexed keywords

4 AMINOBUTYRIC ACID; AMPA RECEPTOR;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEPTH STIMULATION; BRAIN ELECTROPHYSIOLOGY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; EVOKED RESPONSE; GLOBUS PALLIDUS; HIGH FREQUENCY STIMULATION; IN VITRO STUDY; MESENCEPHALON; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROTRANSMISSION; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SUBSTANTIA NIGRA PARS COMPACTA; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS; SYNAPTIC INHIBITION;

2-AMINO-5-PHOSPHONOVALERATE; 6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ACTION POTENTIALS; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ANIMALS; ANIMALS, NEWBORN; BENZOTHIADIAZINES; BICUCULLINE; BIOPHYSICS; DOPAMINERGIC NEURONS; DRUG INTERACTIONS; ELECTRIC STIMULATION; EXCITATORY AMINO ACID AGONISTS; EXCITATORY AMINO ACID ANTAGONISTS; EXCITATORY POSTSYNAPTIC POTENTIALS; GABA-A RECEPTOR ANTAGONISTS; NEURAL PATHWAYS; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS; SYNAPTIC TRANSMISSION;

EID: 84856221729     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2011.10.018     Document Type: Article

References (93)

1. Albin R.L., Young A.B., Penney J.B. The functional anatomy of basal ganglia disorders. Trends Neurosci. 1989, 12:366-375.
2. Alexander G.E., DeLong M.R., Strick P.L. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Annu. Rev. Neurosci. 1986, 9:357-381.
3. Ammari R., Lopez C., Bioulac B., Garcia L., Hammond C. Subthalamic xnucleus evokes similar long lasting glutamatergic excitations in pallidal, entopeduncular and nigral neurons in the basal ganglia slice. Neuroscience 2010, 166:808-818.
4. Ammari R., Bioulac B., Garcia L., Hammond C. The subthalamic nucleus becomes a generator of bursts in the dopamine-depleted state. Its high frequency stimulation dramatically weakens transmission to the globus pallidus. Front. Syst. Neurosci. 2011, 43:1-10.
5. Anderson T.R., Hu B., Iremonger K., Kiss Z.H.T. Selective attenuation of afferent synaptic transmission as a mechanism of thalamic deep brain stimulation-induced tremor arrest. J. Neurosci. 2006, 26:841-850.
6. 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-tetrahydropyridine (MPTP)-induced Parkinsonism in the primate. Mov. Disord. 1991, 6:288-292.
7. Baunez C., Robbins T.W. Bilateral lesions of the subthalamic nucleus induce multiple deficits in an attentional task in rats. Eur. J. Neurosci. 1997, 9:2086-2099.
8. Baunez C., Nieoullon A., Amalric M. In a rat model of Parkinsonism, lesions of the subthalamic nucleus reverse increases of reaction time but induce a dramatic premature responding deficit. J. Neurosci. 1995, 15:6531-6541.
9. 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. 1993, 5:382-389.
10. Benazzouz A., Gao D., Ni Z., Benabid A. High frequency stimulation of the STN influences the activity of dopamine neurons in the rat. NeuroReport 2000, 211:1593-1596.
11. Benazzouz A., Gao D.M., Ni Z.G., Piallat B., Bouali-Benazzouz R., Benabid A.L. Effect of high-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 2000, 99:289-295.
12. Bergman H., Wichmann T., DeLong M.R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990, 249:1436-1438.
13. Bergman H., Wichmann T., Karmon B., DeLong M.R. The primate subthalamic nucleus. II. Neuronal activity in the MPTP model of parkinsonism. J. Neurophysiol. 1994, 72:507-520.
14. Beurrier C., Bezard E., Bioulac B., Gross C. Subthalamic stimulation elicits hemiballismus in normal monkey. NeuroReport 1997, 8:1625-1629.
15. Beurrier C., Bioulac B., Audin J., Hammond C. High frequency stimulation produces a transient blockade of voltage-gated currents in subthalamic neurons. J. Neurophysiol. 2001, 85:1351-1356.
16. Blandini F., Nappi G., Greenamyre J.T. Subthalamic infusion of an NMDA antagonist prevents basal ganglia metabolic changes and nigral degeneration in a rodent model of Parkinson's disease. Ann. Neurol. 2001, 49:525-529.
17. Bosch C., Degos B., Deniau J.M., Venance L. Subthalamic nucleus high frequency stimulation generates a concomitant synaptic excitation-inhibition in substantia nigra pars reticulate. J. Physiol. 2011, 589:4189-4207.
18. Boulet S., Lacombe E., Carcenac C., Feuerstein C., Sgambato-Faure V., Poupard A., Savasta M. Subthalamic stimulation-induced forelimb dyskinesias are linked to an increase in glutamate levels in the substantia nigra pars reticulata. J. Neurosci. 2006, 26:10768-10776.
19. Bruet N., Windels F., Bertrand A., Feuerstein C., Poupard A., Savasta M. High frequency stimulation of the subthalamic nucleus increases the extracellular contents of striatal dopamine in normal and partially dopaminergic denervated rats. J. Neuropathol. Exp. Neurol. 2001, 60:15-24.
20. Carlson J.D., Cleary D.R., Cetas J.S., Heinricher M.M., Burchiel K.J. Deep brain stimulation does not silence neurons in subthalamic nucleus in Parkinson's patients. J. Neurophysiol. 2010, 103:962-967.
21. Carvalho G.A., Nikkhah G. Subthalamic nucleus lesions are neuroprotective against terminal 6-OHDA-induced striatal lesions and restore postural balancing reactions. Exp. Neurol. 2001, 171:405-417.
22. Crossman A.R. Neural mechanisms in disorders of movement. Comp. Biochem. Physiol. 1989, 93:141-149.
23. Crossman A.R., Sambrook M.A., Jackson A. Experimental hemichorea/hemiballismus in the monkey. Studies of the intracerebral site of action in a drug induced dyskinesia. Brain 1984, 107:579-596.
24. DeLong M.R. Primate models of movement disorders of basal ganglia origin. Trends Neurosci. 1990, 13:281-285.
25. Dittman J.S., Regehr W.G. Calcium dependence and recovery kinetics of presynaptic depression at the climbing fiber to Purkinje cell synapse. J. Neurosci. 1998, 18:6147-6162.
26. Do M.T., Bean B.P. Subthreshold sodium currents and pacemaking of subthalamic neurons: modulation by slow inactivation. Neuron 2003, 39:109-120.
27. Filali M., Hutchison W.D., Palter V.N., Lozano A.M., Dostrovsky J.O. Stimulation-induced inhibition of neuronal firing in human subthalamic nucleus. Exp. Brain Res. 2004, 156:274-281.
28. Galati S., Mazzone P., Fedele E., Pisani A., Peppe A., Pierantozzi M., Brusa L., Troppi D., Moschella V., Raiteri M., Stanzione P., Bernardi G., Stefani A. Biochemical and electrophysiological changes of substantia nigra pars reticulata driven by subthalamic stimulation in patients with Parkinson's disease. Eur. J. Neurosci. 2006, 23:2923-2928.
29. Garcia L., Audin J., D'Alessandro G., Bioulac B., Hammond C. Dual effect of high-frequency stimulation on subthalamic neuron activity. J. Neurosci. 2003, 23:8743-8751.
30. Grace A.A., Onn S.P. Morphology and electrophysiological properties of immunocytochemically identified rat dopamine neurons recorded in vitro. J. Neurosci. 1989, 9:3463-3481.
31. Gradinaru V., Mogri M., Thompson K.R., Henderson J.M., Deisseroth K. Optical destruction of parkinsonian neural circuitry. Science 2009, 324:354-359.
32. Greenberg D.A. Glutamate and Parkinson's disease. Ann. Neurol. 1994, 35:655-661.
33. Hamada I., DeLong M.R. Excitotoxic acid lesions of the primate subthalamic nucleus result in transient dyskinesias of the contralateral limbs. J. Neurophysiol. 1992, 68:1850-1858.
34. Hamani C., Saint-Cyr J.A., Fraser J., Kaplitt M., Lozano A.M. The subthalamic nucleus in the context of movement disorders. Brain 2004, 127:4-20.
35. Hammond C., Deniau J.M., Rizk A., Andf'eger J. Electrophysiological demonstration of an excitatory subthalamonigral pathway in the rat. Brain Res. 1978, 151:235-244.
36. Hammond C., FeD́ger J., Bioulac B., Souteyrand J.P. Experimental hemiballism in the monkey produced by unilateral kainic acid lesion in corpus Luysii. Brain Res. 1979, 171:577-580.
37. Harnack D., Meissner W., Jira J.A., Winter C., Morgenstern R., Kupsch A. Placebo-controlled chronic high-frequency stimulation of the subthalamic nucleus preserves dopaminergic nigral neurons in a rat model of progressive Parkinsonism. Exp. Neurol. 2008, 210:257-260.
38. Hassani O.K., Mouroux M., Fed́ger J. Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus. Neuroscience 1996, 72:105-115.
39. Iremonger K.J., Anderson T.R., Hu B., Kiss Z.H. Cellular mechanisms preventing sustained activation of cortex during subcortical high-frequency stimulation. J. Neurophysiol. 2006, 96:613-621.
40. Iribe Y., Moore K., Pang K.C.H., Tepper J.M. Subthalamic stimulation-induced synaptic responses in substantia nigra pars compacta dopaminergic neurons in vitro. J. Neurophysiol. 1999, 82:925-933.
41. Jaffer A., Van der Spuy G.D., Russell V.A., Mintz M., Taljaard J.J. Activation of the subthalamic nucleus and pedunculopontine tegmentum: does it affect dopamine levels in the substantia nigra, nucleus accumbens and striatum?. Neurodegeneration 1995, 4:139-145.
42. Jensen A.L., Durand D.M. High frequency stimulation can block axonal conduction. Exp. Neurol. 2009, 220:57-70.
43. Jones M.V., Westbrook G.L. The impact of receptor desensitization on fast synaptic transmission. Trends Neurosci. 1996, 19:96-101.
44. Kanazawa I., Marshall G.R., Kelly J.S. Afferents to the rat substantia nigra studied with horseradish peroxidase, with special reference to fibres from the subthalamic nucleus. Brain Res. 1976, 115:485-491.
45. 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. 1987, 260:435-452.
46. Kleiner-Fisman G., Herzog J., Fisman D.N., Tamma F., Lyons K.E., Pahwa R., Lang A.E., Deuschl G. Subthalamic nucleus deep brain stimulation: summary and meta-analysis of outcomes. Mov. Disord. 2006, 21:290-304.
47. Lee K.H., Chang S.Y., Roberts D.W., Kim U. Neurotransmitter release from high frequency stimulation of the subthalamic nucleus. J. Neurosurg. 2004, 101:511-517.
48. Lee K.H., Blaha C.D., Harris B.T., Cooper S., Hitti F.L., Leiter J.C., Roberts D.W., Kim U. Dopamine efflux in the rat striatum evoked by electrical stimulation of the subthalamic nucleus: potential mechanism of action in Parkinson's disease. Eur. J. Neurosci. 2006, 23:1005-1014.
49. Levy R., Lang A.E., Dostrovsky J.O., Pahapill P., Romas J., Saint-Cyr J., Hutchison W.D., Lozano A.M. Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 2001, 124:2105-2118.
50. Limousin P., Krack P., Pollak P., Benazzouz A., Ardouin C., Hoffmann D., Benabid A.L. Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N. Engl. J. Med. 1998, 339:1105-1111.
51. Lozano A.M., Mahant N. Deep brain stimulation surgery for Parkinson's disease: mechanisms and consequences. Parkinsonism. Relat. Disord. 2004, 10:49-57.
52. Luquin M.R., Saldise L., Guillén J., Belzunegui S., San Sebastián W., Izal A., Garrido P., Vázquez M. Does increased excitatory drive from the subthalamic nucleus contribute to dopaminergic neuronal death in Parkinson's disease?. Exp. Neurol. 2006, 201:407-415.
53. Maesawa S., Kaneoke Y., Kajita Y., Usui N., Misawa N., Nakayama A., Yoshida J. Long-term stimulation of the subthalamic nucleus in hemiparkinsonian rats: neuroprotection of dopaminergic neurons. J. Neurosurg. 2004, 100:679-687.
54. Magarinos-Ascone C., Pazo J.H., Macadar O., Buno W. High-frequency stimulation of the subthalamic nucleus silences sub-thalamic neurons: a possible cellular mechanism in Parkinson's disease. Neuroscience 2002, 115:1109-1117.
55. Maurice N., Thierry A.M., Glowinski J., Deniau J.M. Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 2003, 23:9929-9936.
56. McIntyre C.C., Grill W.M., Sherman D.L., Thakor N.V. Cellular effects of deep brain stimulation: model-based analysis of activation and inhibition. J. Neurophysiol. 2004, 91:1457-1469.
57. Meissner W., Harnack D., Reese R., Paul G., Reum T., Ansorge M., Kusserow H., Winter C., Morgenstern R., Kupsch A. High-frequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J. Neurochem. 2003, 85:601-609.
58. Mercuri N.B., Bonci A., Calabresi P., Stefani A., Bernardi G. Properties of the hyperpolarization-activated cation current Ih in rat midbrain dopaminergic neurons. Eur. J. Neurosci. 1995, 7:462-469.
59. Mercuri N.B., Bonci A., Bernardi G. Electrophysiological pharmacology of the autoreceptor-mediated responses of dopaminergic cells to antiparkinsonian drugs. Trends Pharmacol. Sci. 1997, 18:232-235.
60. Miocinovic S., Parent M., Butson C.R., Hahn P.J., Russo G.S., Vitek J.L., McIntyre C.C. Computational analysis of subthalamic nucleus and lenticular fasciculus activation during therapeutic deep brain stimulation. J. Neurophysiol. 2006, 96:1569-1580.
61. Moran A., Stein E., Tischler H., Belelovsky K., Bar-Gad I. Dynamic stereotypic responses of Basal Ganglia neurons to subthalamic nucleus high-frequency stimulation in the parkinsonian primate. Front. Syst. Neurosci. 2011, 5:1-11.
62. Nakao N., Nakai E., Nakai K., Itakura T. Ablation of the subthalamic nucleus supports the survival of nigral dopaminergic neurons after nigrostriatal lesions induced by the mitochondrial toxin 3-nitropropionic acid. Ann. Neurol. 1999, 45:640-651.
63. Nugent F.S., Hwong A.R., Udaka Y., Kauer J.A. High-frequency afferent stimulation induces long-term potentiation of field potentials in the ventral tegmental area. Neuropsychopharmacology 2008, 33:1704-1712.
64. Obeso J.A., Rodriguez M.C., DeLong M.R. Basal ganglia pathophysiology: a critical review. Adv. Neurol. 1997, 74:3-18.
65. Overton P.G., Richards C.D., Berry M.S., Clark D. Long-term potentiation at excitatory amino acid synapses on midbrain dopamine neurons. NeuroReport 1999, 10:221-226.
66. Park M.R. Monosynaptic inhibitory postsynaptic potentials from lateral habenula recorded in dorsal raphe neurons. Brain Res. Bull. 1987, 19:581-586.
67. Partin K.M., Patneau D.K., Winters C.A., Mayer M.L., Buonanno A. Selective modulation of desensitization at AMPA versus kainate receptors by cyclothiazide and concanavalin A. Neuron 1993, 11:1069-1082.
68. Paxinos G., Watson C. The Rat Brain Atlas in Stereotaxic Coordinates 1986, Academic press, London. second ed.
69. Piallat B., Benazzouz A., Benabid A.L. Subthalamic nucleus lesion in rats prevents dopaminergic nigral neuron degeneration after striatal 6-OHDA injection: behavioural and immunohistochemical studies. Eur. J. Neurosci. 1996, 8:1408-1414.
70. Robledo P., Feger J. Excitatory influence of rat subthalamic nucleus to substantia nigra pars reticulata and the pallidal complex: electrophysiological data. Brain Res. 1990, 518:47-54.
71. Rodriguez M.C., Obeso J.A., Olanow C.W. Subthalamic nucleus mediated excitotoxicity in Parkinson's disease: a target for neuroprotection. Ann. Neurol. 1998, 44:175-188.
72. Schüpbach W.M., Maltête D., Houeto J.L., du Montcel S.T., Mallet L., Welter M.L., Gargiulo M., Béhar C., Bonnet A.M., Czernecki V., Pidoux B., Navarro S., Dormont D., Cornu P., Agid Y. Neurosurgery at an earlier stage of Parkinson disease: a randomized, controlled trial. Neurology 2007, 68:267-271.
73. Shen K.Z., Johnson S.W. Subthalamic stimulation evokes complex EPSCs in the rat substantia nigra pars reticulata in vitro. J. Physiol. 2006, 573:697-709.
74. Shen K.Z., Johnson S.W. Complex EPSCs evoked in substantia nigra reticulata neurons are disrupted by repetitive stimulation of the subthalamic nucleus. Synapse 2008, 62:237-242.
75. Shon Y.M., Lee K.H., Goerss S.J., Kim I.Y., Kimble C., Van Gompel J.J., Bennet K., Blaha C.D., Chang S.Y. High frequency stimulation of the subthalamic nucleus evokes striatal dopamine release in a large animal model of human DBS neurosurgery. Neurosci. Lett. 2010, 475:136-140.
76. Smith I.D., Grace A.A. Role of the subthalamic nucleus in the regulation of nigral dopamine neuron activity. Synapse 1992, 12:287-303.
77. Smith Y., Parent A. Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res. 1988, 453:353-356.
78. Stevens C.F., Wesseling J.F. Activity-dependent modulation of the rate at which synaptic vesicles become available to undergo exocytosis. Neuron 1998, 21:415-424.
79. Stowe R.L., Wheatley K., Clarke C.E., Ives N.J., Hills R.K., Williams A.C., Daniels J.P., Gray R. Surgery for Parkinson's disease: lack of reliable clinical trial evidence. J. Neurol. Neurosurg. Psychiatry 2003, 74:519-521.
80. Tai C.H., Boraud T., Bezard E., Bioulac B., Gross C., Benazzouz A. Electrophysiological and metabolic evidence that high-frequency stimulation of the subthalamic nucleus bridles neuronal activity in the subthalamic nucleus and the substantia nigra reticulata. FASEB J. 2003, 17:1820-1830.
81. Temel Y., Visser-Vandewalle V., Kaplan S., Kozan R., Daemen M.A., Blokland A., Schmitz C., Steinbusch H.W. Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res. 2006, 1120:100-105.
82. Van der Kooy D., Hattori T. Single subthalamic nucleus neurons project to both the globus pallidus and substantia nigra in rat. J. Comp. Neurol. 1980, 192:751-768.
83. Wallace B.A., Ashkan K., Heise C.E., Foote K.D., Torres N., Mitrofanis J., Benabid A.L. Survival of midbrain dopaminergic cells after lesion or deep brain stimulation of the subthalamic nucleus in MPTP-treated monkeys. Brain 2007, 130:2129-2145.
84. Wang L.Y., Kaczmarek L.K. High-frequency firing helps replenish the readily releasable pool of synaptic vesicles. Nature 1998, 394:384-388.
85. Weaver F.M., Follett K., Stern M., Hur K., Harris C., Marks W.J., Rothlind J., Sagher O., Reda D., May C.S., et al. Bilateral deep brain stimulation vs best medical theraphy with advanced Parkinson's disease: a randomized controlled trial. JAMA 2009, 301:63-73.
86. Whittier J.R., Mettler F.A. Studies of the subthalamus of the rhesus monkey. II. Hyperkinesia and other physiologic effects of subthalamic lesions, with special reference to the subthalamic nucleus of Luys. J. Comp. Neurol. 1949, 90:319-372.
87. Wichmann T., DeLong M.R. Models of basal ganglia function and pathophysiology of movement disorders. Neurosurg. Clin. N. Am. 1998, 9:223-236.
88. Wichmann T., Bergman H., DeLong M.R. 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. 1994, 72:521-530.
89. Windels F., Bruet N., Poupard A., Urbain N., Chouvet G., Feuerstein C., Savasta M. 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. 2000, 12:4141-4146.
90. Windels F., Carcenac C., Poupard A., Savasta M. Pallidal origin of GABA release within the substantia nigra pars reticulata during high-frequency stimulation of the subthalamic nucleus. J. Neurosci. 2005, 25:5079-5086.
91. Wu L.G., Borst J.G. The reduced release probability of releasable vesicles during recovery from short-term synaptic depression. Neuron 1999, 23:821-832.
92. Zheng F., Lammert K., Nixdorf-Bergweiler B.E., Steigerwald F., Volkmann J., Alzheimer C. Axonal failure during high frequency stimulation of rat subthalamic nucleus. J. Physiol. 2011, 589:2781-2793.
93. Zucker R.S., Regehr W.G. Short-term synaptic plasticity. Annu. Rev. Physiol. 2002, 64:355-405.