High frequency stimulation of the subthalamic nucleus leads to presynaptic GABA(B)-dependent depression of subthalamo-nigral afferents

PLoS ONE

Volumn 8, Issue 12, 2013, Pages

  Dvorzhak, Anton ^a   Gertler, Christoph ^a   Harnack, Daniel ^a   Grantyn, Rosemarie ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR; GLUTAMIC ACID;

ACTION POTENTIAL; ANIMAL; BIOLOGICAL MODEL; C57BL MOUSE; CHANNEL GATING; CONDITIONING; DRUG EFFECTS; ELECTROSTIMULATION; EXCITATORY POSTSYNAPTIC POTENTIAL; INHIBITORY POSTSYNAPTIC POTENTIAL; METABOLISM; NERVE CELL PLASTICITY; PHYSIOLOGY; SENSORY NERVE; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS; SYNAPTOSOME;

ACTION POTENTIALS; AFFERENT PATHWAYS; ANIMALS; CONDITIONING (PSYCHOLOGY); ELECTRIC STIMULATION; EXCITATORY POSTSYNAPTIC POTENTIALS; GAMMA-AMINOBUTYRIC ACID; GLUTAMIC ACID; INHIBITORY POSTSYNAPTIC POTENTIALS; ION CHANNEL GATING; MICE, INBRED C57BL; MODELS, NEUROLOGICAL; NEURONAL PLASTICITY; PRESYNAPTIC TERMINALS; RECEPTORS, GABA; SUBSTANTIA NIGRA; SUBTHALAMIC NUCLEUS;

EID: 84893473749     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0082191     Document Type: Article

References (78)

1. Lozano AM, Lipsman N (2013) Probing and regulating dysfunctional circuits using deep brain stimulation. Neuron 77:406-424.
2. Gubellini P, Salin P, Kerkerian-Le Goff L, Baunez C (2009) Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Prog Neurobiol 89:79-123.
3. Sgambato-Faure V, Cenci MA (2012) Glutamatergic mechanisms in the dyskinesias induced by pharmacological dopamine replacement and deep brain stimulation for the treatment of Parkinson's disease. Prog Neurobiol 96:69-86.
4. Benabid AL, Chabardes S, Mitrofanis J, Pollak P (2009) Deep brain stimulation of the subthalamic nucleus for the treatment of Parkinson's disease. Lancet Neurol 8:67-81.
5. Beurrier C, Bonvento G, Kerkerian-Le Goff L, Gubellini P (2009) Role of glutamate transporters in corticostriatal synaptic transmission. Neurosci 158:1608-1615.
6. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 349:1925-1934.
7. Lozano AM, Mahant N (2004) Deep brain stimulation surgery for Parkinson's disease: mechanisms and consequences. Parkinsonism Relat Disord 10 Suppl 1:S49-S57
8. Lozano AM, Mahant N (2004) Deep brain stimulation surgery for Parkinson's disease: mechanisms and consequences. Parkinsonism Relat Disord 10 Suppl 1:S49-S57
9. Wenzelburger R, Kopper F, Zhang BR, Witt K, Hamel W, et al. (2003) Subthalamic nucleus stimulation for Parkinson's disease preferentially improves akinesia of proximal arm movements compared to finger movements. Mov Disord 18:1162-1169.
10. Kuhn AA, Kempf F, Brucke C, Gaynor DL, Martinez-Torres I, et al. (2008) High-frequency stimulation of the subthalamic nucleus suppresses oscillatory beta activity in patients with Parkinson's disease in parallel with improvement in motor performance. J Neurosci 28:6165-6173.
11. Li Q, Ke Y, Chan DC, Qian ZM, Yung KK, et al. (2012) Therapeutic deep brain stimulation in Parkinsonian rats directly influences motor cortex. Neuron 76:1030-1041.
12. Dejean C, Hyland B, Arbuthnott G (2009) Cortical effects of subthalamic stimulation correlate with behavioral recovery from dopamine antagonist induced akinesia. Cereb Cortex 19:1055-1063.
13. Ledonne A, Mango D, Bernardi G, Berretta N, Mercuri NB (2012) A continuous high frequency stimulation of the subthalamic nucleus determines a suppression of excitatory synaptic transmission in nigral dopaminergic neurons recorded in vitro. Exp Neurol 233:292-302.
14. Meissner W, Harnack D, Reese R, Paul G, Reum T, et al. (2003) Highfrequency stimulation of the subthalamic nucleus enhances striatal dopamine release and metabolism in rats. J Neurochem 85:601-609.
15. Lee KH, Blaha CD, Harris BT, Cooper S, Hitti FL, et al. (2006) 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 23:1005-1014.
16. Shimo Y, Wichmann T (2009) Neuronal activity in the subthalamic nucleus modulates the release of dopamine in the monkey striatum. Eur J Neurosci 29:104-113.
17. Maesawa S, Kaneoke Y, Kajita Y, Usui N, Misawa N, et al. (2004) Long-term stimulation of the subthalamic nucleus in hemiparkinsonian rats: neuroprotection of dopaminergic neurons. J Neurosurg 100:679-687.
18. Paul G, Meissner W, Rein S, Harnack D, Winter C, et al. (2004) Ablation of the subthalamic nucleus protects dopaminergic phenotype but not cell survival in a rat model of Parkinson's disease. Exp Neurol 185:272-280.
19. Harnack D, Meissner W, Jira JA, Winter C, Morgenstern R, et al. (2008) Placebo-controlled chronic high-frequency stimulation of the subthalamic nucleus preserves dopaminergic nigral neurons in a rat model of progressive Parkinsonism. Exp Neurol 210:257-260.
20. Temel Y, Visser-Vandewalle V, Kaplan S, Kozan R, Daemen MA, et al. (2006) Protection of nigral cell death by bilateral subthalamic nucleus stimulation. Brain Res 1120:100-105.
21. Whitmer D, de Solages C, Hill B, Yu H, Henderson JM, et al. (2012) High frequency deep brain stimulation attenuates subthalamic and cortical rhythms in Parkinson's disease. Front Hum Neurosci 6:155
22. Tai CH, Boraud T, Bezard E, Bioulac B, Gross C, et al. (2003) 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 17:1820-1830.
23. Bosch C, Degos B, Deniau JM, Venance L (2011) Subthalamic nucleus highf-requency stimulation generates a concomitant synaptic excitation- inhibition in substantia nigra pars reticulata. J Physiol 589:4189-4207.
24. Maurice N, Thierry AM, Glowinski J, Deniau JM (2003) Spontaneous and evoked activity of substantia nigra pars reticulata neurons during high-frequency stimulation of the subthalamic nucleus. J Neurosci 23:9929-9936.
25. Miyazaki T, Lacey MG (1998) Presynaptic inhibition by dopamine of a discrete component of GABA release in rat substantia nigra pars reticulata. J Physiol 513:805-817.
26. Deniau JM, Degos B, Bosch C, Maurice N (2010) Deep brain stimulation mechanisms: beyond the concept of local functional inhibition. Eur J Neurosci 32:1080-1091.
27. Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249:1436-1438.
28. Steigerwald F, Potter M, Herzog J, Pinsker M, Kopper F, et al. (2008) Neuronal activity of the human subthalamic nucleus in the parkinsonian and non-parkinsonian state. J Neurophysiol 100:2515-2524.
29. Levy R, Lang AE, Dostrovsky JO, Pahapill P, Romas J, et al. (2001) Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 124:2105-2118.
30. Smith Y, Parent A (1988) Neurons of the subthalamic nucleus in primates display glutamate but not GABA immunoreactivity. Brain Res 453:353-356.
31. Nambu A (2004) A new dynamic model of the cortico-basal ganglia loop. Prog Brain Res 143:461-466.
32. Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375.
33. DeLong MR (1990) Primate models of movement disorders of basal ganglia origin. Trends Neurosci 13:281-285.
34. Benazzouz A, Gao DM, Ni ZG, Piallat B, Bouali-Benazzouz R, et al. (2000) 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. Neurosci 99:289-295.
35. Zheng F, Lammert K, Nixdorf-Bergweiler BE, Steigerwald F, Volkmann J, et al. (2011) Axonal failure during high frequency stimulation of rat subthalamic nucleus. J Physiol 589:2781-2793.
36. de Jesus AJ, Rueda-Orozco PE, Hernandez R, Plata V, Ibanez-Sandoval O, et al. (2011) Dopaminergic presynaptic modulation of nigral afferents: its role in the generation of recurrent bursting in substantia nigra pars reticulata neurons. Front Syst Neurosci 5:6
37. Connelly WM, Schulz JM, Lees G, Reynolds JN (2010) Differential short-term plasticity at convergent inhibitory synapses to the substantia nigra pars reticulata. J Neurosci 30:14854-14861.
38. Takahashi T (1992) The minimal inhibitory synaptic currents evoked in neonatal rat motoneurones. J Physiol 450:593-611.
39. Henneberger C, Redman SJ, Grantyn R (2007) Cortical efferent control of subcortical sensory neurons by synaptic disinhibition. Cereb Cortex 17:2039-2049.
40. Kirischuk S, Clements JD, Grantyn R (2002) Presynaptic and postsynaptic mechanisms underlie paired pulse depression at single GABAergic boutons. J Physiol 543:99-116.
41. Dvorzhak A, Semtner M, Faber DS, Grantyn R (2013) Tonic mGluR5/CB1-dependent suppression of inhibition as a pathophysiological hallmark in the striatum of mice carrying a mutant form of huntingtin. J Physiol 591:1145-1166.
42. Beurrier C, Ben Ari Y, Hammond C (2006) Preservation of the direct and indirect pathways in an in vitro preparation of the mouse basal ganglia. Neurosci 140:77-86.
43. Grantyn R, Henneberger C, Juettner R, Meier JC, Kirischuk S (2011) Functional hallmarks of GABAergic synapse maturation and the diverse roles of neurotrophins. Front Cell Neurosci 5:13
44. Coombs JS, Eccles JC, Fatt P (1955) The specific ionic conductances and the ionic movements across the motoneuronal membrane that produce the inhibitory post-synaptic potential. J Physiol 130:326-374.
45. Mrachacz-Kersting N, Kristensen SR, Niazi IK, Farina D (2012) Precise temporal association between cortical potentials evoked by motor imagination and afference induces cortical plasticity. J Physiol 590:1669-1682.
46. Frerking M, Schmitz D, Zhou Q, Johansen J, Nicoll RA (2001) Kainate receptors depress excitatory synaptic transmission at CA3→CA1 synapses in the hippocampus via a direct presynaptic action. J Neurosci 21:2958-2966.
47. Lindblom Y, Tapper DN (1966) Integration of impulse activity in a peripheral sensory unit. Exp Neurol 15:63-69.
48. Fukami Y (1980) Interaction of impulse activities originating from individual Golgi tendon organs innervated by branches of a single axon. J Physiol 298:483-499.
49. Shen KZ, Johnson SW (1997) Presynaptic GABAB and adenosine A1 receptors regulate synaptic transmission to rat substantia nigra reticulata neurones. J Physiol 505:153-163.
50. Kirmse K, Kirischuk S (2006) Ambient GABA constrains the strength of GABAergic synapses at Cajal-Retzius cells in the developing visual cortex. J Neurosci 26:4216-4227.
51. Kirmse K, Kirischuk S, Grantyn R (2008) Activity of the GABA transporter 1 regulates GABAergic synaptic transmission in striatal projection neurons. J Physiol 586:5665-5678.
52. Waldmeier PC, Wicki P, Feldtrauer JJ, Mickel SJ, Bittiger H, et al. (1994) GABA and glutamate release affected by GABAB receptor antagonists with similar potency: no evidence for pharmacologically different presynaptic receptors. Br J Pharmacol 113:1515-1521.
53. Wilkins ME, Li X, Smart TG (2008) Tracking cell surface GABAB receptors using an alpha-bungarotoxin tag. J Biol Chem 283:34745-34752.
54. Windels F, Bruet N, Poupard A, Urbain N, Chouvet G, et al. (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.
55. Bruet N, Windels F, Carcenac C, Feuerstein C, Bertrand A, et al. (2003) Neurochemical mechanisms induced by high frequency stimulation of the subthalamic nucleus: increase of extracellular striatal glutamate and GABA in normal and hemiparkinsonian rats. J Neuropathol Exp Neurol 62:1228-1240.
56. Wallmichrath I, Szabo B (2002) Cannabinoids inhibit striatonigral GABAergic neurotransmission in the mouse. Neurosci 113:671-682.
57. Thomson AM (2000) Facilitation, augmentation and potentiation at central synapses. Trends Neurosci 23:305-312.
58. Schneggenburger R, Sakaba T, Neher E (2002) Vesicle pools and short term synaptic depression: lessons from a large synapse. Trends Neurosci 25:206-212.
59. Alabi AA, Tsien RW (2012) Synaptic vesicle pools and dynamics. Cold Spring Harb Perspect Biol 4:a013680
60. Thomson AM (2003) Presynaptic frequency- and pattern-dependent filtering. J Comput Neurosci 15:159-202.
61. Regehr WG (2012) Short-term presynaptic plasticity. Cold Spring Harb Perspect Biol 4:a005702
62. Boyes J, Bolam JP (2003) The subcellular localization of GABA(B) receptor subunits in the rat substantia nigra. Eur J Neurosci 18:3279-3293.
63. Wu LG, Saggau P (1995) GABAB receptor-mediated presynaptic inhibition in guinea-pig hippocampus is caused by reduction of presynaptic Ca2+ influx. J Physiol 485:649-657.
64. Takahashi T, Kajikawa Y, Tsujimoto T (1998) G-Protein-coupled modulation of presynaptic calcium currents and transmitter release by a GABAB receptor. J Neurosci 18:3138-3146.
65. Laviv T, Riven I, Dolev I, Vertkin I, Balana B, et al. (2010) Basal GABA regulates GABA(B)R conformation and release probability at single hippocampal synapses. Neuron 67:253-267.
66. Thanawala MS, Regehr WG (2013) Presynaptic calcium influx controls neurotransmitter release in part by regulating the effective size of the readily releasable pool. J Neurosci 33:4625-4633.
67. Barker JL, Harrison NL (1988) Outward rectification of inhibitory postsynaptic currents in cultured rat hippocampal neurones. J Physiol 403:41-55.
68. Wittmann M, Hubert GW, Smith Y, Conn PJ (2001) Activation of metabotropic glutamate receptor 1 inhibits glutamatergic transmission in the substantia nigra pars reticulata. Neurosci 105:881-889.
69. Hernandez A, Ibanez-Sandoval O, Sierra A, Valdiosera R, Tapia D, et al. (2006) Control of the subthalamic innervation of the rat globus pallidus by D2/3 and D4 dopamine receptors. J Neurophysiol 96:2877-2888.
70. Chang JY, Shi LH, Luo F, Zhang WM, Woodward DJ (2008) Studies of the neural mechanisms of deep brain stimulation in rodent models of Parkinson's disease. Neurosci Biobehav Rev 32:352-366.
71. McIntyre CC, Hahn PJ (2009) Network perspectives on the mechanisms of deep brain stimulation. Neurobiol Dis 38:329-337.
72. Kringelbach ML, Jenkinson N, Owen SL, Aziz TZ (2007) Translational principles of deep brain stimulation. Nat Rev Neurosci 8:623-635.
73. Parent M, Parent A (2007) The microcircuitry of primate subthalamic nucleus. Parkinsonism Relat Disord 13 Suppl 3:S292-S295
74. Kita H, Chang HT, Kitai ST (1983) The morphology of intracellularly labeled rat subthalamic neurons: a light microscopic analysis. J Comp Neurol 215:245-257.
75. Menalled LB, Kudwa AE, Miller S, Fitzpatrick J, Watson-Johnson J, et al. (2012) Comprehensive behavioral and molecular characterization of a new knock-in mouse model of Huntington's disease: zQ175. PLoSOne 7:e49838
76. Wojtowicz AM, Dvorzhak A, Semtner M, Grantyn R (2013) Reduced tonic inhibition in striatal output neurons from Huntington mice due to loss of astrocytic GABA release through GAT-3. Front Neural Circuits
77. Parent A, Hazrati LN (1995) Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev 20:91-127.
78. Tepper JM, Abercrombie ED, Bolam JP (2007) Basal ganglia macrocircuits. Prog Brain Res 160:3-7.