Inhibiting subthalamic d5 receptor constitutive activity alleviates abnormal electrical activity and reverses motor impairment in a rat model of parkinson's disease

Journal of Neuroscience

Volumn 33, Issue 37, 2013, Pages 14840-14849

  Chetrit, Jonathan ^a,b   Taupignon, Anne ^a,b   Froux, Lionel ^a,b   Morin, Stephanie ^a,b   Bouali Benazzouz, Rabia ^c   Naudet, Frédéric ^a,b   Kadiri, Nabila ^a,b   Gross, Christian E ^a,b   Bioulac, Bernard ^a,b   Benazzouz, Abdelhamid ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^c University of Bordeaux   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,4,5 TETRAHYDRO 7,8 DIHYDROXY 1 PHENYL 1H-3 BENAZEPINE HYDROCHLORIDE; 3 AMINO 2 (3 CARBOXYPROPYL) 6 (4 METHOXYPHENYL)PYRIDAZINIUM BROMIDE; 7 CHLORO 8 HYDROXY 3 METHYL 1 PHENYL 2,3,4,5 TETRAHYDRO 1H 3 BENZAZEPINE HYDROCHLORIDE; BUTACLAMOL; CALCISEPTINE; CYTOCHROME C OXIDASE; DOPAMINE 5 RECEPTOR; FLUPENTIXOL; FLUPHENAZINE; OXIDOPAMINE; RACLOPRIDE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTORADIOGRAPHY; BEHAVIOR; CONTROLLED STUDY; DEPOLARIZATION; ELECTROPHYSIOLOGY; FEMALE; HISTOGRAM; LOCOMOTION; MALE; MEDIAL FOREBRAIN BUNDLE; MICROPHOTOGRAPHY; MOTOR DYSFUNCTION; NEUROANATOMY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SPIKE; SUBSTANTIA NIGRA PARS RETICULATA; SUBTHALAMIC NUCLEUS;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; DISEASE MODELS, ANIMAL; DOPAMINE AGONISTS; DOPAMINE ANTAGONISTS; DOSE-RESPONSE RELATIONSHIP, DRUG; FEMALE; FLUPENTHIXOL; LOCOMOTION; MALE; NEURONS; OXIDOPAMINE; PARKINSON DISEASE; RACLOPRIDE; RATS; RATS, WISTAR; RECEPTORS, DOPAMINE D5; STATISTICS, NONPARAMETRIC; SUBTHALAMIC NUCLEUS;

EID: 84883720493     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0453-13.2013     Document Type: Article

References (62)

1. Abedi PM, Delaville C, De Deurwaerdère P, Benjelloun W, Benazzouz A (2013) Intrapallidal administration of 6-hydroxydopamine mimics in large part the electrophysiological and behavioral consequences of major dopamine depletion in the rat. Neuroscience 236:289-297. CrossRef Medline
2. Akaoka H, Aston-Jones G (1991) Opiate withdrawal-induced hyperactivity of locus coeruleus neurons is substantially mediated by augmented excitatory amino acid input. J Neurosci 11:3830-3839.
3. Medline Albin RL, Young AB, Penney JB (1989) The functional anatomy of basal ganglia disorders. Trends Neurosci 12:366-375. CrossRef Medline
4. Atherton JF, Kitano K, Baufreton J, Fan K, Wokosin D, Tkatch T, Shigemoto R, Surmeier DJ, Bevan MD (2010) Selective participation of somatodendriticHCNchannels in inhibitory but not excitatory synaptic integration in neurons of the subthalamic nucleus. J Neurosci 30:16025-16040. CrossRef Medline
5. Augood SJ, Hollingsworth ZR, Standaert DG, Emson PC, Penney JB Jr (2000) Localization of dopaminergic markers in the human subthalamic nucleus. J Comp Neurol 421:247-255. CrossRef Medline
6. Baufreton J, Bevan MD (2008) D2-like dopamine receptor-mediated modulation of activity-dependent plasticity at GABAergic synapses in the subthalamic nucleus. J Physiol 586:2121-2142. CrossRef Medline
7. Baufreton J, Garret M, Rivera A, de la Calle A, Gonon F, Dufy B, Bioulac B, Taupignon A (2003) D5 (not D1) dopamine receptors potentiate burstfiring in neurons of the subthalamic nucleus by modulating an L-type calcium conductance. J Neurosci 23:816-825.
8. Medline Baufreton J, Zhu ZT, Garret M, Bioulac B, Johnson SW, Taupignon AI (2005) Dopamine receptors set the pattern of activity generated in subthalamic neurons. FASEB J 19:1771-1777. CrossRef Medline
9. Belujon P, Bezard E, Taupignon A, Bioulac B, Benazzouz A (2007) Noradrenergic modulation of subthalamic nucleus activity: behavioral and electrophysiological evidence in intact and 6-hydroxydopamine-lesioned rats. J Neurosci 27:9595-9606. CrossRef Medline
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.CrossRef Medline
11. Benazzouz A, Tai CH, Meissner W, Bioulac B, Bezard E, Gross C (2004) High-frequency stimulation of both zona incerta and subthalamic nucleus induces a similar normalization of basal ganglia metabolic activity in experimental parkinsonism. FASEB J 18:528-530. CrossRef Medline
12. Benedetti F, Colloca L, Torre E, Lanotte M, Melcarne A, Pesare M, Bergamasco B, Lopiano L (2004) Placebo-responsive Parkinson patients show decreased activity in single neurons of subthalamic nucleus. Nat Neurosci 7:587-588. CrossRef Medline
13. Bergman H, Wichmann T, DeLong MR (1990) Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 249: 1436-1438. CrossRef Medline
14. 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. Medline
15. Blandini F, Levandis G, Bazzini E, Nappi G, Armentero MT (2007) Timecourse of nigrostriatal damage, basal ganglia metabolic changes and behavioural alterations following intrastriatal injection of 6-hydroxydopamine in the rat: new clues from an old model. Eur J Neurosci 25:397-405. CrossRef Medline
16. Bouali-Benazzouz R, Tai CH, Chetrit J, Benazzouz A (2009) Intrapallidal injection of 6-hydroxydopamine induced changes in dopamine innervation and neuronal activity of globus pallidus. Neuroscience 164:588-596. CrossRef Medline
17. Boyson SJ, McGonigle P, Molinoff PB (1986) Quantitative autoradiographic localization of the D1 and D2 subtypes of dopamine receptors in rat brain. J Neurosci 6:3177-3188. Medline
18. Cavanagh JF, Wiecki TV, Cohen MX, Figueroa CM, Samanta J, Sherman SJ, Frank MJ (2011) Subthalamic nucleus stimulation reverses mediofrontal influence over decision threshold. Nat Neurosci 14:1462-1467. CrossRef Medline
19. Charpentier S, Jarvie KR, Severynse DM, Caron MG, Tiberi M (1996) Silencing of the constitutive activity of the dopamine D1B receptor. Reciprocal mutations between D1 receptor subtypes delineate residues underlying activation properties. J Biol Chem 271:28071-28076. CrossRef Medline
20. Chetrit J, Ballion B, Laquitaine S, Belujon P, Morin S, Taupignon A, Bioulac B, Gross CE, Benazzouz A (2009) Involvement of basal ganglia network in motor disabilities induced by typical antipsychotics. PLoS One 4:e6208. CrossRef Medline
21. Cragg SJ, Baufreton J, Xue Y, Bolam JP, Bevan MD (2004) Synaptic release of dopamine in the subthalamic nucleus. Eur J Neurosci 20:1788-1802. CrossRef Medline
22. Cruz AV, Mallet N, Magill PJ, Brown P, Averbeck BB (2011) Effects of dopamine depletion on information flow between the subthalamic nucleus and external globus pallidus. J Neurophysiol 106:2012-2023. CrossRef Medline
23. D'Aoust JP, Tiberi M (2010) Role of the extracellular amino terminus and first membrane-spanning helix of dopamine D1 and D5 receptors in shaping ligand selectivity and efficacy. Cell Signal 22:106-116. CrossRef Medline
24. Demchyshyn LL, McConkey F, Niznik HB (2000) Dopamine D5 receptor agonist high affinity and constitutive activity profile conferred by carboxyl-terminal tail sequence. J Biol Chem 275:23446-23455. CrossRef Medline
25. Dutton A, Dyball RE (1979) Phasic firing enhances vasopressin release from the rat neurohypophysis. J Physiol 290:433-440. Medline
26. Fremeau RT Jr, Duncan GE, Fornaretto MG, Dearry A, Gingrich JA, Breese GR, Caron MG (1991) Localization of D1 dopamine receptor mRNA in brain supports a role in cognitive, affective, and neuroendocrine aspects of dopaminergic neurotransmission. Proc Natl Acad Sci U S A 88:3772-3776. CrossRef Medline
27. Galvan A, Wichmann T (2008) Pathophysiology of parkinsonism. Clin Neurophysiol 119:1459-1474. CrossRef Medline
28. Gonon FG (1988) Nonlinear relationship between impulse flow and dopamine released by rat midbrain dopaminergic neurons as studied by in vivo electrochemistry. Neuroscience 24:19-28. CrossRef Medline
29. Haynes WI, Haber SN (2013) The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for Basal Ganglia models and deep brain stimulation. J Neurosci 33:4804-4814. CrossRef Medline
30. Hirsch EC, Périer C, Orieux G, François C, Féger J, Yelnik J, Vila M, Levy R, Tolosa ES, Marin C, Trinidad Herrero M, Obeso JA, Agid Y (2000) Metabolic effects of nigrostriatal denervation in basal ganglia. Trends Neurosci 23:S78-S85. CrossRef Medline
31. Kaneoke Y, Vitek JL (1996) Burst and oscillation as disparate neuronal properties. J Neurosci Methods 68:211-223. CrossRef Medline
32. Laffray S, Bouali-Benazzouz R, Papon MA, Favereaux A, Jiang Y, Holm T, Spriet C, Desbarats P, Fossat P, Le Feuvre Y, Decossas M, Héliot L, Langel U, Nagy F, Landry M (2012) Impairment of GABAB receptor dimer by endogenous 14-3-3 in chronic pain conditions. EMBO J 31:3239-3251. CrossRef Medline
33. Leventhal DK, Gage GJ, Schmidt R, Pettibone JR, Case AC, Berke JD (2012) Basal ganglia beta oscillations accompany cue utilization. Neuron 73:523-536. CrossRef Medline
34. Levy R, Lang AE, Dostrovsky JO, Pahapill P, Romas J, Saint-Cyr J, Hutchison WD, Lozano AM (2001) Lidocaine and muscimol microinjections in subthalamic nucleus reverse Parkinsonian symptoms. Brain 124:2105-2118. CrossRef Medline
35. Limousin P, Krack P, Pollak P, Benazzouz A, Ardouin C, Hoffmann D, Benabid AL (1998) Electrical stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med 339:1105-1111. CrossRef Medline
36. Lundberg JM, Rudehill A, Sollevi A, Theodorsson-Norheim E, Hamberger B (1986) Frequency- and reserpine-dependent chemical coding of sympathetic transmission: differential release of noradrenaline and neuropeptide Y from pig spleen. Neurosci Lett 63:96-100. CrossRef Medline
37. Luo J, Kaplitt MG, Fitzsimons HL, Zuzga DS, Liu Y, Oshinsky ML, During MJ (2002) Subthalamic GAD gene therapy in a Parkinson's disease rat model. Science 298:425- 429. CrossRef Medline
38. 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. CrossRef Medline
39. Mallet N, Pogosyan A, Sharott A, Csicsvari J, Bolam JP, Brown P, Magill PJ (2008) Disrupted dopamine transmission and the emergence of exaggerated beta oscillations in subthalamic nucleus and cerebral cortex. J Neurosci 28:4795- 4806. CrossRef Medline
40. Martin MW, Scott AW, Johnston DE Jr, Griffin S, Luedtke RR (2001) Typical antipsychotics exhibit inverse agonist activity at rat dopamine D1-like receptors expressed in Sf9 cells. Eur J Pharmacol 420:73-82. CrossRef Medline
41. Miguelez C, Morin S, Martinez A, Goillandeau M, Bezard E, Bioulac B, Baufreton J (2012) Altered pallido-pallidal synaptic transmission leads to aberrant firing of globus pallidus neurons in a rat model of Parkinson's disease. J Physiol 590:5861-5875. CrossRef Medline
42. Nakanishi H, Kita H, Kitai ST (1987) Electrical membrane properties of rat subthalamic neurons in an in vitro slice preparation. Brain Res 437:35-44. CrossRef Medline
43. Ni Z, Gao D, Bouali-Benazzouz R, Benabid AL, Benazzouz A (2001a) Effect of microiontophoretic application of dopamine on subthalamic nucleus neuronal activity in normal rats and in rats with unilateral lesion of the nigrostriatal pathway. Eur J Neurosci 14:373-381. CrossRef Medline
44. Ni Z, Bouali-Benazzouz R, Gao D, Benabid AL, Benazzouz A (2001b) Intrasubthalamic injection of 6-hydroxydopamine induces changes in the firing rate and pattern of subthalamic nucleus neurons in the rat. Synapse 40:145-153. CrossRef Medline
45. O'Connor KA, Porrino LJ, Davies HM, Childers SR (2005) Time-dependent changes in receptor/G-protein coupling in rat brain following chronicmonoamine transporter blockade. J Pharmacol Exp Ther 313:510-517. CrossRef Medline
46. Olsson M, Nikkhah G, Bentlage C, Björklund A (1995) Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J Neurosci 15:3863-3875. Medline
47. Paxinos G, Watson C (1996) The rat brain in stereotaxic coordinates. New York: Academic.
48. Périer C, Vila M, Féger J, Agid Y, Hirsch EC (2000) Functional activity of zona incerta neurons is altered after nigrostriatal denervation in hemiparkinsonian rats. Exp Neurol 162:215-224. CrossRef Medline
49. Rommelfanger KS, Wichmann T (2010) Extrastriatal dopaminergic circuits of the basal ganglia. Front Neuroanat 4:139. CrossRef Medline
50. Salin P, Manrique C, Forni C, Kerkerian-Le Goff L (2002) High-frequency stimulation of the subthalamic nucleus selectively reverses dopamine denervation-induced cellular defects in the output structures of the basal ganglia in the rat. J Neurosci 22:5137-5148. Medline
51. Sim LJ, Selley DE, Childers SR (1995) In vitro autoradiography of receptoractivated G proteins in rat brain by agonist-stimulated guanylyl 5'- [gamma-[35S]thio]-triphosphate binding. Proc Natl Acad Sci U S A 92: 7242-7246. CrossRef Medline
52. Smith Y, Villalba R (2008) Striatal and extrastriatal dopamine in the basal ganglia: an overview of its anatomical organization in normal and Parkinsonian brains. Mov Disord 23 [Suppl 3]:S534-S547. CrossRef
53. Surmeier DJ, Bevan MD (2003) "The little engine that could": voltagedependent Na() channels and the subthalamic nucleus. Neuron 39:5- 6. CrossRef Medline
54. Svenningsson P, Le Moine C (2002) Dopamine D1/5 receptor stimulation induces c-fos expression in the subthalamic nucleus: possible involvement of local D5 receptors. Eur J Neurosci 15:133-142. CrossRef Medline
55. Tai CH, Boraud T, Bezard E, Bioulac B, Gross C, Benazzouz A (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. CrossRef Medline
56. Tai CH, Pan MK, Lin JJ, Huang CS, Yang YC, Kuo CC (2012) Subthalamic discharges as a causal determinant of parkinsonin motor deficits. Ann Neurol 72:464-476.
57. Tiberi M, Caron MG (1994) High agonist-independent activity is a distinguishing feature of the dopamine D1B receptor subtype. J Biol Chem 269:27925-27931. Medline
58. Tseng KY, Kargieman L, Gacio S, Riquelme LA, Murer MG (2005) Consequences of partial and severe dopaminergic lesion on basal ganglia oscillatory activity and akinesia. Eur J Neurosci 22:2579-2586. CrossRef Medline
59. Tumova K, Iwasiow RM, Tiberi M (2003) Insight into the mechanism of dopamine D1-like receptor activation. Evidence for a molecular interplay between the third extracellular loop and the cytoplasmic tail. J Biol Chem 278:8146-8153. CrossRef Medline
60. Tumova K, Zhang D, Tiberi M (2004) Role of the fourth intracellular loop of D1-like dopaminergic receptors in conferring subtype-specific signaling properties. FEBS Lett 576:461-467. CrossRef Medline
61. Vila M, Périer C, Féger J, Yelnik J, Faucheux B, Ruberg M, Raisman-Vozari 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. CrossRef Medline
62. Wilson CJ, Bevan MD (2011) Intrinsic dynamics and synaptic inputs control the activity patterns of subthalamic nucleus neurons in health and in Parkinson's disease. Neuroscience 198:54-68. CrossRef Medline