High-frequency stimulation of the subthalamic nucleus and L-3,4-dihydroxyphenylalanine inhibit in vivo serotonin release in the prefrontal cortex and hippocampus in a rat model of Parkinson's disease

Journal of Neuroscience

Volumn 30, Issue 6, 2010, Pages 2356-2364

  Navailles, Sylvia ^a   Benazzouz, Abdelhamid ^a,b   Bioulac, Bernard ^a   Gross, Christian ^a   De Deurwaerdère, Philippe ^a  

^a UMR 5287   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

[No Author keywords available]

Indexed keywords

2 DIPROPYLAMINO 8 HYDROXYTETRALIN; BENSERAZIDE; DESIPRAMINE; LEVODOPA; OXIDOPAMINE;

ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN DAMAGE; BRAIN REGION; COGNITION; ELECTROSTIMULATION; HIPPOCAMPUS; IN VIVO STUDY; INNERVATION; MALE; MICRODIALYSIS; MOOD; NERVE CELL; NEUROCHEMISTRY; NEUROMODULATION; NONHUMAN; PARKINSON DISEASE; PREFRONTAL CORTEX; PRIORITY JOURNAL; RAT; SEROTONIN RELEASE; SHAM PROCEDURE; SUBTHALAMIC NUCLEUS;

EID: 76649108189     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5031-09.2010     Document Type: Article

References (64)

1. Abercrombie ED, Bonatz AE, Zigmond MJ (1990) Effects of L-dopa on extracellular dopamine in striatum of normal and 6-hydroxydopamine-treated rats. Brain Res 525:36-44.
2. Adell A, Carceller A, Artigas F (1993) In vivo brain dialysis study of the somatodendritic release of serotonin in the Raphe nuclei of the rat: effects of 8-hydroxy-2-(di-n-propylamino) tetralin. J Neurochem 60:1673-1681.
3. Arai R, Karasawa N, Geffard M, Nagatsu I (1995) L-DOPA is converted to dopamine in serotonergic fibers of the striatum of the rat: a double-labeling immunofluorescence study. Neurosci Lett 195:195-198.
4. Bartholini G, Da Prada M, Pletscher A (1968) Decrease of cerebral 5-hydroxytryptamine by 3,4-dihydroxyphenylalanine after inhibition of extracerebral decarboxylase. J Pharm Pharmacol 20:228 -229.
5. Bejjani BP, Damier P, Arnulf I, Thivard L, Bonnet AM, Dormont D, Cornu P, Pidoux B, Samson Y, Agid Y (1999) Transient acute depression induced by high-frequency deep-brain stimulation. N Engl J Med 340:1476-1480.
6. Benabid AL, Chabardes S, Seigneuret E, Pollak P, Fraix V, Krack P, Lebas JF, Grand S, Piallat B (2005) Functional neurosurgery: past, present, and future. Clin Neurosurg 52:265-270.
7. Bhagwagar Z, Whale R, Cowen PJ (2002) State and trait abnormalities in serotonin function in major depression. Br J Psychiatry 180:24-28.
8. Biggs CS, Starr MS (1997) Dopamine and glutamate control each other's release in the basal ganglia: a microdialysis study of the entopeduncular nucleus and substantia nigra. Neurosci Biobehav Rev 21:497-504.
9. Bosker FJ, de Winter TY, Klompmakers AA, Westenberg HG (1996) Flesinoxan dose-dependently reduces extracellular 5-hydroxytryptamine (5-HT) in rat median raphe and dorsal hippocampus through activation of 5-HT1A receptors. J Neurochem 66:2546-2555.
10. Boulet S, Mounayar S, Poupard A, Bertrand A, Jan C, Pessiglione M, Hirsch EC, Feuerstein C, François C, Féger J, Savasta M, Tremblay L (2008) Behavioral recovery in MPTP-treated monkeys: neurochemical mechanisms studied by intrastriatal microdialysis. J Neurosci 28:9575-9584.
11. Breese GR, Baumeister AA, McCown TJ, Emerick SG, Frye GD, Crotty K, Mueller RA (1984) Behavioral differences between neonatal and adult 6-hydroxydopamine-treated rats to dopamine agonists: relevance to neurological symptoms in clinical syndromes with reduced brain dopamine. J Pharmacol Exp Ther 231:343-354.
12. Carta M, Carlsson T, Kirik D, Björklund A (2007) Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130:1819-1833.
13. Carta M, Carlsson T, Muñoz A, Kirik D, Björklund A (2008) Serotonin-dopamine interaction in the induction and maintenance of L-DOPA-induced dyskinesias. Prog Brain Res 172:465- 478.
14. Casanovas JM, Artigas F (1996) Differential effects of ipsapirone on 5-hydroxytryptamine release in the dorsal and median raphe neuronal pathways. J Neurochem 67:1945-1952.
15. Casanovas JM, Berton O, Celada P, Artigas F (2000) In vivo actions of the selective 5-HT1A receptor agonist BAY X 3702 on serotonergic cell firing and release. Naunyn Schmiedebergs Arch Pharmacol 362:248-254.
16. Commins DL, Shaughnessy RA, Axt KJ, Vosmer G, Seiden LS (1989) Variability among brain regions in the specificity of 6-hydroxydopamine (6-OHDA)-induced lesions. J Neural Transm 77:197-210.
17. Dauer W, Przedborski S (2003) Parkinson's disease: mechanisms and models. Neuron 39:889-909.
18. 3 receptors. J Neurosci 18:6528-6538.
19. De Deurwaerdère P, Navailles S, Berg KA, Clarke WP, Spampinato U (2004) Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J Neurosci 24:3235-3241.
20. Drevets WC, Price JL, Furey ML (2008) Brain structural and functional abnormalities in mood disorders: implications for neurocircuitry models of depression. Brain Struct Funct 213:93-118.
21. Erinoff L, Snodgrass SR (1986) Effects of adult or neonatal treatment with 6-hydroxydopamine or 5,7-dihydroxytryptamine on locomotor activity, monoamine levels, and response to caffeine. Pharmacol Biochem Behav 24:1039-1045.
22. Fraix V, Pollak P, Van Blercom N, Xie J, Krack P, Koudsie A, Benabid AL (2000) Effect of subthalamic nucleus stimulation on levodopa-induced dyskinesia in Parkinson's disease. Neurology 55:1921-1923.
23. Guiard BP, El Mansari M, Merali Z, Blier P (2008) Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. Int J Neuropsychopharmacol 11:625-639.
24. Haber SN, Brucker JL (2009) Cognitive and limbic circuits that are affected by deep brain stimulation. Front Biosci 14:1823-1834.
25. Hauser RA (2009) Levodopa: past, present, and future. Eur Neurol 62:1-8.
26. Hervás I, Bel N, Fernández AG, Palacios JM, Artigas F (1998) In vivo control of 5-hydroxytryptamine release by terminal autoreceptors in rat brain areas differentially innervated by the dorsal and median raphe nuclei. Naunyn Schmiedebergs Arch Pharmacol 358:315-322.
27. Invernizzi R, Velasco C, Bramante M, Longo A, Samanin R (1997) Effect of 5-HT1A receptor antagonists on citalopram-induced increase in extracellular serotonin in the frontal cortex, striatum and dorsal hippocampus. Neuropharmacology 36:467-473.
28. Iwamoto ET, Loh HH, Way EL (1976) Circling behavior in rats with 6-hydroxydopamine or electrolytic nigral lesions. Eur J Pharmacol 37:339-356.
29. Kannari K, Yamato H, Shen H, Tomiyama M, Suda T, Matsunaga M (2001) Activation of 5-HT(1A) but not 5-HT(1B) receptors attenuates an increase in extracellular dopamine derived from exogenously administered L-DOPA in the striatum with nigrostriatal denervation. J Neurochem 76:1346-1353.
30. Kaya AH, Vlamings R, Tan S, Lim LW, Magill PJ, Steinbusch HW, Visser-Vandewalle V, Sharp T, Temel Y (2008) Increased electrical and metabolic activity in the dorsal raphe nucleus of parkinsonian rats. Brain Res 1221:93-97.
31. Kish SJ, Tong J, Hornykiewicz O, Rajput A, Chang LJ, Guttman M, Furukawa Y (2008) Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 131:120-131.
32. Kreiss DS, Lucki I (1994) Differential regulation of serotonin (5-HT) release in the striatum and hippocampus by 5-HT1A autoreceptors of the dorsal and median raphe nuclei. J Pharmacol Exp Ther 269:1268-1279.
33. Lacombe E, Carcenac C, Boulet S, Feuerstein C, Bertrand A, Poupard A, Savasta M (2007) High-frequency stimulation of the subthalamic nucleus prolongs the increase in striatal dopamine induced by acute L-3,4-dihydroxyphenylalanine in dopaminergic denervated rats. Eur J Neurosci 26:1670-1680.
34. Lundblad M, af Bjerkén S, Cenci MA, Pomerleau F, Gerhardt GA, Strömberg I (2009) Chronic intermittent L-DOPA treatment induces changes in dopamine release. J Neurochem 108:998-1008.
35. Mallet N, Ballion B, Le Moine C, Gonon F (2006) Cortical inputs and GABA interneurons imbalance projection neurons in the striatum of parkinsonian rats. J Neurosci 26:3875-3884.
36. Melamed E, Zoldan J, Friedberg G, Ziv I, Weizmann A (1996) Involvement of serotonin in clinical features of Parkinson's disease and complications of L-DOPA therapy. Adv Neurol 69:545-550.
37. Molliver ME (1987) Serotonergic neuronal systems: what their anatomic organization tells us about function. J Clin Psychopharmacol 7: 3S-23S.
38. Moro E, Scerrati M, Romito LM, Roselli R, Tonali P, Albanese A (1999) Chronic subthalamic nucleus stimulation reduces medication requirements in Parkinson's disease. Neurology 53:85-90.
39. Navailles S, Bioulac B, Gross C, De Deurwaerdère P (2010) Serotonergic neurons mediate ectopic release of dopamine induced by L-DOPA in a rat model of Parkinson's disease. Neurobiol Dis. Advance online publication. Retrieved January 29, 2010. doi:10.1016/j.nbd.2010.01.012.
40. Ng KY, Chase TN, Colburn RW, Kopin IJ (1970) L-Dopa-induced release of cerebral monoamines. Science 170:76-77.
41. Nieoullon A (2002) Dopamine and the regulation of cognition and attention. Prog Neurobiol 67:53-83.
42. Nimura T, Yamaguchi K, Ando T, Shibuya S, Oikawa T, Nakagawa A, Shirane R, Itoh M, Tominaga T (2005) Attenuation of fluctuating striatal synaptic dopamine levels in patients with Parkinson disease in response to subthalamic nucleus stimulation: a positron emission tomography study. J Neurosurg 103:968-973.
43. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates. New York: Academic.
44. Piasecki SD, Jefferson JW (2004) Psychiatric complications of deep brain stimulation for Parkinson's disease. J Clin Psychiatry 65:845-849.
45. Piñeyro G, Blier P (1999) Autoregulation of serotonin neurons: role in antidepressant drug action. Pharmacol Rev 51:533-591.
46. Romero L, Artigas F (1997) Preferential potentiation of the effects of serotonin uptake inhibitors by 5-HT1A receptor antagonists in the dorsal raphe pathway: role of somatodendritic autoreceptors. J Neurochem 68:2593-2603.
47. Rommelfanger KS, Weinshenker D (2007) Norepinephrine: the redheaded stepchild of Parkinson's disease. Biochem Pharmacol 74:177-190.
48. Scholtissen B, Verhey FR, Adam JJ, Weber W, Leentjens AF (2006) Challenging the serotonergic system in Parkinson disease patients: effects on cognition, mood, and motor performance. Clin Neuropharmacol 29:276-285.
49. Seeman P (1980) Brain dopamine receptors. Pharmacol Rev 32:229-313.
50. Sharp T, Bramwell SR, Hjorth S, Grahame-Smith DG (1989) Pharmacological characterization of 8-OH-DPAT-induced inhibition of rat hippocampal 5-HT release in vivo as measured by microdialysis. Br J Pharmacol 98:989-997.
51. Siri C, Cilia R, De Gaspari D, Canesi M, Meucci N, Zecchinelli AL, Pezzoli G, Antonini A (2009) Cognitive status of patients with Parkinson's disease and pathological gambling. J Neurol. Advance online publication. Retrieved January 20, 2010. doi:10.1007/s00415-009-5301-5.
52. Smith KA, Fairburn CG, Cowen PJ (1997) Relapse of depression after rapid depletion of tryptophan. Lancet 349:915-919.
53. Sprouse JS, Aghajanian GK (1987) Electrophysiological responses of serotoninergic dorsal raphe neurons to 5-HT1A and 5-HT1B agonists. Synapse 1:3-9.
54. Takeuchi Y, Sawada T, Blunt S, Jenner P, Marsden CD (1991) Effects of 6-hydroxydopamine lesions of the nigrostriatal pathway on striatal serotonin innervation in adult rats. Brain Res 562:301-305.
55. Tanaka H, Kannari K, Maeda T, Tomiyama M, Suda T, Matsunaga M (1999) Role of serotonergic neurons in L-DOPA-derived extracellular dopamine in the striatum of 6-OHDA-lesioned rats. Neuroreport 10:631-634.
56. Taylor TN, Caudle WM, Shepherd KR, Noorian A, Jackson CR, Iuvone PM, Weinshenker D, Greene J, Miller GW (2009) Nonmotor symptoms of Parkinson's disease revealed in an animal model with reduced monoamine storage capacity. J Neurosci 29:8103-8113.
57. Temel Y, Boothman LJ, Blokland A, Magill PJ, Steinbusch HW, Visser-Vandewalle V, Sharp T (2007) Inhibition of 5-HT neuron activity and induction of depressive-like behavior by high-frequency stimulation of the subthalamic nucleus. Proc Natl Acad Sci U S A 104: 17087-17092.
58. Uretsky NJ, Schoenfeld RI (1971) Effect of L-dopa on the locomotor activity of rats pretreated with 6-hydroxydopamine. Nat New Biol 234:157-159.
59. Van Rooden SM, Visser M, Verbaan D, Marinus J, van Hilten JJ (2009) Patterns of motor and non-motor features in Parkinson's disease. J Neurol Neurosurg Psychiatry 80:846-850.
60. Vertes RP (1991) A PHA-L analysis of ascending projections of the dorsal raphe nucleus in the rat. J Comp Neurol 313:643-668.
61. Vertes RP (2006) Interactions among the medial prefrontal cortex, hippocampus and midline thalamus in emotional and cognitive processing in the rat. Neuroscience 142:1-20.
62. Wang S, Zhang QJ, Liu J, Wu ZH, Wang T, Gui ZH, Chen L, Wang Y (2009) Unilateral lesion of the nigrostriatal pathway induces an increase of neuronal firing of the midbrain raphe nuclei 5-HT neurons and a decrease of their response to 5-HT(1A) receptor stimulation in the rat. Neuroscience 159:850-861.
63. Zesiewicz TA, Hauser RA (2002) Depression in Parkinson's disease. Curr Psychiatry Rep 4:69-73.
64. Zhou FC, Bledsoe S, Murphy J (1991) Serotonergic sprouting is induced by dopamine-lesion in substantia nigra of adult rat brain. Brain Res 556: 108-116.