Widespread monoaminergic dysregulation of both motor and non-motor circuits in parkinsonism and dyskinesia

Cerebral Cortex

Volumn 25, Issue 9, 2015, Pages 2783-2792

  Engeln, Michel ^a   De Deurwaerdère, Philippe ^a   Li, Qin ^b   Bezard, Erwan ^a,b   Fernagut, PierreOlivier ^a  

^a INSTITUT DES MALADIES NEURODÉGÉNÉRATIVES   (France)

^b INSTITUTE OF LABORATORY ANIMAL SCIENCE   (China)

Author keywords

Limbic; Monkey; MPTP; Parkinson's disease; Serotonin

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; BRAIN MONOAMINE; DOPAMINE; LEVODOPA; NORADRENALIN; SEROTONIN; ANTIPARKINSON AGENT; BIOGENIC AMINE;

AMYGDALA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; DOPAMINE BRAIN LEVEL; EXPOSURE; FEMALE; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HIPPOCAMPUS; LEVODOPA-INDUCED DYSKINESIA; LIMBIC SYSTEM; LONG TERM CARE; MONOAMINE METABOLISM; MONOAMINE RELEASE; MONOAMINERGIC SYSTEM; MOTOR CORTEX; MPTP-INDUCED PARKINSONISM; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PUTAMEN; RHESUS MONKEY; SEROTONIN BRAIN LEVEL; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; DISEASE MODEL; DYSKINESIA; METABOLISM; MPTP POISONING; NERVE TRACT; PATHOLOGY; TIME FACTOR;

ANALYSIS OF VARIANCE; ANIMALS; ANTIPARKINSON AGENTS; BIOGENIC MONOAMINES; BRAIN; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DISEASE MODELS, ANIMAL; DYSKINESIA, DRUG-INDUCED; FEMALE; LEVODOPA; MACACA MULATTA; MPTP POISONING; NEURAL PATHWAYS; TIME FACTORS;

EID: 84965190258     PISSN: 10473211     EISSN: 14602199     Source Type: Journal    
DOI: 10.1093/cercor/bhu076     Document Type: Article

References (72)

1. Aghajanian GK, Marek GJ. 1997. Serotonin induces excitatory postsynaptic potentials in apical dendrites of neocortical pyramidal cells. Neuropharmacology. 36: 589-599.
2. Ahlskog JE 2007. Beating a dead horse: dopamine and Parkinson disease. Neurology. 69: 1701-1711.
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. Aston-Jones G, Zhu Y, Card JP. 2004. Numerous GABAergic afferents to locus ceruleus in the pericerulear dendritic zone: possible interneuronal pool. J Neurosci. 24: 2313-2321.
5. Azmitia EC, Segal M. 1978. An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol. 179: 641-667.
6. Bastide MF, Dovero S, Charron G, Porras G, Gross CE, Fernagut PO, Bezard E. 2014. Immediate-early gene expression in structures outside the basal ganglia is associated to L-DOPA-induced dyskinesia. Neurobiol Dis. 62: 179-192.
7. Bezard E, Brotchie JM, Gross CE. 2001. Pathophysiology of levodopa-induced dyskinesia: potential for new therapies. Nat Rev Neurosci. 2: 577-588.
8. Bezard E, Dovero S, Prunier C, Ravenscroft P, Chalon S, Guilloteau D, Crossman AR, Bioulac B, Brotchie JM, Gross CE. 2001. Relationship between the appearance of symptoms and the level of nigrostriatal degeneration in a progressive 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-lesioned macaque model of Parkinson's disease. J Neurosci. 21: 6853-6861.
9. Bezard E, Imbert C, Deloire X, Bioulac B, Gross CE. 1997. A chronic MPTP model reproducing the slow evolution of Parkinson's disease: evolution of motor symptoms in the monkey. Brain Res. 766: 107-112.
10. Bjorklund A, Dunnett SB. 2007. Dopamine neuron systems in the brain: an update. Trends Neurosci. 30: 194-202.
11. Blanquat PD, Hok V, Save E, Poucet B, Chaillan FA. 2013. Differential role of the dorsal hippocampus, ventro-intermediate hippocampus, and medial prefrontal cortex in updating the value of a spatial goal. Hippocampus. 23(5):342-351.
12. Bonnet AM, Loria Y, Saint-Hilaire MH, Lhermitte F, Agid Y. 1987. Does long-term aggravation of Parkinson's disease result from nondopa-minergic lesions? Neurology. 37: 1539-1542.
13. Brooks DJ, Piccini P, Turjanski N, Samuel M. 2000. Neuroimaging of dyskinesia. Ann Neurol. 47: S154-S158; discussion S158-S159.
14. Carey RJ, Pinheiro-Carrera M, Dai H, Tomaz C, Huston JP. 1995. L-DOPA and psychosis: evidence for L-DOPA-induced increases in prefrontal cortex dopamine and in serum corticosterone. Biol Psychiatry. 38: 669-676.
15. Carta M, Carlsson T, Kirik D, Bjorklund A. 2007. Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain. 130: 1819-1833.
16. Carta M, Lindgren HS, Lundblad M, Stancampiano R, Fadda F, Cenci MA. 2006. Role of striatal L-DOPA in the production of dyskinesia in 6-hydroxydopamine lesioned rats. J Neurochem. 96: 1718-1727.
17. Chalmers JP, Baldessarini RJ, Wurtman RJ. 1971. Effects of L-dopa on norepinephrine metabolism in the brain. Proc Natl Acad Sci USA. 68: 662-666.
18. Chaudhuri KR, Healy DG, Schapira AH. 2006. Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol. 5: 235-245.
19. Chotibut T, Apple DM, Jefferis R, Salvatore MF. 2012. Dopamine transporter loss in 6-OHDA Parkinson's model is unmet by parallel reduction in dopamine uptake. PLoS One. 7: e52322.
20. Chudasama Y, Doobay VM, Liu Y. 2012. Hippocampal-prefrontal cortical circuit mediates inhibitory response control in the rat. J Neurosci. 32: 10915-10924.
21. De Deurwaerdere P, Bonhomme N, Le Moal M, Spampinato U. 1995. d-Fenfluramine increases striatal extracellular dopamine in vivo independently of serotonergic terminals or dopamine uptake sites. J Neurochem. 65: 1100-1108.
22. De Deurwaerdere P, Stinus L, Spampinato U. 1998. Opposite change of in vivo dopamine release in the rat nucleus accumbens and striatum that follows electrical stimulation of dorsal raphe nucleus: role of 5-HT3 receptors. J Neurosci. 18: 6528-6538.
23. Delaville C, Chetrit J, Abdallah K, Morin S, Cardoit L, De Deurwaerdere P, Benazzouz A. 2012. Emerging dysfunctions consequent to combined monoaminergic depletions in Parkinsonism. Neurobiol Dis. 45: 763-773.
24. Ehringer H, Hornykiewicz O. 1960. [Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system]. Klin Wochenschr. 38: 1236-1239.
25. Eskow Jaunarajs KL, Dupre KB, Ostock CY, Button T, Deak T, Bishop C. 2010. Behavioral and neurochemical effects of chronic L-DOPA treatment on nonmotor sequelae in the hemiparkinsonian rat. Behav Pharmacol. 21: 627-637.
26. Eskow Jaunarajs KL, George JA, Bishop C. 2012. L-DOPA-induced dysregulation of extrastriatal dopamine and serotonin and affective symptoms in a bilateral rat model of Parkinson's disease. Neuroscience. 218: 243-256.
27. Fasano S, Bezard E, D'Antoni A, Francardo V, Indrigo M, Qin L, Dovero S, Cerovic M, Cenci MA, Brambilla R. 2010. Inhibition of Rasguanine nucleotide-releasing factor 1 (Ras-GRF1) signaling in the striatum reverts motor symptoms associated with L-dopa-induced dyskinesia. Proc Natl Acad Sci USA. 107: 21824-21829.
28. Fernagut PO, Li Q, Dovero S, Chan P, Wu T, Ravenscroft P, Hill M, Chen Z, Bezard E. 2010. Dopamine transporter binding is unaffected by L-DOPA administration in normal and MPTP-treated monkeys. PLoS One. 5: e14053.
29. Fitoussi A, Dellu-Hagedorn F, De Deurwaerdere P. 2013. Monoamines tissue content analysis reveals restricted and site-specific correlations in brain regions involved in cognition. Neuroscience. 255: 233-245.
30. Forsaa EB, Larsen JP, Wentzel-Larsen T, Goetz CG, Stebbins GT, Aarsland D, Alves G. 2010. A 12-year population-based study of psychosis in Parkinson disease. Arch Neurol. 67: 996-1001.
31. Fox SH, Johnston TH, Li Q, Brotchie J, Bezard E. 2012. A critique of available scales and presentation of the Non-Human Primate Dyskinesia Rating Scale. Mov Disord. 27: 1373-1378.
32. Frank MJ, Seeberger LC, O'Reilly RC. 2004. By carrot or by stick: cognitive reinforcement learning in parkinsonism. Science. 306: 1940-1943.
33. Gauggel S, Rieger M, Feghoff TA. 2004. Inhibition of ongoing responses in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry. 75: 539-544.
34. Graybiel AM, Canales JJ, Capper-Loup C. 2000. Levodopa-induced dyskinesias and dopamine-dependent stereotypies: a new hypothesis. Trends Neurosci. 23:S71-S77.
35. Guigoni C, Li Q, Aubert I, Dovero S, Bioulac BH, Bloch B, Crossman AR, Gross CE, Bezard E. 2005. Involvement of sensorimotor, limbic, and associative basal ganglia domains in L-3,4-dihydroxyphenylalanineinduced dyskinesia. J Neurosci. 25: 2102-2107.
36. Halliday GM, Li YW, Blumbergs PC, Joh TH, Cotton RG, Howe PR, Blessing WW, Geffen LB. 1990. Neuropathology of immunohisto-chemically identified brainstem neurons in Parkinson's disease. Ann Neurol. 27: 373-385.
37. Hill MP, Ravenscroft P, Bezard E, Crossman AR, Brotchie JM, Michel A, Grimee R, Klitgaard H. 2004. Levetiracetam potentiates the antidyskinetic action of amantadine in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-lesioned primate model of Parkinson's disease. J Pharmacol Exp Ther. 310: 386-394.
38. Imbert C, Bezard E, Guitraud S, Boraud T, Gross CE. 2000. Comparison of eight clinical rating scales used for the assessment of MPTP-induced parkinsonism in the Macaque monkey. J Neurosci Methods. 96: 71-76.
39. Jellinger KA 1991. Pathology of Parkinson's disease. Changes other than the nigrostriatal pathway. Mol Chem Neuropathol. 14: 153-197.
40. Lee AH, Weintraub D. 2012. Psychosis in Parkinson's disease without dementia: common and comorbid with other non-motor symptoms. Mov Disord. 27: 858-863.
41. Lodge DJ, Grace AA. 2008. Amphetamine activation of hippocampal drive of mesolimbic dopamine neurons: a mechanism of behavioral sensitization. J Neurosci. 28: 7876-7882.
42. Loeffler DA, LeWitt PA, Juneau PL, Camp DM, Arnold LA, Hyland K. 1998. Time-dependent effects of levodopa on regional brain dopamine metabolism and lipid peroxidation. Brain Res Bull. 47: 663-667.
43. Lowry OH, Rosebrough NJ, Farr AL, Randall RJ. 1951. Protein measurement with the Folin phenol reagent. J Biol Chem. 193: 265-275.
44. Martin RF, Bowden DM. 2000. Primate brain maps: structure of the macaque brain. Amsterdam: Elsevier Science.
45. Meissner WG, Frasier M, Gasser T, Goetz CG, Lozano A, Piccini P, Obeso JA, Rascol O, Schapira A, Voon V et al. 2011. Priorities in Parkinson's disease research. Nat Rev Drug Discov. 10: 377-393.
46. Melamed E, Hefti F, Pettibone DJ, Liebman J, Wurtman RJ. 1981. Aromatic L-amino acid decarboxylase in rat corpus striatum: implications for action of L-dopa in parkinsonism. Neurology. 31: 651-655.
47. Miguelez C, Berrocoso E, Mico JA, Ugedo L. 2013. l-DOPA modifies the antidepressant-like effects of reboxetine and fluoxetine in rats. Neuropharmacology. 67: 349-358.
48. Mink JW 1996. The basal ganglia: focused selection and inhibition of competing motor programs. Prog Neurobiol. 50: 381-425.
49. Mitchell IJ, Boyce S, Sambrook MA, Crossman AR. 1992. A 2-deoxyglucose study of the effects of dopamine agonists on the parkinsonian primate brain. Implications for the neural mechanisms that mediate dopamine agonist-induced dyskinesia. Brain. 115 (Pt 3):809-824.
50. Navailles S, Bioulac B, Gross C, De Deurwaerdere P. 2011. Chronic L-DOPA therapy alters central serotonergic function and L-DOPA-induced dopamine release in a region-dependent manner in a rat model of Parkinson's disease. Neurobiol Dis. 41: 585-590.
51. Navailles S, De Deurwaerdere P. 2012a. Contribution of serotonergic transmission to the motor and cognitive effects of high-frequency stimulation of the subthalamic nucleus or levodopa in Parkinson's disease. Mol Neurobiol. 45: 173-185.
52. Navailles S, De Deurwaerdere P. 2012b. Imbalanced dopaminergic transmission mediated by serotonergic neurons in L-DOPA-induced dyskinesia. Parkinsons Dis. 2012: 323686.
53. Navailles S, Lagiere M, Contini A, De Deurwaerdere P. 2013. Multisite intracerebral microdialysis to study the mechanism of L-DOPA induced dopamine and serotonin release in the Parkinsonian Brain. ACS Chem Neurosci. 4(5):680-692.
54. Ng KY, Chase TN, Colburn RW, Kopin IJ. 1970. L-Dopa-induced release of cerebral monoamines. Science. 170: 76-77.
55. Ostock CY, Dupre KB, Jaunarajs KL, Walters H, George J, Krolewski D, Walker PD, Bishop C. 2011. Role of the primary motor cortex in L-Dopa-induced dyskinesia and its modulation by 5-HT1A receptor stimulation. Neuropharmacology. 61: 753-760.
56. Perez-Otano I, Herrero MT, Oset C, De Ceballos ML, Luquin MR, Obeso JA, Del Rio J. 1991. Extensive loss of brain dopamine and serotonin induced by chronic administration of MPTP in the marmoset. Brain Res. 567: 127-132.
57. Pifl C, Schingnitz G, Hornykiewicz O. 1991. Effect of 1-methyl4-phenyl-1,2,3,6-tetrahydropyridine on the regional distribution of brain monoamines in the rhesus monkey. Neuroscience. 44: 591-605.
58. Porras G, Berthet A, Dehay B, Li Q, Ladepeche L, Normand E, Dovero S, Martinez A, Doudnikoff E, Martin-Negrier ML et al. 2012. PSD-95 expression controls L-DOPA dyskinesia through dopamine D1 receptor trafficking. J Clin Invest. 122: 3977-3989.
59. Porras G, De Deurwaerdere P, Li Q, Marti M, Morgenstern R, Sohr R, Bezard E, Morari M, Meissner WG. 2014. L-Dopa-induced dyskinesia: beyond an excessive dopamine tone in the striatum. Sci Rep. 4: 3730.
60. Rascol O, Lozano A, Stern M, Poewe W. 2011. Milestones in Parkinson's disease therapeutics. Mov Disord. 26: 1072-1082.
61. Rascol O, Sabatini U, Brefel C, Fabre N, Rai S, Senard JM, Celsis P, Viallard G, Montastruc JL, Chollet F. 1998. Cortical motor overactivation in parkinsonian patients with L-dopa-induced peak-dose dyskinesia. Brain. 121(Pt 3):527-533.
62. Robbins TW, Everitt BJ. 1996. Neurobehavioural mechanisms of reward and motivation. Curr Opin Neurobiol. 6: 228-236.
63. Romero JA, Chalmers JP, Cottman K, Lytle LD, Wurtman RJ. 1972. Regional effects of L-dihydroxyphenylalanine (L-dopa) on norepinephrine metabolism in rat brain. J Pharmacol Exp Ther. 180: 277-285.
64. Rouillon C, Abraini JH, David HN. 2008. Prefrontal cortex and basolateral amygdala modulation of dopamine-mediated locomotion in the nucleus accumbens core. Exp Neurol. 212: 213-217.
65. Rylander D, Parent M, O'Sullivan SS, Dovero S, Lees AJ, Bezard E, Descarries L, Cenci MA. 2010. Maladaptive plasticity of serotonin axon terminals in levodopa-induced dyskinesia. Ann Neurol. 68: 619-628.
66. Santini E, Sgambato-Faure V, Li Q, Savasta M, Dovero S, Fisone G, Bezard E. 2010. Distinct changes in cAMP and extracellular signalregulated protein kinase signalling in L-DOPA-induced dyskinesia. PLoS One. 5: e12322.
67. Tison F, Mons N, Geffard M, Henry P. 1991. The metabolism of exogenous L-dopa in the brain: an immunohistochemical study of its conversion to dopamine in non-catecholaminergic cells of the rat brain. J Neural Transm Park Dis Dement Sect. 3: 27-39.
68. Tison F, Negre-Pages L, Meissner WG, Dupouy S, Li Q, Thiolat ML, Thiollier T, Galitzky M, Ory-Magne F, Milhet A et al. 2013. Simvastatin decreases levodopa-induced dyskinesia in monkeys, but not in a randomized, placebo-controlled, multiple cross-over ("n-of-1") exploratory trial of simvastatin against levodopa-induced dyskinesia in Parkinson's disease patients. Parkinsonism Relat Disord. 19: 416-421.
69. Voon V, Fernagut PO, Wickens J, Baunez C, Rodriguez M, Pavon N, Juncos JL, Obeso JA, Bezard E. 2009. Chronic dopaminergic stimulation in Parkinson's disease: from dyskinesias to impulse control disorders. Lancet Neurol. 8: 1140-1149.
70. Wachtel SR, Abercrombie ED. 1994. L-3,4-dihydroxyphenylalanine-induced dopamine release in the striatum of intact and 6-hydroxydopamine-treated rats: differential effects of monoamine oxidase A and B inhibitors. J Neurochem. 63: 108-117.
71. Wylie SA, Ridderinkhof KR, Bashore TR, van den Wildenberg WP. 2010. The effect of Parkinson's disease on the dynamics of on-line and proactive cognitive control during action selection. J Cogn Neurosci. 22: 2058-2073.
72. Zarow C, Lyness SA, Mortimer JA, Chui HC. 2003. Neuronal loss is greater in the locus coeruleus than nucleus basalis and substantia nigra in Alzheimer and Parkinson diseases. Arch Neurol. 60: 337-341.