Emerging dysfunctions consequent to combined monoaminergic depletions in parkinsonism

Neurobiology of Disease

Volumn 45, Issue 2, 2012, Pages 763-773

  Delaville, Claire ^a   Chetrit, Jonathan ^a   Abdallah, Khaled ^a   Morin, Stéphanie ^a   Cardoit, Laura ^a   De Deurwaerdère, Philippe ^a   Benazzouz, Abdelhamid ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b BORDEAUX UNIVERSITY HOSPITAL   (France)

Author keywords

Dopamine; Monoamine depletion; Motor symptoms; Non motor symptoms; Noradrenaline; Parkinson's disease; Serotonin; Single unit microrecording; Subthalamic nucleus

Indexed keywords

DOPAMINE; NORADRENALIN; SEROTONIN;

ANHEDONIA; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BRAIN FUNCTION; BRAIN REGION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEPRESSION; DISEASE EXACERBATION; DOPAMINE BRAIN LEVEL; FORCED SWIMMING TEST; LOCOMOTION; MALE; MONOAMINE METABOLISM; MOTOR DYSFUNCTION; NONHUMAN; NORADRENALIN BRAIN LEVEL; PARKINSONISM; PRIORITY JOURNAL; RAT; SEROTONIN BRAIN LEVEL; SUBTHALAMIC NUCLEUS; SUGAR INTAKE;

ANIMALS; DOPAMINE; MALE; MOTOR ACTIVITY; NEURONS; NOREPINEPHRINE; PARKINSONIAN DISORDERS; RATS; RATS, WISTAR; SEROTONIN; SUBTHALAMUS;

EID: 84855758077     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.10.023     Document Type: Article

References (74)

1. Archer T., Fredriksson A. Influence of noradrenaline denervation on MPTP-induced deficits in mice. J. Neural Transm. 2006, 113:1119-1129.
2. Aston-Jones G., Akaoka H., Charlety P., Chouvet G. Serotonin selectively attenuates glutamate-evoked activation of noradrenergic locus coeruleus neurons. J. Neurosci. 1991, 11:760-769.
3. Belujon P., Bezard E., Taupignon A., Bioulac B., Benazzouz A. Noradrenergic modulation of subthalamic nucleus activity: behavioral and electrophysiological evidence in intact and 6-hydroxydopamine-lesioned rats. J. Neurosci. 2007, 27:9595-9606.
4. Benabid A.L., Krack P.P., Benazzouz A., Limousin P., Koudsie A., Pollak P. Deep brain stimulation of the subthalamic nucleus for Parkinson's disease: methodologic aspects and clinical criteria. Neurology 2000, 55:S40-S44.
5. Benazzouz A., Gross C., Feger 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.
6. Benazzouz A., Breit S., Koudsie A., Pollak P., Krack P., Benabid A.L. Intraoperative microrecordings of the subthalamic nucleus in Parkinson's disease. Mov. Disord. 2002, 17(Suppl. 3):S145-S149.
7. Bergman H., Wichmann T., DeLong M.R. Reversal of experimental parkinsonism by lesions of the subthalamic nucleus. Science 1990, 249:1436-1438.
8. 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.
9. Bertrand E., Lechowicz W., Szpak G.M., Dymecki J. Qualitative and quantitative analysis of locus coeruleus neurons in Parkinson's disease. Folia Neuropathol. 1997, 35:80-86.
10. Bouali-Benazzouz R., Tai C.H., Chetrit J., Benazzouz A. Intrapallidal injection of 6-hydroxydopamine induced changes in dopamine innervation and neuronal activity of globus pallidus. Neuroscience 2009, 164:588-596.
11. Boyajian C.L., Loughlin S.E., Leslie F.M. Anatomical evidence for alpha-2 adrenoceptor heterogeneity: differential autoradiographic distributions of [3H]rauwolscine and [3H]idazoxan in rat brain. J. Pharmacol. Exp. Ther. 1987, 241:1079-1091.
12. Braak H., Del Tredici K., Rub U., de Vos R.A., Jansen Steur E.N., Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol. Aging 2003, 24:197-211.
13. Canteras N.S., Shammah-Lagnado S.J., Silva B.A., Ricardo J.A. Afferent connections of the subthalamic nucleus: a combined retrograde and anterograde horseradish peroxidase study in the rat. Brain Res. 1990, 513:43-59.
14. Cervo L., Grignaschi G., Rossi C., Samanin R. Role of central serotonergic neurons in the effect of sertraline in rats in the forced swimming test. Eur. J. Pharmacol. 1991, 196:217-222.
15. Chan-Palay V., Asan E. Alterations in catecholamine neurons of the locus coeruleus in senile dementia of the Alzheimer type and in Parkinson's disease with and without dementia and depression. J. Comp. Neurol. 1989, 287:373-392.
16. Chetrit J., Ballion B., Laquitaine S., Belujon P., Morin S., Taupignon A., Bioulac B., Gross C.E., Benazzouz A. Involvement of Basal Ganglia network in motor disabilities induced by typical antipsychotics. PLoS One 2009, 4:e6208.
17. Dailly E., Chenu F., Petit-Demouliere B., Bourin M. Specificity and efficacy of noradrenaline, serotonin depletion in discrete brain areas of Swiss mice by neurotoxins. J. Neurosci. Methods 2006, 150:111-115.
18. Damsa C., Bumb A., Bianchi-Demicheli F., Vidailhet P., Sterck R., Andreoli A., Beyenburg S. "Dopamine-dependent" side effects of selective serotonin reuptake inhibitors: a clinical review. J. Clin. Psychiatry 2004, 65:1064-1068.
19. De Deurwaerdere P., Chesselet M.F. Nigrostriatal lesions alter oral dyskinesia and c-Fos expression induced by the serotonin agonist 1-(m-chlorophenyl)piperazine in adult rats. J. Neurosci. 2000, 20:5170-5178.
20. De Deurwaerdere P., Bonhomme N., Le Moal M., Spampinato U. d-Fenfluramine increases striatal extracellular dopamine in vivo independently of serotonergic terminals or dopamine uptake sites. J. Neurochem. 1995, 65:1100-1108.
21. Delaville C., Deurwaerdere P.D., Benazzouz A. Noradrenaline and Parkinson's disease. Front. Syst. Neurosci. 2011, 5:31.
22. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berl.) 1995, 121:66-72.
23. Deumens R., Blokland A., Prickaerts J. Modeling Parkinson's disease in rats: an evaluation of 6-OHDA lesions of the nigrostriatal pathway. Exp. Neurol. 2002, 175:303-317.
24. Ehringer H., Hornykiewicz O. Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system. Klin. Wochenschr. 1960, 38:1236-1239.
25. Fornai F., Giorgi F.S., Gesi M., Chen K., Alessri M.G., Shih J.C. Biochemical effects of the monoamine neurotoxins DSP-4 and MDMA in specific brain regions of MAO-B-deficient mice. Synapse 2001, 39:213-221.
26. Fornai F., di Poggio A.B., Pellegrini A., Ruggieri S., Paparelli A. Noradrenaline in Parkinson's disease: from disease progression to current therapeutics. Curr. Med. Chem. 2007, 14:2330-2334.
27. Fritschy J.M., Grzanna R. Immunohistochemical analysis of the neurotoxic effects of DSP-4 identifies two populations of noradrenergic axon terminals. Neuroscience 1989, 30:181-197.
28. Fritschy J.M., Grzanna R. Selective effects of DSP-4 on locus coeruleus axons: are there pharmacologically different types of noradrenergic axons in the central nervous system?. Prog. Brain Res. 1991, 88:257-268.
29. Gaspar P., Duyckaerts C., Alvarez C., Javoy-Agid F., Berger B. Alterations of dopaminergic and noradrenergic innervations in motor cortex in Parkinson's disease. Ann. Neurol. 1991, 30:365-374.
30. Grzanna R., Berger U., Fritschy J.M., Geffard M. Acute action of DSP-4 on central norepinephrine axons: biochemical and immunohistochemical evidence for differential effects. J. Histochem. Cytochem. 1989, 37:1435-1442.
31. Gubellini P., Salin P., Kerkerian-Le Goff L., Baunez C. Deep brain stimulation in neurological diseases and experimental models: from molecule to complex behavior. Prog. Neurobiol. 2009, 89:79-123.
32. Guiard B.P., El Mansari M., Merali Z., Blier P. Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. Int. J. Neuropsychopharmacol. 2008, 11:625-639.
33. Guridi J., Obeso J.A. The subthalamic nucleus, hemiballismus and Parkinson's disease: reappraisal of a neurosurgical dogma. Brain 2001, 124:5-19.
34. Hajos-Korcsok E., McTavish S.F., Sharp T. Effect of a selective 5-hydroxytryptamine reuptake inhibitor on brain extracellular noradrenaline: microdialysis studies using paroxetine. Eur. J. Pharmacol. 2000, 407:101-107.
35. Halliday G.M., Blumbergs P.C., Cotton R.G., Blessing W.W., Geffen L.B. Loss of brainstem serotonin- and substance P-containing neurons in Parkinson's disease. Brain Res. 1990, 510:104-107.
36. Hassani O.K., Mouroux M., Feger J. Increased subthalamic neuronal activity after nigral dopaminergic lesion independent of disinhibition via the globus pallidus. Neuroscience 1996, 72:105-115.
37. Hoyer D., Clarke D.E., Fozard J.R., Hartig P.R., Martin G.R., Mylecharane E.J., Saxena P.R., Humphrey P.P. International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). Pharmacol. Rev. 1994, 46:157-203.
38. Hutchison W.D., Allan R.J., Opitz H., Levy R., Dostrovsky J.O., Lang A.E., Lozano A.M. Neurophysiological identification of the subthalamic nucleus in surgery for Parkinson's disease. Ann. Neurol. 1998, 44:622-628.
39. Jenner P., Sheehy M., Marsden C.D. Noradrenaline and 5-hydroxytryptamine modulation of brain dopamine function: implications for the treatment of Parkinson's disease. Br. J. Clin. Pharmacol. 1983, 15(Suppl. 2):277S-289S.
40. Kaneoke Y., Vitek J.L. Burst and oscillation as disparate neuronal properties. J. Neurosci. Methods 1996, 68:211-223.
41. Kish S.J. Biochemistry of Parkinson's disease: is a brain serotonergic deficiency a characteristic of idiopathic Parkinson's disease?. Adv. Neurol. 2003, 91:39-49.
42. Kish S.J., Tong J., Hornykiewicz O., Rajput A., Chang L.J., Guttman M., Furukawa Y. Preferential loss of serotonin markers in caudate versus putamen in Parkinson's disease. Brain 2008, 131:120-131.
43. Labarre D., Meissner W., Boraud T. Measure of the regularity of events in stochastic point processes, application to neuron activity analysis. 33rd IEEE International Conference on Acoustics, Vol. Speech and Signal Processing, Las Vegas, NV 2008, 489-492.
44. Lategan A.J., Marien M.R., Colpaert F.C. Suppression of nigrostriatal and mesolimbic dopamine release in vivo following noradrenaline depletion by DSP-4: a microdialysis study. Life Sci. 1992, 50:995-999.
45. Limousin P., Pollak P., Benazzouz A., Hoffmann D., Le Bas J.F., Broussolle E., Perret J.E., Benabid A.L. Effect of parkinsonian signs and symptoms of bilateral subthalamic nucleus stimulation. Lancet 1995, 345:91-95.
46. Loughlin S.E., Foote S.L., Fallon J.H. Locus coeruleus projections to cortex: topography, morphology and collateralization. Brain Res. Bull. 1982, 9:287-294.
47. Lucki I., O'Leary O.F. Distinguishing roles for norepinephrine and serotonin in the behavioral effects of antidepressant drugs. J. Clin. Psychiatry 2004, 65(Suppl. 4):11-24.
48. Meissner W., Leblois A., Hansel D., Bioulac B., Gross C.E., Benazzouz A., Boraud T. Subthalamic high frequency stimulation resets subthalamic firing and reduces abnormal oscillations. Brain 2005, 128:2372-2382.
49. Menza M.A., Robertson-Hoffman D.E., Bonapace A.S. Parkinson's disease and anxiety: comorbidity with depression. Biol. Psychiatry 1993, 34:465-470.
50. Murai T., Muller U., Werheid K., Sorger D., Reuter M., Becker T., von Cramon D.Y., Barthel H. In vivo evidence for differential association of striatal dopamine and midbrain serotonin systems with neuropsychiatric symptoms in Parkinson's disease. J. Neuropsychiatry Clin. Neurosci. 2001, 13:222-228.
51. Navailles S., Benazzouz A., Bioulac B., Gross C., De Deurwaerdere P. 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. J. Neurosci. 2010, 30:2356-2364.
52. Neve K.A., Kozlowski M.R., Marshall J.F. Plasticity of neostriatal dopamine receptors after nigrostriatal injury: relationship to recovery of sensorimotor functions and behavioral supersensitivity. Brain Res. 1982, 244:33-44.
53. Ni Z.G., Bouali-Benazzouz R., Gao D.M., Benabid A.L., Benazzouz A. Time-course of changes in firing rates and firing patterns of subthalamic nucleus neuronal activity after 6-OHDA-induced dopamine depletion in rats. Brain Res. 2001, 899:142-147.
54. Olsson M., Nikkhah G., Bentlage C., Bjorklund A. Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 1995, 15:3863-3875.
55. Orieux G., Francois C., Feger J., Yelnik J., Vila M., Ruberg M., Agid Y., Hirsch E.C. Metabolic activity of excitatory parafascicular and pedunculopontine inputs to the subthalamic nucleus in a rat model of Parkinson's disease. Neuroscience 2000, 97:79-88.
56. Paxinos G., Watson C. The Rat Brain in Stereotatic Coordinates 1996, Academic Press, San Diego.
57. Ponsen M.M., Stoffers D., Booij J., van Eck-Smit B.L., Wolters E., Berendse H.W. Idiopathic hyposmia as a preclinical sign of Parkinson's disease. Ann. Neurol. 2004, 56:173-181.
58. Porsolt R.D., Anton G., Blavet N., Jalfre M. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur. J. Pharmacol. 1978, 47:379-391.
59. Richard I.H., Schiffer R.B., Kurlan R. Anxiety and Parkinson's disease. J. Neuropsychiatry Clin. Neurosci. 1996, 8:383-392.
60. Rommelfanger K.S., Edwards G.L., Freeman K.G., Liles L.C., Miller G.W., Weinshenker D. Norepinephrine loss produces more profound motor deficits than MPTP treatment in mice. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:13804-13809.
61. Schank J.R., Ventura R., Puglisi-Allegra S., Alcaro A., Cole C.D., Liles L.C., Seeman P., Weinshenker D. Dopamine beta-hydroxylase knockout mice have alterations in dopamine signaling and are hypersensitive to cocaine. Neuropsychopharmacology 2006, 31:2221-2230.
62. Sclafani A., Ackroff K. Reinforcement value of sucrose measured by progressive ratio operant licking in the rat. Physiol. Behav. 2003, 79:663-670.
63. Srinivasan J., Schmidt W.J. Potentiation of parkinsonian symptoms by depletion of locus coeruleus noradrenaline in 6-hydroxydopamine-induced partial degeneration of substantia nigra in rats. Eur. J. Neurosci. 2003, 17:2586-2592.
64. Steinbusch H.W. Distribution of serotonin-immunoreactivity in the central nervous system of the rat-cell bodies and terminals. Neuroscience 1981, 6:557-618.
65. Tadaiesky M.T., Dombrowski P.A., Figueiredo C.P., Cargnin-Ferreira E., Da Cunha C., Takahashi R.N. Emotional, cognitive and neurochemical alterations in a premotor stage model of Parkinson's disease. Neuroscience 2008, 156:830-840.
66. 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.
67. Taquet H., Javoy-Agid F., Cesselin F., Hamon M., Legrand J.C., Agid Y. Microtopography of methionine-enkephalin, dopamine and noradrenaline in the ventral mesencephalon of human control and Parkinsonian brains. Brain Res. 1982, 235:303-314.
68. Taylor T.N., Caudle W.M., Shepherd K.R., Noorian A., Jackson C.R., Iuvone P.M., Weinshenker D., Greene J.G., Miller G.W. Nonmotor symptoms of Parkinson's disease revealed in an animal model with reduced monoamine storage capacity. J. Neurosci. 2009, 29:8103-8113.
69. Temel Y., Blokland A., Steinbusch H.W., Visser-Vandewalle V. The functional role of the subthalamic nucleus in cognitive and limbic circuits. Prog. Neurobiol. 2005, 76:393-413.
70. Temel Y., Boothman L.J., Blokland A., Magill P.J., Steinbusch H.W., Visser-Vandewalle V., Sharp T. 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. 2007, 104:17087-17092.
71. Tordoff M.G., Bachmanov A.A. Mouse taste preference tests: why only two bottles?. Chem. Senses 2003, 28:315-324.
72. Walsh K., Bennett G. Parkinson's disease and anxiety. Postgrad. Med. J. 2001, 77:89-93.
73. Wieland S., Kreider M.S., McGonigle P., Lucki I. Destruction of the nucleus raphe obscurus and potentiation of serotonin-mediated behaviors following administration of the neurotoxin 3-acetylpyridine. Brain Res. 1990, 520:291-302.
74. Witt K., Daniels C., Reiff J., Krack P., Volkmann J., Pinsker M.O., Krause M., Tronnier V., Kloss M., Schnitzler A., Wojtecki L., Botzel K., Danek A., Hilker R., Sturm V., Kupsch A., Karner E., Deuschl G. Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson's disease: a randomised, multicentre study. Lancet Neurol. 2008, 7:605-614.