La présente étude a permis de mettre en évidence la présence de VGluT3 au sein des corps cellulaires et des axones 5-HT. Pratiquement tous les corps cellulaires 5-HT du NRD ainsi que la majorité de ceux retrouvés dans le NRM contiennent du VGluT3. Quelques corps cellulaires de ces mêmes noyaux renferment du VGluT3, sans contenir de 5-HT. En ce qui a trait aux projections axonales, on ne retrouve qu’un faible degré de co-expression du SERT et VGluT3 au sein des varicosités individuelles, et ce, dans presque toutes les composantes des GB. Toutefois, deux groupes de structures se distinguent. Le premier groupe est composé de l’aire tegmentaire ventrale et de la SNc, les deux entités se distinguant par la présence plus forte de terminaison axonale 5-HT contenant du VGluT3. Le deuxième groupe se compose des noyaux NRD et NRM ainsi que du système ventriculaire où une présence massive de VGluT3 dans toutes les fibres 5-HT a été notée. L‘élaboration d’un nouvel anticorps reconnaissant de façon spécifique le VGluT3 chez les singes et l’homme permettra d’éventuelles recherches visant à vérifier si les données que nous avons obtenues chez la souris sont transposables aux primates. En effet, il existe des différences interspécifiques importantes entre rongeurs, singes et humains en ce qui a trait à l’organisation anatomique et neurochimique des GB ainsi que des afférences qu’ils reçoivent en provenance des noyaux du raphé.
La présente étude a permis d’apporter de nouvelles données dans l’espoir de mieux comprendre l’effet du VGluT3 dans les terminaisons axonales 5-HT du striatum sur l’expression des mouvements involontaires anormaux induits par la L-Dopa. Pour la première fois, nous avons observé, de façon non biaisée, que le nombre de terminaisons axonales 5-HT ainsi que la quantité de VGluT3 au sein de ces terminaisons ne semble pas être corrélé avec l’expression des DILs chez la souris. Ces résultats sont surprenants puisque qu’un large pant de la littérature supporte l’hypothèse que le système 5-HT est affecté dans la MP. En effet, plusieurs études indiquent que la conséquence d’une lésion de la voie nigrostriée dopaminergique chez le rongeur se traduit par un bourgeonnement des afférences 5-HT, que ce soit en contexte parkinsonien murin (Zhou et al., 1995 ; Rozas & al., 1998) ou en contexte DILs (Rolander et al., 2010 ; Yamada et al., 2007 ; Carta et al.,2007). Il se pourrait donc fort bien que la taille de notre échantillon ait été trop petite pour détecter un tel effet. Afin de bien déterminer le rôle de VGluT3 dans l’apparition des DILs, de futures recherches chez des souris dont le gène VGluT3 aura été supprimé seront nécessaires pour trancher la question.
Les résultats obtenus dans la présente étude, tant dans des conditions normales que pathologiques, pourraient inspirer de futures recherches ayant pour sujet d’étude principal la SNr. En effet, de par la présence de nombreuses terminaisons axonales contenant du VGluT3, cette composante des GB pourrait être une
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structure de prédilection pour des travaux à venir sur les changements morphologiques induits par la déafférentation dopaminergique menant à l’apparition des DILs. Chung et al., (2006) ont déjà observé une augmentation du VGluT3 dans la SNr. Toutefois, la méthodologie utilisée dans cette dernière étude ne permettait pas de savoir si cette augmentation s’opérait dans les terminaisons axonales 5-HT ou dans d’autres types d’éléments neuronaux. De plus, aucune recherche de ce genre n’a été effectuée chez des souris ayant reçu de la L-Dopa. La découverte d’un changement morphologique dans l’une des principales structures de sortie des GB pourrait se révéler primordiale dans la compréhension des symptômes moteurs de la MP et pourrait ouvrir la porte à de nouveaux traitements pharmacologiques face à une maladie neurologique dégénérative pour laquelle il n’existe toujours aucun traitement curatif.
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Bibliographie
Aarsland, D., Andersen, K., Larsen, J.P., and Lolk, A. (2003). Prevalence and characteristics of dementia in Parkinson disease: an 8-year prospective study. Arch. Neurol. 60, 387–392.
Abrams, J.K., Johnson, P.L., Hollis, J.H., and Lowry, C.A. (2004). Anatomic and Functional Topography of the Dorsal Raphe Nucleus. Ann. N. Y. Acad. Sci. 1018, 46–57.
Aghajanian, G.K., and Gallager, D.W. (1975). Raphe origin of serotonergic nerves terminating in the cerebral ventricles. Brain Res. 88, 221–231.
Akiyama, H., Kaneko, T., Mizuno, N., and McGeer, P.L. (1990). Distribution of phosphate‐activated glutaminase in the human cerebral cortex. J. Comp. Neurol. 297, 239–252.
Amilhon, B., Lepicard, E., Renoir, T., Mongeau, R., Popa, D., Poirel, O., Miot, S., Gras, C., Gardier, A.M., Gallego, J., et al. (2010). VGLUT3 (Vesicular Glutamate Transporter Type 3) Contribution to the Regulation of Serotonergic Transmission and Anxiety. J. Neurosci. 30, 2198–2210.
Arriza, J.L., Eliasof, S., Kavanaugh, M.P., and Amara, S.G. (1997). Excitatory amino acid transporter 5, a retinal glutamate transporter coupled to a chloride conductance. Proc. Natl. Acad. Sci. 94, 4155–4160.
Baba, M., Nakajo, S., Tu, P.-H., Tomita, T., Nakaya, K., Lee, V.M., Trojanowski, J.Q., and Iwatsubo, T. (1998). Aggregation of alpha-synuclein in Lewy bodies of sporadic Parkinson’s disease and dementia with Lewy bodies. Am. J. Pathol. 152, 879.
Baker, K.G., Halliday, G.M., and Törk, I. (1990). Cytoarchitecture of the human dorsal raphe nucleus. J. Comp. Neurol. 301, 147–161.
Baker, K.G., Halliday, G.M., Hornung, J.-P., Geffen, L.B., and Cotton, R.G.H. (1991). Distribution, morphology and number of monoamine-synthesizing and substance P-containing neurons in the human dorsal raphe nucleus. Neuroscience 42, 757–775.
Bellocchio, E.E., Reimer, R.J., Fremeau, R.T., and Edwards, R.H. (2000). Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289, 957–960.
Bennett, D.A., Beckett, L.A., Murray, A.M., Shannon, K.M., Goetz, C.G., Pilgrim, D.M., and Evans, D.A. (1996). Prevalence of parkinsonian signs and associated mortality in a community population of older people. N. Engl. J. Med. 334, 71–76.
Berger, M., Gray, J.A., and Roth, B.L. (2009). The Expanded Biology of Serotonin. Annu. Rev. Med. 60, 355– 366.
Bérubé-Carrière, N., Riad, M., Dal Bo, G., Lévesque, D., Trudeau, L.-É., and Descarries, L. (2009). The dual dopamine-glutamate phenotype of growing mesencephalic neurons regresses in mature rat brain. J. Comp. Neurol. 517, 873–891.
Birkmayer, W., and Hornykiewicz, O. (1961). The effect of 3, 4-dihydroxyphenylaline (= DOPA) on Parkinsonian akinesia. Wien Klin Wochenschr 73, 787–788.
Braak, H., Del Tredici, K., Bratzke, H., Hamm-Clement, J., Sandmann-Keil, D., and Rüd, U. (2002). Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson’s disease (preclinical and clinical stages). J. Neurol. 249, 1–1.
Breese, G.R., and Traylor, T.D. (1971). Depletion of brain noradrenaline and dopamine by 6‐hydroxydopamine. Br. J. Pharmacol. 42, 88–99.
Burn, D.J. (2002). Beyond the iron mask: Towards better recognition and treatment of depression associated with Parkinson’s disease. Mov. Disord. 17, 445–454.
Calne, D.B., Teychenne, P.F., Claveria, L.E., Eastman, R., Greenacre, J.K., and Petrie, A. al (1974). Bromocriptine in parkinsonism. BMJ 4, 442–444.
Carlsson, T., Carta, M., Winkler, C., Bjorklund, A., and Kirik, D. (2007). Serotonin Neuron Transplants Exacerbate L-DOPA- Induced Dyskinesias in a Rat Model of Parkinson’s Disease. J. Neurosci. 27, 8011– 8022.
Carta, M., Carlsson, T., Kirik, D., and Bjorklund, A. (2007). Dopamine released from 5-HT terminals is the cause of L-DOPA-induced dyskinesia in parkinsonian rats. Brain 130, 1819–1833.
50
Carta, M., Carlsson, T., Munoz, A., Kirik, D., and Bjorklund, A. (2008). Serotonin–dopamine interaction in the induction and maintenance of L-DOPA-induced dyskinesias. In Progress in Brain Research, (Elsevier), pp. 465–478.
Chang, J.-W., Wachtel, S.R., Young, D., and Kang, U.-J. (1999). Biochemical and anatomical characterization of forepaw adjusting steps in rat models of Parkinson’s disease: studies on medial forebrain bundle and striatal lesions. Neuroscience 88, 617–628.
Chaudhuri, K.R., and Naidu, Y. (2008). Early Parkinson’s disease and non-motor issues. J. Neurol. 255, 33– 38.
Cheshire, P., Ayton, S., Bertram, K.L., Ling, H., Li, A., McLean, C., Halliday, G.M., O’Sullivan, S.S., Revesz, T., and Finkelstein, D.I. (2015). Serotonergic markers in Parkinson’s disease and levodopa‐induced dyskinesias. Mov. Disord. 30, 796–804.
Choi, D.W. (1985). Glutamate neurotoxicity in cortical cell culture is calcium dependent. Neurosci. Lett. 58, 293–297.
Chung, E.K.Y., Chen, L.W., Chan, Y.S., and Yung, K.K.L. (2006). Up-Regulation in Expression of Vesicular Glutamate Transporter 3 in Substantia Nigra but Not in Striatum of 6-Hydroxydopamine-Lesioned Rats. Neurosignals 15, 238–248.
Cleeter, M.W.J., Cooper, J.M., and Schapira, A.H.V. (1992). Irreversible inhibition of mitochondrial complex I by 1‐methyl‐4‐phenylpyridinium: evidence for free radical involvement. J. Neurochem. 58, 786–789.
Crissman, R.S., Arce, E.A., Bennett-Clarke, C.A., Mooney, R.D., and Rhoades, R.W. (1993). Reduction in the percentage of serotoninergic axons making synapses during the development of the superficial layers of the hamster’s superior colliculus. Dev. Brain Res. 75, 131–135.
Dahlström, A., and Fuxe, K. (1964). Evidence for the existence of monoamine-containing neurons in the central nervous system. I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. Suppl.
Damier, P., Hirsch, E.C., Agid, Y., and Graybiel, A.M. (1999). The substantia nigra of the human brain II Patterns of loss of dopamine-containing neurons in Parkinson’s disease. Brain 122, 1437–1448.
Descarries, L., Soghomonian, J.-J., Garcia, S., Doucet, G., and Bruno, J.P. (1992). Ultrastructural analysis of the serotonin hyperinnervation in adult rat neostriatum following neonatal dopamine denervation with 6- hydroxydopamine. Brain Res. 569, 1–13.
Dinan, T.G. (1996). Serotonin and the regulation of hypothalamic-pituitary-adrenal axis function. Life Sci. 58, 1683–1694.
Ehringer, H., and 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. El Mestikawy, S., Wallén-Mackenzie, Å., Fortin, G.M., Descarries, L., and Trudeau, L.-E. (2011). From glutamate co-release to vesicular synergy: vesicular glutamate transporters. Nat. Rev. Neurosci. 12, 204–216. ERSPAMER, V. (1952). Observations on alleged serotonin-(enteramine)-like nature of cerebral pressor substance of Taylor, Page, and Corcoran. AMA Arch. Intern. Med. 90, 505–512.
Fairman, W.A., Vandenberg, R.J., Arriza, J.L., Kavanaught, M.P., and Amara, S.G. (1995). An excitatory amino-acid transporter with properties of a ligand-gated chloride channel. Nature.
Falck, B., Hillarp, N.A., and Torp, A. (1962). Fluorescence of catcchol amines and related compounds with formaldehyde. J. Histochem. Cytochem. 10, 348–354.
Fearnley, J.M., and Lees, A.J. (1991). Ageing and Parkinson’s disease: substantia nigra regional selectivity. Brain 114, 2283–2301.
Felten, D.L., and Sladek, J.R. (1983). Monoamine distribution in primate brain V. Monoaminergic nuclei: anatomy, pathways and local organization. Brain Res. Bull. 10, 171–284.
Fu, W., Le Maître, E., Fabre, V., Bernard, J.-F., David Xu, Z.-Q., and Hökfelt, T. (2010). Chemical neuroanatomy of the dorsal raphe nucleus and adjacent structures of the mouse brain. J. Comp. Neurol. 518, 3464–3494.
Gagnon, D., and Parent, M. (2014). Distribution of VGLUT3 in Highly Collateralized Axons from the Rat Dorsal Raphe Nucleus as Revealed by Single-Neuron Reconstructions. PLoS ONE 9, e87709.
51 Gagnon, D., Gregoire, L., Di Paolo, T., and Parent, M. (2015). Serotonin hyperinnervation of the striatum with high synaptic incidence in parkinsonian monkeys. Brain Struct. Funct. 1–17.
Gras, C., Herzog, E., Bellenchi, G.C., Bernard, V., Ravassard, P., Pohl, M., Gasnier, B., and El Mestikawy, S. (2002). A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22, 5442–5451.
Gras, C., Amilhon, B., Lepicard, È.M., Poirel, O., Vinatier, J., Herbin, M., Dumas, S., Tzavara, E.T., Wade, M.R., and Nomikos, G.G. (2008). The vesicular glutamate transporter VGLUT3 synergizes striatal acetylcholine tone. Nat. Neurosci. 11, 292–300.
Hale, M.W., Stamper, C.E., Staub, D.R., and Lowry, C.A. (2010). Urocortin 2 increases c-Fos expression in serotonergic neurons projecting to the ventricular/periventricular system. Exp. Neurol. 224, 271–281.
Halliday, G.M., Li, Y.W., Blumbergs, P.C., Joh, T.H., Cotton, R.G.H., Howe, P.R.C., Blessing, W.W., and Geffen, L.B. (1990). Neuropathology of immunohistochemically identified brainstem neurons in Parkinson’s disease. Ann. Neurol. 27, 373–385.
Herzog, E., Gilchrist, J., Gras, C., Muzerelle, A., Ravassard, P., Giros, B., Gaspar, P., and El Mestikawy, S. (2004). Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123, 983–1002.
Hornung, J.-P. (2003). The human raphe nuclei and the serotonergic system. J. Chem. Neuroanat. 26, 331– 343.
Huot, P., Fox, S.H., and Brotchie, J.M. (2011). The serotonergic system in Parkinson’s disease. Prog. Neurobiol. 95, 163–212.
Jacobs, B.L., and Fornal, C.A. (1997). Serotonin and motor activity. Curr. Opin. Neurobiol. 7, 820–825. Juge, N., Gray, J.A., Omote, H., Miyaji, T., Inoue, T., Hara, C., Uneyama, H., Edwards, R.H., Nicoll, R.A., and Moriyama, Y. (2010). Metabolic Control of Vesicular Glutamate Transport and Release. Neuron 68, 99–112. Kanai, Y., and Hediger, M.A. (1992). Primary structure and functional characterization of a high-affinity glutamate transporter. Nature 360, 467–470.
Kosofsky, B.E., and Molliver, M.E. (1987). The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1, 153–168.
Lang, A.E., and Lozano, A.M. (1998). Parkinson’s disease. N. Engl. J. Med. 339, 1030–1043.
Li, Y.-Q., Li, H., Kaneko, T., and Mizuno, N. (2001). Morphological features and electrophysiological properties of serotonergic and non-serotonergic projection neurons in the dorsal raphe nucleus: An intracellular recording and labeling study in rat brain slices. Brain Res. 900, 110–118.
Lidov, H.G.W., Grzanna, R., and Molliver, M.E. (1980). The serotonin innervation of the cerebral cortex in the rat—an immunohistochemical analysis. Neuroscience 5, 207–227.
Lorez, H.P., and Richards, J.G. (1982). Supra-Ependymal Serotoninergic Nerves in Mammalian Brain: Morphological, Pharmacological and Functional Studies. Brain Res. Bull. 9, 727–741.
Marsden, C.D. (1987). Parkinson’s disease in twins. J. Neurol. Neurosurg. Psychiatry 50, 105.
Martinez-Martin, P., Schapira, A.H.V., Stocchi, F., Sethi, K., Odin, P., MacPhee, G., Brown, R.G., Naidu, Y., Clayton, L., Abe, K., et al. (2007). Prevalence of nonmotor symptoms in Parkinson’s disease in an international setting; Study using nonmotor symptoms questionnaire in 545 patients. Mov. Disord. 22, 1623–1629.
Mason, G.F., Rothman, D.L., Behar, K.L., and Shulman, R.G. (1992). NMR determination of the TCA cycle rate and α-ketoglutarate/glutamate exchange rate in rat brain. J. Cereb. Blood Flow Metab. 12, 434–447. Michel, P.P., and Hefti, F. (1990). Toxicity of 6‐hydroxydopamine and dopamine for dopaminergic neurons in culture. J. Neurosci. Res. 26, 428–435.
Moore, D.J., West, A.B., Dawson, V.L., and Dawson, T.M. (2005). Molecular pathophysiology of Parkinson’s disease. Annu Rev Neurosci 28, 57–87.
Naito, S., and Ueda, T. (1985). Characterization of glutamate uptake into synaptic vesicles. 44, 99–109. Ni, B., Rosteck, P.R., Nadi, N.S., and Paul, S.M. (1994). Cloning and expression of a cDNA encoding a brain- specific Na (+)-dependent inorganic phosphate cotransporter. Proc. Natl. Acad. Sci. 91, 5607–5611.
Nieuwenhuys, R., Voogd, J., and van Huijzen, C. (2008). The human Central Nervous System (Germany: Springer).
52
Parent, A., Descarries, L., and Beaudet, A. (1981). Organization of ascending serotonin systems in the adult rat brain. A radioautographic study after intraventricular administration of [3 H] 5-hydroxytryptamine. Neuroscience 6, 115–138.
Paulus, W., and Jellinger, K. (1991). The neuropathologic basis of different clinical subgroups of Parkinson’s disease. J. Neuropathol. Exp. Neurol. 50, 743–755.
Paxinos, G., and Franklin, K.B. (2004). The mouse brain in stereotaxic coordinates (Gulf Professional Publishing).
Petryszyn, S., Beaulieu, J.-M., Parent, A., and Parent, M. (2014). Distribution and morphological characteristics of striatal interneurons expressing calretinin in mice: A comparison with human and nonhuman primates. J. Chem. Neuroanat. 59-60, 51–61.
Porter, C.C., Totaro, J.A., and Stone, C.A. (1963). Effect of 6-hydroxydopamine and some other compounds on the concentration of norepinephrine in the hearts of mice. J. Pharmacol. Exp. Ther. 140, 308–316.
Purves, D., Augustine, G.J., Fitzpatrick, D., Katz, L.C., LaMantia, A.-S., McNamara, J.O., and Williams, S.M. (2001). The Biogenic Amines.
Rajput, A.H., Fenton, M.E., Birdi, S., Macaulay, R., George, D., Rozdilsky, B., Ang, L.C., Senthilselvan, A., and Hornykiewicz, O. (2002). Clinical-Pathological study of levodopa complications. Mov. Disord. 17, 289–296. Rapport, M.M., Green, A., and Page, J. (1949). Serum vasoconstrictor (serotonin). J Biol Chem 176, 1243– 1251.
Reed, M.C., Nijhout, H.F., and Best, J.A. (2012). Mathematical insights into the effects of levodopa. Front. Integr. Neurosci. 6.
Remy, P. (2005). Depression in Parkinson’s disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 128, 1314–1322.
Reul, J.M., and Holsboer, F. (2002). Corticotropin-releasing factor receptors 1 and 2 in anxiety and depression. Curr. Opin. Pharmacol. 2, 23–33.
Richards, J.G., Lorenz, H.P., and Tranzer, J.P. (1973). Indolealkylamine nerve terminals in cerebral ventricles: identification by electron microscopy and fluorescence histochemistry. Brain Res. 57, 277–288.
Rozas, G., Liste, I., Guerra, M.J., and Labandeira-Garcia, J.L. (1998). Sprouting of the serotonergic afferents into striatum after selective lesion of the dopaminergic system by MPTP in adult mice. Neurosci. Lett. 245, 151–154.
Schiffer, R.B., Kurlan, R., Rubin, A., and Boer, S. (1988). Evidence for atypical depression in Parkinson’s disease. Am J Psychiatry 145, 1020–1022.
Senoh, S., Creveling, C.R., Udenfriend, S., and Witkop, B. (1959). Chemical, Enzymatic and Metabolic Studies on the Mechanism of Oxidation of Dopamine1. J. Am. Chem. Soc. 81, 6236–6240.
Shulman, L.M., Taback, R.L., Bean, J., and Weiner, W.J. (2001). Comorbidity of the nonmotor symptoms of Parkinson’s disease. Mov. Disord. 16, 507–510.
Shutoh, F., Ina, A., Yoshida, S., Konno, J., and Hisano, S. (2008). Two distinct subtypes of serotonergic fibers classified by co-expression with vesicular glutamate transporter 3 in rat forebrain. Neurosci. Lett. 432, 132– 136.
Simpson, K.L., Fisher, T.M., Waterhouse, B.D., and Lin, R. (1998). Projection patterns from the raphe nuclear complex to the ependymal wall of the ventricular system in the rat. J. Comp. Neurol. 399, 61–72.
Soghomonian, J.-J., Doucet, G., and Descarries, L. (1987). Serotonin innervation in adult rat neostriatum. I. Quantified regional distribution. Brain Res. 425, 85–100.
Somogyi, J., Baude, A., Omori, Y., Shimizu, H., Mestikawy, S.E., Fukaya, M., Shigemoto, R., Watanabe, M., and Somogyi, P. (2004). GABAergic basket cells expressing cholecystokinin contain vesicular glutamate transporter type 3 (VGLUT3) in their synaptic terminals in hippocampus and isocortex of the rat. Eur. J. Neurosci. 19, 552–569.
Stachowiak, M.K., Bruno, J.P., Snyder, A.M., Stricker, E.M., and Zigmond, M.J. (1984). Apparent sprouting of striatal serotonergic terminals after dopamine-depleting brain lesions in neonatal rats. Brain Res. 291, 164– 167.
Steinbusch, H.W.M. (1981a). Distribution of serotonin-immunoreactivity in the central nervous system of the rat—cell bodies and terminals. Neuroscience 6, 557–618.
53 Stowe, R.L., Ives, N.J., Clarke, C., Van Hilten, J., Ferreira, J., Hawker, R.J., Shah, L., Wheatley, K., and Gray, R. (2008). Dopamine agonist therapy in early Parkinson’s disease. Cochrane Database Syst Rev 2, 1–92. Takeuchi, Y., Sawada, T., Blunt, S., Jenner, P., and Marsden, C.D. (1991). Effects of 6-hydroxydopamine lesions of the nigrostriatal pathway on striatal serotonin innervation in adult rats. Brain Res. 562, 301–305. Ungerstedt, U. (1971). Postsynaptic supersensitivity after 6‐hydroxy‐dopamine induced degeneration of the nigro‐striatal dopamine system. Acta Physiol. Scand. 82, 69–93.
Varoqui, H., Zhu, H., Yao, D., Ming, H., and Erickson, J.D. (2000). Cloning and functional identification of a neuronal glutamine transporter. J. Biol. Chem. 275, 4049–4054.
Vialli, M., and Erspamer, D.V. (1937). Ricerche sul secreto delle cellule enterocromaffini. Z. Für Zellforsch. Mikrosk. Anat. 27, 81–99.
Wallman, M.-J., Gagnon, D., and Parent, M. (2011). Serotonin innervation of human basal ganglia: Serotonin inputs to basal ganglia. Eur. J. Neurosci. 33, 1519–1532.
Woolley, D.W., and Shaw, E. (1954). A biochemical and pharmacological suggestion about certain mental disorders. Proc. Natl. Acad. Sci. U. S. A. 40, 228.
Xie, X.-S., Stone, D.K., and Racker, E. (1983). Determinants of clathrin-coated vesicle acidification. J. Biol. Chem. 258, 14834–14838.
Yamada, H., Aimi, Y., Nagatsu, I., Taki, K., Kudo, M., and Arai, R. (2007a). Immunohistochemical detection of l-DOPA-derived dopamine within serotonergic fibers in the striatum and the substantia nigra pars reticulata in Parkinsonian model rats. Neurosci. Res. 59, 1–7.
Zhou, F.C., Bledsoe, S., and Murphy, J. (1991). Serotonergic sprouting is induced by dopamine-lesion in substantia nigra of adult rat brain. Brain Res. 556, 108–116.
Zhou, F.C., Azmitia, E.C., and Bledsoe, S. (1995). Rapid serotonergic fiber sprouting in response to ibotenic acid lesion in the striatum and hippocampus. Dev. Brain Res. 84, 89–98.