The pathology roadmap in Parkinson disease
Open accessAbstract
An under-appreciated clue about pathogenesis in Parkinson disease (PD) is the distribution of pathology in the early and middle stages of the disease. This pathological 'roadmap' shows that in addition to dopaminergic neurons in the substantia nigra pars compacta (SNc), a significant number of other central and peripheral neuronal populations exhibit Lewy pathology, phenotypic dysregulation or frank degeneration in PD patients. This spatially distributed, at-risk population of neurons shares a number of features, including autonomously generated activity, broad action potentials, low intrinsic calcium buffering capacity and long, poorly myelinated, highly branched axons. Many, and perhaps all, of these traits add to the metabolic burden in these neurons, suggesting that mitochondrial deficits could drive pathogenesis in PD-in agreement with a large segment of the literature. What is less clear is how this neuronal phenotype might shape the susceptibility to proteostatic dysfunction or to the spread of α-synuclein fibrils deposited in the extracellular space. The review explores the literature on these issues and their translational implications.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Parkinson's disease is proposed to start with CNS inflammation low in the brainstem, as in the Braak hypothesis, or with excitotoxic events anywhere, producing microglial •NO and O2•− and causing α-synuclein aggregates and Lewy bodies.
“Summarizing, the proposal is that Parkinson’s disease starts with CNS inflammation low in the brainstem, as in the Braak hypothesis (246), or with excitotoxic events anywhere, producing microglial •NO and O2•− and causing α-synuclein aggregates and Lewy bodies.”
From Chemiexcitation: Mammalian Photochemistry in the Dark<sup>†</sup> (2023) · cites this paper as [246]
The Introduction (page unavailable) describes early Parkinson’s pathology in the brainstem and says Braak and collaborators suggest that neurons in the dorsal motor nucleus of the vagus are first to degenerate. That supports the citation’s brainstem-starting comparison, but the paper does not describe CNS inflammation as the initiating event. The citation is attached to the Braak comparison, not the sentence’s later proposed microglial mechanism. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Staging of brain pathology related to sporadic Parkinson’s disease
Braak, H., Tredici, K. D., Rüb, U., de Vos, R. A. I., Jansen Steur, E. N. H., & Braak, E. (2003) · Neurobiology of Aging · doi:10.1016/s0197-4580(02)00065-9 · Cited by 10,777 · see citing works
Aston-Jones, G., & Cohen, J. D. (2005) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.28.061604.135709 · Cited by 4,472 · see citing works
Stages in the development of Parkinson’s disease-related pathology
Braak, H., Ghebremedhin, E., Rüb, U., Bratzke, H., & Del Tredici, K. (2004) · Cell and Tissue Research · doi:10.1007/s00441-004-0956-9 · Cited by 2,689 · see citing works
Luk, K. C., Kehm, V., Carroll, J., Zhang, B., O’Brien, P., Trojanowski, J. Q., & Lee, V. M.-Y. (2012) · Science · doi:10.1126/science.1227157 · Cited by 2,563 · see citing works
The substantia nigra of the human brain
Damier, P., Hirsch, É. C., Agid, Y., & Graybiel, A. M. (1999) · Brain · doi:10.1093/brain/122.8.1437 · Cited by 1,772 · see citing works
Lewy body–like pathology in long-term embryonic nigral transplants in Parkinson's disease
Kordower, J. H., Chu, Y., Hauser, R. A., Freeman, T. B., & Olanow, C. W. (2008) · Nature Medicine · doi:10.1038/nm1747 · Cited by 1,722 · see citing works
Mice Lacking α-Synuclein Display Functional Deficits in the Nigrostriatal Dopamine System
Abeliovich, A., Schmitz, Y., Fariñas, I., Choi-Lundberg, D., Ho, W.-H., Castillo, P. E., Shinsky, N., Verdugo, J. M. G., Armanini, M., Ryan, A., et al. (2000) · Neuron · doi:10.1016/s0896-6273(00)80886-7 · Cited by 1,722 · see citing works
Self-citationBender, A., Krishnan, K. J., Morris, C. M., Taylor, G. A., Reeve, A. K., Perry, R. H., Jaros, E., Hersheson, J. S., Betts, J., Klopstock, T., et al. (2006) · Nature Genetics · doi:10.1038/ng1769 · Cited by 1,570 · see citing works
Volpicelli-Daley, L. A., Luk, K. C., Patel, T. P., Tanik, S. A., Riddle, D. M., Stieber, A., Meaney, D. F., Trojanowski, J. Q., & Lee, V. M.-Y. (2011) · Neuron · doi:10.1016/j.neuron.2011.08.033 · Cited by 1,569 · see citing works
Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease
Hirsch, E., Graybiel, A. M., & Agid, Y. A. (1988) · Nature · doi:10.1038/334345a0 · Cited by 1,301 · cited 1× · see citing works
“Some Lewy pathology has been reported in the neighboring ventral tegmental area and retrorubral field neurons as well,(53) but neuronal loss in these two regions is variable.(36,37) Profound neuronal loss in the SNc appears to be specific to parkinsonian etiologies(119) and not Alzheimer disease.”
BackgroundEmmanouilidou, E., Melachroinou, K., Roumeliotis, T., Garbis, S. D., Ntzouni, M., Margaritis, L. H., Stefanis, L., & Vekrellis, K. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5699-09.2010 · Cited by 1,115 · see citing works
Nemani, V. M., Lü, W., Berge‐Seidl, V., Nakamura, K., Onoa, B., Lee, M. K., Chaudhry, F. A., Nicoll, R. A., & Edwards, R. H. (2010) · Neuron · doi:10.1016/j.neuron.2009.12.023 · Cited by 1,051 · see citing works
Zarow, C., Lyness, S. A., Mortimer, J. A., & Chui, H. C. (2003) · Archives of Neurology · doi:10.1001/archneur.60.3.337 · Cited by 1,003 · see citing works
Description of Parkinson's Disease as a Clinical Syndrome
Fahn, S. (2003) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2003.tb07458.x · Cited by 979 · see citing works
Neuropathological assessment of Parkinson’s disease: refining the diagnostic criteria
Dickson, D. W., Braak, H., Duda, J. E., Duyckaerts, C., Gasser, T., Halliday, G. M., Hardy, J., Leverenz, J. B., Del Tredici, K., Wszolek, Z. K., et al. (2009) · The Lancet Neurology · doi:10.1016/s1474-4422(09)70238-8 · Cited by 972 · see citing works
Exosomes are released by cultured cortical neurones
Fauré, J., Lachenal, G., Court, M., Hirrlinger, J., Chatellard-Causse, C., Blot, B., Grange, J., Schoehn, G., Goldberg, Y., Boyer, V., et al. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.12.003 · Cited by 896 · see citing works
Mitochondria in the aetiology and pathogenesis of Parkinson's disease
Schapira, A. H. (2008) · The Lancet Neurology · doi:10.1016/s1474-4422(07)70327-7 · Cited by 883 · see citing works
Matsuda, W., Furuta, T., Nakamura, K. C., Hioki, H., Fujiyama, F., Arai, R., & Kaneko, T. (2009) · The Journal of Neuroscience · doi:10.1523/jneurosci.4029-08.2009 · Cited by 865 · see citing works
Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1
Guzmán, J. N., Sánchez-Padilla, J., Wokosin, D. L., Kondapalli, J., Ilijić, E., Schumacker, P. T., & Surmeier, D. J. (2010) · Nature · doi:10.1038/nature09536 · Cited by 836 · see citing works
Self-citationExosome Release Is Regulated by a Calcium-dependent Mechanism in K562 Cells
Savina, A., Furlán, M., Vidal, M., & Colombo, M. I. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m301642200 · Cited by 835 · see citing works
Where Does Parkinson Disease Pathology Begin in the Brain?
Del Tredici, K., Rüb, U., de Vos, R. A. I., Bohl, J. R. E., & Braak, H. (2002) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/61.5.413 · Cited by 773 · see citing works
Dopamine-modified α-synuclein blocks chaperone-mediated autophagy
Martínez‐Vicente, M., Tallóczy, Z., Kaushik, S., Massey, A. C., Mazzulli, J. R., Mosharov, E. V., Hodara, R., Fredenburg, R. A., Wu, D.-C., Follenzi, A., et al. (2008) · Journal of Clinical Investigation · doi:10.1172/jci32806 · Cited by 633 · see citing works
Self-citationNakamura, K., Nemani, V., Azarbal, F., Skibinski, G., Levy, J. M., Egami, K., Munishkina, L. A., Zhang, J., Gardner, B. M., Wakabayashi, J., et al. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m110.213538 · Cited by 590 · see citing works
Hypocretin (orexin) cell loss in Parkinson's disease
Thannickal, T. C., Lai, Y.-Y., & Siegel, J. M. (2007) · Brain · doi:10.1093/brain/awm097 · Cited by 566 · see citing works
Hirsch, É. C., Graybiel, A. M., Duyckaerts, C. J., & Javoy-Agid, F. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.16.5976 · Cited by 554 · see citing works
The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson's disease
Pan, T., Kondo, S., Le, W., & Jankovic, J. J. (2008) · Brain · doi:10.1093/brain/awm318 · Cited by 546 · see citing works
Mosharov, E. V., Larsen, K. E., Kanter, E., Phillips, K. A., Wilson, K., Schmitz, Y., Krantz, D. E., Kobayashi, K., Edwards, R. H., & Sulzer, D. L. (2009) · Neuron · doi:10.1016/j.neuron.2009.01.033 · Cited by 530 · see citing works
Self-citationParkinson's disease: the presence of Lewy bodies in Auerbach's and Meissner's plexuses
Wakabayashi, K., Takahashi, H., Takeda, S., Ohama, E., & Ikuta, F. (1988) · Acta Neuropathologica · doi:10.1007/bf00687767 · Cited by 528 · see citing works
THE BRAIN-STEM LESIONS IN PARKINSONISM
GREENFIELD, J. G., & Bosanquet, F. D. (1953) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.16.4.213 · Cited by 494 · see citing works
Sulzer, D. L., Bogulavsky, J. J., Larsen, K. E., Behr, G. G., Karatekin, E., Kleinman, M. H., Turro, N. J., Krantz, D. E., Edwards, R. H., Greene, L. A., et al. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.22.11869 · Cited by 460 · see citing works
Self-citationNeuropathology of sporadic Parkinson's disease: Evaluation and changes of concepts
Jellinger, K. A. (2011) · Movement Disorders · doi:10.1002/mds.23795 · Cited by 448 · see citing works
Cubells, J. F., Rayport, S., Rajendran, G., & Sulzer, D. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-04-02260.1994 · Cited by 448 · see citing works
Self-citationLebouvier, T., Neunlist, M., Bruley des Varannes, S., Coron, E., Drouard, A., N'Guyen, J.-M., Chaumette, T., Tasselli, M., Paillusson, S., Flamand, M., et al. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012728 · Cited by 427 · see citing works
Larsen, K. E., Schmitz, Y., Troyer, M. D., Mosharov, E. V., Dietrich, P., Quazi, A. Z., Savalle, M., Nemani, V. M., Chaudhry, F. A., Edwards, R. H., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.3821-06.2006 · Cited by 415 · see citing works
Self-citationRobust Pacemaking in Substantia Nigra Dopaminergic Neurons
Guzmán, J. N., Sánchez-Padilla, J., Chan, C. S., & Surmeier, D. J. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.2519-09.2009 · Cited by 411 · see citing works
Self-citationNeuropathology of immunohistochemically identified brainstem neurons in Parkinson's disease
Halliday, G. M., Li, Y. W., Blumbergs, P. C., JOH, T. H., Cotton, R. G. H., Howe, P. R. C., Blessing, W. W., & Geffen, L. B. (1990) · Annals of Neurology · doi:10.1002/ana.410270405 · Cited by 409 · see citing works
Li, Z., Chalazonitis, A., Huang, Y.-Y., Mann, J. J., Margolis, K. G., Yang, Q. M., Kim, D. O., Cote, F., Mallet, J., & Gershon, M. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.6684-10.2011 · Cited by 403 · see citing works
Jellinger, K. A. (1988) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.51.4.540 · Cited by 375 · see citing works
Singaram, C., Gaumnitz, E., Torbey, C., Ashraf, W., Quigley, E. M., Sengupta, A., & Pfeiffer, R. F. (1995) · The Lancet · doi:10.1016/s0140-6736(95)92707-7 · Cited by 364 · see citing works
Membrane properties of rat locus coeruleus neurones
Williams, J. T., North, R. A., Shefner, S. A., Nishi, S., & Egan, T. M. (1984) · Neuroscience · doi:10.1016/0306-4522(84)90265-3 · Cited by 341 · see citing works
Larsen, K. E., Fon, E. A., Hastings, T. G., Edwards, R. H., & Sulzer, D. L. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-20-08951.2002 · Cited by 335 · see citing works
Self-citationWakabayashi, K., Takahashi, H., Ohama, E., & Ikuta, F. (1990) · Acta Neuropathologica · doi:10.1007/bf00294234 · Cited by 319 · see citing works
Puopolo, M., Raviola, E., & Bean, B. P. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.4341-06.2007 · Cited by 319 · see citing works
Neuroanatomy and Pathology of Sporadic Parkinson's Disease
Braak, H., & Tredici, K. D. (2008) · Advances in anatomy, embryology and cell biology · doi:10.1007/978-3-540-79850-7 · Cited by 297 · see citing works
Tredici, K. D., Hawkes, C. H., Ghebremedhin, E., & Braak, H. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0665-2 · Cited by 292 · see citing works
The anterior olfactory nucleus in Parkinson's disease
Pearce, R. K. B., Hawkes, C. H., & Daniel, S. E. (1995) · Movement Disorders · doi:10.1002/mds.870100309 · Cited by 289 · see citing works
Excitotoxicity and nitric oxide in parkinson's disease pathogenesis
Beal, M. F. (1998) · Annals of Neurology · doi:10.1002/ana.410440716 · Cited by 283 · see citing works
Chronic Constipation in the Elderly
Bouras, E. P., & Tangalos, E. G. (2009) · Gastroenterology Clinics of North America · doi:10.1016/j.gtc.2009.06.001 · Cited by 274 · see citing works
L‐type calcium channel blockers and Parkinson disease in Denmark
Ritz, B. R., Rhodes, S. L., Qian, L., Schernhammer, E. S., Olsen, J. H., & Friis, S. (2009) · Annals of Neurology · doi:10.1002/ana.21937 · Cited by 274 · see citing works
Alpha-synuclein cell-to-cell transfer and seeding in grafted dopaminergic neurons in vivo
Angot, E., Steiner, J. A., Lema Tomé, C. M., Ekström, P., Mattsson, B., Björklund, A., & Brundin, P. (2012) · PLoS ONE · doi:10.1371/journal.pone.0039465 · Cited by 270 · see citing works
Neurodegeneration and neuroprotection in Parkinson disease
Fahn, S., & Sulzer, D. L. (2004) · Neurotherapeutics · doi:10.1602/neurorx.1.1.139 · Cited by 266 · see citing works
Self-citationHydroxyl radical attack on dopamine.
Slivka, A., & Cohen, G. (1985) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(17)36277-4 · Cited by 264 · see citing works
Parkinson's disease: Neuron loss in the nucleus basalis without concomitant Alzheimer's disease
Nakano, I., & Hirano, A. (1984) · Annals of Neurology · doi:10.1002/ana.410150503 · Cited by 260 · see citing works
Orthostatic hypotension from sympathetic denervation in Parkinson’s disease
Goldstein, D. S., Holmes, C. S., Dendi, R., BRUCE, S. R., & Li, S.-T. (2002) · Neurology · doi:10.1212/wnl.58.8.1247 · Cited by 258 · see citing works
The second brain and Parkinson’s disease
Lebouvier, T., Chaumette, T., Paillusson, S., Duyckaerts, C. J., Varannes, S. B. D., Neunlist, M., & Derkinderen, P. (2009) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2009.06873.x · Cited by 258 · see citing works
Lewy body-related ?-synucleinopathy in the aged human brain
Jellinger, K. A. (2004) · Journal of Neural Transmission · doi:10.1007/s00702-004-0138-7 · Cited by 253 · see citing works
Henderson, J. M. (2000) · Brain · doi:10.1093/brain/123.7.1410 · Cited by 244 · see citing works
Unregulated Cytosolic Dopamine Causes Neurodegeneration Associated with Oxidative Stress in Mice
Chen, L., Ding, Y., Cagniard, B., Laar, A. D. V., Mortimer, A. D., Chi, W., Hastings, T. G., Kang, U. J., & Zhuang, X. (2008) · Journal of Neuroscience · doi:10.1523/jneurosci.3602-07.2008 · Cited by 238 · see citing works
Molecular Circuitry of Endocytosis at Nerve Terminals
Dittman, J., & Ryan, T. A. (2009) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.042308.113302 · Cited by 238 · see citing works
Use of antihypertensives and the risk of Parkinson disease
Becker, C., Jick, S. S., & Meier, C. R. (2008) · Neurology · doi:10.1212/01.wnl.0000303818.38960.44 · Cited by 230 · see citing works
A critical evaluation of current staging of α-synuclein pathology in Lewy body disorders
Jellinger, K. A. (2008) · Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease · doi:10.1016/j.bbadis.2008.07.006 · Cited by 229 · see citing works
Travagli, R. A., Gillis, R. A., Rossiter, C. D., & Vicini, S. (1991) · American Journal of Physiology-Gastrointestinal and Liver Physiology · doi:10.1152/ajpgi.1991.260.3.g531 · Cited by 213 · see citing works
Anlauf, M., Schäfer, M. K.-H., Eiden, L. E., & Weihe, E. (2003) · The Journal of Comparative Neurology · doi:10.1002/cne.10599 · Cited by 213 · see citing works
Kang, Y., & Kitai, S. T. (1990) · Brain Research · doi:10.1016/0006-8993(90)91826-3 · Cited by 202 · see citing works
Anatomy, physiology, and pathophysiology of the pedunculopontine nucleus
Jenkinson, N., Nandi, D., Muthusamy, K. A., Ray, N. J., Gregory, R. P., Stein, J. F., & Aziz, T. Z. (2008) · Movement Disorders · doi:10.1002/mds.22189 · Cited by 195 · see citing works
Sulzer, D., Mosharov, E. V., Tallóczy, Z., Zucca, F. A., Simon, J. D., & Zecca, L. (2008) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2008.05385.x · Cited by 190 · see citing works
Self-citationLiang, C., Wang, T. T., Luby‐Phelps, K., & German, D. C. (2006) · Experimental Neurology · doi:10.1016/j.expneurol.2006.08.015 · Cited by 186 · see citing works
Lewy pathology and neurodegeneration in premotor Parkinson's disease
Tredici, K. D., & Braak, H. (2012) · Movement Disorders · doi:10.1002/mds.24921 · Cited by 184 · see citing works
Profound Cardiac Sympathetic Denervation Occurs in Parkinson Disease
Amino, T., Orimo, S., Itoh, Y., Takahashi, A., Uchihara, T., & Mizusawa, H. (2006) · Brain Pathology · doi:10.1111/j.1750-3639.2005.tb00097.x · Cited by 178 · see citing works
Chronic Constipation in the Elderly
Gallegos-Orozco, J., Foxx-Orenstein, A., Sterler, S. M., & Stoa, J. (2012) · American Journal of Gastroenterology · doi:10.1038/ajg.2011.349 · Cited by 176 · see citing works
Calcium entry induces mitochondrial oxidant stress in vagal neurons at risk in Parkinson's disease
Goldberg, J. A., Guzmán, J. N., Estep, C. M., Ilijić, E., Kondapalli, J., Sánchez-Padilla, J., & Surmeier, D. J. (2012) · Nature Neuroscience · doi:10.1038/nn.3209 · Cited by 167 · see citing works
Self-citationWeihe, E., Depboylu, C., Schütz, B., Schäfer, M. K.-H., & Eiden, L. E. (2006) · Cellular and Molecular Neurobiology · doi:10.1007/s10571-006-9053-9 · Cited by 162 · see citing works
Spare respiratory capacity, oxidative stress and excitotoxicity
Nicholls, D. G. (2009) · Biochemical Society Transactions · doi:10.1042/bst0371385 · Cited by 161 · see citing works
Use of Calcium Channel Blockers and Parkinson’s Disease
Pasternak, B., Svanström, H., Nielsen, N. M., Fugger, L. H., Melbye, M., & Hviid, A. P. (2012) · American Journal of Epidemiology · doi:10.1093/aje/kwr362 · Cited by 154 · see citing works
Gibb, W. R. G. (1992) · Brain Research · doi:10.1016/0006-8993(92)90719-p · Cited by 152 · see citing works
Putzier, I., Kullmann, P. H. M., Horn, J. P., & Levitan, E. S. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.4742-09.2009 · Cited by 145 · see citing works
Cersosimo, M. G., & Benarroch, E. E. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.09.030 · Cited by 145 · see citing works
Raised calcium promotes α-synuclein aggregate formation
Nath, S., Goodwin, J., Engelborghs, Y., & Pountney, D. L. (2010) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2010.12.004 · Cited by 144 · see citing works
Lysosomal Ca2+ homeostasis: Role in pathogenesis of lysosomal storage diseases
Lloyd‐Evans, E., & Platt, F. M. (2011) · Cell Calcium · doi:10.1016/j.ceca.2011.03.010 · Cited by 141 · see citing works
Serafin, M., Khateb, A., & Mühlethaler, M. (1990) · Neuroscience Letters · doi:10.1016/0304-3940(90)90154-2 · Cited by 135 · see citing works
Specific A10 Dopaminergic Nuclei in the Midbrain Degenerate in Parkinson's Disease
McRitchie, D. A., Cartwright, H., & Halliday, G. M. (1997) · Experimental Neurology · doi:10.1006/exnr.1997.6418 · Cited by 135 · see citing works
Calcium-dependent regulation of exocytosis
Barclay, J. W., Morgan, A., & Burgoyne, R. D. (2005) · Cell Calcium · doi:10.1016/j.ceca.2005.06.012 · Cited by 126 · see citing works
Endogenous Calcium Buffering Capacity of Substantia Nigral Dopamine Neurons
Foehring, R. C., Zhang, X. F., Lee, J. C. F., & Callaway, J. C. (2009) · Journal of Neurophysiology · doi:10.1152/jn.00038.2009 · Cited by 123 · see citing works
Characterization of Myenteric Sensory Neurons in the Mouse Small Intestine
Mao, Y., Wang, B., & Kunze, W. (2006) · Journal of Neurophysiology · doi:10.1152/jn.00204.2006 · Cited by 121 · see citing works
Oxytocin excites gastric-related neurones in rat dorsal vagal complex
McCann, M. J., & Rogers, R. C. (1990) · The Journal of Physiology · doi:10.1113/jphysiol.1990.sp018202 · Cited by 118 · see citing works
Liang, C., Nelson, O. L., Yazdani, U., Pasbakhsh, P., & German, D. C. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20098 · Cited by 117 · see citing works
Liang, C., Sinton, C. M., Sonsalla, P. K., & German, D. C. (1996) · Neurodegeneration · doi:10.1006/neur.1996.0042 · Cited by 116 · see citing works
Physiological Phenotype and Vulnerability in Parkinson's DiseasePreprint
Surmeier, D. J., Guzmán, J. N., Sánchez, J. A., & Schumacker, P. T. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a009290 · Cited by 115 · see citing works
Self-citationClinical availability of skin biopsy in the diagnosis of Parkinson's disease
Miki, Y., Tomiyama, M., Ueno, T., Haga, R., Nishijima, H., Suzuki, C., Mori, F., Kaimori, M., Baba, M., & Wakabayashi, K. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.12.027 · Cited by 114 · see citing works
Relationships between EEA1 binding partners and their role in endosome fusion
Mills, I. G., Urbé, S., & Clague, M. J. (2001) · Journal of Cell Science · doi:10.1242/jcs.114.10.1959 · Cited by 109 · see citing works
THE PATHOLOGY OF CERTAIN MEDULLARY NUCLEI IN PARKINSONISM
Eadie, M. J. (1963) · Brain · doi:10.1093/brain/86.4.781 · Cited by 100 · see citing works
Huisman, E., Uylings, H. B. M., & Hoogland, P. V. J. M. (2008) · Movement Disorders · doi:10.1002/mds.22009 · Cited by 95 · see citing works
Phenotypic Differentiation during Migration of Dopaminergic Progenitor Cells to the Olfactory Bulb
Baker, H. A., Liu, N., Chun, H. S., Saino‐Saito, S., Berlin, R., Volpe, B. T., & Son, J. H. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-21-08505.2001 · Cited by 94 · see citing works
Úbeda‐Bañón, I., Saiz‐Sánchez, D., de la Rosa‐Prieto, C., Argandoña‐Palacios, L., García-Muñozguren, S., & Martı́nez-Marcos, A. (2010) · Acta Neuropathologica · doi:10.1007/s00401-010-0687-9 · Cited by 93 · see citing works
GAI, W. P., Halliday, G. M., Blumbergs, P. C., Geffen, L. B., & Blessing, W. W. (1991) · Brain · doi:10.1093/brain/114.5.2253 · Cited by 89 · see citing works
Dopaminergic midbrain neurons are the prime target for mitochondrial DNA deletions
Bender, A., Schwarzkopf, R.-M., McMillan, A., Krishnan, K. J., Rieder, G., Neumann, M., Elstner, M., Turnbull, D. M., & Klopstock, T. (2008) · Journal of Neurology · doi:10.1007/s00415-008-0892-9 · Cited by 88 · see citing works
Age-related loss of dorsal vagal neurons in Parkinson's disease
Gai, W., Blumbergs, P. C., Geffen, L. B., & Blessing, W. W. (1992) · Neurology · doi:10.1212/wnl.42.11.2106 · Cited by 85 · see citing works
Medullary catecholaminergic neurons in the normal human brain and in Parkinson's disease
Saper, C. B., Sorrentino, D. M., German, D. C., & Lacalle, S. D. (1991) · Annals of Neurology · doi:10.1002/ana.410290602 · Cited by 83 · see citing works
Analysis of Whole-cell Currents by Patch Clamp of Guinea-pig Myenteric Neurones in Intact Ganglia
Rugiero, F., Gola, M., Kunze, W. A. A., Reynaud, J., Furness, J. B., & Clerc, N. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2001.013051 · Cited by 79 · see citing works
Lewy Bodies and Olfactory Dysfunction in Old Age
Wilson, R. S., Yu, L., Schneider, J. A., Arnold, S. E., Buchman, A. S., & Bennett, D. A. (2011) · Chemical Senses · doi:10.1093/chemse/bjq139 · Cited by 78 · see citing works
Clerc, N., Furness, J. B., Bornstein, J. C., & Kunze, W. A. A. (1997) · Neuroscience · doi:10.1016/s0306-4522(97)00318-7 · Cited by 75 · see citing works
Ghebremedhin, E., Tredici, K. D., Langston, J. W., & Braak, H. (2009) · Acta Neuropathologica · doi:10.1007/s00401-009-0596-y · Cited by 74 · see citing works
Lesions outside the CNS in Parkinson's disease
Djaldetti, R., Lev, N., & Melamed, E. (2009) · Movement Disorders · doi:10.1002/mds.22172 · Cited by 68 · see citing works
Controversies over the staging of α-synuclein pathology in Parkinson’s disease
Kalaitzakis, M. E., Graeber, M. B., Gentleman, S. M., & Pearce, R. K. B. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0381-3 · Cited by 68 · see citing works
A not entirely benign procedure: progression of Parkinson’s disease
Tredici, K. D., & Braak, H. (2008) · Acta Neuropathologica · doi:10.1007/s00401-008-0355-5 · Cited by 67 · see citing works
Parkinson's disease with involvement of the parasympathetic ganglia
Takeda, S., Yamazaki, K., Miyakawa, T., & Arai, H. (1993) · Acta Neuropathologica · doi:10.1007/bf00369454 · Cited by 63 · see citing works
Orimo, S., Uchihara, T., Kanazawa, T., Itoh, Y., Wakabayashi, K., Kakita, A., & Takahashi, H. (2011) · Neuropathology and Applied Neurobiology · doi:10.1111/j.1365-2990.2011.01194.x · Cited by 62 · see citing works
Clerc, N., Furness, J. B., Li, Z. S., Bornstein, J. C., & Kunze, W. A. A. (1998) · Neuroscience · doi:10.1016/s0306-4522(98)00025-6 · Cited by 61 · see citing works
Goldberg, J. A., Teagarden, M. A., Foehring, R. C., et al. (2009) · Journal of Neuroscience · doi:10.1523/jneurosci.5582-08.2009 · Cited by 60 · see citing works
Cullen, K. M., & Halliday, G. M. (1998) · Neurobiology of Aging · doi:10.1016/s0197-4580(98)00066-9 · Cited by 59 · see citing works
Intrinsic Bioenergetic Properties and Stress Sensitivity of Dopaminergic Synaptosomes
Choi, S. W., Gerencser, A. A., Lee, D. W., Rajagopalan, S., Nicholls, D. G., Andersen, J. K., & Brand, M. D. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.5817-10.2011 · Cited by 51 · see citing works
Parvalbumin is freely mobile in axons, somata and nuclei of cerebellar Purkinje neurones
Schmidt, H., Arendt, O., Brown, E. B., Schwaller, B., & Eilers, J. (2006) · Journal of Neurochemistry · doi:10.1111/j.1471-4159.2006.04231.x · Cited by 46 · see citing works
Do mtDNA deletions drive premature aging in mtDNA mutator mice?
Kraytsberg, Y., Simon, D. K., Turnbull, D. M., & Khrapko, K. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00484.x · Cited by 42 · see citing works
Tamura, K., Ito, H., & Wade, P. R. (2001) · The Journal of Comparative Neurology · doi:10.1002/cne.1293 · Cited by 34 · see citing works
Szegő, É. M., Gerhardt, E., Outeiro, T. F., & Kermer, P. (2011) · Journal of the Neurological Sciences · doi:10.1016/j.jns.2011.06.048 · Cited by 29 · see citing works
Clinical correlates of similar pathologies in parkinsonian syndromes
Song, Y. J. C., Huang, Y. M., & Halliday, G. M. (2011) · Movement Disorders · doi:10.1002/mds.23336 · Cited by 22 · see citing works
Chan, J. Y. H., & Chan, S. H. H. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90158-4 · Cited by 8 · see citing works
Retinal dopamine sensitivity to MPP+ toxicity: electrophysiological and biochemical evaluation
Harnois, C., Marcotte, G., Daigle, M., & Paolo, T. D. (1989) · Neuroscience Letters · doi:10.1016/0304-3940(89)90784-2 · Cited by 6 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Goldberg JA, Guzman JN, Estep CM, Ilijic E, Kondapalli J, Sanchez-Padilla J, et al. Calcium entry induces mitochondrial oxidant stress in vagal neu- rons at risk in Parkinson's disease. Nat Neurosci 2012; 15:1414-21; PMID:22941107; http://dx.doi. org/10.1038/nn.3209. · DOI
Cited by
Sorted by citations
Interactions of iron, dopamine and neuromelanin pathways in brain aging and Parkinson's disease
Zucca, F. A., Segura-Aguilar, J., Ferrari, E., Muñoz, P., Paris, I., Sulzer, D., Sarna, T., Casella, L., & Zecca, L. (2017) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2015.09.012 · Cited by 659 · see citing works
Self-citationExploring Braak’s hypothesis of Parkinson’s disease
Rietdijk, C. D., Perez-Pardo, P., Garssen, J., van Wezel, R. J. A., & Kraneveld, A. D. (2017) · Frontiers in Neurology · doi:10.3389/fneur.2017.00037 · Cited by 395 · see citing works
Cheng, J., Liao, Y., Dong, Y., Hu, H., Yang, N., Kong, X., Li, S., Li, X., Guo, J., Qin, L., et al. (2020) · Autophagy · doi:10.1080/15548627.2020.1719723 · Cited by 233 · see citing works
Fifel, K., Piggins, H., & Deboer, T. (2016) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2015.02.005 · Cited by 30 · see citing works
Chemiexcitation: Mammalian Photochemistry in the Dark<sup>†</sup>
Brash, D. E., & Goncalves, L. C. P. (2023) · Photochemistry and Photobiology · doi:10.1111/php.13781 · Cited by 16 · see citing works
- Authors
- Surmeier, D. J., & Sulzer, D.
- Affiliations
- Northwestern University (US)
- Columbia University (US)
- Corresponding author
- Surmeier, D. James
- Venue
- Prion
- Publisher
- Informa UK Limited
- Published
- 2013-01
- Volume
- 7
- Issue
- 1
- Pages
- 85-91
- ISSN
- 1933-6896 (ISSN-L)
- 1933-690X
- PMC
- PMC3609055
- OpenAlex
- W1981573235
- Cited by
- 74
- References
- 118
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 4 · 2023: 5 · 2022: 4 · 2021: 2 · 2020: 6 · 2019: 11 · 2018: 3 · 2017: 7 · 2016: 4 · 2015: 7 · 2014: 8 · 2013: 5
- FWCI
- 1.04
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Prion (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Institute of Neurological Disorders and Stroke (P50-NS38370, P50NS038370, P50NS047085)
- Topics
- Health Sciences › Medicine › Neurology › Parkinson's Disease Mechanisms and Treatments
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nuclear Receptors and Signaling
- Health Sciences › Medicine › Neurology › Neurological disorders and treatments
- Keywords
- Parkinson's disease, Lewy body pathology, Lewy bodies, Lewy neurites, dopaminergic neurons, substantia nigra pars compacta, neuronal vulnerability, mitochondrial dysfunction, calcium buffering, axon morphology, pathogenesis, neurodegeneration
- MeSH terms
- Animals, Brain, Calcium, Humans, Mitochondria, Neurons, Parkinson Disease, Substantia Nigra, Oxidative Stress, alpha-Synuclein
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
