Skip to main content

Advertisement

Log in

The significance of neuronal lateralisation in Parkinson’s disease

  • Movement Disorders - Review article
  • Published:
Journal of Neural Transmission Aims and scope Submit manuscript

Abstract

The destruction of the dopaminergic neurons in the substantia nigra (SN) and consequent depletion of striatal dopamine elicits the main movement deficits related to Parkinson’s disease (PD). In the early stages of the illness, the motor symptoms are often exhibited asymmetrically. Thus, the onset of PD features starts on either the right or left side. The side of onset appears to determine the prognosis of the disorder and other features, such as right-side tremor dominance has a better prognosis in contrast to left-side dominant bradykinesia-rigidity. In addition, left-side onset of motor features is associated with cognitive decline. Therefore, an intricate relation appears to exist between the side of disease onset and progression/severity and other non-motor symptoms. Unilateral PD in turn corresponds to neuronal nigrostriatal degeneration in the contralateral hemisphere. Indeed positron emission tomography has demonstrated a positive correlation between symptom asymmetry and brain function (Hoorn et al. Parkinsonism Relat Disord 17:58–60, 2011), which corresponds to a unilateral pattern of degeneration. This phenomenon appears to be exclusive to PD. Additionally, the variation in motor symptom(s) dominance exhibited in the disorder conforms to the notion that PD is a spectrum disease with many sub-groups. Thus, clinical and post mortem studies on “lateralisation” may serve as a vital tool in understanding the mechanism(s) eliciting the characteristic destruction of the SN neurons. Additionally, it may be employed as a predictive indicator for the symptomology and prognosis of the illness thus allowing selective treatment strategies targeted at the pronounced hemispheric degeneration.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Abbas N, Lucking CB, Human RS (1999) A wide variety of mutations in the parkin gene are responsible for autosomal recessive parkinsonism in Europe. Mol Genetics 8:567–574

    Article  CAS  Google Scholar 

  • Androulidakis AG, Kühn AA, Chen CC, Blomstedt P, Kempf F, Kupsch A, Schneider GH, Doyle L, Dowsey-Limousin P, Hariz MI, Brown P (2007) Dopaminergic therapy promotes lateralized motor activity in the subthalamic area in Parkinson’s disease. Brain. 130(2):457–468

    Article  PubMed  Google Scholar 

  • Antony PM, Diederich NJ, Balling R (2011) Parkinson’s disease mouse models in translational research. Mamm Genome 22(7–8):401–419

    Article  PubMed  Google Scholar 

  • Ashkan K, Wallace BA, Mitrofanis J, Pollo C, Brard PY, Fagret D, Benabid AL (2007) SPECT imaging, immunohistochemical and behavioural correlations in the primate models of Parkinson’s disease. Parkinsonism Relat Disord 13(5):266–275

    Article  PubMed  Google Scholar 

  • Avila I, Parr-Brownlie LC, Brazhnik E, Castañeda E, Bergstrom DA, Walters JR (2010) Beta frequency synchronization in basal ganglia output during rest and walk in a hemiparkinsonian rat. Exp Neurol 221(2):307–319

    Article  PubMed  Google Scholar 

  • Baluchnejadmojarad T, Roghani M (2004) Evaluation of functional asymmetry in rats with dose-dependent lesions of dopaminergic nigrostriatal system using elevated body swing test. Physiol Behav 82(2–3):369–373

    Article  PubMed  CAS  Google Scholar 

  • Barber-Singh J, Seo BB, Matsuno-Yagi A, Yagi T (2010) Protective role of rAAV-NDI1, serotype 5, in an acute MPTP mouse Parkinson’s model. Parkinsons Dis 2011:438370

  • Barolin GS, Bernheimer H, Hornykiewicz O (1964) Seitenverschiedenes Verhalten des Dopamins (3-Hydroxytyramin) im Gehirn eines Falles von Hemiparkinsonismus. Schweizer Archiv für Neurologie, Neurochirurgie und Psychiatrie 94(2):241–248

    Google Scholar 

  • Bennett DA, Beckett LA, Murray AM, Shannon KM, Goetz CG, Pilgrim DM, Evans DA (1996) Prevalence of parkinsonian signs and associated mortality in a community population of older people. N Engl J Med 334:71–76

    Article  PubMed  CAS  Google Scholar 

  • Berg D, Becker G, Zeiler B, Tucha O, Hofmann E, Preier M, Benz P, Jost W, Reiners K, Lange KW (1999) Vulnerability of the nigrostriatal system as detected by transcranial ultrasound. Neurology S3:1026–1031

    Article  Google Scholar 

  • Bernheimer H, Birkmayer W, Hornykiewicz O, Jellinger K, Seitelberger F (1973) Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J Neurol Sci 20:415–455

    Article  PubMed  CAS  Google Scholar 

  • Birkmayer W, Hornykiewicz O (1961) Der l-3,4-Dioxyphenylalanin (= DOPA)-Effekt bei der Parkinson-Akinese. Wr. klin. Wschr. 73:787–788

    CAS  Google Scholar 

  • Birkmayer W, Mentasti M (1967) Further experimental studies on the catecholamine metabolism in extrapyramidal diseases (Parkinson and chorea syndromes). Arch Psychiatr Nervenkr. 210(1):29–35

    Article  PubMed  CAS  Google Scholar 

  • Blonder LX, Gur RE, Gur RC, Saykin AJ, Hurtig HI (1989) Neuropsychological functioning in hemiparkinsonism. Brain Cogn 9:244–257

    Article  PubMed  CAS  Google Scholar 

  • Bortolozzi A, Duffard R, de Duffard AM (2003) Asymmetrical development of the monoamine systems in 2,4-dichlorophenoxyacetic acid treated rats. Neurotoxicology. 24(1):149–157

    Article  PubMed  CAS  Google Scholar 

  • Braak H, Del Tredici K, Bratzke H, Hamm-Clement J, Sandmann-Keil D, Rüb U (2002) Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson’s disease (preclinical and clinical stages). J Neurol 249 Suppl 3:III/1–5

    Google Scholar 

  • Braak H, Rub U, Gai WP, Del Tredici K (2003) Idiopathic Parkinson’s disease: possible routes by which vulnerable neuronal types may be subject to neuroinvasion by an unknown pathogen. J Neural Transm 110:517–536

    Article  PubMed  CAS  Google Scholar 

  • Breit S, Martin A, Lessmann L, Cerkez D, Gasser T, Schulz JB (2008) Bilateral changes in neuronal activity of the basal ganglia in the unilateral 6-hydroxydopamine rat model. J Neurosci Res 86(6):1388–1396

    Article  PubMed  CAS  Google Scholar 

  • Brooks DJ, Pavese N (2009) Recent imaging advances in the diagnosis and management of Parkinson’s disease. F1000 Med Rep 1:82

    Google Scholar 

  • Brücke T, Djamshidian S, Bencsits G, Pirker W, Asenbaum S, Podreka I (2000) SPECT and PET imaging of the dopaminergic system in Parkinson’s disease. J Neurol 247 Suppl 4:IV/2–IV/7

  • Burke RE, Dauer WT, Vonsattel JP (2008) A critical evaluation of the Braak staging scheme for Parkinson’s disease. Ann Neurol 64(5):485–491

    Article  PubMed  Google Scholar 

  • Bustos G, Abarca J, Bustos V, Riquelme E, Noriega V, Moya C, Campusano J (2009) NMDA receptors mediate an early up-regulation of brain-derived neurotrophic factor expression in substantia nigra in a rat model of presymptomatic Parkinson’s disease. J Neurosci Res 87(10):2308–2318

    Article  PubMed  CAS  Google Scholar 

  • Cardoso F (2002) HIV-related movement disorders; epidemiology, pathogenesis and management. CNS drugs 16(10):663–668

    Article  PubMed  Google Scholar 

  • Castellano MA, Rodriguez Diaz M (1991) Nigrostriatal dopaminergic cell activity is under control by substantia nigra of the contralateral brain side: electrophysiological evidence. Brain Res Bull 27(2):213–218

    Article  PubMed  CAS  Google Scholar 

  • Castellano MA, Diaz-Palarea MD, Rodriguez M, Barroso J (1987) Lateralization in male rats and dopaminergic system: evidence of right-side population bias. Physiol Behav 40(5):607–612

    Article  PubMed  CAS  Google Scholar 

  • Castellano MA, Diaz-Palarea MD, Barroso J, Rodriguez M (1989) Behavioral lateralization in rats and dopaminergic system: individual and population laterality. Behav Neurosci 103(1):46–53

    Article  PubMed  CAS  Google Scholar 

  • Cheesman AL, Barker RA, Lewis SJG, Robbins TW, Owen AM, Brooks DJ (2005) Lateralisation of striatal function: evidence from 18F-dopa PET in Parkinson’s disease. J Neurol Neurosurg Psychiatry 76:1204–1210

    Article  PubMed  CAS  Google Scholar 

  • Choe BY, Park JW, Lee KS, Son BC, Kim MC, Kim BS, Suh TS, Lee HK, Shinn KS (1998) Neuronal laterality in Parkinson’s disease with unilateral symptom by in vivo 1H magnetic resonance spectroscopy. Invest Radiol 33(8):450–455

    Article  PubMed  CAS  Google Scholar 

  • Collier TJ, Dung Ling Z, Carvey PM, Fletcher-Turner A, Yurek DM, Sladek JR Jr, Kordower JH (2005) Striatal trophic factor activity in aging monkeys with unilateral MPTP-induced parkinsonism. Exp Neurol 191(Suppl 1):S60–S67

    Article  PubMed  CAS  Google Scholar 

  • Colosimo C, Martínez-Martín P, Fabbrini G, Hauser RA, Merello M, Miyasaki J, Poewe W, Sampaio C, Rascol O, Stebbins GT, Schrag A, Goetz CG (2010) Task force report on scales to assess dyskinesia in Parkinson’s disease: critique and recommendations. Movement Disord 25(9):1131–1142

    Article  PubMed  Google Scholar 

  • Cookson MR, Bandmann O (2010) Parkinson’s disease: insights from pathways. Hum Mol Genet 19(R1):R21–R27

    Google Scholar 

  • Cooper CA, Mikos AE, Wood MF, Kirsch-Darrow L, Jacobson CE, Okun MS, Rodriguez RL, Bowers D, Fernandez HH (2009) Does laterality of motor impairment tell us something about cognition in Parkinson disease? Parkinsonism Relat Disorder 15(4):315–317

    Article  CAS  Google Scholar 

  • Cronin-Golomb A (2010) Parkinson’s disease as a disconnection syndrome. Neuropsychol Rev 20(2):191–208

    Article  PubMed  Google Scholar 

  • Cubo E, Martín PM, Martin-Gonzalez JA, Rodríguez-Blázquez C, Kulisevsky J; ELEP Group Members (2010) Motor laterality asymmetry and nonmotor symptoms in Parkinson’s disease. Mov Disord 25(1):70–75

    Google Scholar 

  • Da Cunha C, Wietzikoski EC, Ferro MM, Martinez GR, Vital MA, Hipólide D, Tufik S, Canteras NS (2008) Hemiparkinsonian rats rotate toward the side with the weaker dopaminergic neurotransmission. Behav Brain Res 189(2):364–372

    Article  PubMed  CAS  Google Scholar 

  • Dale RC, Church AJ, Surtees RA, Lees AJ, Adcock JE, Harding B, Neville BG, Giovannoni G (2004) Encephalitits lethargica syndrome: 20 new cases and evidence of basal ganglia autoimmunity. Brain. 127(Pt 1):21–33

    Article  PubMed  Google Scholar 

  • De La Fuente-Fernandez R (2000) Maternal effect on Parkinson’s disease. Ann Neurol 48:782–787

    Article  PubMed  Google Scholar 

  • Dexter DT, Sian J, Rose S, Hindmarsh JG, Mann VM, Cooper JM, Wells FR, Daniel SE, Lees AJ, Schapira AHV, Jenner P, Marsden CD (1992) Indices of oxidative stress in individuals with incidental Lewy body disease. Ann Neurol 35:38–44

    Article  Google Scholar 

  • Ding F, Luan L, Ai Y, Walton A, Gerhardt GA, Gash DM, Grondin R, Zhang Z (2008) Development of a stable, early stage unilateral model of Parkinson’s disease in middle-aged rhesus monkeys. Exp Neurol 212(2):431–439

    Article  PubMed  Google Scholar 

  • Eggers C, Schmidt A, Hagenah J, Brüggemann N, Klein JC, Tadic V, Kertelge L, Kasten M, Binkofski F, Siebner H, Neumaier B, Fink GR, Hilker R, Klein C (2010) Progression of subtle motor signs in PINK1 mutation carriers with mild dopaminergic deficit. Neurology. 74(22):1798–1805

    Article  PubMed  CAS  Google Scholar 

  • Espay AJ, Henderson KK (2011) Postencephalitic parkinsonism and basal ganglia necrosis due to Epstein-Barr virus infection. Neurology 26(17):1529–1530

    Article  Google Scholar 

  • Fallgatter AJ, Neuhauser B, Herrmann MJ, Ehlis A-C, Wagener A, Scheuerpflug P, Reiners K, Riederer P (2003) Far field potentials from the brain stem after transcutaneous vagus nerve stimulation. J Neural Transm 110:1437–1443

    Article  PubMed  CAS  Google Scholar 

  • Gasparoli E, Delibori D, Polesello G, Santelli L, Ermani M, Battistin L, Bracco F (2002) Clinical predictors in Parkinson’s disease. Neurol Sci 23(Suppl. 2):S77–S78

    Article  PubMed  Google Scholar 

  • Gerlach M., Reichmann H., Riederer P (2007) Die Parkinson-Krankheit. Grundlagen, Klinik, Therapie. 4. Auflage. Springer, Wien

  • Giardino L (1996) Right-left asymmetry of D-1 and D-2 receptor density is lost in the basal ganglia of old rats. Brain Res 720:235–238

    Article  PubMed  CAS  Google Scholar 

  • González-Hernández T, Barroso-Chinea P, Rodríguez M (2004) Response of the GABAergic and dopaminergic mesostriatal projections to the lesion of the contralateral dopaminergic mesostriatal pathway in the rat. Mov Disord 19(9):1029–1042

    Article  PubMed  Google Scholar 

  • Grealish S, Mattsson B, Draxler P, Björklund A (2010) Characterisation of behavioural and neurodegenerative changes induced by intranigral 6-hydroxy-dopamine lesions in a mouse model of Parkinson’s disease. Eur J Neurosci 31:2266–2278

    Article  PubMed  Google Scholar 

  • Greffard S, Verny M, Bonnet AM, Seilheart D, Hauw JJ, Duyckaerts C (2010) A stable proportion of Lewy body bearing neurons in the substantia nigra suggests a model in which the Lewy body causes neuronal dead. Neurobiol Aging 31(1):99–103

    Article  PubMed  CAS  Google Scholar 

  • Grünblatt E, Mandel S, Jacob-Hirsch J, Zeligson S, Amariglo N, Rechavi G, Li J, Ravid R, Roggendorf W, Riederer P, Youdim MBH (2004) Gene expression profiling of parkinsonian substantia nigra pars compacta; alterations in ubiquitin-proteasome, heat shock protein, iron and oxidative stress regulated proteins, cell adhesion/cellular matrix and vesicle trafficking genes. J Neural Transm 111:1543–1573

    Article  PubMed  CAS  Google Scholar 

  • Halliday G, Hely M, Reid W, Morris J (2008) The progression of pathology in longitudinally followed patients with Parkinson’s disease. Acta Neuropathol 115:409–415

    Article  PubMed  Google Scholar 

  • Hanakawa T, Katsumi Y, Fukuyama H, Honda M, Hayashi T, Kimura J, Shibasaki H (1999) Mechanisms underlying gait disturbance in Parkinson’s disease: a single photon emission computed tomography study. Brain. 122(Pt 7):1271–1282

    Article  PubMed  Google Scholar 

  • Heim C, Sova L, Kurz T, Kolasiewicz W, Schwegler H, Sontag KH (2002) Partial loss of dopaminergic neurons in the substantia nigra, ventrotegmental area and the retrorubral area - model of the early beginning of Parkinson’s symptomatology? J Neural Transm. 109(5–6):691–709

    Article  PubMed  CAS  Google Scholar 

  • Henderson JM, Stanic D, Tomas D, Patch J, Horne MK, Bourke D, Finkelstein DI (2005) Postural changes after lesions of the substantia nigra pars reticulata in hemiparkinsonian monkeys. Behav Brain Res 160(2):267–276

    Article  PubMed  Google Scholar 

  • Hershey T, Wu J, Weaver PM, Perantie DC, Karimi M, Tabbal SD, Perlmutter JS (2008) Unilateral vs. bilateral STN DBS effects on working memory and motor function in Parkinson disease. Exp Neurol 210(2):402–408

    Article  PubMed  CAS  Google Scholar 

  • Hoehn MM, Yahr MD (2001) Parkinsonism: onset, progression, and mortality. 1967. Neurology 57(10 Suppl 3):S11–S26

    PubMed  CAS  Google Scholar 

  • Huber SJ, Miller H, Bohaska L, Christy JA, Bornstein RA (1992) Asymmetrical cognitive differences associated with hemiparkinsonism. Arch Clin Neuropsychol 7:471–480

    PubMed  CAS  Google Scholar 

  • Iancu R, Mohapel P, Brundin P, Paul G (2005) Behavioral characterization of a unilateral 6-OHDA-lesion model of Parkinson’s disease in mice. Behav Brain Res 162(1):1–10

    Article  PubMed  CAS  Google Scholar 

  • Jellinger KA (2009) Formation and development of Lewy pathology: a critical update. J Neurol 256(Suppl 3):270–279

    Article  PubMed  Google Scholar 

  • Jeon MY, Lee WY, Kang HY, Chung EJ (2007) The effects of l-3,4-dihydroxyphenylalanine and dopamine agonists on dopamine neurons in the progressive hemiparkinsonian rat models. Neurol Res 29(3):289–295

    Article  PubMed  CAS  Google Scholar 

  • Jung KY, Chung CS, Park KW (2007) Bilateral medial temporal lesions in Japanese encephalitis. Neurology. 68(16):1319

    Article  PubMed  Google Scholar 

  • Kalita J, Misra UK (2000) The substantia nigra is involved in Japanese Encephalitis. Am J Neuroradiol 21(10):1978–1980

    PubMed  CAS  Google Scholar 

  • Katzen H, Bonnie E, Levin B, William W (2006) Side and type of motor symptom influence cognition in Parkinson’s disease. Mov Dis 21(11):1947–1953

    Article  Google Scholar 

  • Kopin IJ (1987) MPTP: an industrial chemical and contaminant of illicit narcotics stimulates a new era in research on Parkinson’s disease. Environ Health Perspect 75:45–51

    Article  PubMed  CAS  Google Scholar 

  • Kozlowski DA, Miljan EA, Bremer EG, Harrod CG, Gerin C, Connor B, George D, Larson B, Bohn MC (2004) Quantitative analyses of GFRalpha-1 and GFRalpha-2 mRNAs and tyrosine hydroxylase protein in the nigrostriatal system reveal bilateral compensatory changes following unilateral 6-OHDA lesions in the rat. Brain Res 1016(2):170–181

    Article  PubMed  CAS  Google Scholar 

  • Lees AJ (2009) The Parkinson chimera. Neurology 72(7):S2–S11

    Article  PubMed  Google Scholar 

  • Leh SE, Petrides M, Strafella AP (2010) The neural circuitry of executive functions in healthy subjects and Parkinson’s disease. Neuropsychopharmacology 35(1):70–85

    Article  PubMed  Google Scholar 

  • Lewald J, Schirm SN, Schwarz M (2004) Sound lateralization in Parkinson’s disease. Brain Res Cogn Brain Res. 21(3):335–341

    Article  PubMed  Google Scholar 

  • Lohmann E, Periquet M, Bonifati V, Wood NW, De Michele G, Bonnet AM, Fraix V, Broussolle E, Horstink MW, Vidailhet M, Verpillat P, Gasser T, Nicholl D, Teive H, Raskin S, Rascol O, Destée A, Ruberg M, Gasparini F, Meco G, Agid Y, Durr A, Brice A; French Parkinson’s Disease Genetics Study Group; European Consortium on Genetic Susceptibility in Parkinson’s Disease (2003) How much phenotypic variation can be attributed to parkin genotype? Ann Neurol 54(2):176–185

    Google Scholar 

  • Loius ED, Tang MJ, Cote L, Alfaro B, Mejia MA, Marder K (1999) Progression of parkinsonian signs in Parkinson disease. Arch Neurol 56:334–337

    Article  Google Scholar 

  • Lücking CB, Dürr A, Bonifati V, Vaughan J, De Michele G, Gasser T, Harhangi BS, Meco G, Denefle P, Wood NW, Agid Y, Brice A; European Consortium on Genetic Susceptibility in Parkinson’s Disease and the French Parkinson’s Disease Genetic Study Group (2000) Association between early onset parkinson’s disease and mutations in the PARKIN Gene. N Engl J Med 342(21):1560–1567

    Google Scholar 

  • Marti-Masso JF, Ruiz-Martinez J, Bolano MJ, Ruiz I, Gorostidi A, Moreno F, Ferrer I, Lopez de Munain A (2009) Neuropathology of Parkinson’s disease with the R1441G mutation in LRRK2. Mov Disord 24(13):1998–2001

    Article  PubMed  Google Scholar 

  • Martinez AJ, Utterback RA (1973) Unilateral Parkinson’s disease, clinical and neuropathologic findings. A case report. Neurology 23:164–170

    Article  PubMed  CAS  Google Scholar 

  • Mattay VS, Tessitore A, Callicott JH, Bertolino A et al (2002) Dopaminergic modulation of cortical function in patients with Parkinson’s disease. Ann Neurol 51:156–164

    Article  PubMed  CAS  Google Scholar 

  • Mattock C, Marmot M, Stern G (1988) Could Parkinson’s disease follow intra-uterine influenza? A speculative hypothesis. J Neurol Neurosurg Psychiatry 51(6):753–756

    Article  PubMed  CAS  Google Scholar 

  • McNamara P, Stavitsky K, Harris E, Szent-Imrey O, Durso R (2010) Mood, side of motor symptom onset and pain complaints in Parkinson’s disease. Int J Geriatr Psychiatry. 25(5):519–524

    Article  PubMed  Google Scholar 

  • Metz GA, Piecharka DM, Kleim JA, Whishaw IQ (2004) Preserved ipsilateral-to-lesion motor map organization in the unilateral 6-OHDA-treated rat model of Parkinson’s disease. Brain Res 1026(1):126–135

    Article  PubMed  CAS  Google Scholar 

  • Nakagawa M, Ohgoh M, Nishizawa Y, Ogura H (2004) Dopaminergic agonists and muscarinic antagonists improve lateralization in hemiparkinsonian rats in a novel exploratory Y-maze. J Pharmacol Exp Ther 309(2):737–744

    Article  PubMed  CAS  Google Scholar 

  • Natsopoulos D, Katsarou Z, Alevriadou A, Grouios G, Bostantzopoulou S, Mentenopoulos G (1997) Deductive and inductive reasoning in Parkinson’s disease patients and normal controls: review and experimental evidence. Cortex 33(3):463–481

    Article  PubMed  CAS  Google Scholar 

  • Nikkhah G, Falkenstein G, Rosenthal C (2001) Restorative plasticity of dopamine neuronal transplants depends on the degree of hemispheric dominance. J Neurosci 21(16):6252–6263

    PubMed  CAS  Google Scholar 

  • Nuytemans K, Theuns J, Cruts M, Van Broeckhoven C (2010) Genetic etiology of Parkinson disease associated with mutations in the SNCA, PARK2, PINK1, PARK7, and LRRK2 genes: a mutation update. Hum Mutat 31(7):763–780

    Article  PubMed  CAS  Google Scholar 

  • Pearson RCA, Neal JW, Powell TPS (1987) Bilateral morphological changes in the substantia nigra of the rat following unilateral damage of the striatum. Brain Res 400:127–132

    Article  PubMed  CAS  Google Scholar 

  • Picard F, de Saint-Martin A, Salmon E, Hirsch E, Marescaux C (1996) Postencephalitic stereotyped involuntary movements responsive to l-dopa. Mov Disord 11(5):567–570

    Article  PubMed  CAS  Google Scholar 

  • Piccini P, Burn DJ, Ceravolo R, Maraganore D, Brooks DJ (1999) The role of inheritance in sporadic Parkinson’s disease: evidence from a longitudinal study of dopaminergic function in twins. Ann Neurol 45(5):577–582

    Article  PubMed  CAS  Google Scholar 

  • Polak T, Ehlis AC, Langer J, Plichta M, Metzger F, Ringel TM, Fallgatter AJ (2007) Non-invasive measurement of vagus activity diagnosis of dementias? J Neural Transm 114:613–619

    Article  PubMed  CAS  Google Scholar 

  • Polak T, Weise D, Metzger F, Ehlis AC, Langer JB, Schramm A, Fallgatter AJ, Classen J (2011) Vagus nerve somatosensory evoked potentials in Parkinson’s disease. J Neurol 258:2276–2277

    Article  PubMed  CAS  Google Scholar 

  • Przuntek H, Müller T, Riederer P (2004) Diagnostic staging of Parkinson’s disease: conceptual aspects. J Neural Transm 111:201–216

    Article  PubMed  CAS  Google Scholar 

  • Riederer P, Foley P (2002) Mini-review: multiple developmental forms of parkinsonism. The basis for further research as to the pathogenesis of parkinsonism. J Neural Transm. 109(12):1469–1475

    Article  PubMed  CAS  Google Scholar 

  • Riederer P, Wuketich S (1976) Time course of nigrostriatal degeneration in Parkinson’s disease. J Neural Transm 38:277–301

    Article  PubMed  CAS  Google Scholar 

  • Riederer P, Sofic E, Rausch WD, Schmid B, Reynolds GP, Jellinger K, Youdim MBH (1989) Transition metals, ferritin, glutathione and ascorbic acid in parkinsonian brains. J Neurochem 52:515–520

    Article  PubMed  CAS  Google Scholar 

  • Riederer P, Foley P, Bringmann G, Feineis D, Brückner R, Gerlach M (2002) Biochemical and pharmacological characterization of 1-trichloromethyl-1,2,3,4-tetrahydro-βcarboline: a biologically relevant neurotoxin? European J Pharmacology 442:1–16

    Article  CAS  Google Scholar 

  • Riklan M, Stellar S, Reynolds C (1990) The relationship of memory and cognition in Parkinson’s disease to lateralisation of motor symptoms. J Neurol Neurosurg Psychiatry 53:359–360

    Article  PubMed  CAS  Google Scholar 

  • Rinne JO, Laihinen A, Rinne UK, Någren K, Bergman J, Ruotsalainen U (1993) PET study on striatal dopamine D2 receptor changes during the progression of early Parkinson’s disease. Mov Disord 8:134–138

    Article  PubMed  CAS  Google Scholar 

  • Rissanen E, Paavilainen T, Virta J, Marttila RJ, Rinne JO, Airas L (2010) Carbon monoxide poisoning-induced nigrostriatal dopaminergic dysfunction detected using positron emission tomography (PET). Neurotoxicology. 31(4):403–407

    Article  PubMed  CAS  Google Scholar 

  • Rosvold HE, Delgado JMR (1956) The effect on delayed-alternation test performance of stimulating or destroying electrically structures within the frontal lobes of the monkey’s brain. J Comp Physiol Psychol 49:365–372

    Article  PubMed  CAS  Google Scholar 

  • Schendan HE, Amick MM, Cronin-Golomb A (2009) Role of a lateralized parietal-basal ganglia circuit in hierarchical pattern perception: evidence from Parkinson’s disease. Behav Neurosci 123(1):125–136

    Article  PubMed  Google Scholar 

  • Schneider LH, Murphy RB, Coons EE (1982) Lateralization of striatal dopamine (D2) receptors in normal rats. Neurosci Lett 33(3):281–284

    Article  PubMed  CAS  Google Scholar 

  • Shen YQ, Hebert G, Su Y, Moze E, Neveu PJ, Li KS (2005) In mice, production of plasma IL-1 and IL-6 in response to MPTP is related to behavioral lateralization. Brain Res 1045(1–2):31–37

    Article  PubMed  CAS  Google Scholar 

  • Shinotoh H, Uchida Y, Hisao I, Hattori T (2000) Relationship between striatal [123I]beta-CIT binding and four major clinical signs in Parkinson’s disease. Ann Nucl Med 14:199–203

    Article  PubMed  CAS  Google Scholar 

  • Sian-Hülsmann J, Mandel S, Youdim MB, Riederer P (2011) The relevance of iron in the pathogenesis of Parkinson’s disease. J Neurochem 118(6):939–957

    Article  PubMed  CAS  Google Scholar 

  • Tang CC, Poston KL, Dhawan V, Eidelberg D (2010) Abnormalities in metabolic network activity precede the onset of motor symptoms in Parkinson’s disease. J Neurosci 30(3):1049–1056

    Article  PubMed  CAS  Google Scholar 

  • Tomer R, Levin BE, Weiner WJ (1993) Side of onset of motor symptoms influences cognition in Parkinson’s disease. Ann Neurol 34:579–584

    Article  PubMed  CAS  Google Scholar 

  • Van Camp N, Vreys R, Van Laere K, Lauwers E, Beque D, Verhoye M, Casteels C, Verbruggen A, Debyser Z, Mortelmans L, Sijbers J, Nuyts J, Baekelandt V, Van der Linden A (2010) Morphologic and functional changes in the unilateral 6-hydroxydopamine lesion rat model for Parkinson’s disease discerned with microSPECT and quantitative MRI. MAGMA. 23(2):65–75

    Article  PubMed  CAS  Google Scholar 

  • Van der Hoorn A, Bartels AL, Leenders KL, Jong BM (2011) Handedness and dominant side symptoms in Parkinson’s disease. Parkinsonism Relat Disord 17:58–60

    Article  PubMed  Google Scholar 

  • Wang SJ, Liu RS, Liu HC, Lin KN, Shan DE, Liao KK, Fuh JL, Lee LS (1993) Technetium-99m hexamethyl amine oxime single PET tomography of the brain in early Parkinson’s disease: correlation with dementia and lateralisation. Eur. J. Nucl 20(4):339–344

    CAS  Google Scholar 

  • Wang H, Katz J, Dagostino P, Soghomonian JJ (2007) Unilateral 6-hydroxydopamine lesion of dopamine neurons and subchronic L-DOPA administration in the adult rat alters the expression of the vesicular GABA transporter in different subsets of striatal neurons and in the substantia nigra, pars reticulata. Neuroscience. 145(2):727–737

    Article  PubMed  CAS  Google Scholar 

  • 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(2):850–861

    Article  PubMed  CAS  Google Scholar 

  • Wichmann T, DeLong MR (1998) Models of basal ganglia function and pathophysiology of movement disorders. Neurosurg Clin North Am 9:223–236

    CAS  Google Scholar 

  • Wright WG, Gurfinkel V, King L, Horak F (2007) Parkinson’s disease shows perceptuomotor asymmetry unrelated to motor symptoms. Neurosci Lett 417(1):10–15

    Article  PubMed  CAS  Google Scholar 

  • Wu RM, Shan DE, Sun CM, Liu RS, Hwu WL, Tai CH, Hussey J, West A, Gwinn-Hardy K, Hardy J, Chen J, Farrer M, Lincoln S (2002) Clinical, 18F-dopa PET, and genetic analysis of an ethnic Chinese kindred with early-onset parkinsonism and parkin gene mutations. Mov Disord 17(4):670–675

    Article  PubMed  Google Scholar 

  • Xu ZC, Ling G, Sahr RN, Neal-Beliveau BS (2005) Asymmetrical changes of dopamine receptors in the striatum after unilateral dopamine depletion. Brain Res 1038(2):163–170

    Article  PubMed  CAS  Google Scholar 

  • Xu X, Wang Q, Zhang M (2008) Age, gender, and hemispheric differences in iron deposition in the human brain: an in vivo MRI study. Neuroimage. 40(1):35–42

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P. Riederer.

Additional information

P. Riederer and J. Sian-Hülsmann contributed equally to the text of this manuscript.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Riederer, P., Sian-Hülsmann, J. The significance of neuronal lateralisation in Parkinson’s disease. J Neural Transm 119, 953–962 (2012). https://doi.org/10.1007/s00702-012-0775-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-012-0775-1

Keywords

Navigation