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Erschienen in: Journal of Neurology 6/2017

26.05.2017 | Original Communication

Olfactory impairment in Parkinson’s disease is a consequence of central nervous system decline

verfasst von: Emilia Iannilli, Lars Stephan, Thomas Hummel, Heinz Reichmann, Antje Haehner

Erschienen in: Journal of Neurology | Ausgabe 6/2017

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Abstract

Early diagnosis and timely treatment of Parkinson’s disease are essential factors to provide these patients with a longer period of a better quality of life. Olfactory loss is among the first non-motor symptoms of the disease; however, in light of the many causes of smell loss, it is a very unspecific biomarker and should only be used as part of a diagnostic test battery. In this study, we investigated the olfactory response in 71 subjects, consisting of Parkinson’s disease patients, hyposmic and anosmic patients of other causes, and normosmic individuals searching for sensitive, distinct biomarkers for which we used scalp event-related 64-channel electroencephalography and psychophysical tests. The analysis of the global field power indicated significant measurable differences between patients with Parkinson’s disease and otherwise olfactory dysfunctional and normosmic individuals. The localization of brain sources, in particular, provides evidence for differences in mainly late EEG-components suggesting a decline of central brain networks as a causal factor for olfactory loss in Parkinson’s disease. The findings indicate a different pattern of olfactory processing in patients with Parkinson’s disease compared to olfactory dysfunctions of other origin, which provide further insights into the mechanisms behind olfactory dysfunction in Parkinson’s.
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Literatur
1.
Zurück zum Zitat 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(4):415–455CrossRefPubMed 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(4):415–455CrossRefPubMed
2.
Zurück zum Zitat Berg D, Postuma RB, Adler CH et al (2015) MDS research criteria for prodromal Parkinson’s disease. Mov Disord 30(12):1600–1611CrossRefPubMed Berg D, Postuma RB, Adler CH et al (2015) MDS research criteria for prodromal Parkinson’s disease. Mov Disord 30(12):1600–1611CrossRefPubMed
3.
Zurück zum Zitat Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318(1):121–134CrossRefPubMed Braak H, Ghebremedhin E, Rüb U, Bratzke H, Del Tredici K (2004) Stages in the development of Parkinson’s disease-related pathology. Cell Tissue Res 318(1):121–134CrossRefPubMed
4.
Zurück zum Zitat Del Tredici K, Rub U, De Vos RA, Bohl JR, Braak H (2002) Where does parkinson disease pathology begin in the brain? J Neuropathol Exp Neurol 61(5):413–426CrossRefPubMed Del Tredici K, Rub U, De Vos RA, Bohl JR, Braak H (2002) Where does parkinson disease pathology begin in the brain? J Neuropathol Exp Neurol 61(5):413–426CrossRefPubMed
5.
Zurück zum Zitat Haehner A, Boesveldt S, Berendse HW et al (2009) Prevalence of smell loss in Parkinson’s disease—a multicenter study. Parkinsonism Relat Disord 15(7):490–494CrossRefPubMed Haehner A, Boesveldt S, Berendse HW et al (2009) Prevalence of smell loss in Parkinson’s disease—a multicenter study. Parkinsonism Relat Disord 15(7):490–494CrossRefPubMed
6.
Zurück zum Zitat Doty RL, Shaman P, Dann M (1984) Development of the University of Pennsylvania smell identification test: a standardized microencapsulated test of olfactory function. Physiol Behav 32(3):489–502CrossRefPubMed Doty RL, Shaman P, Dann M (1984) Development of the University of Pennsylvania smell identification test: a standardized microencapsulated test of olfactory function. Physiol Behav 32(3):489–502CrossRefPubMed
7.
Zurück zum Zitat Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22(1):39–52CrossRefPubMed Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) ‘Sniffin’ sticks’: olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chem Senses 22(1):39–52CrossRefPubMed
8.
Zurück zum Zitat Mueller A, Reichman H, Livermore A, Hummel T (2002) Olfactory function in idiopathic Parkinson’s disease: results from cross-sectional studies in IPD patients and long-term follow-up of de-novo IPD patients. J Neural Transm 109:805–811CrossRef Mueller A, Reichman H, Livermore A, Hummel T (2002) Olfactory function in idiopathic Parkinson’s disease: results from cross-sectional studies in IPD patients and long-term follow-up of de-novo IPD patients. J Neural Transm 109:805–811CrossRef
9.
Zurück zum Zitat Wenning GK, Shephard B, Hawkes C, Petruckevitch A, Lees A, Quinn N (1995) Olfactory function in atypical parkinsonian syndromes. Acta Neurol Scand 91(4):247–250CrossRefPubMed Wenning GK, Shephard B, Hawkes C, Petruckevitch A, Lees A, Quinn N (1995) Olfactory function in atypical parkinsonian syndromes. Acta Neurol Scand 91(4):247–250CrossRefPubMed
10.
Zurück zum Zitat Whitcroft KL, Cuevas M, Haehner A, Hummel T (2017) Patterns of olfactory impairment reflect underlying disease etiology. Laryngoscope 127(2):291–295CrossRefPubMed Whitcroft KL, Cuevas M, Haehner A, Hummel T (2017) Patterns of olfactory impairment reflect underlying disease etiology. Laryngoscope 127(2):291–295CrossRefPubMed
11.
Zurück zum Zitat Hummel T, Kobal G (2001) Olfactory event-related potentials. In: Simon SA, Nicolelis MAL (eds) Methods and frontiers in chemosensory research. CRC Press, Boca Raton, pp 129–164 Hummel T, Kobal G (2001) Olfactory event-related potentials. In: Simon SA, Nicolelis MAL (eds) Methods and frontiers in chemosensory research. CRC Press, Boca Raton, pp 129–164
12.
Zurück zum Zitat Harada H, Shiraishi K, Kato T (2003) Olfactory event-related potentials in normal subjects and patients with smell disorders. Clin Electroencephalogr 34(4):191–196CrossRefPubMed Harada H, Shiraishi K, Kato T (2003) Olfactory event-related potentials in normal subjects and patients with smell disorders. Clin Electroencephalogr 34(4):191–196CrossRefPubMed
13.
Zurück zum Zitat Picton TW, Lins OG, Scherg M (1994) Handbook of neurophysiology. Elsevier, Amsterdam Picton TW, Lins OG, Scherg M (1994) Handbook of neurophysiology. Elsevier, Amsterdam
14.
Zurück zum Zitat Picton TW, Hillyard SA, Krausz HI, Galambos R (1974) Human auditory evoked potentials. I. Evaluation of components. Electroencephalogr Clin Neurophysiol 36(2):179–190CrossRefPubMed Picton TW, Hillyard SA, Krausz HI, Galambos R (1974) Human auditory evoked potentials. I. Evaluation of components. Electroencephalogr Clin Neurophysiol 36(2):179–190CrossRefPubMed
15.
Zurück zum Zitat Kobal G, Plattig KH (1978) Objective olfactometry: methodological annotations for recording olfactory EEG-responses from the awake human. EEG EMG Z Elektroenzephalogr Elektromyogr Verwandte Geb 9(3):135–145PubMed Kobal G, Plattig KH (1978) Objective olfactometry: methodological annotations for recording olfactory EEG-responses from the awake human. EEG EMG Z Elektroenzephalogr Elektromyogr Verwandte Geb 9(3):135–145PubMed
16.
Zurück zum Zitat Iannilli E, Beger M, Furer R, Hummel T (2015) A gustatory stimulator. J Neurosci Methods 255:12–16CrossRefPubMed Iannilli E, Beger M, Furer R, Hummel T (2015) A gustatory stimulator. J Neurosci Methods 255:12–16CrossRefPubMed
17.
Zurück zum Zitat Barz S, Hummel T, Pauli E, Majer M, Lang CJ, Kobal G (1997) Chemosensory event-related potentials in response to trigeminal and olfactory stimulation in idiopathic Parkinson’s disease. Neurology 49(5):1424–1431CrossRefPubMed Barz S, Hummel T, Pauli E, Majer M, Lang CJ, Kobal G (1997) Chemosensory event-related potentials in response to trigeminal and olfactory stimulation in idiopathic Parkinson’s disease. Neurology 49(5):1424–1431CrossRefPubMed
18.
19.
Zurück zum Zitat Bocquillon P, Bourriez JL, Palmero-Soler E, Defebvre L, Derambure P, Dujardin K (2015) Impaired early attentional processes in Parkinson’s disease: a high-resolution event-related potentials study. PLoS One 10(7):e0131654CrossRefPubMedPubMedCentral Bocquillon P, Bourriez JL, Palmero-Soler E, Defebvre L, Derambure P, Dujardin K (2015) Impaired early attentional processes in Parkinson’s disease: a high-resolution event-related potentials study. PLoS One 10(7):e0131654CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Solis-Vivanco R, Rodriguez-Violante M, Rodriguez-Agudelo Y, Schilmann A, Rodriguez-Ortiz U, Ricardo-Garcell J (2015) The P3a wave: a reliable neurophysiological measure of Parkinson’s disease duration and severity. Clin Neurophysiol 126(11):2142–2149CrossRefPubMed Solis-Vivanco R, Rodriguez-Violante M, Rodriguez-Agudelo Y, Schilmann A, Rodriguez-Ortiz U, Ricardo-Garcell J (2015) The P3a wave: a reliable neurophysiological measure of Parkinson’s disease duration and severity. Clin Neurophysiol 126(11):2142–2149CrossRefPubMed
21.
Zurück zum Zitat Martinez-Horta S, Riba J, de Bobadilla RF et al (2014) Apathy in Parkinson’s disease: neurophysiological evidence of impaired incentive processing. J Neurosci 34(17):5918–5926CrossRefPubMed Martinez-Horta S, Riba J, de Bobadilla RF et al (2014) Apathy in Parkinson’s disease: neurophysiological evidence of impaired incentive processing. J Neurosci 34(17):5918–5926CrossRefPubMed
22.
Zurück zum Zitat Mensen A, Poryazova R, Schwartz S, Khatami R (2014) Humor as a reward mechanism: event-related potentials in the healthy and diseased brain. PLoS One 9(1):e85978CrossRefPubMedPubMedCentral Mensen A, Poryazova R, Schwartz S, Khatami R (2014) Humor as a reward mechanism: event-related potentials in the healthy and diseased brain. PLoS One 9(1):e85978CrossRefPubMedPubMedCentral
23.
Zurück zum Zitat Dietz J, Bradley MM, Jones J, Okun MS, Perlstein WM, Bowers D (2013) The late positive potential, emotion and apathy in Parkinson’s disease. Neuropsychologia 51(5):960–966CrossRefPubMedPubMedCentral Dietz J, Bradley MM, Jones J, Okun MS, Perlstein WM, Bowers D (2013) The late positive potential, emotion and apathy in Parkinson’s disease. Neuropsychologia 51(5):960–966CrossRefPubMedPubMedCentral
24.
Zurück zum Zitat Desmedt JE, Tomberg C, Noël P, Ozaki I (1990) Beware of the average reference in brain mapping. Electroencephalogr Clin Neurophysiol Suppl 41:22–27PubMed Desmedt JE, Tomberg C, Noël P, Ozaki I (1990) Beware of the average reference in brain mapping. Electroencephalogr Clin Neurophysiol Suppl 41:22–27PubMed
25.
Zurück zum Zitat Lehmann D, Skrandies W (1980) Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48(6):609–621CrossRefPubMed Lehmann D, Skrandies W (1980) Reference-free identification of components of checkerboard-evoked multichannel potential fields. Electroencephalogr Clin Neurophysiol 48(6):609–621CrossRefPubMed
26.
Zurück zum Zitat Pascual-Marqui RD, Lehmann D (1993) Comparison of topographic maps and the reference electrode: comments on two papers by Desmedt and collaborators. Electroencephalogr Clin Neurophysiol 88(530–531):534–536 Pascual-Marqui RD, Lehmann D (1993) Comparison of topographic maps and the reference electrode: comments on two papers by Desmedt and collaborators. Electroencephalogr Clin Neurophysiol 88(530–531):534–536
27.
Zurück zum Zitat Litvan I, Bhatia KP, Burn DJ et al (2003) Movement Disorders Society Scientific Issues Committee report: SIC task force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Mov Disord 18(5):467–486CrossRefPubMed Litvan I, Bhatia KP, Burn DJ et al (2003) Movement Disorders Society Scientific Issues Committee report: SIC task force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Mov Disord 18(5):467–486CrossRefPubMed
28.
Zurück zum Zitat Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198CrossRefPubMed Folstein MF, Folstein SE, McHugh PR (1975) “Mini-mental state”. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198CrossRefPubMed
29.
Zurück zum Zitat Kobal G, Klimek L, Wolfensberger M et al (2000) Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol 257(4):205–211CrossRefPubMed Kobal G, Klimek L, Wolfensberger M et al (2000) Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol 257(4):205–211CrossRefPubMed
31.
Zurück zum Zitat Halliday AM, Halliday E, Kriss A, McDonald WI, Mushin J (1976) The pattern-evoked potential in compression of the anterior visual pathways. Brain 99(2):357–374CrossRefPubMed Halliday AM, Halliday E, Kriss A, McDonald WI, Mushin J (1976) The pattern-evoked potential in compression of the anterior visual pathways. Brain 99(2):357–374CrossRefPubMed
32.
Zurück zum Zitat Bodis-Wollner I, Yahr MD (1978) Measurements of visual evoked potentials in Parkinson’s disease. Brain 101(4):661–671CrossRefPubMed Bodis-Wollner I, Yahr MD (1978) Measurements of visual evoked potentials in Parkinson’s disease. Brain 101(4):661–671CrossRefPubMed
33.
Zurück zum Zitat Bodis-Wollner I, Yahr MD, Mylin L, Thornton J (1982) Dopaminergic deficiency and delayed visual evoked potentials in humans. Ann Neurol 11(5):478–483CrossRefPubMed Bodis-Wollner I, Yahr MD, Mylin L, Thornton J (1982) Dopaminergic deficiency and delayed visual evoked potentials in humans. Ann Neurol 11(5):478–483CrossRefPubMed
34.
Zurück zum Zitat Peppe A, Stanzione P, Pierelli F, De Angelis D, Pierantozzi M, Bernardi G (1995) Visual alterations in de novo Parkinson’s disease: pattern electroretinogram latencies are more delayed and more reversible by levodopa than are visual evoked potentials. Neurology 45(6):1144–1148CrossRefPubMed Peppe A, Stanzione P, Pierelli F, De Angelis D, Pierantozzi M, Bernardi G (1995) Visual alterations in de novo Parkinson’s disease: pattern electroretinogram latencies are more delayed and more reversible by levodopa than are visual evoked potentials. Neurology 45(6):1144–1148CrossRefPubMed
35.
Zurück zum Zitat Grave de Peralta Menendez R, Gonzalez Andino S, Lantz G, Michel CM, Landis T (2001) Noninvasive localization of electromagnetic epileptic activity. I. Method descriptions and simulations. Brain Topogr 14(2):131–137CrossRefPubMed Grave de Peralta Menendez R, Gonzalez Andino S, Lantz G, Michel CM, Landis T (2001) Noninvasive localization of electromagnetic epileptic activity. I. Method descriptions and simulations. Brain Topogr 14(2):131–137CrossRefPubMed
36.
Zurück zum Zitat Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R (2004) EEG source imaging. Clin Neurophysiol 115(10):2195–2222CrossRefPubMed Michel CM, Murray MM, Lantz G, Gonzalez S, Spinelli L, Grave de Peralta R (2004) EEG source imaging. Clin Neurophysiol 115(10):2195–2222CrossRefPubMed
37.
Zurück zum Zitat Pause BM, Sojka B, Krauel K, Ferstl R (1996) The nature of the late positive complex within the olfactory event-related potential (OERP). Psychophysiology 33(4):376–384CrossRefPubMed Pause BM, Sojka B, Krauel K, Ferstl R (1996) The nature of the late positive complex within the olfactory event-related potential (OERP). Psychophysiology 33(4):376–384CrossRefPubMed
38.
Zurück zum Zitat Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Ann N Y Acad Sci 935:107–117CrossRefPubMed Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Ann N Y Acad Sci 935:107–117CrossRefPubMed
39.
Zurück zum Zitat Rosenberg-Katz K, Maidan I, Jacob Y, Giladi N, Mirelman A, Hausdorff JM (2016) Alterations in conflict monitoring are related to functional connectivity in Parkinson’s disease. Cortex 82:277–286CrossRefPubMed Rosenberg-Katz K, Maidan I, Jacob Y, Giladi N, Mirelman A, Hausdorff JM (2016) Alterations in conflict monitoring are related to functional connectivity in Parkinson’s disease. Cortex 82:277–286CrossRefPubMed
40.
Zurück zum Zitat Gaspar P, Berger B, Febvret A, Vigny A, Henry JP (1989) Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-beta-hydroxylase. J Comp Neurol 279(2):249–271CrossRefPubMed Gaspar P, Berger B, Febvret A, Vigny A, Henry JP (1989) Catecholamine innervation of the human cerebral cortex as revealed by comparative immunohistochemistry of tyrosine hydroxylase and dopamine-beta-hydroxylase. J Comp Neurol 279(2):249–271CrossRefPubMed
41.
Zurück zum Zitat Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280(5364):747–749CrossRefPubMed Carter CS, Braver TS, Barch DM, Botvinick MM, Noll D, Cohen JD (1998) Anterior cingulate cortex, error detection, and the online monitoring of performance. Science 280(5364):747–749CrossRefPubMed
42.
Zurück zum Zitat Kuenig G, Leenders KL, Martin C, Magyar S, Schultz W (1999) Reward processing in Parkinsons disease A PET activation study. Neurology 52(2 suppl 2):A349 Kuenig G, Leenders KL, Martin C, Magyar S, Schultz W (1999) Reward processing in Parkinsons disease A PET activation study. Neurology 52(2 suppl 2):A349
43.
Zurück zum Zitat Torack RM, Morris JC (1988) The association of ventral tegmental area histopathology with adult dementia. Arch Neurol 45(5):497–501CrossRefPubMed Torack RM, Morris JC (1988) The association of ventral tegmental area histopathology with adult dementia. Arch Neurol 45(5):497–501CrossRefPubMed
44.
Zurück zum Zitat German DC, Manaye K, Smith WK, Woodward DJ, Saper CB (1989) Midbrain dopaminergic cell loss in Parkinson’s disease: computer visualization. Ann Neurol 26(4):507–514CrossRefPubMed German DC, Manaye K, Smith WK, Woodward DJ, Saper CB (1989) Midbrain dopaminergic cell loss in Parkinson’s disease: computer visualization. Ann Neurol 26(4):507–514CrossRefPubMed
45.
Zurück zum Zitat Rinne JO, Rummukainen J, Paljarvi L, Rinne UK (1989) Dementia in Parkinson’s disease is related to neuronal loss in the medial substantia nigra. Ann Neurol 26(1):47–50CrossRefPubMed Rinne JO, Rummukainen J, Paljarvi L, Rinne UK (1989) Dementia in Parkinson’s disease is related to neuronal loss in the medial substantia nigra. Ann Neurol 26(1):47–50CrossRefPubMed
46.
Zurück zum Zitat Grossman M, Crino P, Reivich M, Stern MB, Hurtig HI (1992) Attention and sentence processing deficits in Parkinson’s disease: the role of anterior cingulate cortex. Cereb Cortex 2(6):513–525CrossRefPubMed Grossman M, Crino P, Reivich M, Stern MB, Hurtig HI (1992) Attention and sentence processing deficits in Parkinson’s disease: the role of anterior cingulate cortex. Cereb Cortex 2(6):513–525CrossRefPubMed
47.
Zurück zum Zitat Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33(3):161–253CrossRefPubMed Witter MP, Groenewegen HJ, Lopes da Silva FH, Lohman AH (1989) Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog Neurobiol 33(3):161–253CrossRefPubMed
48.
Zurück zum Zitat Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL (1984) Alzheimer’s disease: cell-specific pathology isolates the hippocampal formation. Science 225(4667):1168–1170CrossRefPubMed Hyman BT, Van Hoesen GW, Damasio AR, Barnes CL (1984) Alzheimer’s disease: cell-specific pathology isolates the hippocampal formation. Science 225(4667):1168–1170CrossRefPubMed
49.
Zurück zum Zitat Summerfield C, Junque C, Tolosa E et al (2005) Structural brain changes in Parkinson disease with dementia: a voxel-based morphometry study. Arch Neurol 62(2):281–285CrossRefPubMed Summerfield C, Junque C, Tolosa E et al (2005) Structural brain changes in Parkinson disease with dementia: a voxel-based morphometry study. Arch Neurol 62(2):281–285CrossRefPubMed
50.
Zurück zum Zitat Camicioli R, Moore MM, Kinney A, Corbridge E, Glassberg K, Kaye JA (2003) Parkinson’s disease is associated with hippocampal atrophy. Mov Disord 18(7):784–790CrossRefPubMed Camicioli R, Moore MM, Kinney A, Corbridge E, Glassberg K, Kaye JA (2003) Parkinson’s disease is associated with hippocampal atrophy. Mov Disord 18(7):784–790CrossRefPubMed
51.
Zurück zum Zitat Xu Y, Yang J, Hu X, Shang H (2016) Voxel-based meta-analysis of gray matter volume reductions associated with cognitive impairment in Parkinson’s disease. J Neurol 263(6):1178–1187CrossRefPubMed Xu Y, Yang J, Hu X, Shang H (2016) Voxel-based meta-analysis of gray matter volume reductions associated with cognitive impairment in Parkinson’s disease. J Neurol 263(6):1178–1187CrossRefPubMed
52.
Zurück zum Zitat Jahanshahi M, Jones CR, Zijlmans J et al (2010) Dopaminergic modulation of striato-frontal connectivity during motor timing in Parkinson’s disease. Brain 133(Pt 3):727–745CrossRefPubMed Jahanshahi M, Jones CR, Zijlmans J et al (2010) Dopaminergic modulation of striato-frontal connectivity during motor timing in Parkinson’s disease. Brain 133(Pt 3):727–745CrossRefPubMed
53.
Zurück zum Zitat Farrer C, Frey SH, Van Horn JD et al (2008) The angular gyrus computes action awareness representations. Cereb Cortex 18(2):254–261CrossRefPubMed Farrer C, Frey SH, Van Horn JD et al (2008) The angular gyrus computes action awareness representations. Cereb Cortex 18(2):254–261CrossRefPubMed
55.
Zurück zum Zitat Seibyl JP, Marek KL, Quinlan D et al (1995) Decreased single-photon emission computed tomographic [123I]beta-CIT striatal uptake correlates with symptom severity in Parkinson’s disease. Ann Neurol 38(4):589–598CrossRefPubMed Seibyl JP, Marek KL, Quinlan D et al (1995) Decreased single-photon emission computed tomographic [123I]beta-CIT striatal uptake correlates with symptom severity in Parkinson’s disease. Ann Neurol 38(4):589–598CrossRefPubMed
56.
Zurück zum Zitat Gruzelier JH (1999) Functional neuropsychophysiological asymmetry in schizophrenia: a review and reorientation. Schizophr Bull 25(1):91–120CrossRefPubMed Gruzelier JH (1999) Functional neuropsychophysiological asymmetry in schizophrenia: a review and reorientation. Schizophr Bull 25(1):91–120CrossRefPubMed
57.
Zurück zum Zitat Innis RB, Seibyl JP, Scanley BE et al (1993) Single photon emission computed tomographic imaging demonstrates loss of striatal dopamine transporters in Parkinson disease. Proc Natl Acad Sci USA 90(24):11965–11969CrossRefPubMedPubMedCentral Innis RB, Seibyl JP, Scanley BE et al (1993) Single photon emission computed tomographic imaging demonstrates loss of striatal dopamine transporters in Parkinson disease. Proc Natl Acad Sci USA 90(24):11965–11969CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Marek KL, Seibyl JP, Zoghbi SS et al (1996) [123I] beta-CIT/SPECT imaging demonstrates bilateral loss of dopamine transporters in hemi-Parkinson’s disease. Neurology 46(1):231–237CrossRefPubMed Marek KL, Seibyl JP, Zoghbi SS et al (1996) [123I] beta-CIT/SPECT imaging demonstrates bilateral loss of dopamine transporters in hemi-Parkinson’s disease. Neurology 46(1):231–237CrossRefPubMed
Metadaten
Titel
Olfactory impairment in Parkinson’s disease is a consequence of central nervous system decline
verfasst von
Emilia Iannilli
Lars Stephan
Thomas Hummel
Heinz Reichmann
Antje Haehner
Publikationsdatum
26.05.2017
Verlag
Springer Berlin Heidelberg
Erschienen in
Journal of Neurology / Ausgabe 6/2017
Print ISSN: 0340-5354
Elektronische ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-017-8521-0

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