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Published in: Journal of Neurology 12/2019

01-12-2019 | Smelling Disorder | Original Communication

Specific intranasal and central trigeminal electrophysiological responses in Parkinson’s disease

Authors: Cécilia Tremblay, Rosa Emrich, Annachiara Cavazzana, Lisa Klingelhoefer, Moritz D. Brandt, Thomas Hummel, Antje Haehner, Johannes Frasnelli

Published in: Journal of Neurology | Issue 12/2019

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Abstract

Olfactory dysfunction is a frequent early non-motor symptom of Parkinson’s disease (PD). There is evidence that with regard to trigeminal perception, PD-related olfactory dysfunction is different from other olfactory disorders. More specifically, trigeminal sensitivity, when measured behaviorally, was unimpaired in PD patients as opposed to patients with non-Parkinsonian olfactory dysfunction (NPOD). We sought to investigate the trigeminal pathway by measuring electrophysiological recordings from the nasal epithelium and EEG-derived event-related potentials in response to a specific trigeminal stimulus in 21 PD patients and compare them to 23 patients with NPOD and 25 controls (C). The peripheral trigeminal response, as measured by the negative-mucosa potential, showed no difference between patients with PD and controls whereas PD patients showed faster responses than patients with NPOD, the latter having shown slower and larger responses than controls (18 PD, 14 NPOD, 20 C). The central trigeminal response, as measured by event-related potentials, revealed larger early component response in PD patients compared to patients with NPOD (15 PD, 21 NPOD, 23 C). As expected, psychophysical olfactory testing showed impaired olfactory function in both groups of patients as opposed to controls. Discriminant analysis revealed a model that could predict group membership for 80% of participants based on the negative-mucosa potential latency, olfactory threshold and discrimination tests. These results provide novel insights into the pattern of trigeminal activation in PD which will help to differentiate PD-related olfactory loss from NPOD, a crucial step towards establishing early screening batteries for PD including smell tests.
Literature
3.
go back to reference Laska M, Distel H, Hudson R (1997) Trigeminal perception of odorant quality in congenitally anosmic subjects. Chem Senses 22(4):447–456CrossRefPubMed Laska M, Distel H, Hudson R (1997) Trigeminal perception of odorant quality in congenitally anosmic subjects. Chem Senses 22(4):447–456CrossRefPubMed
4.
go back to reference Doty RL, Brugger WE, Jurs PC, Orndorff MA, Snyder PJ, Lowry LD (1978) Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol Behav 20(2):175–185CrossRefPubMed Doty RL, Brugger WE, Jurs PC, Orndorff MA, Snyder PJ, Lowry LD (1978) Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol Behav 20(2):175–185CrossRefPubMed
5.
go back to reference Cain WS, Murphy CL (1980) Interaction between chemoreceptive modalities of odour and irritation. Nature 284(5753):255–257CrossRefPubMed Cain WS, Murphy CL (1980) Interaction between chemoreceptive modalities of odour and irritation. Nature 284(5753):255–257CrossRefPubMed
7.
go back to reference Hummel T, Futschik T, Frasnelli J, Huttenbrink KB (2003) Effects of olfactory function, age, and gender on trigeminally mediated sensations: a study based on the lateralization of chemosensory stimuli. Toxicol Lett 140–141:273–280CrossRefPubMed Hummel T, Futschik T, Frasnelli J, Huttenbrink KB (2003) Effects of olfactory function, age, and gender on trigeminally mediated sensations: a study based on the lateralization of chemosensory stimuli. Toxicol Lett 140–141:273–280CrossRefPubMed
10.
go back to reference Rombaux P, Mouraux A, Keller T, Hummel T (2008) Trigeminal event-related potentials in patients with olfactory dysfunction. Rhinology 46(3):170–174PubMed Rombaux P, Mouraux A, Keller T, Hummel T (2008) Trigeminal event-related potentials in patients with olfactory dysfunction. Rhinology 46(3):170–174PubMed
14.
go back to reference Hummel T, Barz S, Lotsch J, Roscher S, Kettenmann B, Kobal G (1996) Loss of olfactory function leads to a decrease of trigeminal sensitivity. Chem Senses 21(1):75–79CrossRefPubMed Hummel T, Barz S, Lotsch J, Roscher S, Kettenmann B, Kobal G (1996) Loss of olfactory function leads to a decrease of trigeminal sensitivity. Chem Senses 21(1):75–79CrossRefPubMed
15.
go back to reference Kobal G (1985) Pain-related electrical potentials of the human nasal mucosa elicited by chemical stimulation. Pain 22(2):151–163CrossRefPubMed Kobal G (1985) Pain-related electrical potentials of the human nasal mucosa elicited by chemical stimulation. Pain 22(2):151–163CrossRefPubMed
18.
go back to reference 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
21.
go back to reference Litvan I, Bhatia KP, Burn DJ, Goetz CG, Lang AE, McKeith I, Quinn N, Sethi KD, Shults C, Wenning GK (2003) Movement disorders society scientific issues committee report: SIC task force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Mov Disord 18(5):467–486. https://doi.org/10.1002/mds.10459 CrossRefPubMed Litvan I, Bhatia KP, Burn DJ, Goetz CG, Lang AE, McKeith I, Quinn N, Sethi KD, Shults C, Wenning GK (2003) Movement disorders society scientific issues committee report: SIC task force appraisal of clinical diagnostic criteria for Parkinsonian disorders. Mov Disord 18(5):467–486. https://​doi.​org/​10.​1002/​mds.​10459 CrossRefPubMed
25.
go back to reference Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571CrossRefPubMed Beck AT, Ward CH, Mendelson M, Mock J, Erbaugh J (1961) An inventory for measuring depression. Arch Gen Psychiatry 4:561–571CrossRefPubMed
26.
go back to reference Thurauf N, Gunther M, Pauli E, Kobal G (2002) Sensitivity of the negative mucosal potential to the trigeminal target stimulus CO(2). Brain Res 942(1–2):79–86CrossRefPubMed Thurauf N, Gunther M, Pauli E, Kobal G (2002) Sensitivity of the negative mucosal potential to the trigeminal target stimulus CO(2). Brain Res 942(1–2):79–86CrossRefPubMed
27.
go back to reference Ottoson D (1955) Analysis of the electrical activity of the olfactory epithelium. Acta Physiol Scand Suppl 35(122):1–83PubMed Ottoson D (1955) Analysis of the electrical activity of the olfactory epithelium. Acta Physiol Scand Suppl 35(122):1–83PubMed
29.
go back to reference Kobal G, Hummel C, Nuernberg B, Brune K (1990) Effects of pentazocine and acetylsalicylic acid on pain-rating, pain-related evoked potentials and vigilance in relationship to pharmacokinetic parameters. Agents Actions 29(3–4):342–359CrossRefPubMed Kobal G, Hummel C, Nuernberg B, Brune K (1990) Effects of pentazocine and acetylsalicylic acid on pain-rating, pain-related evoked potentials and vigilance in relationship to pharmacokinetic parameters. Agents Actions 29(3–4):342–359CrossRefPubMed
30.
go back to reference Kobal G (1981) Elektrophysiologische untersuchungen des menschlichen geruchssinns. Thieme, Stuttgart Kobal G (1981) Elektrophysiologische untersuchungen des menschlichen geruchssinns. Thieme, Stuttgart
31.
33.
36.
go back to reference Yamagishi M, Fujiwara M, Nakamura H (1994) Olfactory mucosal findings and clinical course in patients with olfactory disorders following upper respiratory viral infection. Rhinology 32(3):113–118PubMed Yamagishi M, Fujiwara M, Nakamura H (1994) Olfactory mucosal findings and clinical course in patients with olfactory disorders following upper respiratory viral infection. Rhinology 32(3):113–118PubMed
37.
39.
go back to reference Pause BM, Krauel K (2000) Chemosensory event-related potentials (CSERP) as a key to the psychology of odors. Int J Psychophysiol 36(2):105–122CrossRefPubMed Pause BM, Krauel K (2000) Chemosensory event-related potentials (CSERP) as a key to the psychology of odors. Int J Psychophysiol 36(2):105–122CrossRefPubMed
44.
go back to reference Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24(2):197–211CrossRefPubMed Braak H, Del Tredici K, Rub U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24(2):197–211CrossRefPubMed
46.
go back to reference Joshi N, Rolheiser TM, Fisk JD, McKelvey JR, Schoffer K, Phillips G, Armstrong M, Khan MN, Leslie RA, Rusak B, Robertson HA, Good KP (2017) Lateralized microstructural changes in early-stage Parkinson’s disease in anterior olfactory structures, but not in substantia nigra. J Neurol 264(7):1497–1505. https://doi.org/10.1007/s00415-017-8555-3 CrossRefPubMed Joshi N, Rolheiser TM, Fisk JD, McKelvey JR, Schoffer K, Phillips G, Armstrong M, Khan MN, Leslie RA, Rusak B, Robertson HA, Good KP (2017) Lateralized microstructural changes in early-stage Parkinson’s disease in anterior olfactory structures, but not in substantia nigra. J Neurol 264(7):1497–1505. https://​doi.​org/​10.​1007/​s00415-017-8555-3 CrossRefPubMed
Metadata
Title
Specific intranasal and central trigeminal electrophysiological responses in Parkinson’s disease
Authors
Cécilia Tremblay
Rosa Emrich
Annachiara Cavazzana
Lisa Klingelhoefer
Moritz D. Brandt
Thomas Hummel
Antje Haehner
Johannes Frasnelli
Publication date
01-12-2019
Publisher
Springer Berlin Heidelberg
Published in
Journal of Neurology / Issue 12/2019
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI
https://doi.org/10.1007/s00415-019-09517-4

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