Evoked potential response in patients with idiopathic Parkinson’s disease and atypical parkinsonian syndromes: A comparative study
Patients with idiopathic Parkinson’s disease (IPD) and atypical parkinsonian syndromes (APSs) suffer from a range of disorders, especially in balance and locomotion, which necessitate visual, auditory, and somatosensory inputs. In this study, IPD patients, APS patients, and healthy controls (HCs) (n = 50 per group) underwent a series of assessments for visual evoked potentials (VEP), brainstem auditory evoked response (BAER), and short-latency somatosensory evoked potentials (SSEP). Results showed that VEP P100 latency was prolonged in multiple system atrophy-cerebellar type (MSA-C), multiple system atrophy-parkinsonian type (MSA-P), and corticobasal ganglionic degeneration (CBD) patients. The latency of peaks III and V was prolonged in IPD, MSA-C, dementia with Lewy bodies (DLB), and Parkinson’s disease dementia (PDD). BAER I-III and I-V interpeak latency were prolonged in IPD, DLB, and PDD, whereas BAER I-III, III-V, and I-V interpeak latencies were increased and the V/I amplitude ratio was decreased in MSA-C. The central sensory conduction time (N20-N13) was increased in MSA-P and MSA-C in SSEP. IPD patients had prolonged VEP P100 latency (P < 0.001), lower VEP N75-P100 amplitude (P < 0.001), prolonged BAER I, II, II, IV, V peak latencies (P < 0.001), I-III, I-V interpeak latencies (P < 0.001), lower BAER V/I amplitude ratio (P < 0.001), and prolonged SSEP N13, N20, central sensory conduction time (N20-N13) (P < 0.001) than HCs. IPD patients also had prolonged BAER I, II, II, IV, V peak latencies (P < 0.001), prolonged I-III, I-V interpeak latencies (P < 0.001), and shorter SSEP N13, N20, central sensory conduction time (N20-N13) (P < 0.001) than APS patients. Moreover, APS patients had prolonged VEP P100 and N145 latencies (P < 0.001) and decreased N75-N145 amplitude (P < 0.001) compared to HCs. APS patients also had prolonged BAER II, II, IV, V peak latencies (P < 0.001), prolonged I-III, III-V, I-V interpeak latencies (P < 0.001), decreased V/I amplitude ratio, and prolonged SSEP N13, N20, central sensory conduction time (N20-N13) (P < 0.001) than HCs. Postural instability and gait disorder (PIGD) IPD had significantly prolonged BAER III, V peak latencies (P < 0.05), and prolonged III-V interpeak latencies (P < 0.05) compared to tremor-dominant IPD. Overall, the IPD and APS patients had significant VEP, BAER, and SSEP abnormalities of demyelination and axonal variety in the visual, auditory, and somatosensory pathways. The changes were also correlated with the disease duration and severity. Although the diseases are predominantly motor disorders with significant non-motor components, these electrophysiological abnormalities might open a new avenue to assess the non-motor symptoms.
- Jankovic J, Mcdermott M, Carter J, et al., 1990, Variable expression of Parkinson’s disease: A base-line analysis of the DATATOP cohort, The Parkinson study group, Neurology, 40: 1529–1534. https://doi.org/10.1212/wnl.40.10.1529
- Marsden CD, 1990, Parkinson’s disease, Lancet, 335: 948–952. https://doi.org/10.1016/0140-6736(90)91006-v
- Jankovic J, 1989, Parkinsonism plus syndromes, Mov Disord, 4: 95119. https://doi.org/10.1002/mds.870040512
- Gawel MJ, Das P, Vincent S, et al., 19881, Visual and auditory evoked responses in patients with Parkinson’s disease, J Neurol Neurosurg Psychiatry 44: 227–232. https://doi.org/10.1136/jnnp.44.3.227
- Gelb DJ, Oliver E, Gilman S, 1999, Diagnostic criteria for Parkinson’s disease, Arch Neurol, 56: 33–39. https://doi.org/10.1001/archneur.56.1.33
- Williams DR, Lees AJ, 2009, Progressive supranuclear palsy: Clinicopathological concepts and diagnostic challenges, Lancet Neurol, 8: 270–279. https://doi.org/10.1016/S1474-4422(09)70042-0
- Gilman S, Wenning GK, Low PA, et al., 2008, Second consensus statement on the diagnosis of multiple system atrophy, Neurology, 71: 670–676. https://doi.org/10.1212/01.wnl.0000324625.00404.15
- Kertesz A, Blair M, McMonagle P, et al., 2007, The diagnosis and course of frontotemporal dementia, Alzheimer Dis Assoc Disord, 21: 155–163. https://doi.org/10.1097/WAD.0b013e31806547eb
- McKeith IG, Galasko D, Kosaka K, et al., 1996, Consensus guidelines for the clinical and pathologic diagnosis of dementia with Lewy bodies (DLB): Report of the consortium on DLB international workshop, Neurology, 47: 1113–1124. https://doi.org/10.1212/wnl.47.5.1113
- Liu C, Zhang Y, Tang W, et al., 2017, Evoked potential changes in patients with Parkinson’s disease, Brain Behav, 7: e00703. https://doi.org/10.1002/brb3.703
- Inzelberg R, Ramirez JA, Nisipeanu P, et al., 2004, Retinal nerve fiber layer thinning in Parkinson disease, Vision Res, 44: 279. https://doi.org/10.1016/j.visres.2004.06.009
- Savy C, Simon A, Nguyenlegros J, 1991, Spatial geometry of the dopamine innervation in the avascular area of the human fovea, Visual Neurosci, 7: 487–498. https://doi.org/10.1017/S0952523800009779
- Harnois C, Di PT, 1990, Decreased dopamine in the retinas of patients with Parkinson’s disease, Invest Ophthalmol Visual Sci, 31: 2473–2475.
- Miri S, Glazman S, Mylin L, et al., 2016, A combination of retinal morphology and visual electrophysiology testing increases diagnostic yield in Parkinson’s disease, Parkinsonism Relat Disord, 1:134–137. https://doi.org/10.1016/j.parkreldis.2015.09.015
- Mart´ıneznavarrete GC, Mart´ınnieto J, Esteverudd J, et al., 2007, Alpha synuclein gene expression profile in the retina of vertebrates, Mol Vis, 13: 949–961.
- Ma X, Li S, Zheng B, et al., 2023, Retinal structure abnormalities in Parkinson’s disease and atypical parkinsonism, Biomolecules, 13: 218. https://doi.org/10.3390/biom13020218
- Ortuño-Lizarán I, Sánchez-Sáez X, Lax P, et al., 2020, Dopaminergic retinal cell loss and visual dysfunction in Parkinson’s disease, Ann Neurol, 88: 893–906. https://doi.org/10.1002/ana.25897
- Ahn J, Lee JY, Kim TW, et al., 2018, Retinal thinning associates with nigral dopaminergic loss in de novo Parkinson’s disease, Neurology, 91: e1003–12. https://doi.org/10.1212/WNL.0000000000006157
- Murueta-Goyena A, Del Pino R, Galdós M, et al., 2021, Retinal thickness predicts the risk of cognitive decline in Parkinson’s disease, Ann Neurol, 89: 165–176. https://doi.org/10.1002/ana.25944
- Zhou Y, Zhao J, Hou Y, et al., 2019, Dopaminergic pathway and primary visual cortex are involved in the freezing of gait in Parkinson’s disease: A PET-CT study, Neuropsychiatr Dis Treat, 15: 1905–1914. https://doi.org/10.2147/NDT.S197879
- Kawabata K, Ohdake R, Watanabe H, et al., 2020, Visuoperceptual disturbances in Parkinson’s disease, Clin Park Relat Disord, 3: 100036. https://doi.org/10.1016/j.prdoa.2020.100036
- Weil RS, Schrag AE, Warren JD, et al., 2016, Visual dysfunction in Parkinson’s disease, Brain, 139: 2827–2843. https://doi.org/10.1093/brain/aww175
- Abele M, Schulz JB, Bu¨rk K, et al., 2000, Evoked potentials in multiple system atrophy (MSA), Acta Neurol Scand, 101: 111–115. https://doi.org/10.1034/j.1600-0404.2000.101002111.x
- Gibb WR, Luthert PJ, Marsden CD, 1989, Corticobasal degeneration, Brain, 112: 1171–1192. https://doi.org/10.1093/brain/awq173
- Bak TH, Caine D, Hearn VC, et al., 2006, Visuospatial functions in atypical Parkinsonian syndromes, J Neurol Neurosurg Psychiatry, 77: 454–456. https://doi.org/10.1136/jnnp.2005.068239
- Hassan DM, Shalash A, 2017, Auditory brainstem evoked responses and vestibular evoked myogenic potentials: Potential biomarkers in Parkinson’s disease, Egypt J Otolaryngol, 33: 508–517. https://doi.org/10.4103/1012-5574.206023
- Shalash AS, Hassan DM, Elrassas HH, et al., 2017, Auditory-and vestibular-evoked potentials correlate with motor and non-motor features of Parkinson’s disease, Front Neurol, 8: 55. https://doi.org/10.3389/fneur.2017.00055
- Alexa D, Alexa L, Popa L, et al., 2013, Brainstem auditory evoked potentials in Parkinson’s disease, Rom J Neurol, 12: 198–201. https://doi.org/10.37897/RJN.2013.4.7
- Venhovens J, Meulstee J, Bloem BR, et al., 2016, Neurovestibular analysis and falls in Parkinson’s disease and atypical parkinsonism, Eur J Neurosci, 43: 1636–1646. https://doi.org/10.1111/ejn.13253
- Akil CM, Weber SN, Park SN, et al., 2008, Localization of synucleins in the mammalian cochlea, J Assoc Res Otoloaryngol, 9: 452–463. htttps://doi.org/10.1007/s10162-008-0134-y
- Carpenter M, 1985, Core Text of Neuroanatomy, Baltimore, MD: Williams and Wilkins, p137–149.
- Yeterian EH, Pandya DN, 1998, Corticostriatal connections of the superior temporal region in rhesus monkeys, J Comp Neurol, 399: 384–402. https://doi.org/10.1002/(SICI)1096-9861(19980928) 399:3<384:AID-CNE7>3.0.CO;2-X
- Selemon LD, Goldman-Rakic PS, 1985, Longitudinal topography and interdigitation of corticostriatal projections in the rhesus monkey, J Neurosci, 5: 776–794. https://doi.org/10.1523/JNEUROSCI.05-03-00776.1985
- Shammah-Lagnado SJ, Alheid GF, Heimer L, 1996, Efferent connections of the caudal part of the globus pallidus in the rat, J Comp Neurol, 376: 489–507. https://doi.org/10.1002/(SICI)1096-9861(19961216) 376:3<489:AID-CNE10>3.0.CO;2-H
- Uematsu D, Hamada J, Gotoh F, 1987, Brainstem auditory evoked responses and CT findings in multiple system atrophy, J Neurol Sci, 77: 161–171. https://doi.org/10.1016/0022-510X(87)90119-5
- Prasher D, Bannister R, 1986, Brain stem auditory evoked potentials in patients with multiple system atrophy with progressive autonomic failure (Shy-Drager syndrome), J Neurol Neurosurg Psychiatry, 49: 278–289. https://doi.org/10.1136/jnnp.49.3.278
- Shy GM, Drager GA, 1960, A neurological syndrome associated with orthostatic hypotension, A clinical pathologic study, Arch Neurol, 2: 511–527. https://doi.org/10.1001/archneur.1960.03840110025004
- Schwarz GA, 1967, The orthostatic hypotension syndrome of shy-drager, A clinicopathologic report, Arch Neurol, 16: 123–139. https://doi.org/10.1001/archneur.1967.00470200011002
- Nick J, Contamin F, Escourolle R, et al., 1967, Idiopathic orthostatic hypotension with a complex neurological syndrome of extrapyramidal predominance, Rev Neurol (Paris), 116: 213–227.
- Johnson RH, Lee GD, Oppenheimer DR, et al., 1966, Autonomic failure with orthostatic hypotension due to intermediolateral column degeneration, A report of two cases with autopsies, Q J Med, 35: 276–292.
- Bannister R, Oppenheimer DR, 1972, Degenerative disease of the nervous system associated with autonomic failure, Brain, 95: 457–474. https://doi.org/10.1093/brain/95.3.457
- Braak H, Tredici KD, Rüb U, et al., 2003, Staging of brain pathology related to sporadic Parkinson’s disease, Neurobiol Aging, 24: 197–211. https://doi.org/10.1016/s0197-4580(02)00065-9
- Pramstaller PP, Wenning GK, Smith SJ, et al., 1995, Nerve conduction studies, skeletal muscle EMG, and sphincter EMG in multiple system atrophy, J Neurol Neurosurg Psychiatry, 58: 618–621. https://doi.org/10.1136/jnnp.58.5.618
- Abbruzzese G, Marchese R, Trompetto C, 1997, Sensory and motor evoked potentials in multiple system atrophy: A comparative study with Parkinson’s disease. Mov Disord, 12, 315–321. https://doi.org/10.1002/mds.870120309
- Takeda M, Tachibana H, Okuda B, et al., 1998, Electrophysiological comparison between corticobasal degeneration and progressive supranuclear palsy, Clin Neurol Neurosurg, 100: 94–98. https://doi.org/10.1016/s0303-8467(98)00007-9
- Conte A, Khan N, Defazio G, et al., 2013, Pathophysiology of somatosensory abnormalities in Parkinson’s disease, Nat Rev Neurol, 9: 687–697. https://doi.org/10.1038/nrneurol.2013.224
- De Beyl ZD, Delberghe X, Herbaut AG, et al., 1988, The somatosensory central conduction time: Physiological considerations and normative data, Electroencephalogr Clin Neurophysiol, 71: 17–26. https://doi.org/10.1016/0168-5597(88)90015-9