Neurophysiology of hypokinetic movement’s disorders: New insights in daily clinical practice
Hypokinetic movement disorders encompass a group of clinically similar diseases that present challenges in discrimination during neurological examinations. Characterizing a specific hypokinetic disorder is necessary for the diagnosis and treatment in daily clinical practice. Neurophysiological tools, such as electromyography (EMG) combined with accelerometry, motor-evoked potentials (MEPs), electroencephalographic recording (EEG), Bereitschaftspotential (BP), auditory-evoked cognitive potential (P300), blink reflex (BR), and R2 blink reflex recovery cycle (R2BRRC), are useful in the differential diagnosis of movement disorders due to the common clinical features. However, neurophysiological assessments of movement disorders, especially hypokinetic diseases, are currently underutilized in clinical practice as compared to a few decades ago. This review aims to summarize practical insights gleaned from reported studies over the past 5 years (i.e., 2019 – 2023) regarding neurophysiological assessments of hypokinetic movement disorders, emphasizing the importance of their routine application. In particular, the methodology of the electrophysiologic evaluations pertaining to hypokinetic movement disorders is assessed. Moreover, a practical approach for the differential diagnosis of similar movement disorder syndromes based on specific neurophysiological features is proposed. Collectively, this review of the most recent neurophysiological implications in hypokinetic movement disorders highlights the practicality of these methods. Despite the advancement of other diagnostic techniques (e.g., neuroradiological methods), neurophysiological assessments may be a promising tool for clinical diagnoses, due to their high accuracy and ability to categorize and manage movement disorders (e.g., hypokinetic movement disorders) in daily clinical practice.
- Fahn S, Jankovic J, editors. Principles and Practice of Movement Disorders. USA, Philadelphia, PA: Churchill Livingstone, Elsevier; 2007. p. 1-652.
- Merchant SH, Vial-Undurraga F, Leodori G, Van Gerpen JA, Hallett M. Myoclonus: An electrophysiological diagnosis. Mov Disord Clin Pract. 2020;7(5):489-499. doi: 10.1002/mdc3.12986
- Postuma RB, Berg D, Stern M, et al. MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2015;30:1591-601. doi: 10.1002/mds.26424
- Postuma RB, Poewe W, Litvan I, et al. Validation of the MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord. 2018;33:1601-1608. doi: 10.1002/mds.27362
- Espay AJ, Litvan I. Parkinsonism and frontotemporal dementia: The clinical overlap. J Mol Neurosci. 2011;45:343-9. doi: 10.1007/s12031-011-9632-1
- Apartis E. Clinical neurophysiology in movement disorders. Handb Clin Neurol. 2013;111:87-92. doi: 10.1016/B978-0-444-52891-9.00008-7
- Sciacca G, Mostile G, Disilvestro I, et al. Long-duration response to levodopa, motor learning, and neuroplasticity in early Parkinson’s disease. Mov Disord. 38(4):626-635. doi: 10.1002/mds.29344
- Wilken M, Bruno V, Rossi M, et al. Sensitivity and specificity of different hand positions to assess upper limb rest tremor. Mov Disord. 2019;34(4):575-579. doi: 10.1002/mds.27648
- Wilken M, Rossi M, Rivero AD, Hallett M, Merello M. Re-emergent tremor provocation. Parkinsonism Relat Disord. 2019;66:241-244. doi: 10.1016/j.parkreldis.2019.08.015
- Wilken M, Rossi MD, Rivero AD, et al. Latency of re-emergent tremor in Parkinson’s disease is influenced by levodopa. Parkinsonism Relat Disord. 2019;61:166-169. doi: 10.1016/j.parkreldis.2018.10.019
- Celicanin M, Harrison AP, Kvistgaard Olsen J, et al. Probing motor dynamics at the muscle level-Acoustic myography in Parkinson’s disease. Physiol Rep. 2023;11(6):e15631. doi: 10.14814/phy2.15631
- Vucic S, Stanley Chen KH, Kiernan MC, et al. Clinical diagnostic utility of transcranial magnetic stimulation in neurological disorders. Updated report of an IFCN committee. Clin Neurophysiol. 2023;150:131-175. doi: 10.1016/j.clinph.2023.03.010
- Khedr EM, Lefaucheur JP, Hasan AM, Osama K. Are there differences in cortical excitability between akinetic-rigid and tremor-dominant subtypes of Parkinson’s disease? Neurophysiol Clin. 2021;51(5):443-453. doi: 10.1016/j.neucli.2021.08.002
- Leodori G, Belvisi D, De Bartolo MI, et al. Re-emergent tremor in parkinson’s disease: the role of the motor cortex. Mov Disord. 2020;35(6):1002-1011. doi: 10.1002/mds.28022
- Leodori G, De Bartolo MI, Fabbrini A, et al. The role of the motor cortex in tremor suppression in parkinson’s disease. J Parkinsons Dis. 2022;12(6):1957-1963. doi: 10.3233/JPD-223316
- Ammann C, Dileone M, Pagge C, et al. Cortical disinhibition in Parkinson’s disease. Brain. 2020;5;143(11):3408-3421. doi: 10.1093/brain/awaa274
- Shirota Y, Ohminami S, Tsutsumi R, et al. Increased facilitation of the primary motor cortex in de novo Parkinson’s disease. Parkinsonism Relat Disord. 2019;66:125-129. doi: 10.1016/j.parkreldis.2019.07.022
- Guerra A, Suppa A, D’Onofrio V, et al. Abnormal cortical facilitation and L-dopa-induced dyskinesia in Parkinson’s disease. Brain Stimul. 2019;12(6):1517-1525. doi: 10.1016/j.brs.2019.06.012
- Saravanamuttu J, Radhu N, Udupa K, Baarbé J, Gunraj C, Chen R. Impaired motor cortical facilitatory-inhibitory circuit interaction in Parkinson’s disease. Clin Neurophysiol. 2021;132(10):2685-2692. doi: 10.1016/j.clinph.2021.05.032
- Moriyasu S, Shimizu T, Honda M, Ugawa Y, Hanajima R. Motor cortical plasticity and its correlation with motor symptoms in Parkinson’s disease. ENeurologicalSci. 2022;29:100422. doi: 10.1016/j.ensci.2022.100422
- Ginanneschi F, Messa LV, Battisti C, Rossi A. Changes in corticomotor pathway excitability after exercise training in Parkinson’s disease. Neurol Sci. 2021;42(8):3375-3381. doi: 10.1007/s10072-020-04960-y
- Tzvetanov P, Lisichkov I, Rousseff RT, Hegde V, Kostadinov S. Abnormality of contingent negative variation correlates with parkinson’s disease severity. Clin Neurosci. 2022;19(7-9):71-76.
- Zang NA, Schneider M, Weiss D. Cortical mechanisms of movement recovery after freezing in Parkinson’s disease. Neurobiol Dis. 2022;174:105871. doi: 10.1016/j.nbd.2022.105871
- Karimi F, Niu J, Gouweleeuw K, Almeida Q, Jiang N. Movement-related EEG signatures associated with freezing of gait in Parkinson’s disease: An integrative analysis. Brain Commun. 2021;3(4):fcab277. doi: 10.1093/braincomms/fcab277
- Betrouni N, Delval A, Chaton L, et al. Electroencephalography-based machine learning for cognitive profiling in Parkinson’s disease: Preliminary results. Mov Disord. 2019;34(2):210-217. doi: 10.1002/mds.27528
- Waninger S, Berka C, Stevanovic Karic M, et al. Neurophysiological biomarkers of parkinson’s disease. J Parkinsons Dis. 2020;10(2):471-480. doi: 10.3233/JPD-191844
- Farashi S, Khazaei M. Effect of levodopa medication on human brain connectome in parkinson’s disease-a combined graph theory and EEG study. Clin EEG Neurosci. 53(6):562-571. doi: 10.1177/15500594221085552
- Donzuso G, Sciacca G, Rascunà C, et al. Structural MRI substrate of long-duration response to levodopa in parkinson’s disease: An exploratory study. J Neurol. 2021;268(11):4258-4264. doi: 10.1007/s00415-021-10550-5
- Quattrone A, Zappia M, Aguglia U, et al. The subacute levodopa test for evaluating long-duration response in Parkinson’s disease. Ann Neurol. 1995;38:389-395. doi: 10.1002/ana.410380308
- Todisco M, Alfonsi E, Isaias IU, et al. Vocal cord electromyographic correlates of stridor in multiple system atrophy phenotypes. Parkinsonism Relat Disord. 2020;70:31-35. doi: 10.1016/j.parkreldis.2019.11.025
- Todisco M, Cosentino G, Scardina S, et al. Diagnostic and prognostic value of external anal sphincter EMG patterns in multiple system atrophy. Mov Disord. 2022;37(5):1069-1074. doi: 10.1002/mds.28938
- Shirota Y, Hanajima R, Shimizu T, Terao Y, Tsuji S, Ugawa Y. Quantitative evaluation of cerebellar function in multiple system atrophy with transcranial magnetic stimulation. Cerebellum. 2022;21:219-224. doi: 10.1007/s12311-021-01293-0
- Honda M, Shimizu T, Moriyasu S, et al. Impaired long-term potentiation-like motor cortical plasticity in progressive supranuclear palsy. Clin Neurophysiol. 2023;155:99-106. doi: 10.1016/j.clinph.2023.07.011
- Fisicaro F, Lanza G, Cantone M, et al. Clinical and electrophysiological hints to TMS in de novo patients with parkinson’s disease and progressive supranuclear palsy. J Pers Med. 2020;12;10(4):274. doi: 10.3390/jpm10040274
- Di Stasio F, Suppa A, Marsili L, et al. Corticobasal syndrome: Neuroimaging and neurophysiological advances. Eur J Neurol. 2019;26(5):701-e52. doi: 10.1111/ene.13928
- Barcelon EA, Mukaino T, Yokoyama J, et al. Grand total EEG score can differentiate parkinson’s disease from parkinson-related disorders. Front Neurol. 2019;10:398. doi: 10.3389/fneur.2019.00398
- Sciacca G, Mostile G, Nicoletti A, et al. Cut-off scores of blink reflex recovery cycle to differentiate atypical parkinsonisms. Eur J Neurol. 2020;27(11):e68. doi: 10.1111/ene.14392
- Sciacca G, Mostile G, Disilvestro I, et al. Asymmetry index of blink reflex recovery cycle differentiates parkinson’s disease from atypical parkinsonian syndromes. J Neurol. 2020;267(6):1859-1863. doi: 10.1007/s00415-020-09900-6
- Donzuso G, Sciacca G, Luca A, et al. Corticobasal syndrome and Parkinson’s disease at the beginning: Asymmetrical patterns of MRI and blink reflex for early diagnosis. J Neural Transm (Vienna). 2022;129(12):1427-1433. doi: 10.1007/s00702-022-02557-7
- Sciacca G, Nicoletti A, Mostile G, et al. Blink reflex recovery cycle to differentiate progressive supranuclear palsy from corticobasal syndrome. Eur J Neurol. 2018;25(8):1100-e85. doi: 10.1111/ene.13673
- Valls-Sole J, Valldeoriola F, Tolosa E, Marti MJ. Distinctive abnormalities of facial reflexes in patients with progressive supranuclear palsy. Brain. 1997;120:1877-1883. doi: 10.1093/brain/120.10.1877
- Kızıltan ME, Gunduz A, Kızıltan G, Tekeoğlu A, Sohtaoğlu M. Brainstem and spinal reflex studies in patients with primary progressive freezing of gait. J Neurol Sci. 2014;343:51-55. doi: 10.1016/j.jns.2014.05.018
- Szmidt-Salkowska E, Gawel M, Jamrozik Z, Salkowska- Wanat J, Gawel D, Kaminska A. Diagnostic value of blink reflex in multisystem atrophy, progressive supranuclear palsy, and Parkinson disease. Neurol Neurochir Pol. 2016;50:336-341. doi: 10.1016/j.pjnns.2016.06.001
- Chen CC, Yeh CH, Chan HL, et al. Subthalamic nucleus oscillations correlate with vulnerability to freezing of gait in patients with Parkinson’s disease. Neurobiol Dis. 2019;132:104605. doi: 10.1016/j.nbd.2019.104605
- Muthukrishnan N, Abbas JJ, Shill HA, Krishnamurthi N. Cueing paradigms to improve gait and posture in Parkinson’s disease: A narrative review. Sensors (Basel). 2019;9(24):5468. doi: 10.3390/s19245468
- Zampogna A, Mileti I, Martelli F, et al. Early balance impairment in Parkinson’s Disease: Evidence from robot-assisted axial rotations. Clin Neurophysiol. 2021;132:2422-2430. doi: 10.1016/j.clinph.2021.06.023
- Di Biase L, Raiano L, Caminiti ML, Pecoraro PM, Di Lazzaro V. Parkinson’s disease wearable gait analysis: Kinematic and dynamic markers for diagnosis. Sensors (Basel). 2022;22(22):8773. doi: 10.3390/s22228773