No CrossRef data available.
Article contents
Short-Latency Afferent Inhibition Correlates with Stage of Disease in Parkinson’s Patients
Published online by Cambridge University Press: 10 June 2022
Abstract:
Background:
Sensory-motor decoupling at the cortical level involving cholinergic circuitry has also been reported in Parkinson’s Disease (PD). Short-latency afferent inhibition (SAI) is a transcranial magnetic stimulation (TMS) paradigm that has been used previously to probe cortical cholinergic circuits in well-characterised subgroups of patients with PD. In the current study, we compared SAI in a cohort of PD patients at various stages of disease and explored correlations between SAI and various clinical measures of disease severity.
Methods:
The modified Hoehn and Yahr (H&Y) scale was used to stage disease in 22 patients with PD. Motor and cognitive function were assessed using the MDS-UPDRS (Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale) part III and MoCA (Montreal Cognitive Assessment) score, respectively. Objective gait assessment was performed using an electronic walkway (GAITRite®). SAI was measured as the average percentage inhibition of test motor-evoked potentials (MEPs) conditioned by electrical stimulation of the contralateral median nerve at the wrist.
Results:
SAI was significantly reduced in patients with advanced PD (H&Y stage 3) compared to early PD patients (H&Y stage 1) on pairwise comparison. The visuospatial executive function and orientation domains of cognition demonstrated significant negative associations with SAI.
Conclusion:
Cortical sensory-motor integration is progressively diminished as disease progresses. The observation that a reduction in SAI is associated with a reduction in cognitive function possibly reflects the progressive involvement of cortical cholinergic circuits in PD with increasing motor stage. Future longitudinal studies are necessary to confirm this preliminary result.
Résumé :
L’inhibition afférente à courte latence peut être corrélée au stade actif de la maladie de Parkinson.
Un découplage sensori-moteur au niveau cortical impliquant les circuits cholinergiques a également été signalé dans le cas de la maladie de Parkinson (MP). L’inhibition afférente à courte latence (IACL) est un paradigme de stimulation magnétique transcrânienne (SMT) qui a été utilisé précédemment pour explorer les circuits cholinergiques corticaux dans des sous-groupes bien caractérisés de patients atteints de la MP. Dans la présente étude, nous nous sommes ainsi penchés sur la IACL au sein d’une cohorte de patients atteints de la MP à différents stades et exploré les corrélations entre cette même IACL et diverses mesures cliniques de la gravité de la maladie.
L’échelle modifiée de Hoehn et Yahr (EMHY) a été utilisée pour déterminer le stade de la MP chez 22 patients qui en étaient atteints. Les fonctions motrices et cognitives ont été respectivement évaluées à l’aide de la section III du MDS-UPDRS (Movement Disorder Society-Sponsored Revision of the Unified Parkinson's Disease Rating Scale) et du MoCA (Montreal Cognitive Assessment). L’évaluation objective de la démarche des patients a été réalisée à l’aide d’une passerelle électronique (GAITRite®). Enfin, l’IACL a été mesurée comme le pourcentage moyen d’inhibition des potentiels évoqués moteurs (PEM) d’un test conditionné par une stimulation électrique du nerf médian controlatéral au niveau du poignet.
L’IACL s’est avérée significativement réduite chez les patients atteints de la MP à un stade avancé (stade 3 selon la EMHY) par rapport aux patients atteints de la MP à un stade précoce (stade 1 selon la EMHY) lors d’une comparaison par paires. Les domaines de la fonction exécutive visuospatiale et de l’orientation de la cognition ont montré des associations négatives significatives avec l’IACL.
L’intégration sensori-motrice corticale est progressivement diminuée au fur et à mesure que la MP progresse. L’observation selon laquelle une réduction de l’IACL est associée à une réduction de la fonction cognitive reflète peut-être l’implication progressive des circuits cholinergiques corticaux avec un accroissement du stade moteur de la maladie. À cet égard, de futures études longitudinales sont nécessaires pour confirmer ce résultat préliminaire.
Keywords
- Type
- Original Article
- Information
- Copyright
- © The Author(s), 2022. Published by Cambridge University Press on behalf of Canadian Neurological Sciences Federation
Footnotes
SC, US, SR contributed equally to this study.
References
Christopher, L, Koshimori, Y, Lang, AE, Criaud, M, Strafella, AP. Uncovering the role of the insula in non-motor symptoms of Parkinson’s disease. Brain. 2014;137:2143–54.CrossRefGoogle ScholarPubMed
Bonnet, A-M, Loria, Y, Saint-Hilaire, M-H, Lhermitte, F, Agid, Y. Does long-term aggravation of Parkinson’s disease result from nondopaminergic lesions? Neurology. 1987;37:1539–.CrossRefGoogle ScholarPubMed
Bonnet, A-M. Involvement of non-dopaminergic pathways in Parkinson’s disease. CNS Drugs. 2000;13:351–64.CrossRefGoogle Scholar
Hu, M, Taylor-Robinson, SD, Chaudhuri, KR, et al. Cortical dysfunction in non-demented Parkinson’s disease patients: a combined 31P-MRS and 18FDG-PET study. Brain. 2000;123:340–52.CrossRefGoogle Scholar
Sabatini, U, Boulanouar, K, Fabre, N, et al. Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain. 2000;123:394–403.CrossRefGoogle ScholarPubMed
Shah, A, Lenka, A, Saini, J, et al. Altered brain wiring in Parkinson’s disease: a structural connectome-based analysis. Brain Connect. 2017;7:347–56.CrossRefGoogle ScholarPubMed
Yau, Y, Zeighami, Y, Baker, T, et al. Network connectivity determines cortical thinning in early Parkinson’s disease progression. Nat Commun. 2018;9:1–10.CrossRefGoogle ScholarPubMed
Hwang, S, Agada, P, Grill, S, Kiemel, T, Jeka, JJ. A central processing sensory deficit with Parkinson’s disease. Exp Brain Res. 2016;234:2369–79.CrossRefGoogle ScholarPubMed
Sailer, A, Molnar, GF, Paradiso, G, Gunraj, CA, Lang, AE, Chen, R. Short and long latency afferent inhibition in Parkinson’s disease. Brain. 2003;126:1883–94.CrossRefGoogle Scholar
Rizzo, V, Arico, I, Liotta, G, et al. Impairment of sensory-motor integration in patients affected by RLS. J Neurol. 2010;257:1979–85.CrossRefGoogle ScholarPubMed
Di Lazzaro, V, Oliviero, A, Profice, P, et al. Muscarinic receptor blockade has differential effects on the excitability of intracortical circuits in the human motor cortex. Exp Brain Res. 2000;135:455–61.CrossRefGoogle ScholarPubMed
Di Lazzaro, V, Pilato, F, Dileone, M, Tonali, PA, Ziemann, U. Dissociated effects of diazepam and lorazepam on short-latency afferent inhibition. J Physiol. 2005;569:315–23.CrossRefGoogle ScholarPubMed
Nardone, R, Bergmann, J, Kronbichler, M, et al. Abnormal short latency afferent inhibition in early Alzheimer’s disease: a transcranial magnetic demonstration. J Neural Transm. 2008;115:1557–62.CrossRefGoogle ScholarPubMed
Celebi, O, Temuçin, Ç.M, Elibol, B, Saka, E. Short latency afferent inhibition in Parkinson’s disease patients with dementia. Mov Disord. 2012;27:1052–5.CrossRefGoogle ScholarPubMed
Rochester, L, Yarnall, AJ, Baker, MR, et al. Cholinergic dysfunction contributes to gait disturbance in early Parkinson’s disease. Brain. 2012;135:2779–88.CrossRefGoogle ScholarPubMed
Stebbins, GT, Goetz, CG, Burn, DJ, Jankovic, J, Khoo, TK, Tilley, BC. How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov Disord. 2013;28:668–70.CrossRefGoogle ScholarPubMed
Turco, CV, El-Sayes, J, Savoie, MJ, Fassett, HJ, Locke, MB, Nelson, AJ. Short-and long-latency afferent inhibition; uses, mechanisms and influencing factors. Brain Stimul. 2018;11:59–74.CrossRefGoogle ScholarPubMed
Bologna, M, Paparella, G, Fasano, A, Hallett, M, Berardelli, A. Evolving concepts on bradykinesia. Brain. 2020;143:727–50.CrossRefGoogle ScholarPubMed
Di Lazzaro, V, Oliviero, A, Pilato, F, et al. Normal or enhanced short-latency afferent inhibition in Parkinson’s disease? Brain. 2004;127:e8–e.CrossRefGoogle ScholarPubMed
Guerra, A, Colella, D, Giangrosso, M, et al. Driving motor cortex oscillations modulates bradykinesia in Parkinson’s disease. Brain. 2021;145:224–36.Google Scholar
Manganelli, F, Vitale, C, Santangelo, G, et al. Functional involvement of central cholinergic circuits and visual hallucinations in Parkinson’s disease. Brain. 2009;132:2350–5.CrossRefGoogle ScholarPubMed
Nardone, R, Bergmann, J, Brigo, F, et al. Functional evaluation of central cholinergic circuits in patients with Parkinson’s disease and REM sleep behavior disorder: a TMS study. J Neural Transm. 2013;120:413–22.CrossRefGoogle ScholarPubMed
Picillo, M, Dubbioso, R, Iodice, R, et al. Short-latency afferent inhibition in patients with Parkinson’s disease and freezing of gait. J Neural Transm. 2015;122:1533–40.CrossRefGoogle ScholarPubMed
Lee, KD, Koo, JH, Song, SH, Jo, KD, Lee, MK, Jang, W. Central cholinergic dysfunction could be associated with oropharyngeal dysphagia in early Parkinson’s disease. J Neural Transm. 2015;122:1553–61.CrossRefGoogle ScholarPubMed
Pelosin, E, Ogliastro, C, Lagravinese, G, et al. Attentional control of gait and falls: is cholinergic dysfunction a common substrate in the elderly and Parkinson’s disease? Front Aging Neurosci. 2016;8:104.CrossRefGoogle ScholarPubMed
Pasquini, J, Brooks, DJ, Pavese, N. The cholinergic brain in Parkinson’s disease. Mov Disord Clin Practice. 2021;8:1012–26.CrossRefGoogle ScholarPubMed
Schirinzi, T, Di Lorenzo, F, Sancesario, GM, et al. Amyloid-mediated cholinergic dysfunction in motor impairment related to Alzheimer’s disease. J Alzheimer’s Dis. 2018;64:525–32.CrossRefGoogle ScholarPubMed
Bologna, M, Guerra, A, Colella, D, et al. Bradykinesia in Alzheimer’s disease and its neurophysiological substrates. Clin Neurophysiol. 2020;131:850–8.CrossRefGoogle ScholarPubMed