Sweet spot for resting-state functional MRI effect of deep brain stimulation in dystonia lies in the lower pallidal area
Jazyk angličtina Země Nizozemsko Médium print-electronic
Typ dokumentu časopisecké články
PubMed
39986202
PubMed Central
PMC11889665
DOI
10.1016/j.nicl.2025.103750
PII: S2213-1582(25)00020-8
Knihovny.cz E-zdroje
- Klíčová slova
- Deep brain stimulation, Dystonia, Internal globus pallidus, Resting-state functional magnetic resonance imaging,
- MeSH
- dospělí MeSH
- dystonické poruchy * terapie diagnostické zobrazování patofyziologie MeSH
- dystonie * terapie diagnostické zobrazování patofyziologie MeSH
- globus pallidus * diagnostické zobrazování patofyziologie MeSH
- hluboká mozková stimulace * metody MeSH
- lidé středního věku MeSH
- lidé MeSH
- magnetická rezonanční tomografie metody MeSH
- průřezové studie MeSH
- senioři MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- mužské pohlaví MeSH
- senioři MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
INTRODUCTION: Deep brain stimulation (DBS) of the internal globus pallidus (GPi) is a well-established, effective treatment for dystonia. Substantial variability of therapeutic success has been the one of the drivers of an ongoing debate about proper stimulation site and settings, with several indications of the notional sweet spot pointing to the lower GPi or even subpallidal area. METHODS: The presented patient-blinded, random-order study with cross-sectional verification against healthy controls enrolled 17 GPi DBS idiopathic, cervical or generalised dystonia patients to compare the effect of the stimulation in the upper and lower GPi area, with the focus on sensorimotor network connectivity and local activity measured using functional magnetic resonance. RESULTS: Stimulation brought both these parameters to levels closer to the state detected in healthy controls. This effect was much more pronounced during the stimulation in the lower GPi area or beneath it than in slightly higher positions, with stimulation-related changes detected by both metrics of interest in the sensorimotor cortex, striatum, thalamus and cerebellum. CONCLUSIONS: All in all, this study not only replicated the results of previous studies on GPi DBS as a modality restoring sensorimotor network connectivity and local activity in dystonia towards the levels in healthy population, but also showed that lower GPi area or even subpallidal structures, be it white matter or even small, but essential nodes in the zona incerta as nucleus basalis of Meynert, are important regions to consider when programming DBS in dystonia patients.
Department of Cybernetics Czech Technical University Prague Prague Czech Republic
Department of stereotactic and radiation neurosurgery Nemocnice Na Homolce Prague Czech Republic
Zobrazit více v PubMed
Albanese A., Bhatia K., Bressman S.B., DeLong M.R., Fahn S., Fung V.S.C., et al. Phenomenology and classification of dystonia: A consensus update. Movement Disorders. 2013 PubMed PMC
Balint B., Mencacci N.E., Valente E.M., Pisani A., Rothwell J., Jankovic J., et al. Dystonia. Nature Reviews Disease Primers. 2018;4:1–23. PubMed
Behrens T.E.J., Johansen-Berg H., Woolrich M.W., Smith S.M., Wheeler-Kingshott C., Boulby P.A., et al. Non-invasive mapping of connections between human thalamus and cortex using diffusion imaging. Nat Neurosci. 2003;6:750–757. doi: 10.1038/nn1075. PubMed DOI
Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B (methodological) 1995;57:289–300.
Burke R.E., Fahn S., Marsden C.D., Bressman S.B., Moskowitz C., Friedman J. Validity and reliability of a rating scale for the primary torsion dystonias. Neurology. 1985;35:73. PubMed
Cheung T., Noecker A.M., Alterman R.L., McIntyre C.C., Tagliati M. Defining a therapeutic target for pallidal deep brain stimulation for dystonia. Annals of Neurology. 2014;76:22–30. doi: 10.1002/ana.24187. PubMed DOI
Consky E.S., Basinski A., Belle L., Ranawaya R., Lang A.E. The Toronto Western Spasmodic Torticollis Rating Scale (TWSTRS): assessment of validity and inter-rater reliability. Neurology. 1990;40:445.
Cox R.W. AFNI: software for analysis and visualization of functional magnetic resonance neuroimages. Computers and Biomedical Research. 1996;29:162–173. PubMed
Delnooz C.C.S., Helmich R.C., Toni I., van de Warrenburg B.P.C. Reduced parietal connectivity with a premotor writing area in writer’s cramp. Movement Disorders. 2012;27:1425–1431. doi: 10.1002/mds.25029. PubMed DOI
Delnooz C.C., Pasman J.W., Beckmann C.F., van de Warrenburg B.P. Task-free functional MRI in cervical dystonia reveals multi-network changes that partially normalize with botulinum toxin. PloS One. 2013;8 PubMed PMC
Diedrichsen J., Balsters J.H., Flavell J., Cussans E., Ramnani N. A probabilistic MR atlas of the human cerebellum. NeuroImage. 2009;46:39–46. doi: 10.1016/j.neuroimage.2009.01.045. PubMed DOI
Ewert S., Plettig P., Li N., Chakravarty M.M., Collins D.L., Herrington T.M., et al. Toward defining deep brain stimulation targets in MNI space: a subcortical atlas based on multimodal MRI, histology and structural connectivity. Neuroimage. 2018;170:271–282. PubMed
Feng C., Jiang W., Xiao Y., Liu Y., Pang L., Liang M., et al. Comparing brain functional activities in patients with blepharospasm and dry eye disease measured with resting-state fMRI. Front Neurol. 2021;12 doi: 10.3389/fneur.2021.607476. PubMed DOI PMC
Filip P., Lungu O.V., Bareš M. Dystonia and the cerebellum: A new field of interest in movement disorders? Clinical Neurophysiology. 2013 doi: 10.1016/j.clinph.2013.01.003. PubMed DOI
Filip P., Gallea C., Lehéricy S., Bertasi E., Popa T., Mareček R., et al. Disruption in cerebellar and basal ganglia networks during a visuospatial task in cervical dystonia. Movement Disorders. 2017;32:757–768. PubMed
Filip P., Jech R., Fečíková A., Havránková P., Ruužička F., Mueller K., et al. Restoration of functional network state towards more physiological condition as the correlate of clinical effects of pallidal deep brain stimulation in dystonia. Brain Stimulation. 2022;15:1269–1278. PubMed
Filip P., Lasica A., Uhrová T., Mana J., Ružička F., Keller J., et al. Mixed anxiety-depressive disorder in Parkinson’s disease associated with worse resting state functional response to deep brain stimulation of subthalamic nucleus. Heliyon. 2024;10 PubMed PMC
Fujita K., Eidelberg D. Imbalance of the direct and indirect pathways in focal dystonia: a balanced view. Brain. 2017;140:3075–3077. doi: 10.1093/brain/awx305. PubMed DOI
Galardi G., Perani D., Grassi F., Bressi S., Amadio S., Antoni M., et al. Basal ganglia and thalamo‐cortical hypermetabolism in patients with spasmodic torticollis. Acta Neurologica Scandinavica. 1996;94:172–176. PubMed
Glasser M.F., Sotiropoulos S.N., Wilson J.A., Coalson T.S., Fischl B., Andersson J.L., et al. The minimal preprocessing pipelines for the Human Connectome Project. Neuroimage. 2013;80:105–124. PubMed PMC
Glasser M.F., Coalson T.S., Robinson E.C., Hacker C.D., Harwell J., Yacoub E., et al. A multi-modal parcellation of human cerebral cortex. Nature. 2016;536:171–178. PubMed PMC
Griffanti L., Rolinski M., Szewczyk-Krolikowski K., Menke R.A., Filippini N., Zamboni G., et al. Challenges in the reproducibility of clinical studies with resting state fMRI: An example in early Parkinson’s disease. NeuroImage. 2016;124:704–713. doi: 10.1016/j.neuroimage.2015.09.021. PubMed DOI PMC
Guell X., Schmahmann J. Springer; 2020. Cerebellar functional anatomy: a didactic summary based on human fMRI evidence. PubMed
Haslinger B., Noé J., Altenmüller E., Riedl V., Zimmer C., Mantel T., et al. Changes in resting-state connectivity in musicians with embouchure dystonia. Movement Disorders. 2017;32:450–458. doi: 10.1002/mds.26893. PubMed DOI
Hepp D.H., Foncke E.M., Berendse H.W., Wassenaar T.M., Olde Dubbelink K.T., Groenewegen H.J., et al. Damaged fiber tracts of the nucleus basalis of Meynert in Parkinson’s disease patients with visual hallucinations. Scientific Reports. 2017;7:10112. PubMed PMC
Ho D., Imai K., King G., Stuart E.A. MatchIt: nonparametric preprocessing for parametric causal inference. Journal of Statistical Software. 2011;42:1–28.
Horn A., Kühn A.A. Lead-DBS: a toolbox for deep brain stimulation electrode localizations and visualizations. Neuroimage. 2015;107:127–135. PubMed
Horn A., Li N., Dembek T.A., Kappel A., Boulay C., Ewert S., et al. Lead-DBS v2: Towards a comprehensive pipeline for deep brain stimulation imaging. Neuroimage. 2019;184:293–316. PubMed PMC
Horn A., Reich M.M., Ewert S., Li N., Al Fatly B., Lange F., et al. Optimal deep brain stimulation sites and networks for cervical vs. generalized dystonia. Proceedings of the National Academy of Sciences. 2022;119 doi: 10.1073/pnas.2114985119. PubMed DOI PMC
Jech R., Mueller K. Elsevier; 2022. Investigating network effects of DBS with fMRI. Connectomic Deep Brain Stimulation; pp. 275–301.
Kannurpatti S.S., Biswal B.B. Detection and scaling of task-induced fMRI-BOLD response using resting state fluctuations. Neuroimage. 2008;40:1567–1574. doi: 10.1016/j.neuroimage.2007.09.040. PubMed DOI PMC
Keuken M.C., Bazin P.-L., Backhouse K., Beekhuizen S., Himmer L., Kandola A., et al. Effects of aging on T1, T2*, and QSM MRI values in the subcortex. Brain Struct Funct. 2017;222:2487–2505. doi: 10.1007/s00429-016-1352-4. PubMed DOI PMC
Kupsch A., Tagliati M., Vidailhet M., Aziz T., Krack P., Moro E., et al. Early postoperative management of DBS in dystonia: Programming, response to stimulation, adverse events, medication changes, evaluations, and troubleshooting. Movement Disorders. 2011;26 doi: 10.1002/mds.23624. PubMed DOI
Liu A.K.L., Chang R.-C.-C., Pearce R.K.B., Gentleman S.M. Nucleus basalis of Meynert revisited: anatomy, history and differential involvement in Alzheimer’s and Parkinson’s disease. Acta Neuropathol. 2015;129:527–540. doi: 10.1007/s00401-015-1392-5. PubMed DOI PMC
Loh A., Elias G.J.B., Germann J., Boutet A., Gwun D., Yamamoto K., et al. Neural correlates of optimal deep brain stimulation for cervical dystonia. Annals of Neurology. 2022;92:418–424. doi: 10.1002/ana.26450. PubMed DOI
Lohmann G., Margulies D.S., Horstmann A., Pleger B., Lepsien J., Goldhahn D., et al. Eigenvector centrality mapping for analyzing connectivity patterns in fmri data of the human brain. PLOS ONE. 2010;5 doi: 10.1371/journal.pone.0010232. PubMed DOI PMC
Lv J., Calamante F. Elsevier; 2023. The synergy of structural and functional connectivity. Connectome Analysis; pp. 247–265.
Magyar-Lehmann S., Antonini A., Roelcke U., Maguire R.P., Missimer J., Meyer M., et al. Cerebral glucose metabolism in patients with spasmodic torticollis. Movement Disorders. 1997;12:704–708. doi: 10.1002/mds.870120513. PubMed DOI
Marrelec G., Daunizeau J., Pelegrini-Issac M., Doyon J., Benali H. Conditional correlation as a measure of mediated interactivity in fMRI and MEG/EEG. IEEE Transactions on Signal Processing. 2005;53:3503–3516. doi: 10.1109/TSP.2005.853211. DOI
Mueller K., Jech R., Hoskovcová M., Ulmanová O., Urgošík D., Vymazal J., et al. General and selective brain connectivity alterations in essential tremor: A resting state fMRI study. NeuroImage: Clinical. 2017;16:468–476. doi: 10.1016/j.nicl.2017.06.004. PubMed DOI PMC
Nazmuddin M., Philippens I.H., van Laar T. Electrical stimulation of the nucleus basalis of meynert: a systematic review of preclinical and clinical data. Scientific Reports. 2021;11:11751. PubMed PMC
Pauls K.A.M., Krauss J.K., Kämpfer C.E., Kühn A.A., Schrader C., Südmeyer M., et al. Causes of failure of pallidal deep brain stimulation in cases with pre-operative diagnosis of isolated dystonia. Parkinsonism & Related Disorders. 2017;43:38–48. PubMed
Reich M.M., Horn A., Lange F., Roothans J., Paschen S., Runge J., et al. Probabilistic mapping of the antidystonic effect of pallidal neurostimulation: a multicentre imaging study. Brain. 2019;142:1386–1398. PubMed
Robinson E.C., Garcia K., Glasser M.F., Chen Z., Coalson T.S., Makropoulos A., et al. Multimodal surface matching with higher-order smoothness constraints. NeuroImage. 2018;167:453–465. doi: 10.1016/j.neuroimage.2017.10.037. PubMed DOI PMC
Rubinov M., Sporns O. Complex network measures of brain connectivity: Uses and interpretations. NeuroImage. 2010;52:1059–1069. doi: 10.1016/j.neuroimage.2009.10.003. PubMed DOI
Schönecker T., Gruber D., Kivi A., Müller B., Lobsien E., Schneider G.-H., et al. Postoperative MRI localisation of electrodes and clinical efficacy of pallidal deep brain stimulation in cervical dystonia. Journal of Neurology, Neurosurgery & Psychiatry. 2015;86:833–839. PubMed
Simonyan K. Neuroimaging applications in dystonia. International Review of Neurobiology. 2018;143:1–30. PubMed PMC
Smith S.M., Beckmann C.F., Andersson J., Auerbach E.J., Bijsterbosch J., Douaud G., et al. Resting-state fMRI in the human connectome project. Neuroimage. 2013;80:144–168. PubMed PMC
Suzuki Y., Mizoguchi S., Kiyosawa M., Mochizuki M., Ishiwata K., Wakakura M., et al. Glucose hypermetabolism in the thalamus of patients with essential blepharospasm. J Neurol. 2007;254:890–896. doi: 10.1007/s00415-006-0468-5. PubMed DOI
Tisch S., Zrinzo L., Limousin P., Bhatia K.P., Quinn N., Ashkan K., et al. Effect of electrode contact location on clinical efficacy of pallidal deep brain stimulation in primary generalised dystonia. Journal of Neurology, Neurosurgery & Psychiatry. 2007;78:1314–1319. PubMed PMC
Tziortzi A.C., Haber S.N., Searle G.E., Tsoumpas C., Long C.J., Shotbolt P., et al. Connectivity-based functional analysis of dopamine release in the striatum using diffusion-weighted MRI and positron emission tomography. Cereb Cortex. 2014;24:1165–1177. doi: 10.1093/cercor/bhs397. PubMed DOI PMC
Vidailhet M., Vercueil L., Houeto J.-L., Krystkowiak P., Benabid A.-L., Cornu P., et al. Bilateral deep-brain stimulation of the globus pallidus in primary generalized dystonia. N Engl J Med. 2005;352:459–467. doi: 10.1056/NEJMoa042187. PubMed DOI
Volkmann J., Wolters A., Kupsch A., Müller J., Kühn A.A., Schneider G.-H., et al. Pallidal deep brain stimulation in patients with primary generalised or segmental dystonia: 5-year follow-up of a randomised trial. The Lancet Neurology. 2012;11:1029–1038. PubMed
Winder A.T., Echagarruga C., Zhang Q., Drew P.J. Weak correlations between hemodynamic signals and ongoing neural activity during the resting state. Nat Neurosci. 2017;20:1761–1769. doi: 10.1038/s41593-017-0007-y. PubMed DOI PMC
Winkler A.M., Ridgway G.R., Webster M.A., Smith S.M., Nichols T.E. Permutation inference for the general linear model. NeuroImage. 2014;92:381–397. doi: 10.1016/j.neuroimage.2014.01.060. PubMed DOI PMC
Yang J., Luo C., Song W., Chen Q., Chen K., Chen X., et al. Altered regional spontaneous neuronal activity in blepharospasm: a resting state fMRI study. Journal of Neurology. 2013;260:2754–2760. PubMed
Zhou B., Wang J., Huang Y., Yang Y., Gong Q., Zhou D. A resting state functional magnetic resonance imaging study of patients with benign essential blepharospasm. Journal of Neuro-Ophthalmology. 2013;33:235. doi: 10.1097/WNO.0b013e31828f69e5. PubMed DOI