Benefits of pallidal stimulation in dystonia are linked to cerebellar volume and cortical inhibition
Jazyk angličtina Země Anglie, Velká Británie Médium electronic
Typ dokumentu časopisecké články, práce podpořená grantem
Grantová podpora
GAČR 16-13323S
Grantová Agentura České Republiky (Grant Agency of the Czech Republic) - International
Progres Q27/LF1
Univerzita Karlova v Praze (Charles University) - International
MJFF-11362
Michael J. Fox Foundation for Parkinson's Research (Michael J. Fox Foundation) - International
MJFF-11362
Michael J. Fox Foundation for Parkinson's Research (Michael J. Fox Foundation) - International
MJFF-11362
Michael J. Fox Foundation for Parkinson's Research (Michael J. Fox Foundation) - International
PDF-IRG-1307
Parkinson's Disease Foundation (Parkinson's Disease Foundation, Inc.) - International
PubMed
30464181
PubMed Central
PMC6249276
DOI
10.1038/s41598-018-34880-z
PII: 10.1038/s41598-018-34880-z
Knihovny.cz E-zdroje
- MeSH
- dospělí MeSH
- dystonie terapie MeSH
- globus pallidus fyziologie MeSH
- hluboká mozková stimulace metody MeSH
- lidé středního věku MeSH
- lidé MeSH
- mladiství MeSH
- mladý dospělý MeSH
- motorické korové centrum fyziologie MeSH
- mozeček fyziologie MeSH
- nervový útlum * MeSH
- senioři MeSH
- výsledek terapie MeSH
- Check Tag
- dospělí MeSH
- lidé středního věku MeSH
- lidé MeSH
- mladiství MeSH
- mladý dospělý MeSH
- mužské pohlaví MeSH
- senioři MeSH
- ženské pohlaví MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
Clinical benefits of pallidal deep brain stimulation (GPi DBS) in dystonia increase relatively slowly suggesting slow plastic processes in the motor network. Twenty-two patients with dystonia of various distribution and etiology treated by chronic GPi DBS and 22 healthy subjects were examined for short-latency intracortical inhibition of the motor cortex elicited by paired transcranial magnetic stimulation. The relationships between grey matter volume and intracortical inhibition considering the long-term clinical outcome and states of the GPi DBS were analysed. The acute effects of GPi DBS were associated with a shortening of the motor response whereas the grey matter of chronically treated patients with a better clinical outcome showed hypertrophy of the supplementary motor area and cerebellar vermis. In addition, the volume of the cerebellar hemispheres of patients correlated with the improvement of intracortical inhibition which was generally less effective in patients than in controls regardless of the DBS states. Importantly, good responders to GPi DBS showed a similar level of short-latency intracortical inhibition in the motor cortex as healthy controls whereas non-responders were unable to increase it. All these results support the multilevel impact of effective DBS on the motor networks in dystonia and suggest potential biomarkers of responsiveness to this treatment.
Clinic for Cognitive Neurology University Hospital Leipzig Germany
Department of Neurosurgery Na Homolce Hospital Prague Czech Republic
Department of Stereotactic and Radiation Neurosurgery Na Homolce Hospital Prague Czech Republic
Faculty of Biomedical Engineering Czech Technical University Prague Prague Czech Republic
Max Planck Institute for Human Cognitive and Brain Sciences Leipzig Germany
Zobrazit více v PubMed
Vidailhet M, 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
Holloway KL, et al. Deep brain stimulation for dystonia: a meta-analysis. Neuromodulation. 2006;9:253–261. doi: 10.1111/j.1525-1403.2006.00067.x. PubMed DOI
Moro E, et al. Efficacy of pallidal stimulation in isolated dystonia: a systematic review and meta-analysis. Eur J Neurol. 2017;24:552–560. doi: 10.1111/ene.13255. PubMed DOI PMC
Coubes Philippe, Cif Laura, El Fertit Hassan, Hemm Simone, Vayssiere Nathalie, Serrat Stephanie, Picot Marie Christine, Tuffery Sylvie, Claustres Mireille, Echenne Bernard, Frerebeau Philippe. Electrical stimulation of the globus pallidus internus in patients with primary generalized dystonia: long-term results. Journal of Neurosurgery. 2004;101(2):189–194. doi: 10.3171/jns.2004.101.2.0189. PubMed DOI
Volkmann J, Benecke R. Deep brain stimulation for dystonia: patient selection and evaluation. Mov Disord. 2002;17(Suppl 3):S112–115. doi: 10.1002/mds.10151. PubMed DOI
McClelland VM, et al. Differences in globus pallidus neuronal firing rates and patterns relate to different disease biology in children with dystonia. J Neurol Neurosurg Psychiatry. 2016;87:958–967. doi: 10.1136/jnnp-2015-311803. PubMed DOI PMC
Vasques X, Cif L, Gonzalez V, Nicholson C, Coubes P. Factors predicting improvement in primary generalized dystonia treated by pallidal deep brain stimulation. Mov Disord. 2009;24:846–853. doi: 10.1002/mds.22433. PubMed DOI
Andrews C, Aviles-Olmos I, Hariz M, Foltynie T. Which patients with dystonia benefit from deep brain stimulation? A metaregression of individual patient outcomes. J Neurol Neurosurg Psychiatry. 2010;81:1383–1389. doi: 10.1136/jnnp.2010.207993. PubMed DOI
Chung Moonyoung, Huh Ryoong. Different clinical course of pallidal deep brain stimulation for phasic- and tonic-type cervical dystonia. Acta Neurochirurgica. 2015;158(1):171–180. doi: 10.1007/s00701-015-2646-7. PubMed DOI
Hallett M. Neurophysiology of dystonia: The role of inhibition. Neurobiol Dis. 2011;42:177–184. doi: 10.1016/j.nbd.2010.08.025. PubMed DOI PMC
Berardelli A, et al. The pathophysiology of primary dystonia. Brain. 1998;121:1195–1212. doi: 10.1093/brain/121.7.1195. PubMed DOI
Abbruzzese G, Marchese R, Buccolieri A, Gasparetto B, Trompetto C. Abnormalities of sensorimotor integration in focal dystonia: a transcranial magnetic stimulation study. Brain. 2001;124:537–545. doi: 10.1093/brain/124.3.537. PubMed DOI
Abbruzzese G, Berardelli A. Sensorimotor integration in movement disorders. Mov Disord. 2003;18:231–240. doi: 10.1002/mds.10327. PubMed DOI
Zheng ZZ, Pan PL, Wang W, Shang HF. Neural network of primary focal dystonia by an anatomic likelihood estimation meta-analysis of gray matter abnormalities. J Neurol Sci. 2012;316:51–55. doi: 10.1016/j.jns.2012.01.032. PubMed DOI
Garraux G, et al. Changes in brain anatomy in focal hand dystonia. Ann Neurol. 2004;55:736–739. doi: 10.1002/ana.20113. PubMed DOI
Egger K, et al. Voxel based morphometry reveals specific gray matter changes in primary dystonia. Mov Disord. 2007;22:1538–1542. doi: 10.1002/mds.21619. PubMed DOI
Obermann M, et al. Morphometric changes of sensorimotor structures in focal dystonia. Mov Disord. 2007;22:1117–1123. doi: 10.1002/mds.21495. PubMed DOI
Kujirai T, et al. Corticocortical inhibition in human motor cortex. J Physiol. 1993;471:501–519. doi: 10.1113/jphysiol.1993.sp019912. PubMed DOI PMC
Ziemann U, Rothwell JC, Ridding MC. Interaction between intracortical inhibition and facilitation in human motor cortex. J Physiol. 1996;496(Pt 3):873–881. doi: 10.1113/jphysiol.1996.sp021734. PubMed DOI PMC
Ridding MC, Sheean G, Rothwell JC, Inzelberg R, Kujirai T. Changes in the balance between motor cortical excitation and inhibition in focal, task specific dystonia. J Neurol Neurosurg Psychiatry. 1995;59:493–498. doi: 10.1136/jnnp.59.5.493. PubMed DOI PMC
Sommer M, et al. Intracortical excitability in the hand motor representation in hand dystonia and blepharospasm. Mov Disord. 2002;17:1017–1025. doi: 10.1002/mds.10205. PubMed DOI
Kuhn AA, et al. Modulation of motor cortex excitability by pallidal stimulation in patients with severe dystonia. Neurology. 2003;60:768–774. doi: 10.1212/01.WNL.0000044396.64752.4C. PubMed DOI
Ruge D, et al. Shaping reversibility? Long-term deep brain stimulation in dystonia: the relationship between effects on electrophysiology and clinical symptoms. Brain. 2011;134:2106–2115. doi: 10.1093/brain/awr122. PubMed DOI
Ruge D, et al. Longterm deep brain stimulation withdrawal: clinical stability despite electrophysiological instability. J Neurol Sci. 2014;342:197–199. doi: 10.1016/j.jns.2014.05.011. PubMed DOI
Wassermann, E. et al. Oxford Handbook of Transcranial Stimulation. (OUP Oxford, 2008).
Beck S, et al. Short intracortical and surround inhibition are selectively reduced during movement initiation in focal hand dystonia. J Neurosci. 2008;28:10363–10369. doi: 10.1523/JNEUROSCI.3564-08.2008. PubMed DOI PMC
Trompetto Carlo, Avanzino Laura, Marinelli Lucio, Mori Laura, Pelosin Elisa, Roccatagliata Luca, Abbruzzese Giovanni. Corticospinal excitability in patients with secondary dystonia due to focal lesions of the basal ganglia and thalamus. Clinical Neurophysiology. 2012;123(4):808–814. doi: 10.1016/j.clinph.2011.06.033. PubMed DOI
Ruge D, et al. Deep brain stimulation effects in dystonia: time course of electrophysiological changes in early treatment. Mov Disord. 2011;26:1913–1921. doi: 10.1002/mds.23731. PubMed DOI PMC
Orth M, Snijders AH, Rothwell JC. The variability of intracortical inhibition and facilitation. Clin Neurophysiol. 2003;114:2362–2369. doi: 10.1016/S1388-2457(03)00243-8. PubMed DOI
Draganski B, Thun-Hohenstein C, Bogdahn U, Winkler J, May A. “Motor circuit” gray matter changes in idiopathic cervical dystonia. Neurology. 2003;61:1228–1231. doi: 10.1212/01.WNL.0000094240.93745.83. PubMed DOI
Ramdhani RA, et al. What’s Special About Task in Dystonia? A Voxel-Based Morphometry and Diffusion Weighted Imaging Study. Mov Disord. 2014;29:1141–1150. doi: 10.1002/mds.25934. PubMed DOI PMC
Rodriguez-Raecke R, et al. Grey matter alterations in patients with Pantothenate Kinase-Associated Neurodegeneration (PKAN) Parkinsonism Relat Disord. 2014;20:975–979. doi: 10.1016/j.parkreldis.2014.06.005. PubMed DOI
Guehl D, et al. Primate models of dystonia. Prog Neurobiol. 2009;87:118–131. doi: 10.1016/j.pneurobio.2008.10.003. PubMed DOI
Shibasaki H. Cortical activities associated with voluntary movements and involuntary movements. Clin Neurophysiol. 2012;123:229–243. doi: 10.1016/j.clinph.2011.07.042. PubMed DOI
Jinnah, H. A. & Hess, E. J. Evolving concepts in the pathogenesis of dystonia. Parkinsonism Relat Disord (2017). PubMed PMC
Filip P, Lungu OV, Bares M. Dystonia and the cerebellum: a new field of interest in movement disorders? Clin Neurophysiol. 2013;124:1269–1276. doi: 10.1016/j.clinph.2013.01.003. PubMed DOI
Nachev P, Kennard C, Husain M. Functional role of the supplementary and pre-supplementary motor areas. Nat Rev Neurosci. 2008;9:856–869. doi: 10.1038/nrn2478. PubMed DOI
Dinomais M, et al. Functional MRI comparison of passive and active movement: possible inhibitory role of supplementary motor area. Neuroreport. 2009;20:1351–1355. doi: 10.1097/WNR.0b013e328330cd43. PubMed DOI
Vidailhet M, Grabli D, Roze E. Pathophysiology of dystonia. Curr Opin Neurol. 2009;22:406–413. doi: 10.1097/WCO.0b013e32832d9ef3. PubMed DOI
Cuny E, et al. Sensory motor mismatch within the supplementary motor area in the dystonic monkey. Neurobiol Dis. 2008;30:151–161. doi: 10.1016/j.nbd.2007.12.011. PubMed DOI
Oga T, et al. Abnormal cortical mechanisms of voluntary muscle relaxation in patients with writer’s cramp: an fMRI study. Brain. 2002;125:895–903. doi: 10.1093/brain/awf083. PubMed DOI
Havrankova P, et al. Repetitive TMS of the somatosensory cortex improves writer’s cramp and enhances cortical activity. Neuro Endocrinol Lett. 2010;31:73–86. PubMed
Coffman KA, Dum RP, Strick PL. Cerebellar vermis is a target of projections from the motor areas in the cerebral cortex. Proc Natl Acad Sci USA. 2011;108:16068–16073. doi: 10.1073/pnas.1107904108. PubMed DOI PMC
Allen GI, Tsukahara N. Cerebrocerebellar communication systems. Physiol Rev. 1974;54:957–1006. doi: 10.1152/physrev.1974.54.4.957. PubMed DOI
Argyelan M, et al. Cerebellothalamocortical connectivity regulates penetrance in dystonia. J Neurosci. 2009;29:9740–9747. doi: 10.1523/JNEUROSCI.2300-09.2009. PubMed DOI PMC
Fierro B, et al. Modulatory effects of 1 Hz rTMS over the cerebellum on motor cortex excitability. Exp Brain Res. 2007;176:440–447. doi: 10.1007/s00221-006-0628-y. PubMed DOI
Harrington A, Hammond-Tooke GD. Theta Burst Stimulation of the Cerebellum Modifies the TMS-Evoked N100 Potential, a Marker of GABA Inhibition. PLoS One. 2015;10:e0141284. doi: 10.1371/journal.pone.0141284. PubMed DOI PMC
Langguth B, et al. Modulating cerebello-thalamocortical pathways by neuronavigated cerebellar repetitive transcranial stimulation (rTMS) Neurophysiologie Clinique-Clinical Neurophysiology. 2008;38:289–295. doi: 10.1016/j.neucli.2008.08.003. PubMed DOI
Koch G, et al. Changes in intracortical circuits of the human motor cortex following theta burst stimulation of the lateral cerebellum. Clinical Neurophysiology. 2008;119:2559–2569. doi: 10.1016/j.clinph.2008.08.008. PubMed DOI
O’Reilly JX, Beckmann CF, Tomassini V, Ramnani N, Johansen-Berg H. Distinct and overlapping functional zones in the cerebellum defined by resting state functional connectivity. Cerebral Cortex. 2010;20:953–965. doi: 10.1093/cercor/bhp157. PubMed DOI PMC
Buckner RL, Krienen FM, Castellanos A, Diaz JC, Yeo BT. The organization of the human cerebellum estimated by intrinsic functional connectivity. J Neurophysiol. 2011;106:2322–2345. doi: 10.1152/jn.00339.2011. PubMed DOI PMC
Hess CW, Mills KR, Murray NM. Responses in small hand muscles from magnetic stimulation of the human brain. J Physiol. 1987;388:397–419. doi: 10.1113/jphysiol.1987.sp016621. PubMed DOI PMC
Hidding U, et al. MEP latency shift after implantation of deep brain stimulation systems in the subthalamic nucleus in patients with advanced Parkinson’s disease. Mov Disord. 2006;21:1471–1476. doi: 10.1002/mds.20951. PubMed DOI
Kuhn AA, Trottenberg T, Kupsch A, Meyer BU. Pseudo-bilateral hand motor responses evoked by transcranial magnetic stimulation in patients with deep brain stimulators. Clin Neurophysiol. 2002;113:341–345. doi: 10.1016/S1388-2457(01)00731-3. PubMed DOI
Burke D, et al. Direct comparison of corticospinal volleys in human subjects to transcranial magnetic and electrical stimulation. J Physiol. 1993;470:383–393. doi: 10.1113/jphysiol.1993.sp019864. PubMed DOI PMC
Di Lazzaro V, Ziemann U, Lemon RN. State of the art: Physiology of transcranial motor cortex stimulation. Brain Stimul. 2008;1:345–362. doi: 10.1016/j.brs.2008.07.004. PubMed DOI
Parent A, Hazrati LN. Functional anatomy of the basal ganglia. I. The cortico-basal ganglia-thalamo-cortical loop. Brain Res Brain Res Rev. 1995;20:91–127. doi: 10.1016/0165-0173(94)00007-C. PubMed DOI
Huang G, Mouraux A. MEP Latencies Predict the Neuromodulatory Effect of cTBS Delivered to the Ipsilateral and Contralateral Sensorimotor Cortex. PLoS One. 2015;10:e0133893. doi: 10.1371/journal.pone.0133893. PubMed DOI PMC
Hamada M, Murase N, Hasan A, Balaratnam M, Rothwell JC. The role of interneuron networks in driving human motor cortical plasticity. Cerebral Cortex. 2013;23:1593–1605. doi: 10.1093/cercor/bhs147. PubMed DOI
Deogaonkar, M. & Vitek, J. L. In Textbook of Stereotactic and functional Neurosurgery Vol. 2 (eds Lozano. A. M., Gildenbert P. L. & Tasker R. R.) 1577–1602 (Springer-Verlag, 2009).
Pietracupa S, et al. Scales for hyperkinetic disorders: A systematic review. J Neurol Sci. 2015;358:9–21. doi: 10.1016/j.jns.2015.08.1544. PubMed DOI
Chen R, Garg RR, Lozano AM, Lang AE. Effects of internal globus pallidus stimulation on motor cortex excitability. Neurology. 2001;56:716–723. doi: 10.1212/WNL.56.6.716. PubMed DOI
Kuhn AA, Huebl J. Safety of transcranial magnetic stimulation for the newer generation of deep brain stimulators. Parkinsonism Relat Disord. 2011;17:647–648. doi: 10.1016/j.parkreldis.2011.05.007. PubMed DOI
Hodges PW, Bui BH. A comparison of computer-based methods for the determination of onset of muscle contraction using electromyography. Electroencephalogr Clin Neurophysiol. 1996;101:511–519. PubMed
Micera S, Vannozzi G, Sabatini AM, Dario P. Improving detection of muscle activation intervals. Ieee Engineering in Medicine and Biology Magazine. 2001;20:38–46. doi: 10.1109/51.982274. PubMed DOI
Rezai AR, et al. Neurostimulation system used for deep brain stimulation (DBS): MR safety issues and implications of failing to follow safety recommendations. Invest Radiol. 2004;39:300–303. doi: 10.1097/01.rli.0000124940.02340.ab. PubMed DOI
Kahan J, et al. The Safety of Using Body-Transmit MRI in Patients with Implanted Deep Brain Stimulation Devices. PLoS One. 2015;10:e0129077. doi: 10.1371/journal.pone.0129077. PubMed DOI PMC
Ashburner J. A fast diffeomorphic image registration algorithm. Neuroimage. 2007;38:95–113. doi: 10.1016/j.neuroimage.2007.07.007. PubMed DOI