The reorganization of motor network in hemidystonia from the perspective of deep brain stimulation
- 362 Downloads
Hemidystonia is usually ‘secondary’ to structural lesions within the cortico-striato-pallido-thalamic or the cerebello-thalamo-cortical loops. Globus pallidus internus Deep Brain Stimulation (GPi DBS) is a validated technique in the treatment of primary dystonia and still under assessment for secondary dystonia. Results of DBS in hemidystonia are limited and heterogeneous. Further knowledge concerning motor network organization after focal brain lesions might contribute to the understanding of this mitigated response to DBS and to the refinement of DBS indications and techniques in secondary dystonia. This study aimed to identify movement-related functional magnetic resonance imaging (fMRI) activation patterns in a group of hemidystonic patients in comparison to healthy controls (HC). Further analysis assessed recruitment pattern in different patient subgroups defined according to clinical and radiological criteria relevant to GPi DBS eligibility (hyperkinetic/hypokinetic and prepallidal/postpallidal). Eleven patients and nine HC underwent fMRI with a block-design alternating active and rest conditions. The motor paradigm consisted of self-paced elbow flexion-extension movements. The main results were as follows: single-subject studies revealed several activation patterns involving motor-related network regions; both ipsilesional and contralesional hemispheres showed abnormal patterns of activity; compared with HC, hemidystonic patients showed decreased brain activity in ipsilesional thalamus, pallidal and temporal areas during affected arm task execution; ‘hypokinetic’ subgroup was commonly related to widespread bilateral overactivity. This study provides additional arguments for case-by-case assessment of DBS surgery indication and target selection in hemidystonia. Single-lead approach might be unable to modulate a highly disorganized network activity in certain patients with this clinical syndrome.
KeywordsHemidystonia Secondary dystonia Functional MRI Deep brain stimulation
The authors thank also the patients and the families who participated in the study.
Conflict of interest
Financial disclosure related to research covered in this article: No conflict of interest related to this work is reported by the authors.
Full financial disclosure: V. Gonzalez, L. Cif and P. Coubes received lecture fees from Medtronic Company. E. Le Bars, L. EH van Dokkum, I. Laffont, N. Menjot de Champfleur, A. Bonafé and M. Zanca: report no disclosures.
This research has been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki. Informed written consent was provided by all subjects participating in the study.
- Didelot, A., Mauguière, F., Redouté, J., Bouvard, S., Lothe, A., Reilhac, A., et al. (2010). Voxel-based analysis of asymmetry index maps increases the specificity of 18F-MPPF PET abnormalities for localizing the epileptogenic zone in temporal lobe epilepsies. Journal of Nuclear Medicine, 51(11), 1732–1739. doi: 10.2967/jnumed.109.070938.CrossRefPubMedGoogle Scholar
- Eltahawy, H. A., Saint-Cyr, J., Giladi, N., Lang, A. E., & Lozano, A. M. (2004). Primary dystonia is more responsive than secondary dystonia to pallidal interventions: outcome after pallidotomy or pallidal deep brain stimulation. Neurosurgery, 54(3), 613–619. discussion 619–621.CrossRefPubMedGoogle Scholar
- Islam, T., Kupsch, A., Bruhn, H., Scheurig, C., Schmidt, S., & Hoffmann, K. T. (2009). Decreased bilateral cortical representation patterns in writer’s cramp: a functional magnetic resonance imaging study at 3.0 T. Neurological Sciences, 30(3), 219–226. doi: 10.1007/s10072-009-0045-7.CrossRefPubMedGoogle Scholar
- Johansen-Berg, H., Rushworth, M. F., Bogdanovic, M. D., Kischka, U., Wimalaratna, S., & Matthews, P. M. (2002). The role of ipsilateral premotor cortex in hand movement after stroke. Proceedings of the National Academy of Sciences of the United States of America, 99(22), 14518–14523. doi: 10.1073/pnas.222536799.CrossRefPubMedCentralPubMedGoogle Scholar
- Kahan, J., Mancini, L., Urner, M., Friston, K., Hariz, M., Holl, E., et al. (2012). Therapeutic subthalamic nucleus deep brain stimulation reverses cortico-thalamic coupling during voluntary movements in Parkinson’s disease. PLoS One, 7(12), e50270. doi: 10.1371/journal.pone.0050270.CrossRefPubMedCentralPubMedGoogle Scholar
- Manto, M., Bower, J. M., Conforto, A. B., Delgado-García, J. M., da Guarda, S. N., Gerwig, M., et al. (2012). Consensus paper: roles of the cerebellum in motor control–the diversity of ideas on cerebellar involvement in movement. Cerebellum, 11(2), 457–487. doi: 10.1007/s12311-011-0331-9.CrossRefPubMedCentralPubMedGoogle Scholar
- McClelland, V., Mills, K., Siddiqui, A., Selway, R., & Lin, J. P. (2011). Central motor conduction studies and diagnostic magnetic resonance imaging in children with severe primary and secondary dystonia. Developmental Medicine and Child Neurology, 53(8), 757–763. doi: 10.1111/j.1469-8749.2011.03981.x.CrossRefPubMedGoogle Scholar
- Thobois, S., Ballanger, B., Xie-Brustolin, J., Damier, P., Durif, F., Azulay, J. P., et al. (2008). Globus pallidus stimulation reduces frontal hyperactivity in tardive dystonia. Journal of Cerebral Blood Flow and Metabolism, 28(6), 1127–1138. doi: 10.1038/sj.jcbfm.9600610.CrossRefPubMedGoogle Scholar
- Vidailhet, M., Yelnik, J., Lagrange, C., Fraix, V., Grabli, D., Thobois, S., et al. (2009). Bilateral pallidal deep brain stimulation for the treatment of patients with dystonia-choreoathetosis cerebral palsy: a prospective pilot study. Lancet Neurology, 8(8), 709–717. doi: 10.1016/S1474-4422(09)70151-6.CrossRefGoogle Scholar
- Wu, C. C., Fairhall, S. L., McNair, N. A., Hamm, J. P., Kirk, I. J., Cunnington, R., et al. (2010). Impaired sensorimotor integration in focal hand dystonia patients in the absence of symptoms. Journal of Neurology, Neurosurgery & Psychiatry, 81(6), 659–665. doi: 10.1136/jnnp.2009.185637.CrossRefGoogle Scholar