Advertisement

Brain Imaging and Behavior

, Volume 11, Issue 4, pp 1139–1153 | Cite as

Subthalamic nucleus stimulation effects on single and combined task performance in Parkinson’s disease patients: a PET study

  • Cyril Atkinson-Clement
  • Audrey Maillet
  • Didier LeBars
  • Franck Lavenne
  • Jérôme Redouté
  • Alexandre Krainik
  • Pierre Pollak
  • Stéphane Thobois
  • Serge PintoEmail author
Original Research

Abstract

Subthalamic nucleus deep brain stimulation (STN-DBS) represents one of the most efficacious treatments for Parkinson’s disease, along with L-dopa therapy. The objective of the present work was to identify the cerebral networks associated with hand movement and speech production tasks performed alone and simultaneously, as well as the effects of STN-DBS on these profiles. Clinical, behavioral, and neuroimaging (oxygen 15-labeled water and Positron Emission Tomography) investigations were used to study single and combined performances of unilateral hand movements and speech production in 11 unmedicated individuals with PD, both off and on STN-DBS. Specifically, a flexible factorial design with the tasks (hand movement, speech production, combined task) and the STN-DBS conditions (off, on) as main factors was chosen for brain activation statistical analysis, using a Family-Wise Error corrected p-value at the cluster level of at least 10 contiguous voxels. Increased activation of fronto-parietal and cingulate areas was observed under STN-DBS for hand movement in single and combined tasks, respectively, reflecting a partial restoration of cortico-sub-cortical connections. The lack of results for speech production for both off and on STN-DBS could illustrate its relatively poor response to the treatment. STN-DBS tended to restore the additive function capacity that can be achieved when performing the combined task. We confirmed with original neuroimaging data that speech is much less responsive to STN-DBS than any other motor function and we concluded that speech outcomes following STN-DBS can be different from those observed pre-operatively following L-dopa administration.

Keywords

Deep brain stimulation Hand movement Neuroimaging Parkinson’s disease Speech Subthalamic nucleus 

Notes

Acknowledgments

The authors wish to thank all the patients who participated in this study. They also wish to thank the PET/CERMEP team (Véronique Berthier, Jamila Lagha, Christian Tourvielle, Fabienne Vey, Christine Vighi, Luc Zimmer) for their helpful support. The authors also thank Ms. Mignard for revising the English of the manuscript.

Compliance with ethical standards

Funding

This study was supported financially by the French Health Ministry (Programme Hospitalier de Recherche Clinique, PHRC 2005). The authors declared that no competing interests exist: the funders had no role in study design, data collection, analyses, decision to publish, or preparation of the manuscript. C. A-C. wishes to thank the PACA Regional Council and Orthomalin© (Ph.D. grant scheme co-funders). A.M. also wishes to thank the Labex Cortex and the Fondation Neurodis for financial support.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all individual participants included in the study.

References

  1. Ackermann, H., Hage, S. R., & Ziegler, W. (2014). Brain mechanisms of acoustic communication in humans and nonhuman primates: An evolutionary perspective. Behavioral and Brain Sciences, 37(6),529–546.Google Scholar
  2. Agid, Y., Graybiel, A. M., Ruberg, M., Hirsch, E., Blin, J., Dubois, B., & Javoy-Agid, F. (1990). The efficacy of levodopa treatment declines in the course of Parkinson’s disease: do nondopaminergic lesions play a role? Advances in Neurology, 53, 83–100.PubMedGoogle Scholar
  3. Altmann, L. J. P., Stegemöller, E., Hazamy, A. A., Wilson, J. P., Okun, M. S., McFarland, N. R., et al. (2015). Unexpected Dual Task Benefits on Cycling in Parkinson Disease and Healthy Adults: A Neuro-Behavioral Model. Plos One, 10(5), e0125470.PubMedPubMedCentralCrossRefGoogle Scholar
  4. Aman, J. E., Abosch, A., Bebler, M., Lu, C.-H., & Konczak, J. (2014). Subthalamic nucleus deep brain stimulation improves somatosensory function in Parkinson’s disease: STN-DBS Improves Haptic Perception in PD. Movement Disorders: Official Journal of the Movement Disorder Society, 29(2), 221–228.CrossRefGoogle Scholar
  5. Ashburner, J., & Friston, K. (1997). Multimodal image coregistration and partitioning--a unified framework. NeuroImage, 6(3), 209–217.PubMedCrossRefGoogle Scholar
  6. Åström, M., Tripoliti, E., Hariz, M. I., Zrinzo, L. U., Martinez-Torres, I., Limousin, P., & Wårdell, K. (2010). Patient-specific model-based investigation of speech intelligibility and movement during deep brain stimulation. Stereotactic and Functional Neurosurgery, 88(4), 224–233.PubMedPubMedCentralCrossRefGoogle Scholar
  7. Ballanger, B., van Eimeren, T., Moro, E., Lozano, A. M., Hamani, C., Boulinguez, P., et al. (2009). Stimulation of the subthalamic nucleus and impulsivity: release your horses. Annals of Neurology, 66(6), 817–824.PubMedPubMedCentralCrossRefGoogle Scholar
  8. Beauchet, O., Annweiler, C., Dubost, V., Allali, G., Kressig, R. W., Bridenbaugh, S., et al. (2009). Stops walking when talking: a predictor of falls in older adults? European Journal of Neurology: The Official Journal of the European Federation of Neurological. Societies, 16(7), 786–795.Google Scholar
  9. Boulinguez, P., Jaffard, M., Granjon, L., & Benraiss, A. (2008). Warning Signals Induce Automatic EMG Activations and Proactive Volitional Inhibition: Evidence From Analysis of Error Distribution in Simple RT. Journal of Neurophysiology, 99(3), 1572–1578.PubMedCrossRefGoogle Scholar
  10. Boulinguez, P., Ballanger, B., Granjon, L., & Benraiss, A. (2009). The paradoxical effect of warning on reaction time: Demonstrating proactive response inhibition with event-related potentials. Clinical Neurophysiology, 120(4), 730–737. CrossRefGoogle Scholar
  11. Braak, H., Braak, E., Yilmazer, D., Schultz, C., de Vos, R. A., & Jansen, E. N. (1995). Nigral and extranigral pathology in Parkinson’s disease. Journal of Neural Transmission. Supplementum, 46, 15–31.PubMedGoogle Scholar
  12. Bradberry, T. J., Metman, L. V., Contreras-Vidal, J. L., van den Munckhof, P., Hosey, L. A., Thompson, J. L. W., et al. (2012). Common and unique responses to dopamine agonist therapy and deep brain stimulation in Parkinson’s disease: an H215O PET study. Brain Stimulation, 5(4), 605–615.PubMedCrossRefGoogle Scholar
  13. Bunton, K., & Keintz, C. K. (2008). The use of a dual-task paradigm for assessing speech intelligibility in clients with Parkinson disease. Journal of Medical Speech-Language Pathology, 16(3), 141–155.PubMedPubMedCentralGoogle Scholar
  14. Ceballos-Baumann, A. O., Boecker, H., Bartenstein, P., von Falkenhayn, I., Riescher, H., Conrad, B., et al. (1999). A positron emission tomographic study of subthalamic nucleus stimulation in Parkinson disease: enhanced movement-related activity of motor-association cortex and decreased motor cortex resting activity. Archives of Neurology, 56(8), 997–1003.PubMedCrossRefGoogle Scholar
  15. Dromey, C., Jarvis, E., Sondrup, S., Nissen, S., Foreman, K. B., & Dibble, L. E. (2010). Bidirectional interference between speech and postural stability in individuals with Parkinson’s disease. International Journal of Speech-Language Pathology, 12(5), 446–454.Google Scholar
  16. Enderby, P., Palmer, R. (2008). Frenchay Dysarthria Assessment. 2nd Edition. (FDA-2). Austin, Texas: Pro-ED.Google Scholar
  17. Fahn, S., Elton, R., & Members of the UPDRS Development Committee. (1987). Recent developments in Parkinson’s Disease (Vol. 2). Florham Park: Macmillan Health Care Information. http://img.medscape.com/fullsize/701/816/58977_UPDRS.pdf. Accessed 18 September 2015
  18. Faw, B. (2003). Pre-frontal executive committee for perception, working memory, attention, long-term memory, motor control, and thinking: a tutorial review. Consciousness and Cognition, 12(1), 83–139.PubMedCrossRefGoogle Scholar
  19. Fernández-Seara, M. A., Mengual, E., Vidorreta, M., Castellanos, G., Irigoyen, J., Erro, E., & Pastor, M. A. (2015). Resting state functional connectivity of the subthalamic nucleus in Parkinson’s disease assessed using arterial spin-labeled perfusion fMRI: ASL Functional Connectivity of the STN in PD. Human Brain Mapping, 36(5), 1937–1950.PubMedCrossRefGoogle Scholar
  20. Frank, M. J. (2006). Hold your horses: a dynamic computational role for the subthalamic nucleus in decision making. Neural Networks: The Official Journal of the International Neural Network Society, 19(8), 1120–1136.CrossRefGoogle Scholar
  21. Frank, M. J., Samanta, J., Moustafa, A. A., & Sherman, S. J. (2007). Hold your horses: impulsivity, deep brain stimulation, and medication in parkinsonism. Science (New York, N.Y.), 318(5854), 1309–1312.CrossRefGoogle Scholar
  22. Friston, K. J., Holmes, A. P., Worsley, K. J., Poline, J.-P., Frith, C. D., & Frackowiak, R. S. J. (1994). Statistical parametric maps in functional imaging: A general linear approach. Human Brain Mapping, 2(4), 189–210.CrossRefGoogle Scholar
  23. Frost, E., Tripoliti, E., Hariz, M. I., Pring, T., & Limousin, P. (2010). Self-perception of speech changes in patients with Parkinson’s disease following deep brain stimulation of the subthalamic nucleus. International Journal of Speech-Language Pathology, 12(5), 399–404.PubMedCrossRefGoogle Scholar
  24. Gibb, W. R., & Lees, A. J. (1988). A comparison of clinical and pathological features of young- and old-onset Parkinson’s disease. Neurology, 38(9), 1402–1406.PubMedCrossRefGoogle Scholar
  25. Gousias, I. S., Rueckert, D., Heckemann, R. A., Dyet, L. E., Boardman, J. P., Edwards, A. D., & Hammers, A. (2008). Automatic segmentation of brain MRIs of 2-year-olds into 83 regions of interest. NeuroImage, 40(2), 672–684.PubMedCrossRefGoogle Scholar
  26. Grossman, M., Crino, P., Reivich, M., Stern, M. B., & Hurtig, H. I. (1992). Attention and sentence processing deficits in Parkinson’s disease: the role of anterior cingulate cortex. Cerebral Cortex (New York, N.Y.: 1991), 2(6), 513–525.CrossRefGoogle Scholar
  27. Halliday, G., Lees, A., & Stern, M. (2011). Milestones in Parkinson’s disease-Clinical and pathologic features. Movement Disorders: Official Journal of the Movement Disorder Society, 26(6), 1015–1021.CrossRefGoogle Scholar
  28. Hammers, A., Allom, R., Koepp, M. J., Free, S. L., Myers, R., Lemieux, L., et al. (2003). Three-dimensional maximum probability atlas of the human brain, with particular reference to the temporal lobe. Human Brain Mapping, 19(4), 224–247.PubMedCrossRefGoogle Scholar
  29. Ho, A. K., Iansek, R., & Bradshaw, J. L. (2002). The effect of a concurrent task on Parkinsonian speech. Journal of Clinical and Experimental Neuropsychology, 24(1), 36–47.PubMedCrossRefGoogle Scholar
  30. Iansek, R., Huxham, F., & McGinley, J. (2006). The sequence effect and gait festination in Parkinson disease: contributors to freezing of gait? Movement Disorders: Official Journal of the Movement Disorder Society, 21(9), 1419–1424.CrossRefGoogle Scholar
  31. Jahanshahi, M., Jenkins, I. H., Brown, R. G., Marsden, C. D., Passingham, R. E., & Brooks, D. J. (1995). Self-initiated versus externally triggered movements. I. An investigation using measurement of regional cerebral blood flow with PET and movement-related potentials in normal and Parkinson’s disease subjects. Brain: A Journal of Neurology, 118(Pt 4), 913–933.CrossRefGoogle Scholar
  32. Jenkins, I. H., Fernandez, W., Playford, E. D., Lees, A. J., Frackowiak, R. S., Passingham, R. E., & Brooks, D. J. (1992). Impaired activation of the supplementary motor area in Parkinson’s disease is reversed when akinesia is treated with apomorphine. Annals of Neurology, 32(6), 749–757.PubMedCrossRefGoogle Scholar
  33. Knight, E. J., Testini, P., Min, H.-K., Gibson, W. S., Gorny, K. R., Favazza, C. P., et al. (2015). Motor and Nonmotor circuitry activation induced by subthalamic nucleus deep brain stimulation in patients with Parkinson disease. Mayo Clinic Proceedings, 90(6), 773–785.PubMedPubMedCentralCrossRefGoogle Scholar
  34. Kosaka, K., Tsuchiya, K., & Yoshimura, M. (1988). Lewy body disease with and without dementia: a clinicopathological study of 35 cases. Clinical Neuropathology, 7(6), 299–305.PubMedGoogle Scholar
  35. Krack, P., Hariz, M. I., Baunez, C., Guridi, J., & Obeso, J. A. (2010). Deep brain stimulation: from neurology to psychiatry? Trends in Neurosciences, 33(10), 474–484.PubMedCrossRefGoogle Scholar
  36. Langston, J. W., Widner, H., Goetz, C. G., Brooks, D., Fahn, S., Freeman, T., & Watts, R. (1992). Core assessment program for intracerebral transplantations (CAPIT). Movement Disorders: Official Journal of the Movement Disorder Society, 7(1), 2–13.CrossRefGoogle Scholar
  37. LaPointe, L. L., Stierwalt, J. A. G., & Maitland, C. G. (2010). Talking while walking: Cognitive loading and injurious falls in Parkinson’s disease. International Journal of Speech-Language Pathology, 12(5), 455–459.Google Scholar
  38. Lee, E., Lee, J. E., Yoo, K., Hong, J. Y., Oh, J., Sunwoo, M. K., et al. (2014). Neural correlates of progressive reduction of bradykinesia in de novo Parkinson’s disease. Parkinsonism & Related Disorders, 20(12), 1376–1381.CrossRefGoogle Scholar
  39. Limousin, P., Greene, J., Pollak, P., Rothwell, J., Benabid, A. L., & Frackowiak, R. (1997). Changes in cerebral activity pattern due to subthalamic nucleus or internal pallidum stimulation in Parkinson’s disease. Annals of Neurology, 42(3), 283–291.PubMedCrossRefGoogle Scholar
  40. Liotti, M., Ramig, L. O., Vogel, D., New, P., Cook, C. I., Ingham, R. J., et al. (2003). Hypophonia in Parkinson’s disease: neural correlates of voice treatment revealed by PET. Neurology, 60(3), 432–440.PubMedCrossRefGoogle Scholar
  41. Maillet, A., Krainik, A., Debû, B., Troprès, I., Lagrange, C., Thobois, S., et al. (2012). Levodopa effects on hand and speech movements in patients with Parkinson’s disease: a fMRI study. PloS One, 7(10), e46541.PubMedPubMedCentralCrossRefGoogle Scholar
  42. McIntyre, C. C., Savasta, M., Walter, B. L., & Vitek, J. L. (2004). How does deep brain stimulation work? Present understanding and future questions. Journal of Clinical Neurophysiology: Official Publication of the American Electroencephalographic Society, 21(1), 40–50.CrossRefGoogle Scholar
  43. Narayana, S., Jacks, A., Robin, D. A., Poizner, H., Zhang, W., Franklin, C., et al. (2009). A noninvasive imaging approach to understanding speech changes following deep brain stimulation in Parkinson’s disease. American Journal of Speech-Language Pathology, 18(2), 146–161.PubMedCrossRefGoogle Scholar
  44. Narayana, S., Fox, P. T., Zhang, W., Franklin, C., Robin, D. A., Vogel, D., & Ramig, L. O. (2010). Neural correlates of efficacy of voice therapy in Parkinson’s disease identified by performance-correlation analysis. Human Brain Mapping, 31(2), 222–236.PubMedPubMedCentralGoogle Scholar
  45. Obeso, I., Wilkinson, L., Rodríguez-Oroz, M.-C., Obeso, J. A., & Jahanshahi, M. (2013). Bilateral stimulation of the subthalamic nucleus has differential effects on reactive and proactive inhibition and conflict-induced slowing in Parkinson’s disease. Experimental Brain Research, 226(3), 451–462.PubMedCrossRefGoogle Scholar
  46. Obeso, I., Wilkinson, L., Casabona, E., Speekenbrink, M., Luisa Bringas, M., Alvarez, M., et al. (2014). The subthalamic nucleus and inhibitory control: impact of subthalamotomy in Parkinson’s disease. Brain: A Journal of Neurology, 137(5), 1470–1480.CrossRefGoogle Scholar
  47. Oldfield, R. C. (1971). The assessment and analysis of handedness: the Edinburgh inventory. Neuropsychologia, 9(1), 97–113.PubMedCrossRefGoogle Scholar
  48. Paschali, A., Constantoyannis, C., Angelatou, F., & Vassilakos, P. (2013). Perfusion brain SPECT in assessing motor improvement after deep brain stimulation in Parkinson’s disease. Acta Neurochirurgica, 155(3), 497–505.PubMedCrossRefGoogle Scholar
  49. Peterson, D. S., Fling, B. W., Mancini, M., Cohen, R. G., Nutt, J. G., & Horak, F. B. (2015). Dual-task interference and brain structural connectivity in people with Parkinson’s disease who freeze. Journal of Neurology, Neurosurgery & Psychiatry, 86(7), 786–792.CrossRefGoogle Scholar
  50. Pinto, S., Thobois, S., Costes, N., Le Bars, D., Benabid, A.-L., Broussolle, E., et al. (2004). Subthalamic nucleus stimulation and dysarthria in Parkinson’s disease: a PET study. Brain: A Journal of Neurology, 127(Pt 3), 602–615.Google Scholar
  51. Pinto, S., Gentil, M., Krack, P., Sauleau, P., Fraix, V., Benabid, A.-L., & Pollak, P. (2005). Changes induced by levodopa and subthalamic nucleus stimulation on parkinsonian speech. Movement Disorders: Official Journal of the Movement Disorder Society, 20(11), 1507–1515. CrossRefGoogle Scholar
  52. Pinto, S., Mancini, L., Jahanshahi, M., Thornton, J. S., Tripoliti, E., Yousry, T. A., & Limousin, P. (2011). Functional magnetic resonance imaging exploration of combined hand and speech movements in Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 26(12), 2212–2219.CrossRefGoogle Scholar
  53. Pinto, S., Ferraye, M., Espesser, R., Fraix, V., Maillet, A., Guirchoum, J., et al. (2014). Stimulation of the pedunculopontine nucleus area in Parkinson’s disease: effects on speech and intelligibility. Brain: A Journal of Neurology, 137(10), 2759–2772.CrossRefGoogle Scholar
  54. Playford, E. D., Jenkins, I. H., Passingham, R. E., Nutt, J., Frackowiak, R. S., & Brooks, D. J. (1992). Impaired mesial frontal and putamen activation in Parkinson’s disease: a positron emission tomography study. Annals of Neurology, 32(2), 151–161. PubMedCrossRefGoogle Scholar
  55. Polito, C., Berti, V., Ramat, S., Vanzi, E., De Cristofaro, M. T., Pellicanò, G., et al. (2012). Interaction of caudate dopamine depletion and brain metabolic changes with cognitive dysfunction in early Parkinson’s disease. Neurobiology of Aging, 33(1), 206.e29–206.e39. CrossRefGoogle Scholar
  56. R Core Team. (2013). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. http://www.R-project.org/.
  57. Rascol, O., Sabatini, U., Chollet, F., Celsis, P., Montastruc, J. L., Marc-Vergnes, J. P., & Rascol, A. (1992). Supplementary and primary sensory motor area activity in Parkinson’s disease. Regional cerebral blood flow changes during finger movements and effects of apomorphine. Archives of Neurology, 49(2), 144–148.PubMedCrossRefGoogle Scholar
  58. Rascol, O., Sabatini, U., Fabre, N., Brefel, C., Loubinoux, I., Celsis, P., et al. (1997). The ipsilateral cerebellar hemisphere is overactive during hand movements in akinetic parkinsonian patients. Brain: A Journal of Neurology, 120(Pt 1), 103–110.CrossRefGoogle Scholar
  59. Rektorova, I., Barrett, J., Mikl, M., Rektor, I., & Paus, T. (2007). Functional abnormalities in the primary orofacial sensorimotor cortex during speech in Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 22(14), 2043–2051. CrossRefGoogle Scholar
  60. Rochester, L., Nieuwboer, A., Baker, K., Hetherington, V., Willems, A.-M., Kwakkel, G., et al. (2008). Walking speed during single and dual tasks in Parkinson’s disease: which characteristics are important? Movement Disorders: Official Journal of the Movement Disorder Society, 23(16), 2312–2318.CrossRefGoogle Scholar
  61. Sabatini, U., Boulanouar, K., Fabre, N., Martin, F., Carel, C., Colonnese, C., et al. (2000). Cortical motor reorganization in akinetic patients with Parkinson’s disease: a functional MRI study. Brain: A Journal of Neurology, 123(Pt 2), 394–403.CrossRefGoogle Scholar
  62. Samuel, M., Ceballos-Baumann, A. O., Blin, J., Uema, T., Boecker, H., Passingham, R. E., & Brooks, D. J. (1997). Evidence for lateral premotor and parietal overactivity in Parkinson’s disease during sequential and bimanual movements. A PET study. Brain: A Journal of Neurology, 120(Pt 6), 963–976.CrossRefGoogle Scholar
  63. Sestini, S., Pupi, A., Ammannati, F., Silvia, R., Sorbi, S., & Castagnoli, A. (2007). Are there adaptive changes in the human brain of patients with Parkinson’s disease treated with long-term deep brain stimulation of the subthalamic nucleus? A 4-year follow-up study with regional cerebral blood flow SPECT. European Journal of Nuclear Medicine and Molecular Imaging, 34(10), 1646–1657. CrossRefGoogle Scholar
  64. Strouwen, C., Molenaar, E. A., Keus, S. H., Münks, L., Munneke, M., Vandenberghe, W., et al. (2014). Protocol for a randomized comparison of integrated versus consecutive dual task practice in Parkinson’s disease: the DUALITY trial. BMC Neurology, 14(1), 61.PubMedPubMedCentralCrossRefGoogle Scholar
  65. Temperli, P., Ghika, J., Villemure, J.-G., Burkhard, P. R., Bogousslavsky, J., & Vingerhoets, F. J. G. (2003). How do parkinsonian signs return after discontinuation of subthalamic DBS? Neurology, 60(1), 78–81.PubMedCrossRefGoogle Scholar
  66. Thobois, S., Dominey, P., Decety, J., Pollak, P., Gregoire, M. C., & Broussolle, E. (2000). Overactivation of primary motor cortex is asymmetrical in hemiparkinsonian patients. Neuroreport, 11(4), 785–789.PubMedCrossRefGoogle Scholar
  67. Thobois, S., Tisch, S., Xie-Brustolin, J., Mertens, P., Hariz, M. I., Benatru, I., et al. (2005). Can chronic subthalamic nucleus stimulation induce de novo tremor in Parkinson’s disease? Movement Disorders: Official Journal of the Movement Disorder Society, 20(8), 1066–1069. CrossRefGoogle Scholar
  68. Thobois, S., Hotton, G. R., Pinto, S., Wilkinson, L., Limousin-Dowsey, P., Brooks, D. J., & Jahanshahi, M. (2007). STN stimulation alters pallidal-frontal coupling during response selection under competition. Journal of Cerebral Blood Flow and Metabolism: Official Journal of the International Society of Cerebral Blood Flow and Metabolism,, 27(6), 1173–1184. CrossRefGoogle Scholar
  69. Tripoliti, E., Zrinzo, L., Martinez-Torres, I., Tisch, S., Frost, E., Borrell, E., et al. (2008). Effects of contact location and voltage amplitude on speech and movement in bilateral subthalamic nucleus deep brain stimulation. Movement Disorders: Official Journal of the Movement Disorder Society, 23(16), 2377–2383. CrossRefGoogle Scholar
  70. Tripoliti, E., Strong, L., Hickey, F., Foltynie, T., Zrinzo, L., Candelario, J., et al. (2011a). Treatment of dysarthria following subthalamic nucleus deep brain stimulation for Parkinson’s disease. Movement Disorders: Official Journal of the Movement Disorder Society, 26(13), 2434–2436.CrossRefGoogle Scholar
  71. Tripoliti, E., Zrinzo, L., Martinez-Torres, I., Frost, E., Pinto, S., Foltynie, T., et al. (2011b). Effects of subthalamic stimulation on speech of consecutive patients with Parkinson disease. Neurology, 76(1), 80–86.PubMedCrossRefGoogle Scholar
  72. Tripoliti, E., Limousin, P., Foltynie, T., Candelario, J., Aviles-Olmos, I., Hariz, M. I., & Zrinzo, L. (2014). Predictive factors of speech intelligibility following subthalamic nucleus stimulation in consecutive patients with Parkinson’s disease: Speech Intelligibility after STN-DBS. Movement Disorders: Official Journal of the Movement Disorder Society, 29(4), 532–538. CrossRefGoogle Scholar
  73. Tsuboi, T., Watanabe, H., Tanaka, Y., Ohdake, R., Yoneyama, N., Hara, K., et al. (2015). Distinct phenotypes of speech and voice disorders in Parkinson’s disease after subthalamic nucleus deep brain stimulation. Journal of Neurology, Neurosurgery, and Psychiatry, 86(8), 856–864.PubMedCrossRefGoogle Scholar
  74. Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15(1), 273–289.PubMedCrossRefGoogle Scholar
  75. Wagle Shukla, A., Moro, E., Gunraj, C., Lozano, A., Hodaie, M., Lang, A., & Chen, R. (2013). Long-term subthalamic nucleus stimulation improves sensorimotor integration and proprioception. Journal of Neurology, Neurosurgery & Psychiatry, 84(9), 1020–1028.CrossRefGoogle Scholar
  76. World Medical Association General Assembly. (2004). Declaration of Helsinki, Amendment. http://www.wma.net/en/30publications/10policies/b3/17c.pdf. Accessed 18 September 2015
  77. Wu, T., & Hallett, M. (2005). A functional MRI study of automatic movements in patients with Parkinson’s disease. Brain: A Journal of Neurology, 128(Pt 10), 2250–2259. CrossRefGoogle Scholar
  78. Wu, T., & Hallett, M. (2008). Neural correlates of dual task performance in patients with Parkinson’s disease. Journal of Neurology, Neurosurgery, and Psychiatry, 79(7), 760–766.PubMedCrossRefGoogle Scholar
  79. Wu, T., Wang, L., Hallett, M., Li, K., & Chan, P. (2010). Neural correlates of bimanual anti-phase and in-phase movements in Parkinson’s disease. Brain: A Journal of Neurology, 133(8), 2394–2409.CrossRefGoogle Scholar
  80. Wu, T., Wang, L., Hallett, M., Chen, Y., Li, K., & Chan, P. (2011). Effective connectivity of brain networks during self-initiated movement in Parkinson’s disease. NeuroImage, 55(1), 204–215.PubMedCrossRefGoogle Scholar
  81. Yu, H., Sternad, D., Corcos, D. M., & Vaillancourt, D. E. (2007). Role of hyperactive cerebellum and motor cortex in Parkinson’s disease. NeuroImage, 35(1), 222–233.PubMedPubMedCentralCrossRefGoogle Scholar
  82. Zgaljardic, D. J., Borod, J. C., Foldi, N. S., & Mattis, P. (2003). A review of the cognitive and behavioral sequelae of Parkinson’s disease: relationship to frontostriatal circuitry. Cognitive and Behavioral Neurology: Official Journal of the Society for Behavioral and Cognitive Neurology, 16(4), 193–210.CrossRefGoogle Scholar
  83. Zgaljardic, D. J., Borod, J. C., Foldi, N. S., Mattis, P. J., Gordon, M. F., Feigin, A., & Eidelberg, D. (2006). An examination of executive dysfunction associated with frontostriatal circuitry in Parkinson’s disease. Journal of Clinical and Experimental Neuropsychology, 28(7), 1127–1144.PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Cyril Atkinson-Clement
    • 1
  • Audrey Maillet
    • 2
  • Didier LeBars
    • 3
  • Franck Lavenne
    • 3
  • Jérôme Redouté
    • 3
  • Alexandre Krainik
    • 4
    • 5
  • Pierre Pollak
    • 4
    • 6
  • Stéphane Thobois
    • 2
    • 3
    • 7
  • Serge Pinto
    • 1
    Email author
  1. 1.Aix Marseille Univ, CNRS, LPLAix-en-ProvenceFrance
  2. 2.Centre de Neurosciences Cognitives, UMR 5229, Université Lyon 1 / CNRSLyonFrance
  3. 3.CERMEPBronFrance
  4. 4.Centre Hospitalier Universitaire (CHU)GrenobleFrance
  5. 5.Grenoble Institut des NeurosciencesU836 INSERM / Université Joseph Fourier / CEA / CHUGrenobleFrance
  6. 6.Hôpitaux UniversitairesGenèveSwitzerland
  7. 7.Hospices Civils de LyonHôpital NeurologiqueLyonFrance

Personalised recommendations