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Parkinson’s Disease
Volume 2017, Article ID 7306192, 14 pages
https://doi.org/10.1155/2017/7306192
Research Article

Impact of Combined Subthalamic Nucleus and Substantia Nigra Stimulation on Neuropsychiatric Symptoms in Parkinson’s Disease Patients

1Department of Neurology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
2Department of Neurophysiology and Pathophysiology, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
3Department of Neurosurgery, University Medical Center Hamburg-Eppendorf, 20246 Hamburg, Germany
4Department for Neurodegenerative Diseases and Hertie Institute for Clinical Brain Research, University of Tübingen, 72076 Tübingen, Germany

Correspondence should be addressed to M. Pötter-Nerger; ed.eku@regren-retteop.m

Received 9 September 2016; Revised 30 November 2016; Accepted 8 December 2016; Published 26 January 2017

Academic Editor: Zoltan Mari

Copyright © 2017 U. Hidding et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. A. Castrioto, S. Thobois, S. Carnicella, A. Maillet, and P. Krack, “Emotional manifestations of PD: neurobiological basis,” Movement Disorders, vol. 31, no. 8, pp. 1103–1113, 2016. View at Publisher · View at Google Scholar · View at Scopus
  2. R. Martinez-Fernandez, P. Pelissier, J.-L. Quesada et al., “Postoperative apathy can neutralise benefits in quality of life after subthalamic stimulation for Parkinson's disease,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 87, no. 3, pp. 311–318, 2016. View at Publisher · View at Google Scholar · View at Scopus
  3. M. Sierra, S. Carnicella, A. P. Strafella et al., “Apathy and impulse control disorders: yin & yang of dopamine dependent behaviors,” Journal of Parkinson's Disease, vol. 5, no. 3, pp. 625–636, 2015. View at Publisher · View at Google Scholar · View at Scopus
  4. D. Weintraub and D. J. Burn, “Parkinson's disease: the quintessential neuropsychiatric disorder,” Movement Disorders, vol. 26, no. 6, pp. 1022–1031, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. C. Pont-Sunyer, A. Hotter, C. Gaig et al., “The onset of nonmotor symptoms in parkinson's disease (The ONSET PD Study),” Movement Disorders, vol. 30, no. 2, pp. 229–237, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. K. Del Tredici and H. Braak, “Dysfunction of the locus coeruleus-norepinephrine system and related circuitry in Parkinson's disease-related dementia,” Journal of Neurology, Neurosurgery & Psychiatry, vol. 84, no. 7, pp. 774–783, 2013. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Braak, K. Del Tredici, H. Bratzke, J. Hamm-Clement, D. Sandmann-Keil, and U. Rüb, “Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson's disease (preclinical and clinical stages),” Journal of Neurology, Supplement, vol. 249, supplement 3, pp. III/1–III/5, 2002. View at Google Scholar · View at Scopus
  8. S. L. Foote, F. E. Bloom, and G. Aston-Jones, “Nucleus locus ceruleus: new evidence of anatomical and physiological specificity,” Physiological Reviews, vol. 63, no. 3, pp. 844–914, 1983. View at Google Scholar · View at Scopus
  9. G. Aston-Jones, “Brain structures and receptors involved in alertness,” Sleep Medicine, vol. 6, no. 1, pp. S3–S7, 2005. View at Publisher · View at Google Scholar · View at Scopus
  10. E. E. Benarroch, “The locus ceruleus norepinephrine system: functional organization and potential clinical significance,” Neurology, vol. 73, no. 20, pp. 1699–1704, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. P. J. Rossi, A. Gunduz, and M. S. Okun, “The Subthalamic Nucleus, Limbic Function, and Impulse Control,” Neuropsychology Review, vol. 25, no. 4, pp. 398–410, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. T. D. Hälbig, W. Tse, P. G. Frisina et al., “Subthalamic deep brain stimulation and impulse control in Parkinson's disease,” European Journal of Neurology, vol. 16, no. 4, pp. 493–497, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. H. M. M. Smeding, A. E. Goudriaan, E. M. J. Foncke, P. R. Schuurman, J. D. Speelman, and B. Schmand, “Pathological gambling after bilateral subthalamic nucleus stimulation in Parkinson disease,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 78, no. 5, pp. 517–519, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. L. Gee, H. Smith, P. De La Cruz et al., “The influence of bilateral subthalamic nucleus deep brain stimulation on impulsivity and prepulse inhibition in Parkinson's disease patients,” Stereotactic and Functional Neurosurgery, vol. 93, no. 4, pp. 265–270, 2015. View at Publisher · View at Google Scholar · View at Scopus
  15. P. Pollak, “Deep brain stimulation for Parkinson's disease—patient selection,” Handbook of Clinical Neurology, vol. 116, pp. 97–105, 2013. View at Publisher · View at Google Scholar
  16. J. L. Houeto, V. Mesnage, L. Mallet et al., “Behavioural disorders, Parkinson's disease and subthalamic stimulation,” Journal of Neurology Neurosurgery and Psychiatry, vol. 72, no. 6, pp. 701–707, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Nandi, T. Z. Aziz, X. Liu, and J. F. Stein, “Brainstem motor loops in the control of movement,” Movement Disorders, vol. 17, no. 3, pp. S22–S27, 2002. View at Publisher · View at Google Scholar · View at Scopus
  18. P. A. Pahapill and A. M. Lozano, “The pedunculopontine nucleus and Parkinson's disease,” Brain, vol. 123, no. 9, pp. 1767–1783, 2000. View at Publisher · View at Google Scholar · View at Scopus
  19. G. E. Alexander, M. D. Crutcher, and M. R. DeLong, “Basal ganglia-thalamocortical circuits: parallel substrates for motor, oculomotor, “prefrontal” and “limbic” functions,” Progress in Brain Research, vol. 85, pp. 119–146, 1990. View at Google Scholar · View at Scopus
  20. M. Pötter, J. Herzog, H. R. Siebner et al., “Subthalamic nucleus stimulation modulates audiospinal reactions in Parkinson disease,” Neurology, vol. 70, no. 16, pp. 1445–1451, 2008. View at Publisher · View at Google Scholar · View at Scopus
  21. M. Pötter, M. Illert, R. Wenzelburger, G. Deuschl, and J. Volkmann, “The effect of subthalamic nucleus stimulation on autogenic inhibition in Parkinson disease,” Neurology, vol. 63, no. 7, pp. 1234–1239, 2004. View at Publisher · View at Google Scholar · View at Scopus
  22. D. Weiss, M. Walach, C. Meisner et al., “Nigral stimulation for resistant axial motor impairment in Parkinson's disease? A randomized controlled trial,” Brain, vol. 136, no. 7, pp. 2098–2108, 2013. View at Publisher · View at Google Scholar · View at Scopus
  23. S. Breit, R. Bouali-Benazzouz, A.-L. Benabid, and A. Benazzouz, “Unilateral lesion of the nigrostriatal pathway induces an increase of neuronal activity of the pedunculopontine nucleus, which is reversed by the lesion of the subthalamic nucleus in the rat,” European Journal of Neuroscience, vol. 14, no. 11, pp. 1833–1842, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. S. Breit, L. Lessmann, A. Benazzouz, and J. B. Schulz, “Unilateral lesion of the pedunculopontine nucleus induces hyperactivity in the subthalamic nucleus and substantia nigra in the rat,” European Journal of Neuroscience, vol. 22, no. 9, pp. 2283–2294, 2005. View at Publisher · View at Google Scholar · View at Scopus
  25. M. M. Hoehn and M. D. Yahr, “Parkinsonism: onset, progression, and mortality,” Neurology, vol. 17, no. 5, pp. 427–442, 1967. View at Publisher · View at Google Scholar · View at Scopus
  26. D. J. Gill, A. Freshman, J. A. Blender, and B. Ravina, “The montreal cognitive assessment as a screening tool for cognitive impairment in Parkinson's disease,” Movement Disorders, vol. 23, no. 7, pp. 1043–1046, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. J. M. Bronstein, M. Tagliati, R. L. Alterman et al., “Deep brain stimulation for Parkinson disease an expert consensus and review of key issues,” Archives of Neurology, vol. 68, no. 2, pp. 165–171, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. C. L. Tomlinson, R. Stowe, S. Patel, C. Rick, R. Gray, and C. E. Clarke, “Systematic review of levodopa dose equivalency reporting in Parkinson's disease,” Movement Disorders, vol. 25, no. 15, pp. 2649–2653, 2010. View at Publisher · View at Google Scholar · View at Scopus
  29. A. Sharott, A. Gulberti, S. Zittel et al., “Activity parameters of subthalamic nucleus neurons selectively predict motor symptom severity in Parkinson's disease,” Journal of Neuroscience, vol. 34, no. 18, pp. 6273–6285, 2014. View at Publisher · View at Google Scholar · View at Scopus
  30. C. K. E. Moll, E. Galindo-Leon, A. Sharott et al., “Asymmetric pallidal neuronal activity in patients with cervical dystonia,” Frontiers in Systems Neuroscience, vol. 8, article no. 15, 2014. View at Publisher · View at Google Scholar · View at Scopus
  31. C. K. E. Moll, S. Payer, A. Gulberti et al., “STN stimulation in general anaesthesia: evidence beyond ‘evidence-based medicine’,” Acta Neurochirurgica. Supplement, no. 117, pp. 19–25, 2013. View at Publisher · View at Google Scholar · View at Scopus
  32. W. Hamel, U. Fietzek, A. Morsnowski et al., “Deep brain stimulation of the subthalamic nucleus in Parkinson's disease: evaluation of active electrode contacts,” Journal of Neurology Neurosurgery and Psychiatry, vol. 74, no. 8, pp. 1036–1046, 2003. View at Publisher · View at Google Scholar · View at Scopus
  33. P. Fischer, J. P. Ossandón, J. Keyser et al., “STN-DBS reduces saccadic hypometria but not visuospatial bias in Parkinson’s disease patients,” Frontiers in Behavioral Neuroscience, vol. 10, article no. 85, 2016. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Sockeel, K. Dujardin, D. Devos, C. Denève, A. Destée, and L. Defebvre, “The Lille apathy rating scale (LARS), a new instrument for detecting and quantifying apathy: validation in Parkinson's disease,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 77, no. 5, pp. 579–584, 2006. View at Publisher · View at Google Scholar · View at Scopus
  35. J. D. Fisk, P. G. Ritvo, L. Ross, D. A. Haase, T. J. Marrie, and W. F. Schlech, “Measuring the functional impact of fatigue: initial validation of the fatigue impact scale,” Clinical Infectious Diseases, vol. 18, pp. S79–S83, 1994. View at Publisher · View at Google Scholar · View at Scopus
  36. P. Flachenecker, T. Kümpfel, B. Kallmann et al., “Fatigue in multiple sclerosis: a comparison of different rating scales and correlation to clinical parameters,” Multiple Sclerosis, vol. 8, no. 6, pp. 523–526, 2002. View at Publisher · View at Google Scholar · View at Scopus
  37. A. T. Beck, C. H. Ward, M. Mendelson, J. Mock, and J. Erbaugh, “An inventory for measuring depression,” Archives of General Psychiatry, vol. 4, no. 6, pp. 561–571, 1961. View at Publisher · View at Google Scholar · View at Scopus
  38. C. C. Probst, L. M. Winter, B. Möller et al., “Validation of the questionnaire for impulsive-compulsive disorders in Parkinson's disease (QUIP) and the QUIP-rating scale in a German speaking sample,” Journal of Neurology, vol. 261, no. 5, pp. 936–942, 2014. View at Publisher · View at Google Scholar
  39. D. Weintraub, E. Mamikonyan, K. Papay, J. A. Shea, S. X. Xie, and A. Siderowf, “Questionnaire for impulsive-compulsive disorders in Parkinson's Disease-Rating Scale,” Movement Disorders, vol. 27, no. 2, pp. 242–247, 2012. View at Publisher · View at Google Scholar · View at Scopus
  40. C. Jenkinson, R. Fitzpatrick, V. Peto, R. Greenhall, and N. Hyman, “The Parkinson's disease questionnaire (PDQ-39): development and validation of a Parkinson's disease summary index score,” Age and Ageing, vol. 26, no. 5, pp. 353–357, 1997. View at Publisher · View at Google Scholar · View at Scopus
  41. D. Devos, C. Moreau, D. Maltête et al., “Rivastigmine in apathetic but dementia and depression-free patients with Parkinson's disease: a double-blind, placebo-controlled, randomised clinical trial,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 85, no. 6, pp. 668–674, 2014. View at Publisher · View at Google Scholar · View at Scopus
  42. D. E. Clarke, J. Y. Ko, E. A. Kuhl, R. van Reekum, R. Salvador, and R. S. Marin, “Are the available apathy measures reliable and valid? A review of the psychometric evidence,” Journal of Psychosomatic Research, vol. 70, no. 1, pp. 73–97, 2011. View at Publisher · View at Google Scholar · View at Scopus
  43. A. Schrag, “Apathy and depression scales in Parkinson's disease: are they good enough?” Journal of the Neurological Sciences, vol. 310, no. 1-2, pp. 216–219, 2011. View at Publisher · View at Google Scholar · View at Scopus
  44. D. M. Schiehser, C. R. Ayers, L. Liu, S. Lessig, D. S. Song, and J. V. Filoteo, “Validation of the modified fatigue impact scale in Parkinson's disease,” Parkinsonism and Related Disorders, vol. 19, no. 3, pp. 335–338, 2013. View at Publisher · View at Google Scholar · View at Scopus
  45. A. F. G. Leentjens, F. R. J. Verhey, G.-J. Luijckx, and J. Troost, “The validity of the Beck depression inventory as a screening and diagnostic instrument for depression in patients with Parkinson's disease,” Movement Disorders, vol. 15, no. 6, pp. 1221–1224, 2000. View at Publisher · View at Google Scholar · View at Scopus
  46. P. Hagell and M. H. Nilsson, “The 39-item Parkinson's Disease Questionnaire (PDQ-39): is it a unidimensional construct?” Therapeutic Advances in Neurological Disorders, vol. 2, no. 4, pp. 205–214, 2009. View at Publisher · View at Google Scholar · View at Scopus
  47. D. Weiss, T. Wachter, C. Meisner et al., “Combined STN/SNr-DBS for the treatment of refractory gait disturbances in Parkinson's disease: study protocol for a randomized controlled trial,” Trials, vol. 12, article 222, 2011. View at Publisher · View at Google Scholar · View at Scopus
  48. L. L. Trépanier, R. Kumar, A. M. Lozano, A. E. Lang, and J. A. Saint-Cyr, “Neuropsychological outcome of GPi pallidotomy and GPi or STN deep brain stimulation in Parkinson's disease,” Brain and Cognition, vol. 42, no. 3, pp. 324–347, 2000. View at Publisher · View at Google Scholar · View at Scopus
  49. M. Ulla, S. Thobois, P.-M. Llorca et al., “Contact dependent reproducible hypomania induced by deep brain stimulation in Parkinson's disease: clinical, anatomical and functional imaging study,” Journal of Neurology, Neurosurgery and Psychiatry, vol. 82, no. 6, pp. 607–614, 2011. View at Publisher · View at Google Scholar · View at Scopus
  50. A. Morel, Stereotactic Atlas of the Human Thalamus and Basal Ganglia, 2007. View at Publisher · View at Google Scholar
  51. D. Weiss, S. Breit, T. Wächter, C. Plewnia, A. Gharabaghi, and R. Krüger, “Combined stimulation of the substantia nigra pars reticulata and the subthalamic nucleus is effective in hypokinetic gait disturbance in Parkinson's disease,” Journal of Neurology, vol. 258, no. 6, pp. 1183–1185, 2011. View at Publisher · View at Google Scholar · View at Scopus
  52. A. Chopra, S. J. Tye, K. H. Lee et al., “Underlying neurobiology and clinical correlates of mania status after subthalamic nucleus deep brain stimulation in Parkinson's disease: a review of the literature,” Journal of Neuropsychiatry and Clinical Neurosciences, vol. 24, no. 1, pp. 102–110, 2012. View at Publisher · View at Google Scholar · View at Scopus
  53. M. Ulla, S. Thobois, J.-J. Lemaire et al., “Manic behaviour induced by deep-brain stimulation in Parkinson's disease: evidence of substantia nigra implication?” Journal of Neurology, Neurosurgery and Psychiatry, vol. 77, no. 12, pp. 1363–1366, 2006. View at Publisher · View at Google Scholar · View at Scopus
  54. B.-P. Bejjani, P. Damier, I. Arnulf et al., “Transient acute depression induced by high-frequency deep-brain stimulation,” New England Journal of Medicine, vol. 340, no. 19, pp. 1476–1480, 1999. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Dujardin, C. Langlois, L. Plomhause et al., “Apathy in untreated early-stage Parkinson disease: relationship with other non-motor symptoms,” Movement Disorders, vol. 29, no. 14, pp. 1796–1801, 2014. View at Publisher · View at Google Scholar
  56. J. Pagonabarraga, J. Kulisevsky, A. P. Strafella, and P. Krack, “Apathy in Parkinson's disease: clinical features, neural substrates, diagnosis, and treatment,” The Lancet Neurology, vol. 14, no. 5, pp. 518–531, 2015. View at Publisher · View at Google Scholar · View at Scopus
  57. H. Alzahrani and A. Venneri, “Cognitive and neuroanatomical correlates of neuropsychiatric symptoms in Parkinson's disease: a systematic review,” Journal of the Neurological Sciences, vol. 356, no. 1-2, pp. 32–44, 2015. View at Publisher · View at Google Scholar · View at Scopus
  58. G. Santangelo, C. Vitale, L. Trojano et al., “Relationship between apathy and cognitive dysfunctions in de novo untreated Parkinson's disease: a prospective longitudinal study,” European Journal of Neurology, vol. 22, no. 2, pp. 253–260, 2015. View at Publisher · View at Google Scholar · View at Scopus
  59. Y. Bogdanova and A. Cronin-Golomb, “Neurocognitive correlates of apathy and anxiety in parkinson's disease,” Parkinson's Disease, vol. 2012, Article ID 793076, 9 pages, 2012. View at Publisher · View at Google Scholar · View at Scopus
  60. G. Deuschl, C. Schade-Brittinger, P. Krack et al., “A randomized trial of deep-brain stimulation for Parkinson’s disease,” New England Journal of Medicine, vol. 355, no. 9, pp. 896–908, 2006. View at Publisher · View at Google Scholar
  61. A. Williams, S. Gill, T. Varma et al., “Deep brain stimulation plus best medical therapy versus best medical therapy alone for advanced Parkinson's disease (PD SURG trial): a randomised, open-label trial,” The Lancet Neurology, vol. 9, no. 6, pp. 581–591, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. K. A. Follett, F. M. Weaver, M. Stern et al., “Pallidal versus subthalamic deep-brain stimulation for Parkinson's disease,” New England Journal of Medicine, vol. 362, no. 22, pp. 2077–2091, 2010. View at Publisher · View at Google Scholar · View at Scopus
  63. M. S. Okun, B. V. Gallo, G. Mandybur et al., “Subthalamic deep brain stimulation with a constant-current device in Parkinson's disease: an open-label randomised controlled trial,” The Lancet Neurology, vol. 11, no. 2, pp. 140–149, 2012. View at Publisher · View at Google Scholar · View at Scopus
  64. A. Maillet, P. Krack, E. Lhommée et al., “The prominent role of serotonergic degeneration in apathy, anxiety and depression in de novo Parkinson’s disease,” Brain, vol. 139, no. 9, pp. 2486–2502, 2016. View at Publisher · View at Google Scholar
  65. L. Loued-Khenissi and K. Preuschoff, “Apathy and noradrenaline: silent partners to mild cognitive impairment in Parkinson's disease?” Current Opinion in Neurology, vol. 28, no. 4, pp. 344–350, 2015. View at Publisher · View at Google Scholar · View at Scopus
  66. A. Feldmann, Z. Illes, P. Kosztolanyi et al., “Morphometric changes of gray matter in Parkinson's disease with depression: a voxel-based morphometry study,” Movement Disorders, vol. 23, no. 1, pp. 42–46, 2008. View at Publisher · View at Google Scholar · View at Scopus
  67. C. Luo, Q. Chen, W. Song et al., “Resting-state fMRI study on drug-naive patients with Parkinson's disease and with depression,” Journal of Neurology, Neurosurgery & Psychiatry, vol. 85, no. 6, pp. 675–683, 2014. View at Publisher · View at Google Scholar
  68. X. Hu, X. Song, Y. Yuan et al., “Abnormal functional connectivity of the amygdala is associated with depression in Parkinson's disease,” Movement Disorders, vol. 30, no. 2, pp. 238–244, 2015. View at Publisher · View at Google Scholar
  69. J. S. A. M. Reijnders, B. Scholtissen, W. E. J. Weber, P. Aalten, F. R. J. Verhey, and A. F. G. Leentjens, “Neuroanatomical correlates of apathy in Parkinson's disease: a magnetic resonance imaging study using voxel-based morphometry,” Movement Disorders, vol. 25, no. 14, pp. 2318–2325, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. N. Carriere, P. Besson, K. Dujardin et al., “Apathy in Parkinson's disease is associated with nucleus accumbens atrophy: a magnetic resonance imaging shape analysis,” Movement Disorders, vol. 29, no. 7, pp. 897–903, 2014. View at Publisher · View at Google Scholar · View at Scopus
  71. H. C. Baggio, B. Segura, J. L. Garrido-Millan et al., “Resting-state frontostriatal functional connectivity in Parkinson's disease-related apathy,” Movement Disorders, vol. 30, no. 5, pp. 671–679, 2015. View at Publisher · View at Google Scholar · View at Scopus
  72. K. N. Ochsner, R. R. Ray, B. Hughes et al., “Bottom-up and top-down processes in emotion generation: common and distinct neural mechanisms,” Psychological Science, vol. 20, no. 11, pp. 1322–1331, 2009. View at Publisher · View at Google Scholar
  73. F. Le Jeune, D. Drapier, A. Bourguignon et al., “Subthalamic nucleus stimulation in Parkinson disease induces apathy: a PET study,” Neurology, vol. 73, no. 21, pp. 1746–1751, 2009. View at Publisher · View at Google Scholar · View at Scopus
  74. G. Aston-Jones, J. Rajkowski, and J. Cohen, “Locus coeruleus and regulation of behavioral flexibility and attention,” Progress in Brain Research, vol. 126, pp. 165–182, 2000. View at Publisher · View at Google Scholar · View at Scopus
  75. G. Aston-Jones, J. Rajkowski, P. Kubiak, R. J. Valentino, and M. T. Shipley, “Role of the locus coeruleus in emotional activation,” Progress in Brain Research, vol. 107, pp. 379–402, 1996. View at Publisher · View at Google Scholar · View at Scopus