Mood Effects After Deep Brain Stimulation for Parkinson's Disease: An Update

Ettore A Accolla, Claudio Pollo, Ettore A Accolla, Claudio Pollo

Abstract

Depression in Parkinson's Disease (PD) is a prevalent and invalidating symptom. Deep brain stimulation (DBS) allows for an improvement of PD motor features, but its effects on mood are difficult to predict. Here, we review the evidence regarding mood effects after DBS of either subthalamic nucleus (STN) or globus pallidus pars interna (GPi). Different influences of multiple factors contribute to impact the neuropsychiatric outcome after surgery. Psychosocial presurgical situation, postsurgical coping mechanisms, dopaminergic treatment modifications, and direct effects of the stimulation of either target are all playing a distinct role on the psychological well-being of patients undergoing DBS. No clear advantage of either target (STN vs. GPi) has been consistently found, both being effective and with a favorable profile on depression symptoms. However, specific patients' characteristics or anatomical considerations can guide the neurosurgeon in the target choice. Further research together with technological advances are expected to confine the stimulation area within dysfunctional circuits causing motor symptoms of PD.

Keywords: DBS; GPi; STN; basal ganglia; depression; hypomania.

References

    1. Karlsen KH, Larsen JP, Tandberg E, Maeland JG. Influence of clinical and demographic variables on quality of life in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry. (1999) 66:431–5. 10.1136/jnnp.66.4.431
    1. Reijnders JSAM, Ehrt U, Weber WEJ, Aarsland D, Leentjens AFG. A systematic review of prevalence studies of depression in Parkinson's disease. Mov Disord. (2008) 23:183–9; quiz 313. 10.1002/mds.21803
    1. Hely MA, Morris JGL, Reid WGJ, Trafficante R. Sydney multicenter study of parkinson's disease: non-l-dopa-responsive problems dominate at 15 years. Mov Disord. (2005) 20:190–9. 10.1002/mds.20324
    1. Menza M, Dobkin RD, Marin H, Mark MH, Gara M, Buyske S, et al. . The impact of treatment of depression on quality of life, disability and relapse in patients with Parkinson's disease. Mov Disord. (2009) 24:1325–32. 10.1002/mds.22586
    1. Ravina B, Camicioli R, Como PG, Marsh L, Jankovic J, Weintraub D, et al. . The impact of depressive symptoms in early Parkinson disease. Neurology. (2007) 69:342–7. 10.1212/01.wnl.0000268695.63392.10
    1. Ishihara L, Brayne C. A systematic review of depression and mental illness preceding Parkinson's disease. Acta Neurol Scand. (2006) 113:211–20. 10.1111/j.1600-0404.2006.00579.x
    1. Braak H, Del Tredici K, Rüb U, de Vos RAI, Jansen Steur ENH, Braak E. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging. (2003) 24:197–211. 10.1016/S0197-4580(02)00065-9
    1. Halliday GM, Blumbergs PC, Cotton RG, Blessing WW, Geffen LB. Loss of brainstem serotonin- and substance P-containing neurons in Parkinson's disease. Brain Res. (1990) 510:104–7. 10.1016/0006-8993(90)90733-R
    1. Politis M, Wu K, Loane C, Kiferle L, Molloy S, Brooks DJ, et al. . Staging of serotonergic dysfunction in Parkinson's disease: an in vivo 11C-DASB PET study. Neurobiol Dis. (2010) 40:216–21. 10.1016/j.nbd.2010.05.028
    1. Richard IH, McDermott MP, Kurlan R, Lyness JM, Como PG, Pearson N, et al. . A randomized, double-blind, placebo-controlled trial of antidepressants in Parkinson disease. Neurology. (2012) 78:1229–36. 10.1212/WNL.0b013e3182516244
    1. Remy P, Doder M, Lees A, Turjanski N, Brooks D. Depression in Parkinson's disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain. (2005) 128:1314–22. 10.1093/brain/awh445
    1. Wen M-C, Chan LL, Tan LCS, Tan EK. Depression, anxiety, and apathy in Parkinson's disease: insights from neuroimaging studies. Eur J Neurol. (2016) 23:1001–19. 10.1111/ene.13002
    1. Agid Y, Schüpbach M, Gargiulo M, Mallet L, Houeto JL, Behar C, et al. . Neurosurgery in Parkinson's disease: the doctor is happy, the patient less so? In: Riederer P, Reichmann H, Youdim MBH, Gerlach M, editors. Parkinson's Disease and Related Disorders. Vienna: Springer. p 409–14. 10.1007/978-3-211-45295-0_61
    1. Schüpbach M, Gargiulo M, Welter ML, Mallet L, Béhar C, Houeto JL, et al. . Neurosurgery in Parkinson disease: a distressed mind in a repaired body? Neurology. (2006) 66:1811–6. 10.1212/01.wnl.0000234880.51322.16
    1. Bell E, Maxwell B, McAndrews MP, Sadikot AF, Racine E. A review of social and relational aspects of deep brain stimulation in Parkinson's disease informed by healthcare provider experiences. Parkinson's Dis. (2011) 2011:871874.10.4061/2011/871874
    1. Okun MS, Fernandez HH, Wu SS, Kirsch-Darrow L, Bowers D, Bova F, et al. Cognition and mood in parkinson disease in STN versus GPi DBS: the COMPARE trial. Ann Neurol. (2009) 65:586–95. 10.1002/ana.21596
    1. Ardouin C, Pillon B, Peiffer E, Bejjani P, Limousin P, Damier P, et al. . Bilateral subthalamic or pallidal stimulation for Parkinson's disease affects neither memory nor executive functions: a consecutive series of 62 patients. Ann Neurol. (1999) 46:217–23. 10.1002/1531-8249(199908)46:2<217::AID-ANA11>;2-Z
    1. Combs HL, Folley BS, Berry DTR, Segerstrom SC, Han DY, Anderson-Mooney AJ, et al. . Cognition and depression following deep brain stimulation of the subthalamic nucleus and globus pallidus pars internus in parkinson's disease: a meta-analysis. Neuropsychol Rev. (2015) 25:439–54. 10.1007/s11065-015-9302-0
    1. Stefani A, Trendafilov V, Liguori C, Fedele E, Galati S. Subthalamic nucleus deep brain stimulation on motor-symptoms of Parkinson's disease: focus on neurochemistry. Progr Neurobiol. (2017) 151:157–74. 10.1016/j.pneurobio.2017.01.003
    1. Faggiani E, Delaville C, Benazzouz A. The combined depletion of monoamines alters the effectiveness of subthalamic deep brain stimulation. Neurobiol Dis. (2015) 82:342–8. 10.1016/j.nbd.2015.07.010
    1. Houeto J, Mesnage V, Mallet L, Pillon B, Gargiulo M, du Moncel ST, et al. . Behavioural disorders, Parkinson's disease and subthalamic stimulation. J Neurol Neurosurg Psychiatry. (2002) 72:701–7. 10.1136/jnnp.72.6.701
    1. Krack P, Batir A, Van Blercom N, Chabardes S, Fraix V, Ardouin C, et al. . Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson's disease. N Engl J Med. (2003) 349:1925–34. 10.1056/NEJMoa035275
    1. Burkhard PR, Vingerhoets FJG, Berney A, Bogousslavsky J, Villemure J-G, Ghika J. Suicide after successful deep brain stimulation for movement disorders. Neurology. (2004) 63:2170–2. 10.1212/01.WNL.0000145603.48221.B5
    1. Foncke EMJ, Schuurman PR, Speelman JD. Suicide after deep brain stimulation of the internal globus pallidus for dystonia. Neurology. (2006) 66:142–3. 10.1212/01.wnl.0000191328.05752.e2
    1. Castrioto A, Lhommée E, Moro E, Krack P. Mood and behavioural effects of subthalamic stimulation in Parkinson's disease. Lancet Neurol. (2014) 13:287–305. 10.1016/S1474-4422(13)70294-1
    1. Witt K, Daniels C, Reiff J, Krack P, Volkmann J, Pinsker MO, et al. . Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson's disease: a randomised, multicentre study. Lancet Neurol. (2008) 7:605–14. 10.1016/S1474-4422(08)70114-5
    1. Castelli L, Perozzo P, Zibetti M, Crivelli B, Morabito U, Lanotte M, et al. . Chronic deep brain stimulation of the subthalamic nucleus for Parkinson's disease: effects on cognition, mood, anxiety, and personality traits. Eur Neurol. (2006) 55:136–44. 10.1159/000093213
    1. Schuepbach WMM, Rau J, Knudsen K, Volkmann J, Krack P, Timmermann L, et al. . Neurostimulation for Parkinson's Disease with early motor complications. N Engl J Med. (2013) 368:610–22. 10.1056/NEJMoa1205158
    1. Voon V, Kubu C, Krack P, Houeto J-L, Tröster AI. Deep brain stimulation: neuropsychological and neuropsychiatric issues. Mov Disord. (2006) 21 (Suppl. 14):S305–27. 10.1002/mds.20963
    1. Thobois S, Ardouin C, Lhommée E, Klinger H, Lagrange C, Xie J, et al. . Non-motor dopamine withdrawal syndrome after surgery for Parkinson's disease: predictors and underlying mesolimbic denervation. Brain. (2010) 133:1111–27. 10.1093/brain/awq032
    1. Thobois S, Lhommée E, Klinger H, Ardouin C, Schmitt E, Bichon A, et al. . Parkinsonian apathy responds to dopaminergic stimulation of D2/D3 receptors with piribedil. Brain. (2013) 136:1568–77. 10.1093/brain/awt067
    1. Krack P, Kumar R, Ardouin C, Dowsey PL, McVicker JM, Benabid A-L, et al. . Mirthful laughter induced by subthalamic nucleus stimulation. Movement Disord. (2001) 16:867–75. 10.1002/mds.1174
    1. Accolla EA, Dukart J, Helms G, Weiskopf N, Kherif F, Lutti A, et al. . Brain tissue properties differentiate between motor and limbic basal ganglia circuits. Hum Brain Mapp. (2014) 35:5083–92. 10.1002/hbm.22533
    1. Accolla EA, Herrojo Ruiz M, Horn A, Schneider G-H, Schmitz-Hübsch T, Draganski B, et al. . Brain networks modulated by subthalamic nucleus deep brain stimulation. Brain. (2016) 139:2503–15. 10.1093/brain/aww182
    1. Alkemade A, Forstmann BU. Do we need to revise the tripartite subdivision hypothesis of the human subthalamic nucleus (STN)? Neuroimage. (2014) 95:326–9. 10.1016/j.neuroimage.2014.03.010
    1. Keuken MC, Uylings HBM, Geyer S, Schäfer A, Turner R, Forstmann BU. Are there three subdivisions in the primate subthalamic nucleus? Front Neuroanat. (2012) 6:14. 10.3389/fnana.2012.00014
    1. Horn A, Neumann W-J, Degen K, Schneider G-H, Kühn AA. Toward an electrophysiological “sweet spot” for deep brain stimulation in the subthalamic nucleus. Hum Brain Mapp. (2017) 38:3377–90. 10.1002/hbm.23594
    1. Haynes WIA, Haber SN. The organization of prefrontal-subthalamic inputs in primates provides an anatomical substrate for both functional specificity and integration: implications for basal ganglia models and deep brain stimulation. J Neurosci. (2013) 33:4804–14. 10.1523/JNEUROSCI.4674-12.2013
    1. Kumar R, Lozano AM, Montgomery E, Lang AE. Pallidotomy and deep brain stimulation of the pallidum and subthalamic nucleus in advanced Parkinson's disease. Mov Disord. (1998) 13(Suppl. 1):73–82.
    1. Ghika J, Villemure JG, Fankhauser H, Favre J, Assal G, Ghika-Schmid F. Efficiency and safety of bilateral contemporaneous pallidal stimulation (deep brain stimulation) in levodopa-responsive patients with Parkinson's disease with severe motor fluctuations: a 2-year follow-up review. J Neurosurg. (1998) 89:713–8. 10.3171/jns.1998.89.5.0713
    1. The Deep-Brain Stimulation for Parkinson's Disease Study Group. Deep-brain stimulation of the subthalamic nucleus or the pars interna of the globus pallidus in Parkinson's disease. N Engl J Med. (2001) 345:956–63. 10.1056/NEJMoa000827
    1. Krack P, Pollak P, Limousin P, Hoffmann D, Xie J, Benazzouz A, et al. . Subthalamic nucleus or internal pallidal stimulation in young onset Parkinson's disease. Brain. (1998) 121 (Pt 3):451–7. 10.1093/brain/121.3.451
    1. Weaver FM, Follett KA, Stern M, Luo P, Harris CL, Hur K, et al. . Randomized trial of deep brain stimulation for Parkinson disease: thirty-six-month outcomes. Neurology. (2012) 79:55–65. 10.1212/WNL.0b013e31825dcdc1
    1. Odekerken VJJ, van Laar T, Staal MJ, Mosch A, Hoffmann CFE, Nijssen PCG, et al. . Subthalamic nucleus versus globus pallidus bilateral deep brain stimulation for advanced Parkinson's disease (NSTAPS study): a randomised controlled trial. Lancet Neurol. (2013) 12:37–44. 10.1016/S1474-4422(12)70264-8
    1. Williams NR, Foote KD, Okun MS. Subthalamic nucleus versus globus pallidus internus deep brain stimulation: translating the rematch into clinical practice. Mov Disord Clin Pract. (2014) 1:24–35. 10.1002/mdc3.12004
    1. Odekerken VJJ, Boel JA, Schmand BA, de Haan RJ, Figee M, van den Munckhof P, et al. For the NSTAPS study group. GPi vs STN deep brain stimulation for Parkinson disease: three-year follow-up. Neurology. (2016) 86:755–61. 10.1212/WNL.0000000000002401
    1. Anderson VC, Burchiel KJ, Hogarth P, Favre J, Hammerstad JP. Pallidal vs subthalamic nucleus deep brain stimulation in parkinson disease. Arch Neurol. (2005) 62:554–60. 10.1001/archneur.62.4.554
    1. Okun MS, Wu SS, Fayad S, Ward H, Bowers D, Rosado C, et al. . Acute and chronic mood and apathy outcomes from a randomized study of unilateral STN and GPi DBS. PLoS ONE. (2014) 9:e114140. 10.1371/journal.pone.0114140
    1. Weintraub D, Duda JE, Carlson K, Luo P, Sagher O, Stern M, et al. . Suicide ideation and behaviours after STN and GPi DBS surgery for Parkinson's disease: results from a randomised, controlled trial. J Neurol Neurosurg Psychiatry. (2013) 84:1113–8. 10.1136/jnnp-2012-304396
    1. Bari AA, Fasano A, Munhoz RP, Lozano AM. Improving outcomes of subthalamic nucleus deep brain stimulation in Parkinson's disease. Expert Rev Neurother. (2015) 15:1151–60. 10.1586/14737175.2015.1081815
    1. Munhoz RP, Picillo M, Fox SH, Bruno V, Panisset M, Honey CR, et al. . Eligibility criteria for deep brain stimulation in Parkinson's disease, tremor, and dystonia. Can J Neurol Sci. (2016) 43:462–71. 10.1017/cjn.2016.35
    1. Okun MS, Foote KD. Parkinson's disease DBS: what, when, who and why? The time has come to tailor DBS targets. Expert Rev Neurother. (2010) 10:1847–57. 10.1586/ern.10.156
    1. Okun MS, Wu SS, Foote KD, Bowers D, Gogna S, Price C, et al. . Do stable patients with a premorbid depression history have a worse outcome after deep brain stimulation for Parkinson disease? Neurosurgery. (2011) 69:357–61. 10.1227/NEU.0b013e3182160456
    1. Alexander GE, DeLong MR, Strick PL. Parallel organization of functionally segregated circuits linking basal ganglia and cortex. Ann Rev Neurosci. (1986) 9:357–81. 10.1146/annurev.ne.09.030186.002041
    1. Alexander GE, Crutcher MD. Functional architecture of basal ganglia circuits: neural substrates of parallel processing. Trends Neurosci. (1990) 13:266–71. 10.1016/0166-2236(90)90107-L
    1. Ulla M, Thobois S, Llorca P-M, Derost P, Lemaire J-J, Chereau-Boudet I, et al. . Contact dependent reproducible hypomania induced by deep brain stimulation in Parkinson's disease: clinical, anatomical, and functional imaging study. J Neurol Neurosurg Psychiatry. (2011) 82:607–14. 10.1136/jnnp.2009.199323
    1. Welter M-L, Schüpbach M, Czernecki V, Karachi C, Fernandez-Vidal S, Golmard J-L, et al. . Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology. (2014) 82:1352–61. 10.1212/WNL.0000000000000315
    1. Bejjani BP, Damier P, Arnulf I, Thivard L, Bonnet AM, Dormont D, et al. . Transient acute depression induced by high-frequency deep-brain stimulation. N Engl J Med. (1999) 340:1476–80. 10.1056/NEJM199905133401905
    1. Karachi C, Francois C, Parain K, Bardinet E, Tande D, Hirsch E, et al. . Three-dimensional cartography of functional territories in the human striatopallidal complex by using calbindin immunoreactivity. J Comp Neurol. (2002) 450:122–34. 10.1002/cne.10312
    1. Patriat R, Cooper SE, Duchin Y, Niederer J, Lenglet C, Aman J, et al. . Individualized tractography-based parcellation of the globus pallidus pars interna using 7T MRI in movement disorder patients prior to DBS surgery. NeuroImage. (2018) 178:198–209. 10.1016/j.neuroimage.2018.05.048
    1. Pollo C, Kaelin-Lang A, Oertel MF, Stieglitz L, Taub E, Fuhr P, et al. . Directional deep brain stimulation: an intraoperative double-blind pilot study. Brain. (2014) 137:2015–26. 10.1093/brain/awu102
    1. Steigerwald F, Matthies C, Volkmann J. Directional deep brain stimulation. Neurotherapeutics. (2019) 16:100–4. 10.1007/s13311-018-0667-7
    1. Tinkhauser G, Pogosyan A, Little S, Beudel M, Herz DM, Tan H. The modulatory effect of adaptive deep brain stimulation on beta bursts in Parkinson's disease. Brain. (2017) 140:1053–67. 10.1093/brain/awx010
    1. Priori A, Foffani G, Rossi L, Marceglia S. Adaptive deep brain stimulation (aDBS) controlled by local field potential oscillations. Exp Neurol. (2013) 245:77–86. 10.1016/j.expneurol.2012.09.013

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