Skip to main content

Advertisement

SpringerLink
Log in

Anatomical predictors of cognitive decline after subthalamic stimulation in Parkinson’s disease

  • Original Article
  • Published:
Brain Structure and Function Aims and scope Submit manuscript

Abstract

We investigated whether pre-operative MRI measures of focal brain atrophy could predict cognitive decline occurring after deep brain stimulation (DBS) of the subthalamic nucleus (STN) in patients with Parkinson’s disease (PD). For that purpose, we prospectively collected data of 42 consecutive patients with PD who underwent bilateral STN-DBS. Normalized brain structure volumes and cortical thicknesses were measured on pre-operative T1-weighted MRI. Patients were tested for their cognitive performances before surgery and 1 year after. After controlling for age, gender, pre-operative disease severity, change in dopaminomimetic dose after surgery and contact location, we found correlations: (1) between the variation of the total Mattis dementia rating scale (MDRS) score and left lateral ventricle volume (p = 0.032), (2) between the variation of the initiation/perseveration subscore of the MDRS and the left nucleus accumbens volume (p = 0.042) and the left lateral ventricle volume (p = 0.017) and (3) between the variation of the backward digit-span task and the right and left superior frontal gyrus thickness (p = 0.004 and p = 0.007, respectively). Left nucleus accumbens atrophy was associated with decline in the initiation/perseveration subscore with the largest effect size (d = − 1.64). Pre-operative left nucleus accumbens volume strongly predicted postoperative decline in the initiation/attention subscore (AUC = 0.92, p < 0.001, 96.3% sensitivity, 80.0% specificity, 92.9% PPV and 92.9% NPV). We conclude that the morphometric measures of brain atrophy usually associated with cognitive impairment in PD can also explain or predict a part of cognitive decline after bilateral STN-DBS. In particular, the left accumbens nucleus volume could be considered as a promising marker for guiding surgical decisions.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Alegret M, Junqué C, Valldeoriola F et al (2001) Effects of bilateral subthalamic stimulation on cognitive function in Parkinson disease. Arch Neurol 58:1223–1227

    Article  CAS  Google Scholar 

  • Altman DG (1990) Practical statistics for medical research. CRC Press, Boca Raton

    Google Scholar 

  • Aybek S, Lazeyras F, Gronchi-Perrin A et al (2009) Hippocampal atrophy predicts conversion to dementia after STN-DBS in Parkinson’s disease. Parkinsonism Relat Disord 15:521–524

    Article  Google Scholar 

  • Bonneville F, Welter ML, Elie C et al (2005) Parkinson disease, brain volumes, and subthalamic nucleus stimulation. Neurology 64:1598–1604

    Article  CAS  Google Scholar 

  • Camicioli R, Sabino J, Gee M et al (2011) Ventricular dilatation and brain atrophy in patients with Parkinson’s disease with incipient dementia. Mov Disord 26:1443–1450

    Article  Google Scholar 

  • Carriere N, Besson P, Dujardin K et al (2014) Apathy in Parkinson’s disease is associated with nucleus accumbens atrophy: a magnetic resonance imaging shape analysis. Mov Disord 29:897–903

    Article  Google Scholar 

  • Charles PD, Van Blercom N, Krack P et al (2002) Predictors of effective bilateral subthalamic nucleus stimulation for PD. Neurology 59:932–934

    Article  CAS  Google Scholar 

  • Contarino MF, Daniele A, Sibilia AH et al (2007) Cognitive outcome 5 years after bilateral chronic stimulation of subthalamic nucleus in patients with Parkinson’s disease. J Neurol Neurosurg Psychiatry 78:248–252

    Article  CAS  Google Scholar 

  • Daniels C, Krack P, Volkmann J et al (2010) Risk factors for executive dysfunction after subthalamic nucleus stimulation in Parkinson’s disease. Mov Disord 25:1583–1589

    Article  Google Scholar 

  • de Chazeron I, Pereira B, Chereau-Boudet I et al (2016) Impact of localisation of deep brain stimulation electrodes on motor and neurobehavioural outcomes in Parkinson’s disease. J Neurol Neurosurg Psychiatry 87:758–766

    Article  Google Scholar 

  • Desikan RS, Ségonne F, Fischl B et al (2006) An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage 31:968–980

    Article  Google Scholar 

  • Dujardin K, Devos D, Duhem S et al (2006) Utility of the Mattis dementia rating scale to assess the efficacy of rivastigmine in dementia associated with Parkinson’s disease. J Neurol 253:1154–1159

    Article  CAS  Google Scholar 

  • Emre M (2004) Dementia in Parkinson’s disease: cause and treatment. Curr Opin Neurol 17:399–404

    Article  Google Scholar 

  • Fischl B, Dale AM (2000) Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci USA 97:11050–11055

    Article  CAS  Google Scholar 

  • Funkiewiez A, Ardouin C, Caputo E et al (2004) Long term effects of bilateral subthalamic nucleus stimulation on cognitive function, mood, and behaviour in Parkinson’s disease. J Neurol Neurosurg Psychiatry 75:834–839

    Article  CAS  Google Scholar 

  • Hanganu A, Bedetti C, Degroot C et al (2014) Mild cognitive impairment is linked with faster rate of cortical thinning in patients with Parkinson’s disease longitudinally. Brain 137:1120–1129

    Article  Google Scholar 

  • Houvenaghel J-F, Le Jeune F, Dondaine T et al (2015) Reduced verbal fluency following subthalamic deep brain stimulation: a frontal-related cognitive deficit? PloS One 10:e0140083

    Article  Google Scholar 

  • Hughes AJ, Daniel SE, Kilford L, Lees AJ (1992) Accuracy of clinical diagnosis of idiopathic Parkinson’s disease: a clinico-pathological study of 100 cases. J Neurol Neurosurg Psychiatry 55:181–184

    Article  CAS  Google Scholar 

  • Ibarretxe-Bilbao N, Junque C, Segura B et al (2012) Progression of cortical thinning in early Parkinson’s disease. Mov Disord 27:1746–1753

    Article  Google Scholar 

  • Kim H-J, Jeon BS, Paek SH et al (2014) Long-term cognitive outcome of bilateral subthalamic deep brain stimulation in Parkinson’s disease. J Neurol 261:1090–1096

    Article  Google Scholar 

  • Krack P, Batir A, Van Blercom N et al (2003) Five-year follow-up of bilateral stimulation of the subthalamic nucleus in advanced Parkinson’s disease. N Engl J Med 349:1925–1934

    Article  CAS  Google Scholar 

  • Lang AE, Houeto J-L, Krack P et al (2006) Deep brain stimulation: preoperative issues. Mov Disord 21(Suppl 14):S171–S196

    Article  Google Scholar 

  • Le Goff F, Derrey S, Lefaucheur R et al (2015) Decline in verbal fluency after subthalamic nucleus deep brain stimulation in Parkinson’s disease: a microlesion effect of the electrode trajectory? J Park Dis 5:95–104

    Google Scholar 

  • Lemaire J-J, Coste J, Ouchchane L et al (2007) Brain mapping in stereotactic surgery: a brief overview from the probabilistic targeting to the patient-based anatomic mapping. NeuroImage 37(Suppl 1):S109-115

    Google Scholar 

  • Lemaire J-J, Pereira B, Derost P et al (2016) Subthalamus stimulation in Parkinson disease: accounting for the bilaterality of contacts. Surg Neurol Int 7:S837–S847

    Article  Google Scholar 

  • Mak E, Su L, Williams GB et al (2015) Baseline and longitudinal grey matter changes in newly diagnosed Parkinson’s disease: ICICLE-PD study. Brain 138:2974–2986

    Article  Google Scholar 

  • Manjón JV, Coupé P (2016) volBrain: an online MRI brain volumetry system. Front Neuroinform 10:30

    Article  Google Scholar 

  • Markser A, Maier F, Lewis CJ et al (2015) Deep brain stimulation and cognitive decline in Parkinson’s disease: the predictive value of electroencephalography. J Neurol 262:2275–2284. d

    Article  CAS  Google Scholar 

  • Marson DC, Dymek MP, Duke LW, Harrell LE (1997) Subscale validity of the Mattis dementia rating scale. Arch Clin Neuropsychol 12:269–275

    Article  CAS  Google Scholar 

  • Næss-Schmidt E, Tietze A, Blicher JU et al (2016) Automatic thalamus and hippocampus segmentation from MP2RAGE: comparison of publicly available methods and implications for DTI quantification. Int J Comput Assist Radiol Surg 11:1979–1991

    Article  Google Scholar 

  • Parsons TD, Rogers SA, Braaten AJ et al (2006) Cognitive sequelae of subthalamic nucleus deep brain stimulation in Parkinson’s disease: a meta-analysis. Lancet Neurol 5:578–588

    Article  Google Scholar 

  • Pessoa L (2009) How do emotion and motivation direct executive control? Trends Cognit Sci 13:160–166

    Article  Google Scholar 

  • Pigott K, Rick J, Xie SX et al (2015) Longitudinal study of normal cognition in Parkinson disease. Neurology 85:1276–1282

    Article  CAS  Google Scholar 

  • Saint-Cyr JA, Trépanier LL, Kumar R et al (2000) Neuropsychological consequences of chronic bilateral stimulation of the subthalamic nucleus in Parkinson’s disease. Brain 123(Pt 10):2091–2108

    Article  Google Scholar 

  • Schuepbach WMM, Rau J, Knudsen K et al (2013) Neurostimulation for Parkinson’s disease with early motor complications. N Engl J Med 368:610–622

    Article  CAS  Google Scholar 

  • Segura B, Baggio HC, Marti MJ et al (2014) Cortical thinning associated with mild cognitive impairment in Parkinson’s disease. Mov Disord 29:1495–1503

    Article  Google Scholar 

  • Smeding HMM, Speelman JD, Huizenga HM et al (2011) Predictors of cognitive and psychosocial outcome after STN DBS in Parkinson’s Disease. J Neurol Neurosurg Psychiatry 82:754–760

    Article  Google Scholar 

  • Thobois S (2006) Proposed dose equivalence for rapid switch between dopamine receptor agonists in Parkinson’s disease: a review of the literature. Clin Ther 28:1–12

    Article  CAS  Google Scholar 

  • Tsai S-T, Lin S-H, Lin S-Z et al (2007) Neuropsychological effects after chronic subthalamic stimulation and the topography of the nucleus in Parkinson’s disease. Neurosurgery 61:E1024–E1029 (discussion E1029–E1030).

    Article  Google Scholar 

  • Welter ML, Houeto JL, Tezenas du Montcel S et al (2002) Clinical predictive factors of subthalamic stimulation in Parkinson’s disease. Brain 125:575–583

    Article  CAS  Google Scholar 

  • Welter M-L, Schüpbach M, Czernecki V et al (2014) Optimal target localization for subthalamic stimulation in patients with Parkinson disease. Neurology 82:1352–1361

    Article  Google Scholar 

  • Witt K, Daniels C, Reiff J et al (2008) Neuropsychological and psychiatric changes after deep brain stimulation for Parkinson’s disease: a randomised, multicentre study. Lancet Neurol 7:605–614

    Article  Google Scholar 

  • Witt K, Granert O, Daniels C et al (2013) Relation of lead trajectory and electrode position to neuropsychological outcomes of subthalamic neurostimulation in Parkinson’s disease: results from a randomized trial. Brain 136:2109–2119

    Article  Google Scholar 

Download references

Acknowledgements

The authors want to thank Christine Delaigue, coordinating nurse for the Parkinson’s Disease Center in Clermont-Ferrand University Hospital. They also thank Prof. Thomas Tourdias and Prof. Vincent Dousset from Bordeaux University Hospital for making available their MRI analysis facilities, and Celine Lambert from Clermont-Ferrand University Hospital for her technical assistance.

Funding

Hospital Program for Clinical Research at Clermont-Ferrand University Hospital.

Author information

Authors and Affiliations

  1. Service de Neurologie, CHU Clermont-Ferrand, Université Clermont Auvergne, 58 rue Montalembert, 63000, Clermont-Ferrand, France

    Vincent Planche, Philippe Derost, Bérangère Debilly, Ana Marques & Franck Durif

  2. Service de Neuroradiologie diagnostique et thérapeutique, CHU Bordeaux, Université Bordeaux, 33000, Bordeaux, France

    Fanny Munsch

  3. Unité de Biostatistiques, Direction à la Recherche Clinique et à l’Innovation (DRCI), CHU Clermont-Ferrand, 63000, Clermont-Ferrand, France

    Bruno Pereira & Dominique Morand

  4. Service de Neurochirurgie, CHU Clermont-Ferrand, Centre National de la Recherche Scientifique (CNRS), Université Clermont Auvergne, 63000, Clermont-Ferrand, France

    Emmanuel de Schlichting, Jerome Coste & Jean-Jacques Lemaire

  5. Centre Mémoire de Ressources et de Recherche (CMRR), CHU Clermont-Ferrand, 63000, Clermont-Ferrand, France

    Tiphaine Vidal

  6. Centre Médico-Psychologique B (CMP-B), CHU Clermont-Ferrand, Université Clermont Auvergne, 63000, Clermont-Ferrand, France

    Ingrid de Chazeron & Pierre-Michel Llorca

Authors
  1. Vincent Planche
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fanny Munsch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Bruno Pereira
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emmanuel de Schlichting
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Tiphaine Vidal
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jerome Coste
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Dominique Morand
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Ingrid de Chazeron
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Philippe Derost
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Bérangère Debilly
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Pierre-Michel Llorca
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Jean-Jacques Lemaire
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Ana Marques
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Franck Durif
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conception of the project: VP and FD. Organization: FD. Execution: all authors. Statistical Analysis: VP and BP. Writing of the first draft: VP. Review and Critique: all authors. Study concept and design: VP, BP, JJL and FD.

Corresponding author

Correspondence to Vincent Planche.

Ethics declarations

Conflict of interest

VP received travel expenses and/or consulting fees from the ARSEP Foundation, Biogen, Teva-Lundbeck and Merk-Serono, unrelated to the submitted work. FD serves on scientific advisory boards and has received honoraria and research support for his institution from Novartis, Teva-Lundbeck, Allergan, Aguettant, Servier and Merz, unrelated to the submitted work. Other authors: no conflict of interests.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Planche, V., Munsch, F., Pereira, B. et al. Anatomical predictors of cognitive decline after subthalamic stimulation in Parkinson’s disease. Brain Struct Funct 223, 3063–3072 (2018). https://doi.org/10.1007/s00429-018-1677-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00429-018-1677-2

Keywords

Search

Navigation