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Uncovering neuroanatomical correlates of impaired coordinated movement after pallidal deep brain stimulation
  1. Brendan Santyr1,
  2. Aaron Loh1,
  3. Artur Vetkas1,
  4. Dave Gwun1,
  5. Wilson KW Fung2,
  6. Shakeel Qazi1,
  7. Jurgen Germann1,
  8. Alexandre Boutet1,3,
  9. Can Sarica1,
  10. Andrew Yang1,
  11. Gavin Elias1,
  12. Suneil K Kalia1,4,5,
  13. Alfonso Fasano2,4,5,6,
  14. Andres M Lozano1,4
  1. 1 Division of Neurosurgery, University of Toronto, Toronto, Ontario, Canada
  2. 2 Edmond J. Safra Program in Parkinson's Disease and Morton and Gloria Shulman Movement Disorders Centre, Toronto Western Hospital, Toronto, Ontario, Canada
  3. 3 Joint Department of Medical Imaging, Toronto Western Hospital, Toronto, Ontario, Canada
  4. 4 Krembil Brain Institute, University Health Network, Toronto, Ontario, Canada
  5. 5 Center for Advancing Neurotechnological Innovation to Application (CRANIA), University Health Network, Toronto, Ontario, Canada
  6. 6 Division of Neurology, University of Toronto, Toronto, Ontario, Canada
  1. Correspondence to Dr Andres M Lozano, Division of Neurosurgery, Toronto Western Hospital, Toronto, Canada; andres.lozano{at}uhnresearch.ca

Abstract

Background The loss of the ability to swim following deep brain stimulation (DBS), although rare, poses a worrisome risk of drowning. It is unclear what anatomic substrate and neural circuitry underlie this phenomenon. We report a case of cervical dystonia with lost ability to swim and dance during active stimulation of globus pallidus internus. We investigated the anatomical underpinning of this phenomenon using unique functional and structural imaging analysis.

Methods Tesla (3T) functional MRI (fMRI) of the patient was used during active DBS and compared with a cohort of four matched patients without this side effect. Structural connectivity mapping was used to identify brain network engagement by stimulation.

Results fMRI during stimulation revealed significant (Pbonferroni<0.0001) stimulation-evoked responses (DBS ON<OFF) in the supplementary motor area (SMA). Probabilistic tractography revealed that the patient’s VTAs engaged streamlines projecting to SMA. Compared with a cohort of matched controls, the stimulation-dependent change in blood oxygen level-dependent response at the SMA was 2.18 SD below the mean.

Conclusions These stimulation-induced impairments are likely a manifestation of a broader deficit in interlimb coordination mediated by stimulation effects on the SMA. This neuroanatomical underpinning can help inform future patient-specific stimulation and targeting.

  • ELECTRICAL STIMULATION
  • DYSTONIA
  • FUNCTIONAL IMAGING
  • MRI
  • NEUROSURGERY

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Footnotes

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  • Contributors BS and AL: substantial contributions to the conception and design of the work; the acquisition, analysis and interpretation of data, drafting the manuscript and approving the final version for publication. AV, DG, WKWF, SQ, JG, AB, CS, AY and GE: made substantial contributions to analysis and interpretation of data, revising the manuscript, and approving the final version for publication. SKK, AF and AML: made substantial contributions to the conception and design of the work, revising the manuscript and approving the final version for publication.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

  • Competing interests AML is a consultant to Abbott, Boston Scientific, Insightec and Medtronic and Scientific Director at Functional Neuromodulation. SKK holds honoraria, speakers fees and/or indirect support Abbott/Boston/Medtronic. AF holds honoraria, speakers fees and/or indirect support Abbott/Boston/Medtronic.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.