Motor neuroprosthesis implanted with neurointerventional surgery improves capacity for activities of daily living tasks in severe paralysis: first in-human experience

Thomas J Oxley; Peter E Yoo; Gil S Rind; Stephen M Ronayne; C M Sarah Lee; Christin Bird; Victoria Hampshire; Rahul P Sharma; Andrew Morokoff; Daryl L Williams; Christopher MacIsaac; Mark E Howard; Lou Irving; Ivan Vrljic; Cameron Williams; Sam E John; Frank Weissenborn; Madeleine Dazenko; Anna H Balabanski; David Friedenberg; Anthony N Burkitt; Yan T Wong; Katharine J Drummond; Patricia Desmond; Douglas Weber; Timothy Denison; Leigh R Hochberg; Susan Mathers; Terence J O'Brien; Clive N May; J Mocco; David B Grayden; Bruce C V Campbell; Peter Mitchell; Nicholas L Opie

doi:10.1136/neurintsurg-2020-016862

Motor neuroprosthesis implanted with neurointerventional surgery improves capacity for activities of daily living tasks in severe paralysis: first in-human experience

J Neurointerv Surg. 2021 Feb;13(2):102-108. doi: 10.1136/neurintsurg-2020-016862. Epub 2020 Oct 28.

Authors

Thomas J Oxley^#^{1

2}, Peter E Yoo^#^{3

2}, Gil S Rind^{3

2}, Stephen M Ronayne^{3

2}, C M Sarah Lee⁴, Christin Bird³, Victoria Hampshire², Rahul P Sharma⁵, Andrew Morokoff^{3

6}, Daryl L Williams⁷, Christopher MacIsaac⁸, Mark E Howard⁹, Lou Irving¹⁰, Ivan Vrljic¹¹, Cameron Williams¹¹, Sam E John^{3

12}, Frank Weissenborn^{3

13}, Madeleine Dazenko⁴, Anna H Balabanski¹⁴, David Friedenberg¹⁵, Anthony N Burkitt¹², Yan T Wong¹⁶, Katharine J Drummond^{3

6}, Patricia Desmond^{3

11}, Douglas Weber¹⁷, Timothy Denison^{2

18}, Leigh R Hochberg¹⁹, Susan Mathers⁴, Terence J O'Brien^{3

14}, Clive N May¹³, J Mocco²⁰, David B Grayden¹², Bruce C V Campbell^{21

22}, Peter Mitchell¹¹, Nicholas L Opie^#^{3

2}

Affiliations

¹ Vascular Bionics Laboratory, Departments of Medicine, Neurology and Surgery, Melbourne Brain Centre at the Royal Melbourne Hospital, The University of Melbourne, Melbourne, Victoria, Australia thomas.oxley@unimelb.edu.au.
² Synchron, Inc, Campbell, California, USA.
³ Vascular Bionics Laboratory, Departments of Medicine, Neurology and Surgery, Melbourne Brain Centre at the Royal Melbourne Hospital, The University of Melbourne, Melbourne, Victoria, Australia.
⁴ Neurology, Calvary Health Care Bethlehem, South Caulfield, Victoria, Australia.
⁵ Interventional Cardiology, Cardiovascular Medicine Faculty, Stanford University, Stanford, California, USA.
⁶ Neurosurgery, Melbourne Health, Parkville, Victoria, Australia.
⁷ Anaesthesia, Melbourne Health, Parkville, Victoria, Australia.
⁸ Intensive Care Unit, Melbourne Health, Parkville, Victoria, Australia.
⁹ Institute for Breathing and Sleep, Austin Health, Heidelberg, Victoria, Australia.
¹⁰ Respiratory Medicine, Melbourne Health, Parkville, Victoria, Australia.
¹¹ Radiology, Melbourne Health, Parkville, Victoria, Australia.
¹² Department of Biomedical Engineering, University of Melbourne, Melbourne, Victoria, Australia.
¹³ Florey Institute of Neuroscience and Mental Health, University of Melbourne, Parkville, Victoria, Australia.
¹⁴ Neurology, Melbourne Health, Parkville, Victoria, Australia.
¹⁵ Battelle Memorial Institute, Columbus, Ohio, USA.
¹⁶ Department of Electrical and Computer Systems Engineering, Monash University, Clayton, Victoria, Australia.
¹⁷ Department of Mechanical Engineering and Neuroscience Institute, Carnegie Mellon University, Pittsburgh, Pennsylvania, USA.
¹⁸ Institute of Biomedical Engineering, Oxford University, Oxford, Oxfordshire, UK.
¹⁹ Center for Neurotechnology and Neurorecovery, Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Harvard University, Cambridge, Massachusetts, USA.
²⁰ Neurosurgery, The Mount Sinai Health System, New York, New York, USA.
²¹ Medicine, University of Melbourne, Parkville, Victoria, Australia.
²² Neurology, Royal Melbourne Hospital, Melbourne, Victoria, Australia.

^# Contributed equally.

Abstract

Background: Implantable brain-computer interfaces (BCIs), functioning as motor neuroprostheses, have the potential to restore voluntary motor impulses to control digital devices and improve functional independence in patients with severe paralysis due to brain, spinal cord, peripheral nerve or muscle dysfunction. However, reports to date have had limited clinical translation.

Methods: Two participants with amyotrophic lateral sclerosis (ALS) underwent implant in a single-arm, open-label, prospective, early feasibility study. Using a minimally invasive neurointervention procedure, a novel endovascular Stentrode BCI was implanted in the superior sagittal sinus adjacent to primary motor cortex. The participants undertook machine-learning-assisted training to use wirelessly transmitted electrocorticography signal associated with attempted movements to control multiple mouse-click actions, including zoom and left-click. Used in combination with an eye-tracker for cursor navigation, participants achieved Windows 10 operating system control to conduct instrumental activities of daily living (IADL) tasks.

Results: Unsupervised home use commenced from day 86 onwards for participant 1, and day 71 for participant 2. Participant 1 achieved a typing task average click selection accuracy of 92.63% (100.00%, 87.50%-100.00%) (trial mean (median, Q1-Q3)) at a rate of 13.81 (13.44, 10.96-16.09) correct characters per minute (CCPM) with predictive text disabled. Participant 2 achieved an average click selection accuracy of 93.18% (100.00%, 88.19%-100.00%) at 20.10 (17.73, 12.27-26.50) CCPM. Completion of IADL tasks including text messaging, online shopping and managing finances independently was demonstrated in both participants.

Conclusion: We describe the first-in-human experience of a minimally invasive, fully implanted, wireless, ambulatory motor neuroprosthesis using an endovascular stent-electrode array to transmit electrocorticography signals from the motor cortex for multiple command control of digital devices in two participants with flaccid upper limb paralysis.

Keywords: brain; device; intervention; technology; vein.

Publication types

Case Reports

MeSH terms

Activities of Daily Living* / psychology
Aged
Brain-Computer Interfaces* / psychology
Feasibility Studies
Female
Humans
Imaging, Three-Dimensional / methods
Implantable Neurostimulators*
Male
Middle Aged
Motor Cortex / diagnostic imaging
Motor Cortex / physiology*
Paralysis / diagnostic imaging
Paralysis / physiopathology
Paralysis / therapy*
Prospective Studies
Severity of Illness Index*