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

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.

Figure 1

Endovascular motor neuroprosthesis system. The internal and external system components in a participant with flaccid upper limb paralysis due to motor neurone disease are demonstrated. The device was implanted within the superior sagittal sinus, immediately adjacent to the precentral gyrus. The highlighted yellow region in the brain depicts the activation of primary motor cortex that occurs with attempted limb movement. The transmission lead, exiting the internal jugular vein between the heads of sternocleidomastoid, was tunneled subcutaneously and connected to the internal telemetry unit (ITU) placed within a subclavicular pocket. The external telemetry unit (ETU) inductively powers the ITU and receives the electrocorticography signal via infrared light transmission. The signal is sent to a tablet computer via a signal control unit and translated into multiple-click actions by the custom decoder, including a zoom function and single-click command. Multiple command control was combined with eye-tracking to enable general operation of Windows 10.

Figure 2

Pre- and post-neurointervention imaging. Panel A displays the baseline computed tomography venography study of the superior sagittal sinus in sagittal, axial and coronal views for participant 1. Panel B panel displays the repeat study at 3 months, and Panel C at 12 months following implantation of the Stentrode in the superior sagittal sinus, which revealed no evidence of thrombosis, stenosis or device migration. Panel D shows the regions of lower limb blood-oxygen-level-dependent (BOLD) activation relative to cortical and vascular structures derived from a preoperative magnetic resonance imaging study, co-registered to the superior sagittal sinus on intra-operative 3D digital subtraction angiography image.

Figure 3

Training and testing timeline. The timeline depicts specific training and testing events that occurred following neurointervention. The number of runs performed for a given task is provided when tests were performed, presented in the order that the tasks were conducted.

Figure 4

System control performance metrics. Boxplots depict the system control performance of participant 1 (P1) and participant 2 (P2). Plots show the mean, median, interquartile range (IQR) and outliers (>±1.5*IQR) per specified performance metric calculated per trial during the typing tasks. Click selection accuracy measures the proportion of correct selections compared to the total selections made. Correct characters per minute (CCPM) measures the typing speed, correcting for errors. Bitrate measures bits transmitted per trial, irrespective of the time taken to make the selection. Information transfer rate (ITR) measures the rate of bits transferred per selection. Bitrate and ITR were calculated for the motor neuroprosthesis + eye-tracking (MN +ET) and motor neuroprosthesis alone (MN).