Quantifying physical degradation alongside recording and stimulation performance of 980 intracortical microelectrodes chronically implanted in three humans for 956-2130 days

Abstract

The clinical success of brain computer interfaces (BCI) depends on overcoming both biological and material challenges to ensure a long-term stable connection for neural recording and stimulation. This study systematically quantified damage that microelectrodes sustained during chronical implantation in three people with tetraplegia for 956-2130 days. Using scanning electron microscopy (SEM), we imaged 980 microelectrodes from eleven Neuroport arrays tipped with platinum (Pt, n = 8) and sputtered iridium oxide film (SIROF, n = 3). Arrays were implanted/explanted from posterior parietal, motor and somatosensory cortices across three clinical sites (Caltech/UCLA, Caltech/USC, APL/Johns Hopkins). From the electron micrographs, we quantified and correlated physical damage with functional outcomes measured in vivo, prior to explant (recording quality, noise, impedance and stimulation ability). Despite greater physical degradation, SIROF electrodes were twice as likely to record neural activity than Pt (measured by SNR). For SIROF, 1 kHz impedance significantly correlated with all physical damage metrics, recording metrics, and stimulation performance, suggesting a reliable measurement of in vivo degradation. We observed a new degradation type, primarily on stimulated electrodes ("pockmarked" vs "cracked") electrodes; however, no significant degradation due to stimulation or amount of charge delivered. We hypothesize erosion of the silicon shank accelerates damage to the electrode / tissue interface, following damage to the tip metal. These findings link quantitative measurements to the microelectrodes' physical condition and their capacity to record/stimulate. These data could lead to improved manufacturing processes or novel electrode designs to improve long-term performance of BCIs, making them vitally important as multi-year clinical trials of BCIs are becoming more common. STATEMENT OF SIGNIFICANCE: Long-term performance stability of the electrode-tissue interface is essential for clinical viability of brain computer interface (BCI) devices; currently, materials degradation is a critical component for performance loss. Across three human participants, ten micro-electrode arrays (plus one control) were implanted for 956-2130 days. Using scanning electron microscopy (SEM), we analyzed degradation of 980 electrodes, comparing two types of commonly implanted electrode tip metals: Platinum (Pt) and Sputtered Iridium Oxide Film (SIROF). We correlated observed degradation with in vivo electrode performance: recording (signal-to-noise ratio, noise, impedance) and stimulation (evoked somatosensory percepts). We hypothesize penetration of the electrode tip by biotic processes leads to erosion of the supporting silicon core, which then accelerates further tip metal damage. These data could lead to improved manufacturing processes or novel electrode designs towards the goal of a stable BCI electrical interface, spanning a multi-decade participant lifetime.

Keywords: Brain computer interface; Electrode; Intra-cortical; Scanning electron microscopy.