Neural stimulation and recording performance in human sensorimotor cortex over 1500 days

Abstract

Objective: Intracortical microstimulation (ICMS) in somatosensory cortex can restore sensation to people who have lost it due to spinal cord injury or other conditions. One potential challenge for chronic ICMS is whether neural recording and stimulation can remain stable over many years. This is particularly relevant since the recording quality of implanted microelectrode arrays frequently experience degradation over time and stimulation safety has been considered a potential barrier to the clinical use of ICMS. Our objective is to evaluate stability of recordings on intracortical stimulated and non-stimulated electrodes in a human participant across a long period of implantation. Additionally, we would like to assess the ability to evoke sensations with ICMS over time.Approach: In a study investigating intracortical implants for a bidirectional brain-computer interface, we implanted microelectrode arrays with sputtered iridium oxide tips in the somatosensory cortex of a human participant with a cervical spinal cord injury. We regularly stimulated through electrodes on these microelectrode arrays to evoke tactile sensations on the hand. Here, we quantify the stability of these electrodes in comparison to non-stimulated electrodes implanted in motor cortex over 1500 days in two ways: recorded signal quality and electrode impedances. Additionally, we quantify the perceptual stability of ICMS-evoked sensations with detection thresholds.Main results: We found that recording quality, as assessed by the number of electrodes with highamplitude waveform recordings (> 100 µV), peak-to-peak voltage, noise, and signal-to-noise ratio, generally decreased over time on stimulated and non-stimulated electrodes. However, stimulated electrodes were much more likely to continue to record high-amplitude signals than non-stimulated electrodes. Interestingly, the detection thresholds for stimulus-evoked tactile sensations decreased over All rights reserved. No reuse allowed without permission. perpetuity.

Explant Analysis of Utah Electrode Arrays Implanted in Human Cortex for Brain-Computer-Interfaces

“…The difference between the final impedance values recorded in P1 and P2 can be explained by the difference in length of implantation. Previous studies have determined that impedance values of stimulated and non-stimulated intracortical electrodes decrease dramatically over the first couple of years after implantation in humans ( Hughes et al, 2021 ) and monkeys ( Suner et al, 2005 ; Chestek et al, 2011 ). Since P2 was implanted for a significantly shorter period, we would expect the electrode impedance values to be larger and more variable, which the data supports.…”

“…This interesting result indicates that despite the IrOx delamination and insulation cracking, the electrode is capable of recording neural signal. While electrodes receiving stimulation have previously been shown to be able to record signal for up to 1,500 days ( Hughes et al, 2021 ), whether this recording capability is maintained over periods of time greater than this remains to be investigated.…”

“…In recent years intracortical implants in motor cortex have been used for BCI control in primates and human participants with up to 10 degrees of freedom ( Hochberg et al, 2006 ; Santhanam et al, 2006 ; Velliste et al, 2008 ; Collinger et al, 2013 ; Wodlinger et al, 2014 ; Bouton et al, 2016 ; Ajiboye et al, 2017 ). More recently, somatosensory feedback has also been added to these systems by stimulating through electrodes in the somatosensory cortex ( Flesher et al, 2016 ; Armenta Salas et al, 2018 ; Fifer et al, 2020 ; Hughes et al, 2020 ; Flesher et al, 2021 ; Hughes et al, 2021 ). Given that intracortical BCIs require surgical implantation, they must be stable over many years to be clinically viable.…”

“…Given that intracortical BCIs require surgical implantation, they must be stable over many years to be clinically viable. This issue has been studied in both humans and primates, demonstrating that signals can be reliably recorded from electrodes in the motor cortex for over 6 years when devices do not fail, although there is considerable inter-subject variability and signals typically deteriorate over time ( Suner et al, 2005 ; Chestek et al, 2011 ; Simeral et al, 2011 ; James et al, 2013 ; Downey et al, 2018 ; Bullard et al, 2020 ; Hughes et al, 2021 ).…”

“…Using these established parameters, we would not expect stimulation to cause further damage to the brain tissue after implantation or have deleterious effects on behavior. In fact, stimulation over 5 years in a participant with these established parameters has not resulted in significant differences in signal between stimulated and non-stimulated arrays and detection thresholds have improved over time ( Hughes et al, 2021 ). However, to our knowledge there have been no post-implant examinations of the material properties of intracortical arrays implanted in humans.…”