Cynthia A. Chestek

A high-performance neural prosthesis enabled by control algorithm design

Neural prostheses translate neural activity from the brain into control signals for guiding prosthetic devices, such as computer cursors and robotic limbs, and thus offer individuals with disabilities greater interaction with the world. However, relatively low performance remains a critical barrier to successful clinical translation; current neural prostheses are considerably slower, with less accurate control, than the native arm. Here we present a new control algorithm, the recalibrated feedback intention–trained Kalman filter (ReFIT-KF) that incorporates assumptions about the nature of closed-loop neural prosthetic control. When tested in rhesus monkeys implanted with motor cortical electrode arrays, the ReFIT-KF algorithm outperformed existing neural prosthetic algorithms in all measured domains and halved target acquisition time. This control algorithm permits sustained, uninterrupted use for hours and generalizes to more challenging tasks without retraining. Using this algorithm, we demonstrate repeatable high performance for years after implantation in two monkeys, thereby increasing the clinical viability of neural prostheses.

Wireless Neural Recording With Single Low-Power Integrated Circuit

We present benchtop and in vivo experimental results from an integrated circuit designed for wireless implantable neural recording applications. The chip, which was fabricated in a commercially available 0.6- mum 2P3M BiCMOS process, contains 100 amplifiers, a 10-bit analog-to-digital converter (ADC), 100 threshold-based spike detectors, and a 902-928 MHz frequency-shift-keying (FSK) transmitter. Neural signals from a selected amplifier are sampled by the ADC at 15.7 kSps and telemetered over the FSK wireless data link. Power, clock, and command signals are sent to the chip wirelessly over a 2.765-MHz inductive (coil-to-coil) link. The chip is capable of operating with only two off-chip components: a power/command receiving coil and a 100-nF capacitor.

Long-term stability of neural prosthetic control signals from silicon cortical arrays in rhesus macaque motor cortex

Cortically-controlled prosthetic systems aim to help disabled patients by translating neural signals from the brain into control signals for guiding prosthetic devices. Recent reports have demonstrated reasonably high levels of performance and control of computer cursors and prosthetic limbs, but to achieve true clinical viability, the long-term operation of these systems must be better understood. In particular, the quality and stability of the electrically-recorded neural signals require further characterization. Here, we quantify action potential changes and offline neural decoder performance over 382 days of recording from four intracortical arrays in three animals. Action potential amplitude decreased by 2.4% per month on average over the course of 9.4, 10.4, and 31.7 months in three animals. During most time periods, decoder performance was not well correlated with action potential amplitude (p > 0.05 for three of four arrays). In two arrays from one animal, action potential amplitude declined by an average of 37% over the first 2 months after implant. However, when using simple threshold-crossing events rather than well-isolated action potentials, no corresponding performance loss was observed during this time using an offline decoder. One of these arrays was effectively used for online prosthetic experiments over the following year. Substantial short-term variations in waveforms were quantified using a wireless system for contiguous recording in one animal, and compared within and between days for all three animals. Overall, this study suggests that action potential amplitude declines more slowly than previously supposed, and performance can be maintained over the course of multiple years when decoding from threshold-crossing events rather than isolated action potentials. This suggests that neural prosthetic systems may provide high performance over multiple years in human clinical trials.

Challenges and Opportunities for Next-Generation Intracortically Based Neural Prostheses

Neural prosthetic systems aim to help disabled patients by translating neural signals from the brain into control signals for guiding computer cursors, prosthetic arms, and other assistive devices. Intracortical electrode arrays measure action potentials and local field potentials from individual neurons, or small populations of neurons, in the motor cortices and can provide considerable information for controlling prostheses. Despite several compelling proof-of-concept laboratory animal experiments and an initial human clinical trial, at least three key challenges remain which, if left unaddressed, may hamper the translation of these systems into widespread clinical use. We review these challenges: achieving able-bodied levels of performance across tasks and across environments, achieving robustness across multiple decades, and restoring able-bodied quality proprioception and somatosensation. We also describe some emerging opportunities for meeting these challenges. If these challenges can be largely or fully met, intracortically based neural prostheses may achieve true clinical viability and help increasing numbers of disabled patients.

Single-neuron stability during repeated reaching in macaque premotor cortex.

Some movements that animals and humans make are highly stereotyped, repeated with little variation. The patterns of neural activity associated with repeats of a movement may be highly similar, or the same movement may arise from different patterns of neural activity, if the brain exploits redundancies in the neural projections to muscles. We examined the stability of the relationship between neural activity and behavior. We asked whether the variability in neural activity that we observed during repeated reaching was consistent with a noisy but stable relationship, or with a changing relationship, between neural activity and behavior. Monkeys performed highly similar reaches under tight behavioral control, while many neurons in the dorsal aspect of premotor cortex and the primary motor cortex were simultaneously monitored for several hours. Neural activity was predominantly stable over time in all measured properties: firing rate, directional tuning, and contribution to a decoding model that predicted kinematics from neural activity. The small changes in neural activity that we did observe could be accounted for primarily by subtle changes in behavior. We conclude that the relationship between neural activity and practiced behavior is reasonably stable, at least on timescales of minutes up to 48 h. This finding has significant implications for the design of neural prosthetic systems because it suggests that device recalibration need not be overly frequent, It also has implications for studies of neural plasticity because a stable baseline permits identification of nonstationary shifts.

HermesC: Low-Power Wireless Neural Recording System for Freely Moving Primates

Neural prosthetic systems have the potential to restore lost functionality to amputees or patients suffering from neurological injury or disease. Current systems have primarily been designed for immobile patients, such as tetraplegics functioning in a rather static, carefully tailored environment. However, an active patient such as amputee in a normal dynamic, everyday environment may be quite different in terms of the neural control of movement. In order to study motor control in a more unconstrained natural setting, we seek to develop an animal model of freely moving humans. Therefore, we have developed and tested HermesC-INI3, a system for recording and wirelessly transmitting neural data from electrode arrays implanted in rhesus macaques who are freely moving. This system is based on the integrated neural interface (INI3) microchip which amplifies, digitizes, and transmits neural data across a ~ 900 MHz wireless channel. The wireless transmission has a range of ~ 4 m in free space. All together this device consumes 15.8 mA and 63.2 mW. On a single 2 A-hr battery pack, this device runs contiguously for approximately six days. The smaller size and power consumption of the custom IC allows for a smaller package (51 times 38 times 38 mm3) than previous primate systems. The HermesC-INI3 system was used to record and telemeter one channel of broadband neural data at 15.7 kSps from a monkey performing routine daily activities in the home cage.

Hand posture classification using electrocorticography signals in the gamma band over human sensorimotor brain areas

OBJECTIVE Brain-machine interface systems translate recorded neural signals into command signals for assistive technology. In individuals with upper limb amputation or cervical spinal cord injury, the restoration of a useful hand grasp could significantly improve daily function. We sought to determine if electrocorticographic (ECoG) signals contain sufficient information to select among multiple hand postures for a prosthetic hand, orthotic, or functional electrical stimulation system. APPROACH We recorded ECoG signals from subdural macro- and microelectrodes implanted in motor areas of three participants who were undergoing inpatient monitoring for diagnosis and treatment of intractable epilepsy. Participants performed five distinct isometric hand postures, as well as four distinct finger movements. Several control experiments were attempted in order to remove sensory information from the classification results. Online experiments were performed with two participants. MAIN RESULTS Classification rates were 68%, 84% and 81% for correct identification of 5 isometric hand postures offline. Using 3 potential controls for removing sensory signals, error rates were approximately doubled on average (2.1×). A similar increase in errors (2.6×) was noted when the participant was asked to make simultaneous wrist movements along with the hand postures. In online experiments, fist versus rest was successfully classified on 97% of trials; the classification output drove a prosthetic hand. Online classification performance for a larger number of hand postures remained above chance, but substantially below offline performance. In addition, the long integration windows used would preclude the use of decoded signals for control of a BCI system. SIGNIFICANCE These results suggest that ECoG is a plausible source of command signals for prosthetic grasp selection. Overall, avenues remain for improvement through better electrode designs and placement, better participant training, and characterization of non-stationarities such that ECoG could be a viable signal source for grasp control for amputees or individuals with paralysis.

Neural prosthetic systems: Current problems and future directions

By decoding neural activity into useful behavioral commands, neural prosthetic systems seek to improve the lives of severely disabled human patients. Motor decoding algorithms, which map neural spiking data to control parameters of a device such as a prosthetic arm, have received particular attention in the literature. Here, we highlight several outstanding problems that exist in most current approaches to decode algorithm design. These include two problems that we argue will unlikely result in further dramatic increases in performance, specifically spike sorting and spiking models. We also discuss three issues that have been less examined in the literature, and we argue that addressing these issues may result in dramatic future increases in performance. These include: non-stationarity of recorded waveforms, limitations of a linear mappings between neural activity and movement kinematics, and the low signal to noise ratio of the neural data. We demonstrate these problems with data from 39 experimental sessions with a non-human primate performing reaches and with recent literature. In all, this study suggests that research in cortically-controlled prosthetic systems may require reprioritization to achieve performance that is acceptable for a clinically viable human system.

Performance measurement for brain–computer or brain–machine interfaces: a tutorial

OBJECTIVE Brain-computer interfaces (BCIs) have the potential to be valuable clinical tools. However, the varied nature of BCIs, combined with the large number of laboratories participating in BCI research, makes uniform performance reporting difficult. To address this situation, we present a tutorial on performance measurement in BCI research. APPROACH A workshop on this topic was held at the 2013 International BCI Meeting at Asilomar Conference Center in Pacific Grove, California. This paper contains the consensus opinion of the workshop members, refined through discussion in the following months and the input of authors who were unable to attend the workshop. MAIN RESULTS Checklists for methods reporting were developed for both discrete and continuous BCIs. Relevant metrics are reviewed for different types of BCI research, with notes on their use to encourage uniform application between laboratories. SIGNIFICANCE Graduate students and other researchers new to BCI research may find this tutorial a helpful introduction to performance measurement in the field.

Insertion of linear 8.4 μm diameter 16 channel carbon fiber electrode arrays for single unit recordings

OBJECTIVE Single carbon fiber electrodes (d = 8.4 μm) insulated with parylene-c and functionalized with PEDOT pTS have been shown to record single unit activity but manual implantation of these devices with forceps can be difficult. Without an improvement in the insertion method any increase in the channel count by fabricating carbon fiber arrays would be impractical. In this study, we utilize a water soluble coating and structural backbones that allow us to create, implant, and record from fully functionalized arrays of carbon fibers with ∼150 μm pitch. APPROACH Two approaches were tested for the insertion of carbon fiber arrays. The first method used a poly(ethylene glycol) (PEG) coating that temporarily stiffened the fibers while leaving a small portion at the tip exposed. The small exposed portion (500 μm-1 mm) readily penetrated the brain allowing for an insertion that did not require the handling of each fiber by forceps. The second method involved the fabrication of silicon support structures with individual shanks spaced 150 μm apart. Each shank consisted of a small groove that held an individual carbon fiber. MAIN RESULTS Our results showed that the PEG coating allowed for the chronic implantation of carbon fiber arrays in five rats with unit activity detected at 31 days post-implant. The silicon support structures recorded single unit activity in three acute rat surgeries. In one of those surgeries a stacked device with three layers of silicon support structures and carbon fibers was built and shown to readily insert into the brain with unit activity on select sites. SIGNIFICANCE From these studies we have found that carbon fibers spaced at ∼150 μm readily insert into the brain. This greatly increases the recording density of chronic neural probes and paves the way for even higher density devices that have a minimal scarring response.