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1. Benchtop and bedside validation of a low-cost programmable cortical stimulator in a testbed for bi-directional brain-computer-interface research

   https://doi.org/10.3389/fnins.2022.1075971  

   Sohn, Won Joon; Lim, Jeffrey; Wang, Po T.; Pu, Haoran; Malekzadeh-Arasteh, Omid; Shaw, Susan J.; Armacost, Michelle; Gong, Hui; Kellis, Spencer; Andersen, Richard A.; et al (January 2023, Frontiers in Neuroscience)

   Introduction Bi-directional brain-computer interfaces (BD-BCI) to restore movement and sensation must achieve concurrent operation of recording and decoding of motor commands from the brain and stimulating the brain with somatosensory feedback. Methods A custom programmable direct cortical stimulator (DCS) capable of eliciting artificial sensorimotor response was integrated into an embedded BCI system to form a safe, independent, wireless, and battery powered testbed to explore BD-BCI concepts at a low cost. The BD-BCI stimulator output was tested in phantom brain tissue by assessing its ability to deliver electrical stimulation equivalent to an FDA-approved commercial electrical cortical stimulator. Subsequently, the stimulator was tested in an epilepsy patient with subcortical electrocorticographic (ECoG) implants covering the sensorimotor cortex to assess its ability to elicit equivalent responses as the FDA-approved counterpart. Additional safety features (impedance monitoring, artifact mitigation, and passive and active charge balancing mechanisms) were also implemeneted and tested in phantom brain tissue. Finally, concurrent operation with interleaved stimulation and BCI decoding was tested in a phantom brain as a proof-of-concept operation of BD-BCI system. Results The benchtop prototype BD-BCI stimulator's basic output features (current amplitude, pulse frequency, pulse width, train duration) were validated by demonstrating the output-equivalency to an FDA-approved commercial cortical electrical stimulator ( R 2 > 0.99). Charge-neutral stimulation was demonstrated with pulse-width modulation-based correction algorithm preventing steady state voltage deviation. Artifact mitigation achieved a 64.5% peak voltage reduction. Highly accurate impedance monitoring was achieved with R 2 > 0.99 between measured and actual impedance, which in-turn enabled accurate charge density monitoring. An online BCI decoding accuracy of 93.2% between instructional cues and decoded states was achieved while delivering interleaved stimulation. The brain stimulation mapping via ECoG grids in an epilepsy patient showed that the two stimulators elicit equivalent responses. Significance This study demonstrates clinical validation of a fully-programmable electrical stimulator, integrated into an embedded BCI system. This low-cost BD-BCI system is safe and readily applicable as a testbed for BD-BCI research. In particular, it provides an all-inclusive hardware platform that approximates the limitations in a near-future implantable BD-BCI. This successful benchtop/human validation of the programmable electrical stimulator in a BD-BCI system is a critical milestone toward fully-implantable BD-BCI systems. 

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2. Suppression of cortical electrostimulation artifacts using pre-whitening and null projection

   https://doi.org/10.1088/1741-2552/acf68b  

   Lim, Jeffrey; Wang, Po T; Bashford, Luke; Kellis, Spencer; Shaw, Susan J; Gong, Hui; Armacost, Michelle; Heydari, Payam; Do, An H; Andersen, Richard A; et al (September 2023, Journal of Neural Engineering)

   Abstract Objective.Invasive brain–computer interfaces (BCIs) have shown promise in restoring motor function to those paralyzed by neurological injuries. These systems also have the ability to restore sensation via cortical electrostimulation. Cortical stimulation produces strong artifacts that can obscure neural signals or saturate recording amplifiers. While front-end hardware techniques can alleviate this problem, residual artifacts generally persist and must be suppressed by back-end methods.Approach.We have developed a technique based on pre-whitening and null projection (PWNP) and tested its ability to suppress stimulation artifacts in electroencephalogram (EEG), electrocorticogram (ECoG) and microelectrode array (MEA) signals from five human subjects.Main results.In EEG signals contaminated by narrow-band stimulation artifacts, the PWNP method achieved average artifact suppression between 32 and 34 dB, as measured by an increase in signal-to-interference ratio. In ECoG and MEA signals contaminated by broadband stimulation artifacts, our method suppressed artifacts by 78%–80% and 85%, respectively, as measured by a reduction in interference index. When compared to independent component analysis, which is considered the state-of-the-art technique for artifact suppression, our method achieved superior results, while being significantly easier to implement.Significance.PWNP can potentially act as an efficient method of artifact suppression to enable simultaneous stimulation and recording in bi-directional BCIs to biomimetically restore motor function. 

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3. Artifact propagation in electrocorticography stimulation

   Lim, J.; Wang, P.T.; Shaw, S.J.; Armacost, M.; Gong, H.; Liu, C.Y.; Heydari, P.; Do, A.H.; Nenadic, Z. (May 2018, Seventh International BCI Meeting, Abstract Book)

   Introduction:Current brain-computer interfaces (BCIs) primarily rely on visual feedback. However, visual feedback may not be sufficient for applications such as movement restoration, where somatosensory feedback plays a crucial role. For electrocorticography (ECoG)-based BCIs, somatosensory feedback can be elicited by cortical surface electro-stimulation [1]. However, simultaneous cortical stimulation and recording is challenging due to stimulation artifacts. Depending on the orientation of stimulating electrodes, their distance to the recording site, and the stimulation intensity, these artifacts may overwhelm the neural signals of interest and saturate the recording bioamplifiers, making it impossible to recover the underlying information [2]. To understand how these factors affect artifact propagation, we performed a preliminary characterization of ECoG signals during cortical stimulation.Materials/Methods/ResultsECoG electrodes were implanted in a 39-year old epilepsy patient as shown in Fig. 1. Pairs of adjacent electrodes were stimulated as a part of language cortical mapping. For each stimulating pair, a charge-balanced biphasic square pulse train of current at 50 Hz was delivered for five seconds at 2, 4, 6, 8 and 10 mA. ECoG signals were recorded at 512 Hz. The signals were then high-pass filtered (≥1.5 Hz, zero phase), and the 5-second stimulation epochs were segmented. Within each epoch, artifact-induced peaks were detected for each electrode, except the stimulating pair, where signals were clipped due to amplifier saturation. These peaks were phase-locked across electrodes and were 20 ms apart, thus matching the pulse train frequency. The response was characterized by calculating the median peak within the 5-second epochs. Fig. 1 shows a representative response of the right temporal grid (RTG), with the stimulation channel at RTG electrodes 14 and 15. It also shows a hypothetical amplifier saturation contour of an implantable, bi-directional, ECoG-based BCI prototype [2], assuming the supply voltage of 2.2 V and a gain of 66 dB. Finally, we quantify the worstcase scenario by calculating the largest distance between the saturation contour and the midpoint of each stimulating channel.Discussion:Our results indicate that artifact propagation follows a dipole potential distribution with the extent of the saturation region (the interior of the white contour) proportional to the stimulation amplitude. In general, the artifacts propagated farthest when a 10 mA current was applied with the saturation regions extending from 17 to 32 mm away from the midpoint of the dipole. Consistent with the electric dipole model, this maximum spread happened along the direction of the dipole moment. An exception occurred at stimulation channel RTG11-16, for which an additional saturation contour emerged away from the dipole contour (not shown), extending the saturation region to 41 mm. Also, the worst-case scenario was observed at 6 mA stimulation amplitude. This departure could be a sign of a nonlinear, switch-like behavior, wherein additional conduction pathways could become engaged in response to sufficiently high stimulation.Significance:While ECoG stimulation is routinely performed in the clinical setting, quantitative studies of the resulting signals are lacking. Our preliminary study demonstrates that stimulation artifacts largely obey dipole distributions, suggesting that the dipole model could be used to predict artifact propagation. Further studies are necessary to ascertain whether these results hold across other subjects and combinations of stimulation/recording grids. Once completed, these studies will reveal practical design constraints for future implantable bi-directional ECoG-based BCIs. These include parameters such as the distances between and relative orientations of the stimulating and recording electrodes, the choice of the stimulating electrodes, the optimal placement of the reference electrode, and the maximum stimulation amplitude. These findings would also have important implications for the design of custom, low-power bioamplifiers for implantable bi-directional ECoG-based BCIs.References:[1] Hiremath, S. V., et al. "Human perception of electrical stimulation on the surface of somatosensory cortex." PloS one 12.5 (2017): e0176020.[2] Rouse, A. G., et al. "A chronic generalized bi-directional brain-machine interface." Journal of Neural Engineering 8.3 (2011): 036018 

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4. Artifact propagation in subdural cortical electrostimulation: Characterization and modeling

   https://doi.org/10.3389/fnins.2022.1021097  

   Lim, Jeffrey; Wang, Po T.; Shaw, Susan J.; Gong, Hui; Armacost, Michelle; Liu, Charles Y.; Do, An H.; Heydari, Payam; Nenadic, Zoran (October 2022, Frontiers in Neuroscience)

   Cortical stimulationviaelectrocorticography (ECoG) may be an effective method for inducing artificial sensation in bi-directional brain-computer interfaces (BD-BCIs). However, strong electrical artifacts caused by electrostimulation may significantly degrade or obscure neural information. A detailed understanding of stimulation artifact propagation through relevant tissues may improve existing artifact suppression techniques or inspire the development of novel artifact mitigation strategies. Our work thus seeks to comprehensively characterize and model the propagation of artifacts in subdural ECoG stimulation. To this end, we collected and analyzed data from eloquent cortex mapping procedures of four subjects with epilepsy who were implanted with subdural ECoG electrodes. From this data, we observed that artifacts exhibited phase-locking and ratcheting characteristics in the time domain across all subjects. In the frequency domain, stimulation caused broadband power increases, as well as power bursts at the fundamental stimulation frequency and its super-harmonics. The spatial distribution of artifacts followed the potential distribution of an electric dipole with a median goodness-of-fit ofR²= 0.80 across all subjects and stimulation channels. Artifacts as large as ±1,100 μV appeared anywhere from 4.43 to 38.34 mm from the stimulation channel. These temporal, spectral and spatial characteristics can be utilized to improve existing artifact suppression techniques, inspire new strategies for artifact mitigation, and aid in the development of novel cortical stimulation protocols. Taken together, these findings deepen our understanding of cortical electrostimulation and provide critical design specifications for future BD-BCI systems. 

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5. High-resolution awake mouse fMRI at 14 Tesla

   https://doi.org/10.1101/2023.12.08.570803  

   Hike, David; Liu, Xiaochen; Xie, Zeping; Zhang, Bei; Choi, Sangcheon; Zhou, Xiaoqing Alice; Liu, Andy; Murstein, Alyssa; Jiang, Yuanyuan; Devor, Anna; et al (December 2023, bioRxiv)

   Abstract High-resolution awake mouse fMRI remains challenging despite extensive efforts to address motion-induced artifacts and stress. This study introduces an implantable radiofrequency (RF) surface coil design that minimizes image distortion caused by the air/tissue interface of mouse brains while simultaneously serving as a headpost for fixation during scanning. Using a 14T scanner, high-resolution fMRI enabled brain-wide functional mapping of visual and vibrissa stimulation at 100x100x200µm resolution with a 2s per frame sampling rate. Besides activated ascending visual and vibrissa pathways, robust BOLD responses were detected in the anterior cingulate cortex upon visual stimulation and spread through the ventral retrosplenial area (VRA) with vibrissa air-puff stimulation, demonstrating higher-order sensory processing in association cortices of awake mice. In particular, the rapid hemodynamic responses in VRA upon vibrissa stimulation showed a strong correlation with the hippocampus, thalamus, and prefrontal cortical areas. Cross-correlation analysis with designated VRA responses revealed early positive BOLD signals at the contralateral barrel cortex (BC) occurring 2 seconds prior to the air-puff in awake mice with repetitive stimulation, which was not detectable with the randomized stimulation paradigm. This early BC activation indicated learned anticipation through the vibrissa system and association cortices in awake mice under continuous training of repetitive air-puff stimulation. This work establishes a high-resolution awake mouse fMRI platform, enabling brain-wide functional mapping of sensory signal processing in higher association cortical areas. Significance StatementThis awake mouse fMRI platform was developed by implementing an advanced implantable radiofrequency (RF) coil scheme, which simultaneously served as a headpost to secure the mouse head during scanning. The ultra-high spatial resolution (100x100x200µm) BOLD fMRI enabled the brain-wide mapping of activated visual and vibrissa systems during sensory stimulation in awake mice, including association cortices, e.g. anterior cingulate cortex and retrosplenial cortex, for high order sensory processing. Also, the activation of barrel cortex at 2 s prior to the air-puff indicated a learned anticipation of awake mice under continuous training of the repetitive vibrissa stimulation. 

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