Utility and lower limits of frequency detection in surface electrode stimulation for somatosensory brain-computer interface in humans.

OBJECTIVE: Stimulation of the primary somatosensory cortex (S1) has been successful in evoking artificial somatosensation in both humans and animals, but much is unknown about the optimal stimulation parameters needed to generate robust percepts of somatosensation. In this study, the authors investigated frequency as an adjustable stimulation parameter for artificial somatosensation in a closed-loop brain-computer interface (BCI) system. METHODS: Three epilepsy patients with subdural mini-electrocorticography grids over the hand area of S1 were asked to compare the percepts elicited with different stimulation frequencies. Amplitude, pulse width, and duration were held constant across all trials. In each trial, subjects experienced 2 stimuli and reported which they thought was given at a higher stimulation frequency. Two paradigms were used: first, 50 versus 100 Hz to establish the utility of comparing frequencies, and then 2, 5, 10, 20, 50, or 100 Hz were pseudorandomly compared. RESULTS: As the magnitude of the stimulation frequency was increased, subjects described percepts that were "more intense" or "faster." Cumulatively, the participants achieved 98.0% accuracy when comparing stimulation at 50 and 100 Hz. In the second paradigm, the corresponding overall accuracy was 73.3%. If both tested frequencies were less than or equal to 10 Hz, accuracy was 41.7% and increased to 79.4% when one frequency was greater than 10 Hz (p = 0.01). When both stimulation frequencies were 20 Hz or less, accuracy was 40.7% compared with 91.7% when one frequency was greater than 20 Hz (p < 0.001). Accuracy was 85% in trials in which 50 Hz was the higher stimulation frequency. Therefore, the lower limit of detection occurred at 20 Hz, and accuracy decreased significantly when lower frequencies were tested. In trials testing 10 Hz versus 20 Hz, accuracy was 16.7% compared with 85.7% in trials testing 20 Hz versus 50 Hz (p < 0.05). Accuracy was greater than chance at frequency differences greater than or equal to 30 Hz. CONCLUSIONS: Frequencies greater than 20 Hz may be used as an adjustable parameter to elicit distinguishable percepts. These findings may be useful in informing the settings and the degrees of freedom achievable in future BCI systems.

Stereotactic Frame-Based Electrode Insertion: The Accuracy of Increasingly Oblique Insertion Angles.

AIM: To investigate the relationship between planned drill approach angle and angular deviation of the stereotactically placed intracranial electrode tips. MATERIAL AND METHODS: Stereotactic electrode implantation was performed in 13 patients with drug resistant epilepsy. A total of 136 electrodes were included in our analysis. Stereotactic targets were planned on pre-operative magnetic resonance imaging (MRI) scans and implantation was carried out using a Cosman-Roberts-Wells stereotactic frame with the Ad-Tech drill guide and electrodes. Post implant electrode angles in the axial, coronal, and sagittal planes were determined from post-operative computerized tomography (CT) scans and compared with planned angles using Bland-Altman plots and linear regression. RESULTS: Qualitative assessment of correlation plots between planned and actual angles demonstrated a linear relationship for axial, coronal, and sagittal planes, with no overt angular deflection for any magnitude of the planned angle. CONCLUSION: The accuracy of CRW frame-based electrode placement using the Ad-Tech drill guide and electrodes is not significantly affected by the magnitude of the planning angle. Based on our results, oblique electrode insertion is a safe and accurate procedure.

Beta-band power modulation in the human amygdala differentiates between go/no-go responses in an arm-reaching task.

Objective. Traditionally known for its involvement in emotional processing, the amygdala's involvement in motor control remains relatively unexplored, with sparse investigations into the neural mechanisms governing amygdaloid motor movement and inhibition. This study aimed to characterize the amygdaloid beta-band (13-30 Hz) power between 'Go' and 'No-go' trials of an arm-reaching task.Approach. Ten participants with drug-resistant epilepsy implanted with stereoelectroencephalographic (SEEG) electrodes in the amygdala were enrolled in this study. SEEG data was recorded throughout discrete phases of a direct reach Go/No-go task, during which participants reached a touchscreen monitor or withheld movement based on a colored cue. Multitaper power analysis along with Wilcoxon signed-rank and Yates-correctedZtests were used to assess significant modulations of beta power between the Response and fixation (baseline) phases in the 'Go' and 'No-go' conditions.Main results. In the 'Go' condition, nine out of the ten participants showed a significant decrease in relative beta-band power during the Response phase (p⩽ 0.0499). In the 'No-go' condition, eight out of the ten participants presented a statistically significant increase in relative beta-band power during the response phase (p⩽ 0.0494). Four out of the eight participants with electrodes in the contralateral hemisphere and seven out of the eight participants with electrodes in the ipsilateral hemisphere presented significant modulation in beta-band power in both the 'Go' and 'No-go' conditions. At the group level, no significant differences were found between the contralateral and ipsilateral sides or between genders.Significance.This study reports beta-band power modulation in the human amygdala during voluntary movement in the setting of motor execution and inhibition. This finding supplements prior research in various brain regions associating beta-band power with motor control. The distinct beta-power modulation observed between these response conditions suggests involvement of amygdaloid oscillations in differentiating between motor inhibition and execution.

Understanding the human conflict processing network: A review of the literature on direct neural recordings during performance of a modified stroop task.

The Stroop Task is a well-known neuropsychological task developed to investigate conflict processing in the human brain. Our group has utilized direct intracranial neural recordings in various brain regions during performance of a modified color-word Stroop Task to gain a mechanistic understanding of non-emotional human conflict processing. The purpose of this review article is to: 1) synthesize our own studies into a model of human conflict processing, 2) review the current literature on the Stroop Task and other conflict tasks to put our research in context, and 3) describe how these studies define a network in conflict processing. The figures presented are reprinted from our prior publications and key publications referenced in the manuscript. We summarize all studies to date that employ invasive intracranial recordings in humans during performance of conflict-inducing tasks. For our own studies, we analyzed local field potentials (LFPs) from patients with implanted stereotactic electroencephalography (SEEG) electrodes, and we observed intracortical oscillation patterns as well as intercortical temporal relationships in the hippocampus, amygdala, and orbitofrontal cortex (OFC) during the cue-processing phase of a modified Stroop Task. Our findings suggest that non-emotional human conflict processing involves modulation across multiple frequency bands within and between brain structures.

A review of neurophysiological effects and efficiency of waveform parameters in deep brain stimulation.

Neurostimulation has diverse clinical applications and potential as a treatment for medically refractory movement disorders, epilepsy, and other neurological disorders. However, the parameters used to program electrodes-polarity, pulse width, amplitude, and frequency-and how they are adjusted have remained largely untouched since the 1970 s. This review summarizes the state-of-the-art in Deep Brain Stimulation (DBS) and highlights the need for further research to uncover the physiological mechanisms of neurostimulation. We focus on studies that reveal the potential for clinicians to use waveform parameters to selectively stimulate neural tissue for therapeutic benefit, while avoiding activating tissue associated with adverse effects. DBS uses cathodic monophasic rectangular pulses with passive recharging in clinical practice to treat neurological conditions such as Parkinson's Disease. However, research has shown that stimulation efficiency can be improved, and side effects reduced, through modulating parameters and adding novel waveform properties. These developments can prolong implantable pulse generator lifespan, reducing costs and surgery-associated risks. Waveform parameters can stimulate neurons based on axon orientation and intrinsic structural properties, providing clinicians with more precise targeting of neural pathways. These findings could expand the spectrum of diseases treatable with neuromodulation and improve patient outcomes.

A Phantom Study of the Spatial Precision and Accuracy of Stereotactic Localization Using Computed Tomography Imaging with the Leksell Stereotactic System.

BACKGROUND: Stereotactic localization of neurosurgical targets traditionally relies on computed tomography (CT), which is considered the optimal imaging modality for geometric accuracy. However, in-depth investigations that characterize the precision and accuracy of CT images are lacking. We used a CT phantom to examine interscanner precision and interprotocol accuracy in coordinate localization. METHODS: A polymethylacrylate phantom was scanned with Toshiba Aquilion 64 and GE Healthcare LightSpeed 16 CT scanners, using both helical and incremental single-slice (SS) image acquisition protocols. The X, Y, and Z coordinates of 94 points across 6 surfaces of the phantom were physically measured. The CT scan-derived coordinates were compared with the phantom coordinates and with each other to determine accuracy and precision, respectively. RESULTS: Using the SS imaging protocol, the mean (SD) interscanner disparity in localization was 0.93 (0.39) mm, given by the average Euclidean distance between the coordinates of the 2 scanners. This discrepancy significantly varied by axis and surface, with the greatest discrepancy in the Z-axis of 0.30 mm (95% confidence interval, 0.25-0.35; P = 0.05) and on the superior surface of 1.30 mm (95% confidence interval, 1.15-1.45; P = 0.05). SS acquisition was significantly more accurate than the helical protocol. CONCLUSIONS: We found evidence of clinically relevant inconsistency between 2 CT scanners used for stereotactic localization. SS image acquisition was superior to helical scanning with respect to localization accuracy. Interscanner consistency cannot be assumed. Institutions would benefit from identifying the errors inherent in their CT scanners.

Human neocortical electrical activity recorded on nonpenetrating microwire arrays: applicability for neuroprostheses.

OBJECT: The goal of this study was to determine whether a nonpenetrating, high-density microwire array could provide sufficient information to serve as the interface for decoding motor cortical signals. METHODS: Arrays of nonpenetrating microwires were implanted over the human motor cortex in 2 patients. The patients performed directed stereotypical reaching movements in 2 directions. The resulting data were used to determine whether the reach direction could be distinguished through a frequency power analysis. RESULTS: Correlation analysis revealed decreasing signal correlation with distance. The gamma-band power during motor planning allowed binary classification of gross directionality in the reaching movements. The degree of power change was correlated to the underlying gyral pattern. CONCLUSIONS: The nonpenetrating microwire platform showed good potential for allowing differentiated signals to be recorded with high spatial fidelity without cortical penetration.

Functional Frequency Discrimination From Cortical Somatosensory Stimulation in Humans.

Recently, efforts to produce artificial sensation through cortical stimulation of primary somatosensory cortex (PSC) in humans have proven safe and reliable. Changes in stimulation parameters like frequency and amplitude have been shown to elicit different percepts, but without clearly defined psychometric profiles. This study investigates the functionally useful limits of frequency changes on the percepts felt by three epilepsy patients with subdural electrocorticography (ECoG) grids. Subjects performing a hidden target task were stimulated with parameters of constant amplitude, pulse-width, and pulse-duration, and a randomly selected set of two frequencies (20, 30, 40, 50, 60, and 100 Hz). They were asked to decide which target had the "higher" frequency. Objectively, an increase in frequency differences was associated with an increase in perceived intensity. Reliable detection of stimulation occurred at and above 40 Hz with a lower limit of detection around 20 Hz and a just-noticeable difference estimated at less than 10 Hz. These findings suggest that frequency can be used as a reliable, adjustable parameter and may be useful in establishing settings and thresholds of functionality in future BCI systems.

Multivariate regression methods for estimating velocity of ictal discharges from human microelectrode recordings.

OBJECTIVE: Epileptiform discharges, an electrophysiological hallmark of seizures, can propagate across cortical tissue in a manner similar to traveling waves. Recent work has focused attention on the origination and propagation patterns of these discharges, yielding important clues to their source location and mechanism of travel. However, systematic studies of methods for measuring propagation are lacking. APPROACH: We analyzed epileptiform discharges in microelectrode array recordings of human seizures. The array records multiunit activity and local field potentials at 400 micron spatial resolution, from a small cortical site free of obstructions. We evaluated several computationally efficient statistical methods for calculating traveling wave velocity, benchmarking them to analyses of associated neuronal burst firing. MAIN RESULTS: Over 90% of discharges met statistical criteria for propagation across the sampled cortical territory. Detection rate, direction and speed estimates derived from a multiunit estimator were compared to four field potential-based estimators: negative peak, maximum descent, high gamma power, and cross-correlation. Interestingly, the methods that were computationally simplest and most efficient (negative peak and maximal descent) offer non-inferior results in predicting neuronal traveling wave velocities compared to the other two, more complex methods. Moreover, the negative peak and maximal descent methods proved to be more robust against reduced spatial sampling challenges. Using least absolute deviation in place of least squares error minimized the impact of outliers, and reduced the discrepancies between local field potential-based and multiunit estimators. SIGNIFICANCE: Our findings suggest that ictal epileptiform discharges typically take the form of exceptionally strong, rapidly traveling waves, with propagation detectable across millimeter distances. The sequential activation of neurons in space can be inferred from clinically-observable EEG data, with a variety of straightforward computation methods available. This opens possibilities for systematic assessments of ictal discharge propagation in clinical and research settings.

The ictal wavefront is the spatiotemporal source of discharges during spontaneous human seizures.

The extensive distribution and simultaneous termination of seizures across cortical areas has led to the hypothesis that seizures are caused by large-scale coordinated networks spanning these areas. This view, however, is difficult to reconcile with most proposed mechanisms of seizure spread and termination, which operate on a cellular scale. We hypothesize that seizures evolve into self-organized structures wherein a small seizing territory projects high-intensity electrical signals over a broad cortical area. Here we investigate human seizures on both small and large electrophysiological scales. We show that the migrating edge of the seizing territory is the source of travelling waves of synaptic activity into adjacent cortical areas. As the seizure progresses, slow dynamics in induced activity from these waves indicate a weakening and eventual failure of their source. These observations support a parsimonious theory for how large-scale evolution and termination of seizures are driven from a small, migrating cortical area.

Information transfer along the ventral auditory processing stream in the awake macaque.

Few studies have examined the physiology of the auditory cortical processing streams in the context of information transfer among cortical areas. This study examines information transfer in two cortical areas in the ventral auditory processing stream in an awake macaque. We show conditional information examined over different durations of neural responses provides insight into the time scale and direction of cortical hierarchical processing.