Electrocorticographic Signals Research Articles

Real-time detection of spoken speech from unlabeled ECoG signals: A pilot study with an ALS participant.

Brain-Computer Interfaces (BCIs) hold significant promise for restoring communication in individuals with partial or complete loss of the ability to speak due to paralysis from amyotrophic lateral sclerosis (ALS), brainstem stroke, and other neurological disorders. Many of the approaches to speech decoding reported in the BCI literature have required time-aligned target representations to allow successful training - a major challenge when translating such approaches to people who have already lost their voice. In this pilot study, we made a first step toward scenarios in which no ground truth is available. We utilized a graph-based clustering approach to identify temporal segments of speech production from electrocorticographic (ECoG) signals alone. We then used the estimated speech segments to train a voice activity detection (VAD) model using only ECoG signals. We evaluated our approach using held-out open-loop recordings of a single dysarthric clinical trial participant living with ALS, and we compared the resulting performance to previous solutions trained with ground truth acoustic voice recordings. Our approach achieves a median error rate of around 0.5 seconds with respect to the actual spoken speech. Embedded into a real-time BCI, our approach is capable of providing VAD results with a latency of only 10 ms. To the best of our knowledge, our results show for the first time that speech activity can be predicted purely from unlabeled ECoG signals, a crucial step toward individuals who cannot provide this information anymore due to their neurological condition, such as patients with locked-in syndrome. ClinicalTrials.gov, registration number NCT03567213.

Novel cyclic homogeneous oscillation detection method for high accuracy and specific characterization of neural dynamics.

Determining the presence and frequency of neural oscillations is essential to understanding dynamic brain function. Traditional methods that detect peaks over 1/f noise within the power spectrum fail to distinguish between the fundamental frequency and harmonics of often highly non-sinusoidal neural oscillations. To overcome this limitation, we define fundamental criteria that characterize neural oscillations and introduce the cyclic homogeneous oscillation (CHO) detection method. We implemented these criteria based on an autocorrelation approach to determine an oscillation's fundamental frequency. We evaluated CHO by verifying its performance on simulated non-sinusoidal oscillatory bursts and validated its ability to determine the fundamental frequency of neural oscillations in electrocorticographic (ECoG), electroencephalographic (EEG), and stereoelectroencephalographic (SEEG) signals recorded from 27 human subjects. Our results demonstrate that CHO outperforms conventional techniques in accurately detecting oscillations. In summary, CHO demonstrates high precision and specificity in detecting neural oscillations in time and frequency domains. The method's specificity enables the detailed study of non-sinusoidal characteristics of oscillations, such as the degree of asymmetry and waveform of an oscillation. Furthermore, CHO can be applied to identify how neural oscillations govern interactions throughout the brain and to determine oscillatory biomarkers that index abnormal brain function.

Customized Flexible Osteoid Electrode for Traumatic Brain Injury Induced Posttraumatic Epilepsy Monitoring

AbstractTraumatic brain injury (TBI)‐induced post‐traumatic epilepsy (PTE) is a serious brain disease that causes the loss of motor functions, cognitive impairments, and even death. Real‐time and long‐term electrophysiological signal monitoring has significant implication for the treatment of patient with TBI. Brain–computer interfaces (BCIs) utilizing flexible electrodes enable accurate epilepsy identification by electrocorticography (ECoG) signal monitoring. In this study, a customized flexible osteoid electrode is developed, which contributes to demands and personal differentiation among patients with TBI. The end product of osteoid electrode after full osseointegration will be a stable and firmly integrated structure within the bone tissue, providing a secure platform for continuous electrophysiological signal monitoring. The flexibility and conductivity of the osteoid electrode enables high‐quality and long‐term epilepsy monitoring. Biocompatibility of the osteoid electrode is also demonstrated by in vitro cell experiments. Simultaneously, the porous osteoid electrode also exhibits osseointegration ability based on potential long‐term ECoG signal monitoring, which suggests its potential for the comprehensive treatment of TBI patients. This work not only introduces a potential therapeutic scaffold for TBI‐related diseases, but also provides promising techniques for clinical ECoG monitoring in patients with TBI.

Decoding micro-electrocorticographic signals by using explainable 3D convolutional neural network to predict finger movements

BackgroundElectroencephalography (EEG) and electrocorticography (ECoG) recordings have been used to decode finger movements by analyzing brain activity. Traditional methods focused on single bandpass power changes for movement decoding, utilizing machine learning models requiring manual feature extraction. New methodThis study introduces a 3D convolutional neural network (3D-CNN) model to decode finger movements using ECoG data. The model employs adaptive, explainable AI (xAI) techniques to interpret the physiological relevance of brain signals. ECoG signals from epilepsy patients during awake craniotomy were processed to extract power spectral density across multiple frequency bands. These data formed a 3D matrix used to train the 3D-CNN to predict finger trajectories. ResultsThe 3D-CNN model showed significant accuracy in predicting finger movements, with root-mean-square error (RMSE) values of 0.26–0.38 for single finger movements and 0.20–0.24 for combined movements. Explainable AI techniques, Grad-CAM and SHAP, identified the high gamma (HG) band as crucial for movement prediction, showing specific cortical regions involved in different finger movements. These findings highlighted the physiological significance of the HG band in motor control. Comparison with existing methodsThe 3D-CNN model outperformed traditional machine learning approaches by effectively capturing spatial and temporal patterns in ECoG data. The use of xAI techniques provided clearer insights into the model's decision-making process, unlike the "black box" nature of standard deep learning models. ConclusionsThe proposed 3D-CNN model, combined with xAI methods, enhances the decoding accuracy of finger movements from ECoG data. This approach offers a more efficient and interpretable solution for brain-computer interface (BCI) applications, emphasizing the HG band's role in motor control.

Gamma amplitude-envelope correlations are strongly elevated within hyperexcitable networks in focal epilepsy

Methods to quantify cortical hyperexcitability are of enormous interest for mapping epileptic networks in patients with focal epilepsy. We hypothesize that, in the resting state, cortical hyperexcitability increases firing-rate correlations between neuronal populations within seizure onset zones (SOZs). This hypothesis predicts that in the gamma frequency band (40–200 Hz), amplitude envelope correlations (AECs), a relatively straightforward measure of functional connectivity, should be elevated within SOZs compared to other areas. To test this prediction, we analyzed archived samples of interictal electrocorticographic (ECoG) signals recorded from patients who became seizure-free after surgery targeting SOZs identified by multiday intracranial recordings. We show that in the gamma band, AECs between nodes within SOZs are markedly elevated relative to those elsewhere. AEC-based node strength, eigencentrality, and clustering coefficient are also robustly increased within the SOZ with maxima in the low-gamma band (permutation test Z-scores > 8) and yield moderate discriminability of the SOZ using ROC analysis (maximal mean AUC ~ 0.73). By contrast to AECs, phase locking values (PLVs), a measure of narrow-band phase coupling across sites, and PLV-based graph metrics discriminate the seizure onset nodes weakly. Our results suggest that gamma band AECs may provide a clinically useful marker of cortical hyperexcitability in focal epilepsy.

Stability of ECoG high gamma signals during speech and implications for a speech BCI system in an individual with ALS: a year-long longitudinal study

Objective. Speech brain–computer interfaces (BCIs) have the potential to augment communication in individuals with impaired speech due to muscle weakness, for example in amyotrophic lateral sclerosis (ALS) and other neurological disorders. However, to achieve long-term, reliable use of a speech BCI, it is essential for speech-related neural signal changes to be stable over long periods of time. Here we study, for the first time, the stability of speech-related electrocorticographic (ECoG) signals recorded from a chronically implanted ECoG BCI over a 12 month period. Approach. ECoG signals were recorded by an ECoG array implanted over the ventral sensorimotor cortex in a clinical trial participant with ALS. Because ECoG-based speech decoding has most often relied on broadband high gamma (HG) signal changes relative to baseline (non-speech) conditions, we studied longitudinal changes of HG band power at baseline and during speech, and we compared these with residual high frequency noise levels at baseline. Stability was further assessed by longitudinal measurements of signal-to-noise ratio, activation ratio, and peak speech-related HG response magnitude (HG response peaks). Lastly, we analyzed the stability of the event-related HG power changes (HG responses) for individual syllables at each electrode. Main Results. We found that speech-related ECoG signal responses were stable over a range of syllables activating different articulators for the first year after implantation. Significance. Together, our results indicate that ECoG can be a stable recording modality for long-term speech BCI systems for those living with severe paralysis. Clinical Trial Information. ClinicalTrials.gov, registration number NCT03567213.

Spike-phase coupling of subthalamic neurons to posterior opercular cortex predicts speech sound accuracy.

Speech provides a rich context for understanding how cortical interactions with the basal ganglia contribute to unique human behaviors, but opportunities for direct intracranial recordings across cortical-basal ganglia networks are rare. We recorded electrocorticographic signals in the cortex synchronously with single units in the basal ganglia during awake neurosurgeries where subjects spoke syllable repetitions. We discovered that individual STN neurons have transient (200ms) spike-phase coupling (SPC) events with multiple cortical regions. The spike timing of STN neurons was coordinated with the phase of theta-alpha oscillations in the posterior supramarginal and superior temporal gyrus during speech planning and production. Speech sound errors occurred when this STN-cortical interaction was delayed. Our results suggest that the STN supports mechanisms of speech planning and auditory-sensorimotor integration during speech production that are required to achieve high fidelity of the phonological and articulatory representation of the target phoneme. These findings establish a framework for understanding cortical-basal ganglia interaction in other human behaviors, and additionally indicate that firing-rate based models are insufficient for explaining basal ganglia circuit behavior.

Purkinje cell dysfunction causes disrupted sleep in ataxic mice.

Purkinje cell dysfunction disrupts movement and causes disorders such as ataxia. Recent evidence suggests that Purkinje cell dysfunction may also alter sleep regulation. Here, we used an ataxic mouse model generated by silencing Purkinje cell neurotransmission (L7Cre;Vgatfx/fx) to better understand how cerebellar dysfunction impacts sleep physiology. We focused our analysis on sleep architecture and electrocorticography (ECoG) patterns based on their relevance to extracting physiological measurements during sleep. We found that circadian activity was unaltered in the mutant mice, although their sleep parameters and ECoG patterns were modified. The L7Cre;Vgatfx/fx mutant mice had decreased wakefulness and rapid eye movement (REM) sleep, whereas non-REM sleep was increased. The mutants had an extended latency to REM sleep, which is also observed in human patients with ataxia. Spectral analysis of ECoG signals revealed alterations in the power distribution across different frequency bands defining sleep. Therefore, Purkinje cell dysfunction may influence wakefulness and equilibrium of distinct sleep stages in ataxia. Our findings posit a connection between cerebellar dysfunction and disrupted sleep and underscore the importance of examining cerebellar circuit function in sleep disorders.

Fast, accurate, and interpretable decoding of electrocorticographic signals using dynamic mode decomposition

Dynamic mode (DM) decomposition decomposes spatiotemporal signals into basic oscillatory components (DMs). DMs can improve the accuracy of neural decoding when used with the nonlinear Grassmann kernel, compared to conventional power features. However, such kernel-based machine learning algorithms have three limitations: large computational time preventing real-time application, incompatibility with non-kernel algorithms, and low interpretability. Here, we propose a mapping function corresponding to the Grassmann kernel that explicitly transforms DMs into spatial DM (sDM) features, which can be used in any machine learning algorithm. Using electrocorticographic signals recorded during various movement and visual perception tasks, the sDM features were shown to improve the decoding accuracy and computational time compared to conventional methods. Furthermore, the components of the sDM features informative for decoding showed similar characteristics to the high-γ power of the signals, but with higher trial-to-trial reproducibility. The proposed sDM features enable fast, accurate, and interpretable neural decoding.

Distributed representations of prediction error signals across the cortical hierarchy are synergistic

A relevant question concerning inter-areal communication in the cortex is whether these interactions are synergistic. Synergy refers to the complementary effect of multiple brain signals conveying more information than the sum of each isolated signal. Redundancy, on the other hand, refers to the common information shared between brain signals. Here, we dissociated cortical interactions encoding complementary information (synergy) from those sharing common information (redundancy) during prediction error (PE) processing. We analyzed auditory and frontal electrocorticography (ECoG) signals in five common awake marmosets performing two distinct auditory oddball tasks and investigated to what extent event-related potentials (ERP) and broadband (BB) dynamics encoded synergistic and redundant information about PE processing. The information conveyed by ERPs and BB signals was synergistic even at lower stages of the hierarchy in the auditory cortex and between auditory and frontal regions. Using a brain-constrained neural network, we simulated the synergy and redundancy observed in the experimental results and demonstrated that the emergence of synergy between auditory and frontal regions requires the presence of strong, long-distance, feedback, and feedforward connections. These results indicate that distributed representations of PE signals across the cortical hierarchy can be highly synergistic.

A hierarchical recursive feature elimination algorithm to develop brain computer interface application of user behavior for statistical reasoning and decision making

BackgroundWith the aid of a brain computer interface (BCI), users can communicate and receive signals wirelessly or over wired connections to operate smart devices. A BCI classifier's architecture is quite difficult since numerous elements should be combined. These elements are made up of brain signals, which also include high levels of weak sounds that could provide reliable participant recordings of daily activities. We must use computer vision techniques to create a model in order to control those information. The high dimension and volume of signals present the classification classifier with its primary obstacles. New methodDue to this, we extracted and classified the brain activity in this study, and we also presented a novel hierarchical recursive feature elimination method that we refer to as HRFE embracing noisy additions. HRFE makes a variety of categorization suggestions to eliminate bias in classifying BCI systems of different types. We put the HRFE to the test on two BCI signal data sets—specifically, dataset I and BCI contests III—using shallow and deep convolution network classification techniques. Just a grid of assets is used to create electrocorticography (ECoG) signals on the contralateral (right) motor cortex, and these signals are recorded in the BCI contests III database. ResultsUsing ECoG signals, we choose the top 20 features that have the biggest effects on distortion and classification selection. Comparison with existing methodsThe simulation findings show that HRFE has a significant computer vision enhancement when compared to comparable feature selection methods in the literature, particularly for ECoG signal, which achieves about 93% reliability.

Online speech synthesis using a chronically implanted brain–computer interface in an individual with ALS

Brain–computer interfaces (BCIs) that reconstruct and synthesize speech using brain activity recorded with intracranial electrodes may pave the way toward novel communication interfaces for people who have lost their ability to speak, or who are at high risk of losing this ability, due to neurological disorders. Here, we report online synthesis of intelligible words using a chronically implanted brain-computer interface (BCI) in a man with impaired articulation due to ALS, participating in a clinical trial (ClinicalTrials.gov, NCT03567213) exploring different strategies for BCI communication. The 3-stage approach reported here relies on recurrent neural networks to identify, decode and synthesize speech from electrocorticographic (ECoG) signals acquired across motor, premotor and somatosensory cortices. We demonstrate a reliable BCI that synthesizes commands freely chosen and spoken by the participant from a vocabulary of 6 keywords previously used for decoding commands to control a communication board. Evaluation of the intelligibility of the synthesized speech indicates that 80% of the words can be correctly recognized by human listeners. Our results show that a speech-impaired individual with ALS can use a chronically implanted BCI to reliably produce synthesized words while preserving the participant’s voice profile, and provide further evidence for the stability of ECoG for speech-based BCIs.

A neural speech decoding framework leveraging deep learning and speech synthesis

Decoding human speech from neural signals is essential for brain–computer interface (BCI) technologies that aim to restore speech in populations with neurological deficits. However, it remains a highly challenging task, compounded by the scarce availability of neural signals with corresponding speech, data complexity and high dimensionality. Here we present a novel deep learning-based neural speech decoding framework that includes an ECoG decoder that translates electrocorticographic (ECoG) signals from the cortex into interpretable speech parameters and a novel differentiable speech synthesizer that maps speech parameters to spectrograms. We have developed a companion speech-to-speech auto-encoder consisting of a speech encoder and the same speech synthesizer to generate reference speech parameters to facilitate the ECoG decoder training. This framework generates natural-sounding speech and is highly reproducible across a cohort of 48 participants. Our experimental results show that our models can decode speech with high correlation, even when limited to only causal operations, which is necessary for adoption by real-time neural prostheses. Finally, we successfully decode speech in participants with either left or right hemisphere coverage, which could lead to speech prostheses in patients with deficits resulting from left hemisphere damage.

Automatic sleep-wake classification and Parkinson's disease recognition using multifeature fusion with support vector machine.

Sleep disturbance is a prevalent nonmotor symptom of Parkinson's disease (PD), however, assessing sleep conditions is always time-consuming and labor-intensive. In this study, we performed an automatic sleep-wake state classification and early diagnosis of PD by analyzing the electrocorticography (ECoG) and electromyogram (EMG) signals of both normal and PD rats. The study utilized ECoG power, EMG amplitude, and corticomuscular coherence values extracted from normal and PD rats to construct sleep-wake scoring models based on the support vector machine algorithm. Subsequently, we incorporated feature values that could act as diagnostic markers for PD and then retrained the models, which could encompass the identification of vigilance states and the diagnosis of PD. Features extracted from occipital ECoG signals were more suitable for constructing sleep-wake scoring models than those from frontal ECoG (average Cohen's kappa: 0.73 vs. 0.71). Additionally, after retraining, the new models demonstrated increased sensitivity to PD and accurately determined the sleep-wake states of rats (average Cohen's kappa: 0.79). This study accomplished the precise detection of substantia nigra lesions and the monitoring of sleep-wake states. The integration of circadian rhythm monitoring and disease state assessment has the potential to improve the efficacy of therapeutic strategies considerably.

Chronic subdural electrocorticography in nonhuman primates by an implantable wireless device for brain-machine interfaces.

Subdural electrocorticography (ECoG) signals have been proposed as a stable, good-quality source for brain-machine interfaces (BMIs), with a higher spatial and temporal resolution than electroencephalography (EEG). However, long-term implantation may lead to chronic inflammatory reactions and connective tissue encapsulation, resulting in a decline in signal recording quality. However, no study has reported the effects of the surrounding tissue on signal recording and device functionality thus far. In this study, we implanted a wireless recording device with a customized 32-electrode-ECoG array subdurally in two nonhuman primates for 15 months. We evaluated the neural activities recorded from and wirelessly transmitted to the devices and the chronic tissue reactions around the electrodes. In addition, we measured the gain factor of the newly formed ventral fibrous tissue in vivo. Time-frequency analyses of the acute and chronic phases showed similar signal features. The average root mean square voltage and power spectral density showed relatively stable signal quality after chronic implantation. Histological examination revealed thickening of the reactive tissue around the electrode array; however, no evident inflammation in the cortex. From gain factor analysis, we found that tissue proliferation under electrodes reduced the amplitude power of signals. This study suggests that subdural ECoG may provide chronic signal recordings for future clinical applications and neuroscience research. This study also highlights the need to reduce proliferation of reactive tissue ventral to the electrodes to enhance long-term stability.

Mapping information flow between the inferotemporal and prefrontal cortices via neural oscillations in memory retrieval and maintenance

Interaction between the inferotemporal (ITC) and prefrontal (PFC) cortices is critical for retrieving information from memory and maintaining it in working memory. Neural oscillations provide a mechanism for communication between brain regions. However, it remains unknown how information flow via neural oscillations is functionally organized in these cortices during these processes. In this study, we apply Granger causality analysis to electrocorticographic signals from both cortices of monkeys performing visual association tasks to map information flow. Our results reveal regions within the ITC where information flow to and from the PFC increases via specific frequency oscillations to form clusters during memory retrieval and maintenance. Theta-band information flow in both directions increases in similar regions in both cortices, suggesting reciprocal information exchange in those regions. These findings suggest that specific subregions function as nodes in the memory information-processing network between the ITC and the PFC.

Characterization of High-Gamma Activity in Electrocorticographic Signals.

Electrocorticographic (ECoG) high-gamma activity (HGA) is a widely recognized and robust neural correlate of cognition and behavior. However, fundamental signal properties of HGA, such as the high-gamma frequency band or temporal dynamics of HGA, have never been systematically characterized. As a result, HGA estimators are often poorly adjusted, such that they miss valuable physiological information. To address these issues, we conducted a thorough qualitative and quantitative characterization of HGA in ECoG signals. Our study is based on ECoG signals recorded from 18 epilepsy patients while performing motor control, listening, and visual perception tasks. In this study, we first categorize HGA into HGA types based on the cognitive/behavioral task. For each HGA type, we then systematically quantify three fundamental signal properties of HGA: the high-gamma frequency band, the HGA bandwidth, and the temporal dynamics of HGA. The high-gamma frequency band strongly varies across subjects and across cognitive/behavioral tasks. In addition, HGA time courses have lowpass character, with transients limited to 10 Hz. The task-related rise time and duration of these HGA time courses depend on the individual subject and cognitive/behavioral task. Task-related HGA amplitudes are comparable across the investigated tasks. This study is of high practical relevance because it provides a systematic basis for optimizing experiment design, ECoG acquisition and processing, and HGA estimation. Our results reveal previously unknown characteristics of HGA, the physiological principles of which need to be investigated in further studies.

Partial maximum correntropy regression for robust electrocorticography decoding.

The Partial Least Square Regression (PLSR) method has shown admirable competence for predicting continuous variables from inter-correlated electrocorticography signals in the brain-computer interface. However, PLSR is essentially formulated with the least square criterion, thus, being considerably prone to the performance deterioration caused by the brain recording noises. To address this problem, this study aims to propose a new robust variant for PLSR. To this end, the maximum correntropy criterion (MCC) is utilized to propose a new robust implementation of PLSR, called Partial Maximum Correntropy Regression (PMCR). The half-quadratic optimization is utilized to calculate the robust projectors for the dimensionality reduction, and the regression coefficients are optimized by a fixed-point optimization method. The proposed PMCR is evaluated with a synthetic example and a public electrocorticography dataset under three performance indicators. For the synthetic example, PMCR realized better prediction results compared with the other existing methods. PMCR could also abstract valid information with a limited number of decomposition factors in a noisy regression scenario. For the electrocorticography dataset, PMCR achieved superior decoding performance in most cases, and also realized the minimal neurophysiological pattern deterioration with the interference of the noises. The experimental results demonstrate that, the proposed PMCR could outperform the existing methods in a noisy, inter-correlated, and high-dimensional decoding task. PMCR could alleviate the performance degradation caused by the adverse noises and ameliorate the electrocorticography decoding robustness for the brain-computer interface.

Infraclavicular de novo placement of a responsive neurostimulator for a patient with eloquent glioma-associated epilepsy: illustrative case.

The authors present a 50-year-old female with high-grade glioma involving the motor cortex as the cause of her drug-resistant epilepsy (DRE). Responsive neurostimulation (RNS) was chosen for epilepsy treatment. Due to concerns regarding the generator impeding the regular imaging surveillance required for treatment and monitoring of her glioma, surgeons placed the internal pulse generator (IPG) within an infraclavicular chest pocket. Implantation of the RNS device and IPG within the infraclavicular pocket was uneventful. However, both subdural and depth electrodes were used and connected to the IPG, and subdural electrodes are considerably shorter than depth electrodes (37 vs 44 cm). The shorter strip leads presumably generated significant tension, leading to fracture of the leads. Therefore, surgery was repeated using only depth electrodes for more length and less tension. The device has good-quality electrocorticography signals that continue to be used for device programming. The seizure burden was reduced, and quality of life improved for the patient. The RNS system with infraclavicular IPG placement reduced the seizure burden and improved the quality of life of a patient with glioma-associated epilepsy. Surgeons may consider the infraclavicular location as an alternative site for implantation for RNS candidates who require recurrent intracranial magnetic resonance imaging.

Simple method for detecting sleep episodes in rats ECoG using machine learning

In this paper we propose a new method for the automatic recognition of the state of behavioral sleep (BS) and waking state (WS) in freely moving rats using their electrocorticographic (ECoG) data. Three-channels ECoG signals were recorded from frontal left, frontal right and occipital right cortical areas. We employed a simple artificial neural network (ANN), in which the mean values and standard deviations of ECoG signals from two or three channels were used as inputs for the ANN. Results of wavelet-based recognition of BS/WS in the same data were used to train the ANN and evaluate correctness of our classifier. We tested different combinations of ECoG channels for detecting BS/WS.Our results showed that the accuracy of ANN classification did not depend on ECoG-channel. For any ECoG-channel, networks were trained on one rat and applied to another rat with an accuracy of at least 80 %. Itis important that we used a very simple network topology to achieve a relatively high accuracy of classification. Our classifier was based on a simple linear combination of input signals with some weights, and these weights could be replaced by the averaged weights of all trained ANNs without decreases in classification accuracy. In all, we introduce a new sleep recognition method that does not require additional network training. It is enough to know the coefficients and the equations suggested in this paper. The proposed method showed very fast performance and simple computations, therefore it could be used in real time experiments. It might be of high demand in preclinical studies in rodents that require vigilance control or monitoring of sleep-wake patterns.