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 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 (vSMC) in a clinical trial participant with ALS. Because ECoG-based speech decoding has most often relied on broadband high gamma signal changes relative to baseline (non-speech) conditions, we studied longitudinal changes of high gamma band (HG) power at baseline and during speech, and we compared these with residual high frequency (HF) noise levels at baseline. Stability was further assessed by longitudinal measurements of signal-to-noise ratio (SNR), activation ratio (ActR), 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. CLINICALTRIALS: gov, registration number NCT03567213.

Boosting brain-computer interfaces with functional electrical stimulation: potential applications in people with locked-in syndrome.

Individuals with a locked-in state live with severe whole-body paralysis that limits their ability to communicate with family and loved ones. Recent advances in brain-computer interface (BCI) technology have presented a potential alternative for these people to communicate by detecting neural activity associated with attempted hand or speech movements and translating the decoded intended movements to a control signal for a computer. A technique that could potentially enrich the communication capacity of BCIs is functional electrical stimulation (FES) of paralyzed limbs and face to restore body and facial movements of paralyzed individuals, allowing to add body language and facial expression to communication BCI utterances. Here, we review the current state of the art of existing BCI and FES work in people with paralysis of body and face and propose that a combined BCI-FES approach, which has already proved successful in several applications in stroke and spinal cord injury, can provide a novel promising mode of communication for locked-in individuals.

Stable Decoding from a Speech BCI Enables Control for an Individual with ALS without Recalibration for 3 Months.

Brain-computer interfaces (BCIs) can be used to control assistive devices by patients with neurological disorders like amyotrophic lateral sclerosis (ALS) that limit speech and movement. For assistive control, it is desirable for BCI systems to be accurate and reliable, preferably with minimal setup time. In this study, a participant with severe dysarthria due to ALS operates computer applications with six intuitive speech commands via a chronic electrocorticographic (ECoG) implant over the ventral sensorimotor cortex. Speech commands are accurately detected and decoded (median accuracy: 90.59%) throughout a 3-month study period without model retraining or recalibration. Use of the BCI does not require exogenous timing cues, enabling the participant to issue self-paced commands at will. These results demonstrate that a chronically implanted ECoG-based speech BCI can reliably control assistive devices over long time periods with only initial model training and calibration, supporting the feasibility of unassisted home use.

Using fMRI to localize target regions for implanted brain-computer interfaces in locked-in syndrome.

OBJECTIVE: Electrocorticography (ECoG)-based brain-computer interface (BCI) systems have the potential to improve quality of life of people with locked-in syndrome (LIS) by restoring their ability to communicate independently. Before implantation of such a system, it is important to localize ECoG electrode target regions. Here, we assessed the predictive value of functional magnetic resonance imaging (fMRI) for the localization of suitable target regions on the sensorimotor cortex for ECoG-based BCI in people with locked-in syndrome. METHODS: Three people with locked-in syndrome were implanted with a chronic, fully implantable ECoG-BCI system. We compared pre-surgical fMRI activity with post-implantation ECoG activity from areas known to be active and inactive during attempted hand movement (sensorimotor hand region and dorsolateral prefrontal cortex, respectively). RESULTS: Results showed a spatial match between fMRI activity and changes in ECoG low and high frequency band power (10 - 30 and 65 - 95 Hz, respectively) during attempted movement. Also, we found that fMRI can be used to select a sub-set of electrodes that show strong task-related signal changes that are therefore likely to generate adequate BCI control. CONCLUSIONS: Our findings indicate that fMRI is a useful non-invasive tool for the pre-surgical workup of BCI implant candidates. SIGNIFICANCE: If these results are confirmed in more BCI studies, fMRI might be used for more efficient surgical BCI procedures with focused cortical coverage and lower participant burden.

Association between lesion location and sensorimotor rhythms in stroke - a systematic review with narrative synthesis.

BACKGROUND: Stroke causes alterations in the sensorimotor rhythms (SMRs) of the brain. However, little is known about the influence of lesion location on the SMRs. Understanding this relationship is relevant for the use of SMRs in assistive and rehabilitative therapies, such as Brain-Computer Interfaces (BCIs).. METHODS: We reviewed current evidence on the association between stroke lesion location and SMRs through systematically searching PubMed and Embase and generated a narrative synthesis of findings. RESULTS: We included 12 articles reporting on 161 patients. In resting-state studies, cortical and pontine damage were related to an overall decrease in alpha (∼8-12 Hz) and increase in delta (∼1-4 Hz) power. In movement paradigm studies, attenuated alpha and beta (∼15-25 Hz) event-related desynchronization (ERD) was shown in stroke patients during (attempted) paretic hand movement, compared to controls. Stronger reductions in alpha and beta ERD in the ipsilesional, compared to contralesional hemisphere, were observed for cortical lesions. Subcortical stroke was found to affect bilateral ERD and ERS, but results were highly variable. CONCLUSIONS: Findings suggest a link between stroke lesion location and SMR alterations, but heterogeneity across studies and limited lesion location descriptions precluded a meta-analysis. SIGNIFICANCE: Future research would benefit from more uniformly defined outcome measures, homogeneous methodologies, and improved lesion location reporting.

Direct speech reconstruction from sensorimotor brain activity with optimized deep learning models.

Objective.Development of brain-computer interface (BCI) technology is key for enabling communication in individuals who have lost the faculty of speech due to severe motor paralysis. A BCI control strategy that is gaining attention employs speech decoding from neural data. Recent studies have shown that a combination of direct neural recordings and advanced computational models can provide promising results. Understanding which decoding strategies deliver best and directly applicable results is crucial for advancing the field.Approach.In this paper, we optimized and validated a decoding approach based on speech reconstruction directly from high-density electrocorticography recordings from sensorimotor cortex during a speech production task.Main results.We show that (1) dedicated machine learning optimization of reconstruction models is key for achieving the best reconstruction performance; (2) individual word decoding in reconstructed speech achieves 92%-100% accuracy (chance level is 8%); (3) direct reconstruction from sensorimotor brain activity produces intelligible speech.Significance.These results underline the need for model optimization in achieving best speech decoding results and highlight the potential that reconstruction-based speech decoding from sensorimotor cortex can offer for development of next-generation BCI technology for communication.

Nine decades of electrocorticography: A comparison between epidural and subdural recordings.

In recent years, electrocorticography (ECoG) has arisen as a neural signal recording tool in the development of clinically viable neural interfaces. ECoG electrodes are generally placed below the dura mater (subdural) but can also be placed on top of the dura (epidural). In deciding which of these modalities best suits long-term implants, complications and signal quality are important considerations. Conceptually, epidural placement may present a lower risk of complications as the dura is left intact but also a lower signal quality due to the dura acting as a signal attenuator. The extent to which complications and signal quality are affected by the dura, however, has been a matter of debate. To improve our understanding of the effects of the dura on complications and signal quality, we conducted a literature review. We inventorized the effect of the dura on signal quality, decodability and longevity of acute and chronic ECoG recordings in humans and non-human primates. Also, we compared the incidence and nature of serious complications in studies that employed epidural and subdural ECoG. Overall, we found that, even though epidural recordings exhibit attenuated signal amplitude over subdural recordings, particularly for high-density grids, the decodability of epidural recorded signals does not seem to be markedly affected. Additionally, we found that the nature of serious complications was comparable between epidural and subdural recordings. These results indicate that both epidural and subdural ECoG may be suited for long-term neural signal recordings, at least for current generations of clinical and high-density ECoG grids.

Brain-Computer interfaces for communication: preferences of individuals with locked-in syndrome, caregivers and researchers.

OBJECTIVES: The development of Brain-Computer Interfaces to restore communication (cBCIs) in people with severe motor impairment ideally relies on a close collaboration between end-users and other stakeholders, such as caregivers and researchers. Awareness about potential differences in opinion between these groups is crucial for development of usable cBCIs and access technology (AT) in general. In this study, we compared the opinions of prospective cBCI users, their caregivers and cBCI researchers regarding: (1) what applications would users like to control with a cBCI; (2) what mental strategies would users prefer to use for cBCI control; and (3) at what stage of their clinical trajectory would users like to be informed about AT and cBCIs. METHODS: We collected data from 28 individuals with locked-in syndrome, 29 of their caregivers and 28 cBCI researchers. The questionnaire was supported with animation videos to explain different cBCI concepts, the utility of which was also assessed. RESULTS: Opinions of the three groups were aligned with respect to the most desired cBCI applications, but diverged regarding mental strategies and the timing of being informed about cBCIs. Animation videos were regarded as clear and useful tools to explain cBCIs and mental strategies to end-users and other stakeholders. CONCLUSIONS: Disagreements were clear between stakeholders regarding which mental strategies users prefer to use and when they would like to be informed about cBCIs. To move forward in the development and clinical implementation of cBCIs, it will be necessary to align the research agendas with the needs of the end-users and caregivers.IMPLICATIONS FOR REHABILITATIONBrain-Computer Interfaces may offer people with severe motor impairment a brain-based and muscle-independent approach to control communication-technology. The successful development of communication BCIs (cBCIs) relies on a close collaboration between end-users and other stakeholders, such as caregivers and researchers.Our work reveals that people with locked-in syndrome (end-users), their caregivers and researchers developing cBCIs agree that direct and private forms of communication are the most desired cBCI applications, but disagree regarding the preferred mental strategies for cBCI control and when to be informed about cBCIs.Animation videos are an effective tool for providing information to individuals, independent of their level of health literacy, regarding the concept of cBCIs and mental strategies for control.The misalignment in opinions of different groups of stakeholders about cBCIs strengthens the argument for a user-centered design approach in the development of cBCIs and access technology designed for daily life usage.

Towards clinical application of implantable brain-computer interfaces for people with late-stage ALS: medical and ethical considerations.

Individuals with amyotrophic lateral sclerosis (ALS) frequently develop speech and communication problems in the course of their disease. Currently available augmentative and alternative communication technologies do not present a solution for many people with advanced ALS, because these devices depend on residual and reliable motor activity. Brain-computer interfaces (BCIs) use neural signals for computer control and may allow people with late-stage ALS to communicate even when conventional technology falls short. Recent years have witnessed fast progression in the development and validation of implanted BCIs, which place neural signal recording electrodes in or on the cortex. Eventual widespread clinical application of implanted BCIs as an assistive communication technology for people with ALS will have significant consequences for their daily life, as well as for the clinical management of the disease, among others because of the potential interaction between the BCI and other procedures people with ALS undergo, such as tracheostomy. This article aims to facilitate responsible real-world implementation of implanted BCIs. We review the state of the art of research on implanted BCIs for communication, as well as the medical and ethical implications of the clinical application of this technology. We conclude that the contribution of all BCI stakeholders, including clinicians of the various ALS-related disciplines, will be needed to develop procedures for, and shape the process of, the responsible clinical application of implanted BCIs.

Methodological Recommendations for Studies on the Daily Life Implementation of Implantable Communication-Brain-Computer Interfaces for Individuals With Locked-in Syndrome.

Implantable brain-computer interfaces (BCIs) promise to be a viable means to restore communication in individuals with locked-in syndrome (LIS). In 2016, we presented the world-first fully implantable BCI system that uses subdural electrocorticography electrodes to record brain signals and a subcutaneous amplifier to transmit the signals to the outside world, and that enabled an individual with LIS to communicate via a tablet computer by selecting icons in spelling software. For future clinical implementation of implantable communication-BCIs, however, much work is still needed, for example, to validate these systems in daily life settings with more participants, and to improve the speed of communication. We believe the design and execution of future studies on these and other topics may benefit from the experience we have gained. Therefore, based on relevant literature and our own experiences, we here provide an overview of procedures, as well as recommendations, for recruitment, screening, inclusion, imaging, hospital admission, implantation, training, and support of participants with LIS, for studies on daily life implementation of implantable communication-BCIs. With this article, we not only aim to inform the BCI community about important topics of concern, but also hope to contribute to improved methodological standardization of implantable BCI research.

Intracranial recordings show evidence of numerosity tuning in human parietal cortex.

Numerosity is the set size of a group of items. Numerosity perception is a trait shared across numerous species. Numerosity-selective neural populations are thought to underlie numerosity perception. These neurons have been identified primarily using electrical recordings in animal models and blood oxygen level dependent (BOLD) functional magnetic resonance imaging (fMRI) in humans. Here we use electrical intracranial recordings to investigate numerosity tuning in humans, focusing on high-frequency transient activations. These recordings combine a high spatial and temporal resolution and can bridge the gap between animal models and human recordings. In line with previous studies, we find numerosity-tuned responses at parietal sites in two out of three participants. Neuronal populations at these locations did not respond to other visual stimuli, i.e. faces, houses, and letters, in contrast to several occipital sites. Our findings further corroborate the specificity of numerosity tuning of in parietal cortex, and further link fMRI results and electrophysiological recordings.

Towards predicting ECoG-BCI performance: assessing the potential of scalp-EEG.

Objective. Implanted brain-computer interfaces (BCIs) employ neural signals to control a computer and may offer an alternative communication channel for people with locked-in syndrome (LIS). Promising results have been obtained using signals from the sensorimotor (SM) area. However, in earlier work on home-use of an electrocorticography (ECoG)-based BCI by people with LIS, we detected differences in ECoG-BCI performance, which were related to differences in the modulation of low frequency band (LFB) power in the SM area. For future clinical implementation of ECoG-BCIs, it will be crucial to determine whether reliable performance can be predicted before electrode implantation. To assess if non-invasive scalp-electroencephalography (EEG) could serve such prediction, we here investigated if EEG can detect the characteristics observed in the LFB modulation of ECoG signals.Approach. We included three participants with LIS of the earlier study, and a control group of 20 healthy participants. All participants performed a Rest task, and a Movement task involving actual (healthy) or attempted (LIS) hand movements, while their EEG signals were recorded.Main results.Data of the Rest task was used to determine signal-to-noise ratio, which showed a similar range for LIS and healthy participants. Using data of the Movement task, we selected seven EEG electrodes that showed a consistent movement-related decrease in beta power (13-30 Hz) across healthy participants. Within the EEG recordings of this subset of electrodes of two LIS participants, we recognized the phenomena reported earlier for the LFB in their ECoG recordings. Specifically, strong movement-related beta band suppression was observed in one, but not the other, LIS participant, and movement-related alpha band (8-12 Hz) suppression was practically absent in both. Results of the third LIS participant were inconclusive due to technical issues with the EEG recordings.Significance. Together, these findings support a potential role for scalp EEG in the presurgical assessment of ECoG-BCI candidates.

Advances in human intracranial electroencephalography research, guidelines and good practices.

Since the second-half of the twentieth century, intracranial electroencephalography (iEEG), including both electrocorticography (ECoG) and stereo-electroencephalography (sEEG), has provided an intimate view into the human brain. At the interface between fundamental research and the clinic, iEEG provides both high temporal resolution and high spatial specificity but comes with constraints, such as the individual's tailored sparsity of electrode sampling. Over the years, researchers in neuroscience developed their practices to make the most of the iEEG approach. Here we offer a critical review of iEEG research practices in a didactic framework for newcomers, as well addressing issues encountered by proficient researchers. The scope is threefold: (i) review common practices in iEEG research, (ii) suggest potential guidelines for working with iEEG data and answer frequently asked questions based on the most widespread practices, and (iii) based on current neurophysiological knowledge and methodologies, pave the way to good practice standards in iEEG research. The organization of this paper follows the steps of iEEG data processing. The first section contextualizes iEEG data collection. The second section focuses on localization of intracranial electrodes. The third section highlights the main pre-processing steps. The fourth section presents iEEG signal analysis methods. The fifth section discusses statistical approaches. The sixth section draws some unique perspectives on iEEG research. Finally, to ensure a consistent nomenclature throughout the manuscript and to align with other guidelines, e.g., Brain Imaging Data Structure (BIDS) and the OHBM Committee on Best Practices in Data Analysis and Sharing (COBIDAS), we provide a glossary to disambiguate terms related to iEEG research.

Open multimodal iEEG-fMRI dataset from naturalistic stimulation with a short audiovisual film.

Intracranial human recordings are a valuable and rare resource of information about the brain. Making such data publicly available not only helps tackle reproducibility issues in science, it helps make more use of these valuable data. This is especially true for data collected using naturalistic tasks. Here, we describe a dataset collected from a large group of human subjects while they watched a short audiovisual film. The dataset has several unique features. First, it includes a large amount of intracranial electroencephalography (iEEG) data (51 participants, age range of 5-55 years, who all performed the same task). Second, it includes functional magnetic resonance imaging (fMRI) recordings (30 participants, age range of 7-47) during the same task. Eighteen participants performed both iEEG and fMRI versions of the task, non-simultaneously. Third, the data were acquired using a rich audiovisual stimulus, for which we provide detailed speech and video annotations. This dataset can be used to study neural mechanisms of multimodal perception and language comprehension, and similarity of neural signals across brain recording modalities.

FMRI and intra-cranial electrocorticography recordings in the same human subjects reveals negative BOLD signal coupled with silenced neuronal activity.

Positive blood oxygenation level-dependent (BOLD) responses (PBR), as measured by functional Magnetic Resonance Imaging (fMRI), are the most utilized measurements to non-invasively map activity in the brain. Recent studies have consistently shown that BOLD responses are not exclusively positive. Negative BOLD responses (NBR) have been reported in response to specific sensory stimulations and tasks. However, the exact relationship between NBR and the underlying metabolic and neuronal demand is still under debate. In this study, we investigated the neurophysiological basis of negative BOLD using fMRI and intra-cranial electrophysiology (electrocorticography, ECoG) measurements from the same human participants. We show that, for those electrodes that responded to visual stimulation, PBR are correlated with high-frequency band (HFB) responses. Crucially, NBR were associated with an absence of HFB power responses and an unpredicted decrease in the alpha power responses.

Workshops of the Eighth International Brain-Computer Interface Meeting: BCIs: The Next Frontier.

The Eighth International Brain-Computer Interface (BCI) Meeting was held June 7-9th, 2021 in a virtual format. The conference continued the BCI Meeting series' interactive nature with 21 workshops covering topics in BCI (also called brain-machine interface) research. As in the past, workshops covered the breadth of topics in BCI. Some workshops provided detailed examinations of specific methods, hardware, or processes. Others focused on specific BCI applications or user groups. Several workshops continued consensus building efforts designed to create BCI standards and increase the ease of comparisons between studies and the potential for meta-analysis and large multi-site clinical trials. Ethical and translational considerations were both the primary topic for some workshops or an important secondary consideration for others. The range of BCI applications continues to expand, with more workshops focusing on approaches that can extend beyond the needs of those with physical impairments. This paper summarizes each workshop, provides background information and references for further study, presents an overview of the discussion topics, and describes the conclusion, challenges, or initiatives that resulted from the interactions and discussion at the workshop.

Distinct representation of ipsilateral hand movements in sensorimotor areas.

There is ample evidence that the contralateral sensorimotor areas play an important role in movement generation, with the primary motor cortex and the primary somatosensory cortex showing a detailed spatial organization of the representation of contralateral body parts. Interestingly, there are also indications for a role of the motor cortex in controlling the ipsilateral side of the body. However, the precise function of ipsilateral sensorimotor cortex in unilateral movement control is still unclear. Here, we show hand movement representation in the ipsilateral sensorimotor hand area, in which hand gestures can be distinguished from each other and from contralateral hand gestures. High-field functional magnetic resonance imaging (fMRI) data acquired during the execution of six left- and six right-hand gestures by healthy volunteers showed ipsilateral activation mainly in the anterior section of precentral gyrus and the posterior section of the postcentral gyrus. Despite the lower activation in ipsilateral areas closer to the central sulcus, activity patterns for the 12 hand gestures could be mutually distinguished in these areas. The existence of a unique representation of ipsilateral hand movements in the human sensorimotor cortex favours the notion of transcallosal integrative processes that support optimal coordination of hand movements.

Narrative comprehension and production abilities of children with 22q11.2 deletion syndrome.

BACKGROUND: The 22q11.2 Deletion Syndrome (22q11DS) is associated with language deficits and weak intellectual functioning. In other clinical groups, linguistic and cognitive difficulties have been associated with impaired acquisition of narrative abilities. However, little is known about the narrative abilities of children with 22q11DS. AIMS: To describe the ability of children with 22q11DS to produce and comprehend narrative macrostructure. Additionally, to examine the role of intellectual functioning in explaining their narrative difficulties. METHODS AND PROCEDURES: Narrative skills of 14 school-aged children with 22q11DS were compared to those of younger typically developing (TD) children matched on mental age and same-aged peers with Developmental Language Disorder (DLD). OUTCOMES AND RESULTS: Children with 22q11DS had significantly lower scores on narrative comprehension than younger TD children. No significant differences emerged on narrative production. Children with 22q11DS and children with DLD did not differ significantly on any of the narrative measures. CONCLUSIONS AND IMPLICATIONS: Narrative comprehension in children with 22q11DS seems more affected than production. Narrative comprehension difficulties cannot be entirely explained by a low level of intellectual functioning. Narrative comprehension and production abilities in 22q11DS require further consideration.

Decoding four hand gestures with a single bipolar pair of electrocorticography electrodes.

Objective.Electrocorticography (ECoG) based brain-computer interfaces (BCIs) can be used to restore communication in individuals with locked-in syndrome. In motor-based BCIs, the number of degrees-of-freedom, and thus the speed of the BCI, directly depends on the number of classes that can be discriminated from the neural activity in the sensorimotor cortex. When considering minimally invasive BCI implants, the size of the subdural ECoG implant must be minimized without compromising the number of degrees-of-freedom.Approach.Here we investigated if four hand gestures could be decoded using a single ECoG strip of four consecutive electrodes spaced 1 cm apart and compared the performance between a unipolar and a bipolar montage. For that we collected data of seven individuals with intractable epilepsy implanted with ECoG grids, covering the hand region of the sensorimotor cortex. Based on the implanted grids, we generated virtual ECoG strips and compared the decoding accuracy between (a) a single unipolar electrode (Unipolar Electrode), (b) a combination of four unipolar electrodes (Unipolar Strip), (c) a single bipolar pair (Bipolar Pair) and (d) a combination of six bipolar pairs (Bipolar Strip).Main results.We show that four hand gestures can be equally well decoded using 'Unipolar Strips' (mean 67.4 ± 11.7%), 'Bipolar Strips' (mean 66.6 ± 12.1%) and 'Bipolar Pairs' (mean 67.6 ± 9.4%), while 'Unipolar Electrodes' (61.6 ± 5.9%) performed significantly worse compared to 'Unipolar Strips' and 'Bipolar Pairs'.Significance.We conclude that a single bipolar pair is a potential candidate for minimally invasive motor-based BCIs and encourage the use of ECoG as a robust and reliable BCI platform for multi-class movement decoding.

Reduced brain activation during spoken language processing in children with developmental language disorder and children with 22q11.2 deletion syndrome.

Language difficulties of children with Developmental Language Disorder (DLD) have been associated with multiple underlying factors and are still poorly understood. One way of investigating the mechanisms of DLD language problems is to compare language-related brain activation patterns of children with DLD to those of a population with similar language difficulties and a uniform etiology. Children with 22q11.2 deletion syndrome (22q11DS) constitute such a population. Here, we conducted an fMRI study, in which children (6-10yo) with DLD and 22q11DS listened to speech alternated with reversed speech. We compared language laterality and language-related brain activation levels with those of typically developing (TD) children who performed the same task. The data revealed no significant differences between groups in language lateralization, but task-related activation levels were lower in children with language impairment than in TD children in several nodes of the language network. We conclude that language impairment in children with DLD and in children with 22q11DS may involve (partially) overlapping cortical areas.