Voluntary Motor Command Release Coincides with Restricted Sensorimotor Beta Rhythm Phases.

Sensory perception and memory are enhanced during restricted phases of ongoing brain rhythms, but whether voluntary movement is constrained by brain rhythm phase is not known. Voluntary movement requires motor commands to be released from motor cortex (M1) and transmitted to spinal motoneurons and effector muscles. Here, we tested the hypothesis that motor commands are preferentially released from M1 during circumscribed phases of ongoing sensorimotor rhythms. Healthy humans of both sexes performed a self-paced finger movement task during electroencephalography (EEG) and electromyography (EMG) recordings. We first estimated the time of motor command release preceding each finger movement by subtracting individually measured corticomuscular transmission latencies from EMG-determined movement onset times. Then, we determined the phase of ipsilateral and contralateral sensorimotor mu (8-12 Hz) and beta (13-35 Hz) rhythms during release of each motor command. We report that motor commands were most often released between 120 and 140° along the contralateral beta cycle but were released uniformly along the contralateral mu cycle. Motor commands were also released uniformly along ipsilateral mu and beta cycles. Results demonstrate that motor command release coincides with restricted phases of the contralateral sensorimotor beta rhythm, suggesting that sensorimotor beta rhythm phase may sculpt the timing of voluntary human movement.SIGNIFICANCE STATEMENT Perceptual and cognitive function is optimal during specific brain rhythm phases. Although brain rhythm phase influences motor cortical neuronal activity and communication between the motor cortex and spinal cord, its role in voluntary movement is poorly understood. Here, we show that the motor commands needed to produce voluntary movements are preferentially released from the motor cortex during contralateral sensorimotor beta rhythm phases. Our findings are consistent with the notion that sensorimotor rhythm phase influences the timing of voluntary human movement.

Disentangling the origins of confidence in speeded perceptual judgments through multimodal imaging.

The human capacity to compute the likelihood that a decision is correct-known as metacognition-has proven difficult to study in isolation as it usually cooccurs with decision making. Here, we isolated postdecisional from decisional contributions to metacognition by analyzing neural correlates of confidence with multimodal imaging. Healthy volunteers reported their confidence in the accuracy of decisions they made or decisions they observed. We found better metacognitive performance for committed vs. observed decisions, indicating that committing to a decision may improve confidence. Relying on concurrent electroencephalography and hemodynamic recordings, we found a common correlate of confidence following committed and observed decisions in the inferior frontal gyrus and a dissociation in the anterior prefrontal cortex and anterior insula. We discuss these results in light of decisional and postdecisional accounts of confidence and propose a computational model of confidence in which metacognitive performance naturally improves when evidence accumulation is constrained upon committing a decision.

Sensory threshold neuromuscular electrical stimulation fosters motor imagery performance.

Motor imagery (MI) has been largely studied as a way to enhance motor learning and to restore motor functions. Although it is agreed that users should emphasize kinesthetic imagery during MI, recordings of MI brain patterns are not sufficiently reliable for many subjects. It has been suggested that the usage of somatosensory feedback would be more suitable than standardly used visual feedback to enhance MI brain patterns. However, somatosensory feedback should not interfere with the recorded MI brain pattern. In this study we propose a novel feedback modality to guide subjects during MI based on sensory threshold neuromuscular electrical stimulation (St-NMES). St-NMES depolarizes sensory and motor axons without eliciting any muscular contraction. We hypothesize that St-NMES does not induce detectable ERD brain patterns and fosters MI performance. Twelve novice subjects were included in a cross-over design study. We recorded their EEG, comparing St-NMES with visual feedback during MI or resting tasks. We found that St-NMES not only induced significantly larger desynchronization over sensorimotor areas (p<0.05) but also significantly enhanced MI brain connectivity patterns. Moreover, classification accuracy and stability were significantly higher with St-NMES. Importantly, St-NMES alone did not induce detectable artifacts, but rather the changes in the detected patterns were due to an increased MI performance. Our findings indicate that St-NMES is a promising feedback in order to foster MI performance and cold be used for BMI online applications.

Human EEG reveals distinct neural correlates of power and precision grasping types.

Hand grasping is a sophisticated motor task that has received much attention by the neuroscientific community, which demonstrated how grasping activates a network involving parietal, pre-motor and motor cortices using fMRI, ECoG, LFPs and spiking activity. Yet, there is a need for a more precise spatio-temporal analysis as it is still unclear how these brain activations over large cortical areas evolve at the sub-second level. In this study, we recorded ten human participants (1 female) performing visually-guided, self-paced reaching and grasping with precision or power grips. Following the results, we demonstrate the existence of neural correlates of grasping from broadband EEG in self-paced conditions and show how neural correlates of precision and power grasps differentially evolve as grasps unfold. 100 ms before the grasp is secured, bilateral parietal regions showed increasingly differential patterns. Afterwards, sustained differences between both grasps occurred over the bilateral motor and parietal regions, and medial pre-frontal cortex. Furthermore, these differences were sufficiently discriminable to allow single-trial decoding with 70% decoding performance. Functional connectivity revealed differences at the network level between grasps in fronto-parietal networks, in terms of upper-alpha cortical oscillatory power with a strong involvement of ipsilateral hemisphere. Our results supported the existence of fronto-parietal recurrent feedback loops, with stronger interactions for precision grips due to the finer motor control required for this grasping type.

Invariability of EEG error-related potentials during continuous feedback protocols elicited by erroneous actions at predicted or unpredicted states.

Objective.When humans perceive an erroneous action, an EEG error-related potential (ErrP) is elicited as a neural response. ErrPs have been largely investigated in discrete feedback protocols, where actions are executed at discrete steps, to enable seamless brain-computer interaction. However, there are only a few studies that investigate ErrPs in continuous feedback protocols. The objective of the present study is to better understand the differences between two types of ErrPs elicited during continuous feedback protocols, where errors may occur either at predicted or unpredicted states. We hypothesize that ErrPs of the unpredicted state is associated with longer latency as it requires higher cognitive workload to evaluate actions compared to the predicted states.Approach.Participants monitored the trajectory of an autonomous cursor that occasionally made erroneous actions on its way to the target in two conditions, namely, predicted or unpredicted states. After characterizing the ErrP waveform elicited by erroneous actions in the two conditions, we performed single-trial decoding of ErrPs in both synchronous (i.e. time-locked to the onset of the erroneous action) and asynchronous manner. Furthermore, we explored the possibility to transfer decoders built with data of one of the conditions to the other condition.Main results.As hypothesized, erroneous actions at unpredicted states gave rise to ErrPs with higher latency than erroneous actions at predicted states, a correlate of higher cognitive effort in the former condition. Moreover, ErrP decoders trained in a given condition successfully transferred to the other condition with a slight loss of classification performance. This was the case for synchronous as well as asynchronous ErrP decoding, showing the invariability of ErrPs across conditions.Significance.These results advance the characterization of ErrPs during continuous feedback protocols, enlarging the potential use of ErrPs during natural operation of brain-controlled devices as it is not necessary to have different decoders for each kind of erroneous conditions.

General principles of machine learning for brain-computer interfacing.

Brain-computer interfaces (BCIs) are systems that translate brain activity patterns into commands that can be executed by an artificial device. This enables the possibility of controlling devices such as a prosthetic arm or exoskeleton, a wheelchair, typewriting applications, or games directly by modulating our brain activity. For this purpose, BCI systems rely on signal processing and machine learning algorithms to decode the brain activity. This chapter provides an overview of the main steps required to do such a process, including signal preprocessing, feature extraction and selection, and decoding. Given the large amount of possible methods that can be used for these processes, a comprehensive review of them is beyond the scope of this chapter, and it is focused instead on the general principles that should be taken into account, as well as discussing good practices on how these methods should be applied and evaluated for proper design of reliable BCI systems.

Mechanisms of offline motor learning at a microscale of seconds in large-scale crowdsourced data.

Performance improvements during early human motor skill learning are suggested to be driven by short periods of rest during practice, at the scale of seconds. To reveal the unknown mechanisms behind these "micro-offline" gains, we leveraged the sampling power offered by online crowdsourcing (cumulative N over all experiments = 951). First, we replicated the original in-lab findings, demonstrating generalizability to subjects learning the task in their daily living environment (N = 389). Second, we show that offline improvements during rest are equivalent when significantly shortening practice period duration, thus confirming that they are not a result of recovery from performance fatigue (N = 118). Third, retroactive interference immediately after each practice period reduced the learning rate relative to interference after passage of time (N = 373), indicating stabilization of the motor memory at a microscale of several seconds. Finally, we show that random termination of practice periods did not impact offline gains, ruling out a contribution of predictive motor slowing (N = 71). Altogether, these results demonstrate that micro-offline gains indicate rapid, within-seconds consolidation accounting for early skill learning.

The Confidence Database.

Understanding how people rate their confidence is critical for the characterization of a wide range of perceptual, memory, motor and cognitive processes. To enable the continued exploration of these processes, we created a large database of confidence studies spanning a broad set of paradigms, participant populations and fields of study. The data from each study are structured in a common, easy-to-use format that can be easily imported and analysed using multiple software packages. Each dataset is accompanied by an explanation regarding the nature of the collected data. At the time of publication, the Confidence Database (which is available at https://osf.io/s46pr/) contained 145 datasets with data from more than 8,700 participants and almost 4 million trials. The database will remain open for new submissions indefinitely and is expected to continue to grow. Here we show the usefulness of this large collection of datasets in four different analyses that provide precise estimations of several foundational confidence-related effects.

A Rapid Form of Offline Consolidation in Skill Learning.

The brain strengthens memories through consolidation, defined as resistance to interference (stabilization) or performance improvements between the end of a practice session and the beginning of the next (offline gains) [1]. Typically, consolidation has been measured hours or days after the completion of training [2], but the same concept may apply to periods of rest that occur interspersed in a series of practice bouts within the same session. Here, we took an unprecedented close look at the within-seconds time course of early human procedural learning over alternating short periods of practice and rest that constitute a typical online training session. We found that performance did not markedly change over short periods of practice. On the other hand, performance improvements in between practice periods, when subjects were at rest, were significant and accounted for early procedural learning. These offline improvements were more prominent in early training trials when the learning curve was steep and no performance decrements during preceding practice periods were present. At the neural level, simultaneous magnetoencephalographic recordings showed an anatomically defined signature of this phenomenon. Beta-band brain oscillatory activity in a predominantly contralateral frontoparietal network predicted rest-period performance improvements. Consistent with its role in sensorimotor engagement [3], modulation of beta activity may reflect replay of task processes during rest periods. We report a rapid form of offline consolidation that substantially contributes to early skill learning and may extend the concept of consolidation to a time scale in the order of seconds, rather than the hours or days traditionally accepted.

Decoding Inner Speech Using Electrocorticography: Progress and Challenges Toward a Speech Prosthesis.

Certain brain disorders resulting from brainstem infarcts, traumatic brain injury, cerebral palsy, stroke, and amyotrophic lateral sclerosis, limit verbal communication despite the patient being fully aware. People that cannot communicate due to neurological disorders would benefit from a system that can infer internal speech directly from brain signals. In this review article, we describe the state of the art in decoding inner speech, ranging from early acoustic sound features, to higher order speech units. We focused on intracranial recordings, as this technique allows monitoring brain activity with high spatial, temporal, and spectral resolution, and therefore is a good candidate to investigate inner speech. Despite intense efforts, investigating how the human cortex encodes inner speech remains an elusive challenge, due to the lack of behavioral and observable measures. We emphasize various challenges commonly encountered when investigating inner speech decoding, and propose potential solutions in order to get closer to a natural speech assistive device.

Differential contributions of subthalamic beta rhythms and 1/f broadband activity to motor symptoms in Parkinson's disease.

Excessive beta oscillatory activity in the subthalamic nucleus (STN) is linked to Parkinson's Disease (PD) motor symptoms. However, previous works have been inconsistent regarding the functional role of beta activity in untreated Parkinsonian states, questioning such role. We hypothesized that this inconsistency is due to the influence of electrophysiological broadband activity -a neurophysiological indicator of synaptic excitation/inhibition ratio- that could confound measurements of beta activity in STN recordings. Here we propose a data-driven, automatic and individualized mathematical model that disentangles beta activity and 1/f broadband activity in the STN power spectrum, and investigate the link between these individual components and motor symptoms in thirteen Parkinsonian patients. We show, using both modeled and actual data, how beta oscillatory activity significantly correlates with motor symptoms (bradykinesia and rigidity) only when broadband activity is not considered in the biomarker estimations, providing solid evidence that oscillatory beta activity does correlate with motor symptoms in untreated PD states as well as the significant impact of broadband activity. These findings emphasize the importance of data-driven models and the identification of better biomarkers for characterizing symptom severity and closed-loop applications.

Workshops of the Sixth International Brain-Computer Interface Meeting: brain-computer interfaces past, present, and future.

The Sixth International Brain-Computer Interface (BCI) Meeting was held 30 May-3 June 2016 at the Asilomar Conference Grounds, Pacific Grove, California, USA. The conference included 28 workshops covering topics in BCI and brain-machine interface research. Topics included BCI for specific populations or applications, advancing BCI research through use of specific signals or technological advances, and translational and commercial issues to bring both implanted and non-invasive BCIs to market. BCI research is growing and expanding in the breadth of its applications, the depth of knowledge it can produce, and the practical benefit it can provide both for those with physical impairments and the general public. Here we provide summaries of each workshop, illustrating the breadth and depth of BCI research and highlighting important issues and calls for action to support future research and development.

Word pair classification during imagined speech using direct brain recordings.

People that cannot communicate due to neurological disorders would benefit from an internal speech decoder. Here, we showed the ability to classify individual words during imagined speech from electrocorticographic signals. In a word imagery task, we used high gamma (70-150 Hz) time features with a support vector machine model to classify individual words from a pair of words. To account for temporal irregularities during speech production, we introduced a non-linear time alignment into the SVM kernel. Classification accuracy reached 88% in a two-class classification framework (50% chance level), and average classification accuracy across fifteen word-pairs was significant across five subjects (mean = 58%; p < 0.05). We also compared classification accuracy between imagined speech, overt speech and listening. As predicted, higher classification accuracy was obtained in the listening and overt speech conditions (mean = 89% and 86%, respectively; p < 0.0001), where speech stimuli were directly presented. The results provide evidence for a neural representation for imagined words in the temporal lobe, frontal lobe and sensorimotor cortex, consistent with previous findings in speech perception and production. These data represent a proof of concept study for basic decoding of speech imagery, and delineate a number of key challenges to usage of speech imagery neural representations for clinical applications.

Analysis and asynchronous detection of gradually unfolding errors during monitoring tasks.

Human studies on cognitive control processes rely on tasks involving sudden-onset stimuli, which allow the analysis of these neural imprints to be time-locked and relative to the stimuli onset. Human perceptual decisions, however, comprise continuous processes where evidence accumulates until reaching a boundary. Surpassing the boundary leads to a decision where measured brain responses are associated to an internal, unknown onset. The lack of this onset for gradual stimuli hinders both the analyses of brain activity and the training of detectors. This paper studies electroencephalographic (EEG)-measurable signatures of human processing for sudden and gradual cognitive processes represented as a trajectory mismatch under a monitoring task. Time-locked potentials and brain-source analysis of the EEG of sudden mismatches revealed the typical components of event-related potentials and the involvement of brain structures related to cognitive control processing. For gradual mismatch events, time-locked analyses did not show any discernible EEG scalp pattern, despite related brain areas being, to a lesser extent, activated. However, and thanks to the use of non-linear pattern recognition algorithms, it is possible to train an asynchronous detector on sudden events and use it to detect gradual mismatches, as well as obtaining an estimate of their unknown onset. Post-hoc time-locked scalp and brain-source analyses revealed that the EEG patterns of detected gradual mismatches originated in brain areas related to cognitive control processing. This indicates that gradual events induce latency in the evaluation process but that similar brain mechanisms are present in sudden and gradual mismatch events. Furthermore, the proposed asynchronous detection model widens the scope of applications of brain-machine interfaces to other gradual processes.

Decoding fast-paced error-related potentials in monitoring protocols.

Error-related EEG potentials (ErrP) can be used for brain-machine interfacing (BMI). Decoding of these signals, indicating subject's perception of erroneous system decisions or actions can be used to correct these actions or to improve the overall interfacing system. Multiple studies have shown the feasibility of decoding these potentials in single-trial using different types of experimental protocols and feedback modalities. However, previously reported approaches are limited by the use of long inter-stimulus intervals (ISI > 2 s). In this work we assess if it is possible to overcome this limitation. Our results show that it is possible to decode error-related potentials elicited by stimuli presented with ISIs lower than 1 s without decrease in performance. Furthermore, the increase in the presentation rate did not increase the subject workload. This suggests that the presentation rate for ErrP-based BMI protocols using serial monitoring paradigms can be substantially increased with respect to previous works.

Teaching brain-machine interfaces as an alternative paradigm to neuroprosthetics control.

Brain-machine interfaces (BMI) usually decode movement parameters from cortical activity to control neuroprostheses. This requires subjects to learn to modulate their brain activity to convey all necessary information, thus imposing natural limits on the complexity of tasks that can be performed. Here we demonstrate an alternative and complementary BMI paradigm that overcomes that limitation by decoding cognitive brain signals associated with monitoring processes relevant for achieving goals. In our approach the neuroprosthesis executes actions that the subject evaluates as erroneous or correct, and exploits the brain correlates of this assessment to learn suitable motor behaviours. Results show that, after a short user's training period, this teaching BMI paradigm operated three different neuroprostheses and generalized across several targets. Our results further support that these error-related signals reflect a task-independent monitoring mechanism in the brain, making this teaching paradigm scalable. We anticipate this BMI approach to become a key component of any neuroprosthesis that mimics natural motor control as it enables continuous adaptation in the absence of explicit information about goals. Furthermore, our paradigm can seamlessly incorporate other cognitive signals and conventional neuroprosthetic approaches, invasive or non-invasive, to enlarge the range and complexity of tasks that can be accomplished.

Detecting intention to grasp during reaching movements from EEG.

Brain-computer interfaces (BCI) have been shown to be a promising tool in rehabilitation and assistive scenarios. Within these contexts, brain signals can be decoded and used as commands for a robotic device, allowing to translate user's intentions into motor actions in order to support the user's impaired neuro-muscular system. Recently, it has been suggested that slow cortical potentials (SCPs), negative deflections in the electroencephalographic (EEG) signals peaking around one second before the initiation of movements, might be of interest because they offer an accurate time resolution for the provided feedback. Many state-of-the-art studies exploiting SCPs have focused on decoding intention of movements related to walking and arm reaching, but up to now few studies have focused on decoding the intention to grasp, which is of fundamental importance in upper-limb tasks. In this work, we present a technique that exploits EEG to decode grasping correlates during reaching movements. Results obtained with four subjects show the existence of SCPs prior to the execution of grasping movements and how they can be used to classify, with accuracy rates greater than 70% across all subjects, the intention to grasp. Using a sliding window approach, we have also demonstrated how this intention can be decoded on average around 400 ms before the grasp movements for two out of four subjects, and after the onset of grasp itself for the two other subjects.

Exploiting Task Constraints for Self-Calibrated Brain-Machine Interface Control Using Error-Related Potentials.

This paper presents a new approach for self-calibration BCI for reaching tasks using error-related potentials. The proposed method exploits task constraints to simultaneously calibrate the decoder and control the device, by using a robust likelihood function and an ad-hoc planner to cope with the large uncertainty resulting from the unknown task and decoder. The method has been evaluated in closed-loop online experiments with 8 users using a previously proposed BCI protocol for reaching tasks over a grid. The results show that it is possible to have a usable BCI control from the beginning of the experiment without any prior calibration. Furthermore, comparisons with simulations and previous results obtained using standard calibration hint that both the quality of recorded signals and the performance of the system were comparable to those obtained with a standard calibration approach.

Brain connectivity in continuous error tasks.

Error-related potentials (ErrP) have been recently incorporated in brain-machine interfaces (BMIs) due to its ability to adapt and correct both the output of the BMI or the behavior of the machine. Most of these applications rely on synchronous tasks with different user's evaluations associated to correct and wrong events. Asynchronous detection during the continuous evaluation of the task, however, has to cope with background noise and an increased number of misdetections common in event-related potential detection. This paper studies a different characteristic that may carry additional information to be exploited by asynchronous ErrP detectors: brain connectivity coherence patterns appearing while the user monitors the continuous operation of a device. The results obtained with five subject revealed the presence of an error potential in an asynchronous reaching task an showed an increase in the coherency within the theta band.

Shared-control brain-computer interface for a two dimensional reaching task using EEG error-related potentials.

One of the main problems of EEG-based brain computer interfaces (BCIs) is their low information rate, thus for complex tasks the user needs large amounts of time to solve the task. In an attempt to reduce this time and improve the application robustness, recent works have explored shared-control strategies where the device does not only execute the decoded commands, but it is also involved in executing the task. This work proposes a shared-control BCI using error potentials for a 2D reaching task with discrete actions and states. The proposed system has several interesting properties: the system is scalable without increasing the complexity of the user's mental task; the interaction is natural for the user, as the mental task is to monitor the device performance to promote its task learning (in this context the reaching task); and the system has the potential to be combined with additional brain signals to recover or learn from interaction errors. Online control experiments were performed with four subjects, showing that it was possible to reach a goal location from any starting point within a 5×5 grid in around 23 actions (about 19 seconds of EEG signal), both with fixed goals and goals freely chosen by the users.