Discrimination of finger movements by magnetomyography with optically pumped magnetometers.

Optically pumped magnetometers (OPM) are quantum sensors that offer new possibilities to measure biomagnetic signals. Compared to the current standard surface electromyography (EMG), in magnetomyography (MMG), OPM sensors offer the advantage of contactless measurements of muscle activity. However, little is known about the relative performance of OPM-MMG and EMG, e.g. in their ability to detect and classify finger movements. To address this in a proof-of-principle study, we recorded simultaneous OPM-MMG and EMG of finger flexor muscles for the discrimination of individual finger movements on a single human participant. Using a deep learning model for movement classification, we found that both sensor modalities were able to discriminate finger movements with above 89% accuracy. Furthermore, model predictions for the two sensor modalities showed high agreement in movement detection (85% agreement; Cohen's kappa: 0.45). Our findings show that OPM sensors can be employed for contactless discrimination of finger movements and incentivize future applications of OPM in magnetomyography.

Mental Tasks Modulate Motor-Units Above 10 Hz and are a Potential Control Signal for Movement Augmentation: a Preliminary Study.

Spinal motor neurons receive a wide range of input frequencies. However, only frequencies below ca. 10 Hz are directly translated into motor output. Frequency components above 10 Hz are filtered out by neural pathways and muscle dynamics. These higher frequency components may have an indirect effect on motor output, or may simply represent movement-independent oscillations that leak down from supraspinal areas such as the motor cortex. If movement-independent oscillations leak down from supraspinal areas, they could provide a potential control signal in movement augmentation applications. We analysed high-density electromyography (HD-EMG) signals from the tibialis anterior muscle while human subjects performed various mental tasks. The subjects performed an isometric dorsiflexion of the right foot at a low level of force while simultaneously (1) imagining a movement of the right foot, (2) imagining a movement of both hands, (3) performing a mathematical task, or (4) performing no additional task. We classified the channel-averaged HD-EMG signals and the cumulative spike train (CST) of motor-units using a filter bank and a linear classifier. We found that in some subjects, the mental task can be classified from the channel-averaged HD-EMG signals and the CST in oscillations above 10 Hz. Furthermore, we found that these oscillation modulations are incompatible with a systematic and task-dependent change in force level. Our preliminary findings from a limited number of subjects suggest that some mental task-induced oscillations from supraspinal areas leak down to spinal motor neurons and are discriminable via EMG or CST signals at the innervated muscle.

Morphology, Connectivity, and Encoding Features of Tactile and Motor Representations of the Fingers in the Human Precentral and Postcentral Gyrus.

Despite the tight coupling between sensory and motor processing for fine manipulation in humans, it is not yet totally clear which specific properties of the fingers are mapped in the precentral and postcentral gyrus. We used fMRI to compare the morphology, connectivity, and encoding of the motor and tactile finger representations (FRs) in the precentral and postcentral gyrus of 25 5-fingered participants (8 females). Multivoxel pattern and structural and functional connectivity analyses demonstrated the existence of distinct motor and tactile FRs within both the precentral and postcentral gyrus, integrating finger-specific motor and tactile information. Using representational similarity analysis, we found that the motor and tactile FRs in the sensorimotor cortex were described by the perceived structure of the hand better than by the actual hand anatomy or other functional models (finger kinematics, muscles synergies). We then studied a polydactyly individual (i.e., with a congenital 6-fingered hand) showing superior manipulation abilities and divergent anatomic-functional hand properties. The perceived hand model was still the best model for tactile representations in the precentral and postcentral gyrus, while finger kinematics better described motor representations in the precentral gyrus. We suggest that, under normal conditions (i.e., in subjects with a standard hand anatomy), the sensorimotor representations of the 5 fingers in humans converge toward a model of perceived hand anatomy, deviating from the real hand structure, as the best synthesis between functional and structural features of the hand.SIGNIFICANCE STATEMENT Distinct motor and tactile finger representations exist in both the precentral and postcentral gyrus, supported by a finger-specific pattern of anatomic and functional connectivity across modalities. At the representational level, finger representations reflect the perceived structure of the hand, which might result from an adapting process harmonizing (i.e., uniformizing) the encoding of hand function and structure in the precentral and postcentral gyrus. The same analyses performed in an extremely rare polydactyly subject showed that the emergence of such representational geometry is also found in neuromechanical variants with different hand anatomy and function. However, the harmonization process across the precentral and postcentral gyrus might not be possible because of divergent functional-structural properties of the hand and associated superior manipulation abilities.

The control and training of single motor units in isometric tasks are constrained by a common input signal.

Recent developments in neural interfaces enable the real-time and non-invasive tracking of motor neuron spiking activity. Such novel interfaces could provide a promising basis for human motor augmentation by extracting potentially high-dimensional control signals directly from the human nervous system. However, it is unclear how flexibly humans can control the activity of individual motor neurons to effectively increase the number of degrees of freedom available to coordinate multiple effectors simultaneously. Here, we provided human subjects (N = 7) with real-time feedback on the discharge patterns of pairs of motor units (MUs) innervating a single muscle (tibialis anterior) and encouraged them to independently control the MUs by tracking targets in a 2D space. Subjects learned control strategies to achieve the target-tracking task for various combinations of MUs. These strategies rarely corresponded to a volitional control of independent input signals to individual MUs during the onset of neural activity. Conversely, MU activation was consistent with a common input to the MU pair, while individual activation of the MUs in the pair was predominantly achieved by alterations in de-recruitment order that could be explained by history-dependent changes in motor neuron excitability. These results suggest that flexible MU recruitment based on independent synaptic inputs to single MUs is unlikely, although de-recruitment might reflect varying inputs or modulations in the neuron's intrinsic excitability.

Distinct neurocomputational mechanisms support informational and socially normative conformity.

A change of mind in response to social influence could be driven by informational conformity to increase accuracy, or by normative conformity to comply with social norms such as reciprocity. Disentangling the behavioural, cognitive, and neurobiological underpinnings of informational and normative conformity have proven elusive. Here, participants underwent fMRI while performing a perceptual task that involved both advice-taking and advice-giving to human and computer partners. The concurrent inclusion of 2 different social roles and 2 different social partners revealed distinct behavioural and neural markers for informational and normative conformity. Dorsal anterior cingulate cortex (dACC) BOLD response tracked informational conformity towards both human and computer but tracked normative conformity only when interacting with humans. A network of brain areas (dorsomedial prefrontal cortex (dmPFC) and temporoparietal junction (TPJ)) that tracked normative conformity increased their functional coupling with the dACC when interacting with humans. These findings enable differentiating the neural mechanisms by which different types of conformity shape social changes of mind.

Principles of human movement augmentation and the challenges in making it a reality.

Augmenting the body with artificial limbs controlled concurrently to one's natural limbs has long appeared in science fiction, but recent technological and neuroscientific advances have begun to make this possible. By allowing individuals to achieve otherwise impossible actions, movement augmentation could revolutionize medical and industrial applications and profoundly change the way humans interact with the environment. Here, we construct a movement augmentation taxonomy through what is augmented and how it is achieved. With this framework, we analyze augmentation that extends the number of degrees-of-freedom, discuss critical features of effective augmentation such as physiological control signals, sensory feedback and learning as well as application scenarios, and propose a vision for the field.

Motor skill learning decreases movement variability and increases planning horizon.

We investigated motor skill learning using a path tracking task, where human subjects had to track various curved paths at a constant speed while maintaining the cursor within the path width. Subjects' accuracy increased with practice, even when tracking novel untrained paths. Using a "searchlight" paradigm, where only a short segment of the path ahead of the cursor was shown, we found that subjects with a higher tracking skill differed from the novice subjects in two respects. First, they had lower movement variability, in agreement with previous findings. Second, they took a longer section of the future path into account when performing the task, i.e., had a longer planning horizon. We estimate that between one-third and one-half of the performance increase in the expert group was due to the longer planning horizon. An optimal control model with a fixed horizon (receding horizon control) that increases with tracking skill quantitatively captured the subjects' movement behavior. These findings demonstrate that human subjects not only increase their motor acuity but also their planning horizon when acquiring a motor skill.NEW & NOTEWORTHY We show that when learning a motor skill humans are using information about the environment from an increasingly longer amount of the movement path ahead to improve performance. Crucial features of the behavioral performance can be captured by modeling the behavioral data with a receding horizon optimal control model.

Reciprocity of social influence.

Humans seek advice, via social interaction, to improve their decisions. While social interaction is often reciprocal, the role of reciprocity in social influence is unknown. Here, we tested the hypothesis that our influence on others affects how much we are influenced by them. Participants first made a visual perceptual estimate and then shared their estimate with an alleged partner. Then, in alternating trials, the participant either revised their decisions or observed how the partner revised theirs. We systematically manipulated the partner's susceptibility to influence from the participant. We show that participants reciprocated influence with their partner by gravitating toward the susceptible (but not insusceptible) partner's opinion. In further experiments, we showed that reciprocity is both a dynamic process and is abolished when people believed that they interacted with a computer. Reciprocal social influence is a signaling medium for human-to-human communication that goes beyond aggregation of evidence for decision improvement.

Modifying response times in the Simon task with transcranial random noise stimulation.

Perceptual decisions pervade our every-day lives, and can align or conflict with inbuilt biases. We investigated these conflicting biases by applying transcranial random noise stimulation (tRNS) while subjects took part in a visual Simon task - a paradigm where irrelevant spatial cues influence the response times of subjects to relevant colour cues. We found that tRNS reduces the response time of subjects independent of the congruence between spatial and colour cues, but dependent on the baseline response time, both between subjects and across conditions within subjects. We consider the reduction in response time to be non-specific to the Simon task, and cast our interpretations in terms of drift-diffusion models, which have been previously used as mechanistic explanations for decision-making processes. However, there have been few extensions of the drift-diffusion model to the Simon effect, and so we first elaborate on this interpretation, and further extend it by incorporating the potential action of tRNS.

Ownership and Agency of an Independent Supernumerary Hand Induced by an Imitation Brain-Computer Interface.

To study body ownership and control, illusions that elicit these feelings in non-body objects are widely used. Classically introduced with the Rubber Hand Illusion, these illusions have been replicated more recently in virtual reality and by using brain-computer interfaces. Traditionally these illusions investigate the replacement of a body part by an artificial counterpart, however as brain-computer interface research develops it offers us the possibility to explore the case where non-body objects are controlled in addition to movements of our own limbs. Therefore we propose a new illusion designed to test the feeling of ownership and control of an independent supernumerary hand. Subjects are under the impression they control a virtual reality hand via a brain-computer interface, but in reality there is no causal connection between brain activity and virtual hand movement but correct movements are observed with 80% probability. These imitation brain-computer interface trials are interspersed with movements in both the subjects' real hands, which are in view throughout the experiment. We show that subjects develop strong feelings of ownership and control over the third hand, despite only receiving visual feedback with no causal link to the actual brain signals. Our illusion is crucially different from previously reported studies as we demonstrate independent ownership and control of the third hand without loss of ownership in the real hands.

Variance Based Measure for Optimization of Parametric Realignment Algorithms.

Neuronal responses to sensory stimuli or neuronal responses related to behaviour are often extracted by averaging neuronal activity over large number of experimental trials. Such trial-averaging is carried out to reduce noise and to diminish the influence of other signals unrelated to the corresponding stimulus or behaviour. However, if the recorded neuronal responses are jittered in time with respect to the corresponding stimulus or behaviour, averaging over trials may distort the estimation of the underlying neuronal response. Temporal jitter between single trial neural responses can be partially or completely removed using realignment algorithms. Here, we present a measure, named difference of time-averaged variance (dTAV), which can be used to evaluate the performance of a realignment algorithm without knowing the internal triggers of neural responses. Using simulated data, we show that using dTAV to optimize the parameter values for an established parametric realignment algorithm improved its efficacy and, therefore, reduced the jitter of neuronal responses. By removing the jitter more effectively and, therefore, enabling more accurate estimation of neuronal responses, dTAV can improve analysis and interpretation of the neural responses.

Epidural electrocorticography of phantom hand movement following long-term upper-limb amputation.

INTRODUCTION: Prostheses for upper-limb amputees are currently controlled by either myoelectric or peripheral neural signals. Performance and dexterity of these devices is still limited, particularly when it comes to controlling hand function. Movement-related brain activity might serve as a complementary bio-signal for motor control of hand prosthesis. METHODS: We introduced a methodology to implant a cortical interface without direct exposure of the brain surface in an upper-limb amputee. This bi-directional interface enabled us to explore the cortical physiology following long-term transhumeral amputation. In addition, we investigated neurofeedback of electrocorticographic brain activity related to the patient's motor imagery to open his missing hand, i.e., phantom hand movement, for real-time control of a virtual hand prosthesis. RESULTS: Both event-related brain activity and cortical stimulation revealed mutually overlapping cortical representations of the phantom hand. Phantom hand movements could be robustly classified and the patient required only three training sessions to gain reliable control of the virtual hand prosthesis in an online closed-loop paradigm that discriminated between hand opening and rest. CONCLUSION: Epidural implants may constitute a powerful and safe alternative communication pathway between the brain and external devices for upper-limb amputees, thereby facilitating the integrated use of different signal sources for more intuitive and specific control of multi-functional devices in clinical use.

Concurrent stable and unstable cortical correlates of human wrist movements.

Cortical activity has been shown to correlate with different parameters of movement. However, the dynamic properties of cortico-motor mappings still remain unexplored in humans. Here, we show that during the repetition of simple stereotyped wrist movements both stable and unstable correlates simultaneously emerge in human sensorimotor cortex. Using visual feedback of wrist movement target inferred online from MEG, we assessed the dynamics of the tuning properties of two neuronal signals: the MEG signal below 1.6 Hz and within the 4 to 6 Hz range. We found that both components are modulated by wrist movement allowing for closed-loop inference of movement targets. Interestingly, while tuning of 4 to 6 Hz signals remained stable over time leading to stable inference of movement target using a static classifier, the tuning of cortical signals below 1.6 Hz significantly changed resulting in steadily decreasing inference accuracy. Our findings demonstrate that non-invasive neuronal population signals in human sensorimotor cortex can reflect a stable correlate of voluntary movements. Hence, we provide first evidence for a stable control signal in non-invasive human brain-machine interface research. However, as not all neuronal signals initially tuned to movement were stable across days, a careful selection of features for real-life applications seems to be mandatory.

Low-latency multi-threaded processing of neuronal signals for brain-computer interfaces.

Brain-computer interfaces (BCIs) require demanding numerical computations to transfer brain signals into control signals driving an external actuator. Increasing the computational performance of the BCI algorithms carrying out these calculations enables faster reaction to user inputs and allows using more demanding decoding algorithms. Here we introduce a modular and extensible software architecture with a multi-threaded signal processing pipeline suitable for BCI applications. The computational load and latency (the time that the system needs to react to user input) are measured for different pipeline implementations in typical BCI applications with realistic parameter settings. We show that BCIs can benefit substantially from the proposed parallelization: firstly, by reducing the latency and secondly, by increasing the amount of recording channels and signal features that can be used for decoding beyond the amount which can be handled by a single thread. The proposed software architecture provides a simple, yet flexible solution for BCI applications.

Detection of error related neuronal responses recorded by electrocorticography in humans during continuous movements.

BACKGROUND: Brain-machine interfaces (BMIs) can translate the neuronal activity underlying a user's movement intention into movements of an artificial effector. In spite of continuous improvements, errors in movement decoding are still a major problem of current BMI systems. If the difference between the decoded and intended movements becomes noticeable, it may lead to an execution error. Outcome errors, where subjects fail to reach a certain movement goal, are also present during online BMI operation. Detecting such errors can be beneficial for BMI operation: (i) errors can be corrected online after being detected and (ii) adaptive BMI decoding algorithm can be updated to make fewer errors in the future. METHODOLOGY/PRINCIPAL FINDINGS: Here, we show that error events can be detected from human electrocorticography (ECoG) during a continuous task with high precision, given a temporal tolerance of 300-400 milliseconds. We quantified the error detection accuracy and showed that, using only a small subset of 2×2 ECoG electrodes, 82% of detection information for outcome error and 74% of detection information for execution error available from all ECoG electrodes could be retained. CONCLUSIONS/SIGNIFICANCE: The error detection method presented here could be used to correct errors made during BMI operation or to adapt a BMI algorithm to make fewer errors in the future. Furthermore, our results indicate that smaller ECoG implant could be used for error detection. Reducing the size of an ECoG electrode implant used for BMI decoding and error detection could significantly reduce the medical risk of implantation.

Grasp detection from human ECoG during natural reach-to-grasp movements.

Various movement parameters of grasping movements, like velocity or type of the grasp, have been successfully decoded from neural activity. However, the question of movement event detection from brain activity, that is, decoding the time at which an event occurred (e.g. movement onset), has been addressed less often. Yet, this may be a topic of key importance, as a brain-machine interface (BMI) that controls a grasping prosthesis could be realized by detecting the time of grasp, together with an optional decoding of which type of grasp to apply. We, therefore, studied the detection of time of grasps from human ECoG recordings during a sequence of natural and continuous reach-to-grasp movements. Using signals recorded from the motor cortex, a detector based on regularized linear discriminant analysis was able to retrieve the time-point of grasp with high reliability and only few false detections. Best performance was achieved using a combination of signal components from time and frequency domains. Sensitivity, measured by the amount of correct detections, and specificity, represented by the amount of false detections, depended strongly on the imposed restrictions on temporal precision of detection and on the delay between event detection and the time the event occurred. Including neural data from after the event into the decoding analysis, slightly increased accuracy, however, reasonable performance could also be obtained when grasping events were detected 125 ms in advance. In summary, our results provide a good basis for using detection of grasping movements from ECoG to control a grasping prosthesis.

Unsupervised adaptation of brain-machine interface decoders.

The performance of neural decoders can degrade over time due to non-stationarities in the relationship between neuronal activity and behavior. In this case, brain-machine interfaces (BMI) require adaptation of their decoders to maintain high performance across time. One way to achieve this is by use of periodical calibration phases, during which the BMI system (or an external human demonstrator) instructs the user to perform certain movements or behaviors. This approach has two disadvantages: (i) calibration phases interrupt the autonomous operation of the BMI and (ii) between two calibration phases the BMI performance might not be stable but continuously decrease. A better alternative would be that the BMI decoder is able to continuously adapt in an unsupervised manner during autonomous BMI operation, i.e., without knowing the movement intentions of the user. In the present article, we present an efficient method for such unsupervised training of BMI systems for continuous movement control. The proposed method utilizes a cost function derived from neuronal recordings, which guides a learning algorithm to evaluate the decoding parameters. We verify the performance of our adaptive method by simulating a BMI user with an optimal feedback control model and its interaction with our adaptive BMI decoder. The simulation results show that the cost function and the algorithm yield fast and precise trajectories toward targets at random orientations on a 2-dimensional computer screen. For initially unknown and non-stationary tuning parameters, our unsupervised method is still able to generate precise trajectories and to keep its performance stable in the long term. The algorithm can optionally work also with neuronal error-signals instead or in conjunction with the proposed unsupervised adaptation.

fNIRS exhibits weak tuning to hand movement direction.

Functional near-infrared spectroscopy (fNIRS) has become an established tool to investigate brain function and is, due to its portability and resistance to electromagnetic noise, an interesting modality for brain-machine interfaces (BMIs). BMIs have been successfully realized using the decoding of movement kinematics from intra-cortical recordings in monkey and human. Recently, it has been shown that hemodynamic brain responses as measured by fMRI are modulated by the direction of hand movements. However, quantitative data on the decoding of movement direction from hemodynamic responses is still lacking and it remains unclear whether this can be achieved with fNIRS, which records signals at a lower spatial resolution but with the advantage of being portable. Here, we recorded brain activity with fNIRS above different cortical areas while subjects performed hand movements in two different directions. We found that hemodynamic signals in contralateral sensorimotor areas vary with the direction of movements, though only weakly. Using these signals, movement direction could be inferred on a single-trial basis with an accuracy of ∼65% on average across subjects. The temporal evolution of decoding accuracy resembled that of typical hemodynamic responses observed in motor experiments. Simultaneous recordings with a head tracking system showed that head movements, at least up to some extent, do not influence the decoding of fNIRS signals. Due to the low accuracy, fNIRS is not a viable alternative for BMIs utilizing decoding of movement direction. However, due to its relative resistance to head movements, it is promising for studies investigating brain activity during motor experiments.

Review of the BCI Competition IV.

The BCI competition IV stands in the tradition of prior BCI competitions that aim to provide high quality neuroscientific data for open access to the scientific community. As experienced already in prior competitions not only scientists from the narrow field of BCI compete, but scholars with a broad variety of backgrounds and nationalities. They include high specialists as well as students. The goals of all BCI competitions have always been to challenge with respect to novel paradigms and complex data. We report on the following challenges: (1) asynchronous data, (2) synthetic, (3) multi-class continuous data, (4) session-to-session transfer, (5) directionally modulated MEG, (6) finger movements recorded by ECoG. As after past competitions, our hope is that winning entries may enhance the analysis methods of future BCIs.

Adaptation paths to novel motor tasks are shaped by prior structure learning.

After extensive practice with motor tasks sharing structural similarities (e.g., different dancing movements, or different sword techniques), new tasks of the same type can be learned faster. According to the recent "structure learning" hypothesis (Braun et al., 2009a), such rapid generalization of related motor skills relies on learning the dynamic and kinematic relationships shared by this set of skills. As a consequence, motor adaptation becomes constrained, effectively leading to a dimensionality reduction of the learning problem; at the same time, adaptation to tasks lying outside the structure becomes biased toward the structure. We tested these predictions by investigating how previously learned structures influence subsequent motor adaptation. Human subjects were making reaching movements in 3D virtual reality, experiencing perturbations either in the vertical or in the horizontal plane. Perturbations were either visuomotor rotations of varying angle or velocity-dependent forces of varying strength. We found that, after extensive training with both kinematic or dynamic perturbations, adaptation to unpracticed, diagonal, perturbations happened along the previously learned structure (vertical or horizontal), and resulting adaptation trajectories were curved. This effect is robust, can be observed on the single-subject level, and occurs during adaptation both within and across trials. Additionally, we demonstrate that structure learning changes involuntary visuomotor reflexes and therefore is not exclusively a high-level cognitive phenomenon.