A toolbox for decoding BCI commands based on event-related potentials.

Commands in brain-computer interface (BCI) applications often rely on the decoding of event-related potentials (ERP). For instance, the P300 potential is frequently used as a marker of attention to an oddball event. Error-related potentials and the N2pc signal are further examples of ERPs used for BCI control. One challenge in decoding brain activity from the electroencephalogram (EEG) is the selection of the most suitable channels and appropriate features for a particular classification approach. Here we introduce a toolbox that enables ERP-based decoding using the full set of channels, while automatically extracting informative components from relevant channels. The strength of our approach is that it handles sequences of stimuli that encode multiple items using binary classification, such as target vs. nontarget events typically used in ERP-based spellers. We demonstrate examples of application scenarios and evaluate the performance of four openly available datasets: a P300-based matrix speller, a P300-based rapid serial visual presentation (RSVP) speller, a binary BCI based on the N2pc, and a dataset capturing error potentials. We show that our approach achieves performances comparable to those in the original papers, with the advantage that only conventional preprocessing is required by the user, while channel weighting and decoding algorithms are internally performed. Thus, we provide a tool to reliably decode ERPs for BCI use with minimal programming requirements.

Distinct interacting cortical networks for stimulus-response and repetition-suppression.

Non-invasive studies consider the initial neural stimulus response (SR) and repetition suppression (RS) - the decreased response to repeated sensory stimuli - as engaging the same neurons. That is, RS is a suppression of the SR. We challenge this conjecture using electrocorticographic (ECoG) recordings with high spatial resolution in ten patients listening to task-irrelevant trains of auditory stimuli. SR and RS were indexed by high-frequency activity (HFA) across temporal, parietal, and frontal cortices. HFASR and HFARS were temporally and spatially distinct, with HFARS emerging later than HFASR and showing only a limited spatial intersection with HFASR: most HFASR sites did not demonstrate HFARS, and HFARS was found where no HFASR could be recorded. ß activity was enhanced in HFARS compared to HFASR cortical sites. θ activity was enhanced in HFASR compared to HFARS sites. Furthermore, HFASR sites propagated information to HFARS sites via transient θ:ß phase-phase coupling. In contrast to predictive coding (PC) accounts our results indicate that HFASR and HFARS are functionally linked but have minimal spatial overlap. HFASR might enable stable and rapid perception of environmental stimuli across extended temporal intervals. In contrast HFARS might support efficient generation of an internal model based on stimulus history.

Mind-wandering Is Accompanied by Both Local Sleep and Enhanced Processes of Spatial Attention Allocation.

Mind-wandering (MW) is a subjective, cognitive phenomenon, in which thoughts move away from the task toward an internal train of thoughts, possibly during phases of neuronal sleep-like activity (local sleep, LS). MW decreases cortical processing of external stimuli and is assumed to decouple attention from the external world. Here, we directly tested how indicators of LS, cortical processing, and attentional selection change in a pop-out visual search task during phases of MW. Participants' brain activity was recorded using magnetoencephalography, MW was assessed via self-report using randomly interspersed probes. As expected, the performance decreased under MW. Consistent with the occurrence of LS, MW was accompanied by a decrease in high-frequency activity (HFA, 80-150 Hz) and an increase in slow wave activity (SWA, 1-6 Hz). In contrast, visual attentional selection as indexed by the N2pc component was enhanced during MW with the N2pc amplitude being directly linked to participants' performance. This observation clearly contradicts accounts of attentional decoupling that would predict a decrease in attention-related responses to external stimuli during MW. Together, our results suggest that MW occurs during phases of LS with processes of attentional target selection being upregulated, potentially to compensate for the mental distraction during MW.

Frontotemporal Regulation of Subjective Value to Suppress Impulsivity in Intertemporal Choices.

Impulsive decisions arise from preferring smaller but sooner rewards compared with larger but later rewards. How neural activity and attention to choice alternatives contribute to reward decisions during temporal discounting is not clear. Here we probed (1) attention to and (2) neural representation of delay and reward information in humans (both sexes) engaged in choices. We studied behavioral and frequency-specific dynamics supporting impulsive decisions on a fine-grained temporal scale using eye tracking and MEG recordings. In one condition, participants had to decide for themselves but pretended to decide for their best friend in a second prosocial condition, which required perspective taking. Hence, conditions varied in the value for themselves versus that pretending to choose for another person. Stronger impulsivity was reliably found across three independent groups for prosocial decisions. Eye tracking revealed a systematic shift of attention from the delay to the reward information and differences in eye tracking between conditions predicted differences in discounting. High-frequency activity (175-250 Hz) distributed over right frontotemporal sensors correlated with delay and reward information in consecutive temporal intervals for high value decisions for oneself but not the friend. Collectively, the results imply that the high-frequency activity recorded over frontotemporal MEG sensors plays a critical role in choice option integration.SIGNIFICANCE STATEMENT Humans face decisions between sooner smaller rewards and larger later rewards daily. An objective benefit of losing weight over a longer time might be devalued in face of ice cream because they prefer currently available options because of insufficiently considering long-term alternatives. The degree of contribution of neural representation and attention to choice alternatives is not clear. We investigated correlates of such decisions in participants deciding for themselves or pretending to choose for a friend. Behaviorally participants discounted less in self-choices compared with the prosocial condition. Eye movement and MEG recordings revealed how participants represent choice options most evident for options with high subjective value. These results advance our understanding of neural mechanisms underlying decision-making in humans.

Impact of Stimulus Features on the Performance of a Gaze-Independent Brain-Computer Interface Based on Covert Spatial Attention Shifts.

Regaining communication abilities in patients who are unable to speak or move is one of the main goals in decoding brain waves for brain-computer interface (BCI) control. Many BCI approaches designed for communication rely on attention to visual stimuli, commonly applying an oddball paradigm, and require both eye movements and adequate visual acuity. These abilities may, however, be absent in patients who depend on BCI communication. We have therefore developed a response-based communication BCI, which is independent of gaze shifts but utilizes covert shifts of attention to the left or right visual field. We recorded the electroencephalogram (EEG) from 29 channels and coregistered the vertical and horizontal electrooculogram. Data-driven decoding of small attention-based differences between the hemispheres, also known as N2pc, was performed using 14 posterior channels, which are expected to reflect correlates of visual spatial attention. Eighteen healthy participants responded to 120 statements by covertly directing attention to one of two colored symbols (green and red crosses for "yes" and "no," respectively), presented in the user's left and right visual field, respectively, while maintaining central gaze fixation. On average across participants, 88.5% (std: 7.8%) of responses were correctly decoded online. In order to investigate the potential influence of stimulus features on accuracy, we presented the symbols with different visual angles, by altering symbol size and eccentricity. The offline analysis revealed that stimulus features have a minimal impact on the controllability of the BCI. Hence, we show with our novel approach that spatial attention to a colored symbol is a robust method with which to control a BCI, which has the potential to support severely paralyzed people with impaired eye movements and low visual acuity in communicating with their environment.

Early Shift of Attention Is Not Regulated by Mind Wandering in Visual Search.

Unique to humans is the ability to report subjective awareness of a broad repertoire of external and internal events. Even when asked to focus on external information, the human's mind repeatedly wanders to task-unrelated thoughts, which limits reading comprehension or the ability to withhold automated manual responses. This led to the attentional decoupling account of mind wandering (MW). However, manual responses are not an ideal parameter to study attentional decoupling, given that during MW, the online adjustment of manual motor responses is impaired. Hence, whether early attentional mechanisms are indeed downregulated during MW or only motor responses being slowed is not clear. In contrast to manual motor responses, eye movements are considered a sensitive proxy of attentional shifts. Using a simple target detection task, we asked subjects to indicate whether a target was presented within a visual search display by pressing a button while we recorded eye movements and unpredictably asked the subjects to rate their actual level of MW. Generally, manual reaction times increased with MW, both in target absent and present trials. But importantly, even in trials with MW, subjects detected earlier a presented than an absent target. The decoupling account would predict more fixations of the target before pressing the button during MW. However, our results did not corroborate this assumption. Most importantly, subject's time to direct gaze at the target was equally fast in trials with and without MW. Our results corroborate our hypothesis that during MW early, bottom-up driven attentional processes are not decoupled but selectively manual motor responses are slowed.

Decoding the covert shift of spatial attention from electroencephalographic signals permits reliable control of a brain-computer interface.

OBJECTIVE: One of the main goals of brain-computer interfaces (BCI) is to restore communication abilities in patients. BCIs often use event-related potentials (ERPs) like the P300 which signals the presence of a target in a stream of stimuli. The P300 and related approaches, however, are inherently limited, as they require many stimulus presentations to obtain a usable control signal. Many approaches depend on gaze direction to focus the target, which is also not a viable approach in many cases, because eye movements might be impaired in potential users. Here we report on a BCI that avoids both shortcomings by decoding spatial target information, independent of gaze shifts. APPROACH: We present a new method to decode from the electroencephalogram (EEG) covert shifts of attention to one out of four targets simultaneously presented in the left and right visual field. The task is designed to evoke the N2pc component-a hemisphere lateralized response, elicited over the occipital scalp contralateral to the attended target. The decoding approach involves decoding of the N2pc based on data-driven estimation of spatial filters and a correlation measure. MAIN RESULTS: Despite variability of decoding performance across subjects, 22 out of 24 subjects performed well above chance level. Six subjects even exceeded 80% (cross-validated: 89%) correct predictions in a four-class discrimination task. Hence, the single-trial N2pc proves to be a component that allows for reliable BCI control. An offline analysis of the EEG data with respect to their dependence on stimulation time and number of classes demonstrates that the present method is also a workable approach for two-class tasks. SIGNIFICANCE: Our method extends the range of strategies for gaze-independent BCI control. The proposed decoding approach has the potential to be efficient in similar applications intended to decode ERPs.

Self-regulated critical brain dynamics originate from high frequency-band activity in the MEG.

Brain function requires the flexible coordination of billions of neurons across multiple scales. This could be achieved by scale-free, critical dynamics balanced at the edge of order and disorder. Criticality has been demonstrated in several, often reduced neurophysiological model systems. In the intact human brain criticality has yet been only verified for the resting state. A more direct link between the concept of criticality and oscillatory brain physiology, which is strongly related to cognition, is yet missing. In the present study we therefore carried out a frequency-specific analysis of criticality in the MEG, recorded while subjects were in a defined cognitive state through mindfulness meditation. In a two-step approach we assessed whether the macroscopic neural avalanche dynamics is scale-free by evaluating the goodness of a power-law fits of cascade size and duration distributions of MEG deflections in different frequency bands. In a second step we determined the closeness of the power-law exponents to a critical value of -1.5. Power-law fitting was evaluated by permutation testing, fitting of alternative distributions, and cascade shape analysis. Criticality was verified by defined relationships of exponents of cascade size and duration distributions. Behavioral relevance of criticality was tested by correlation of indices of criticality with individual scores of the Mindful Attention Awareness Scale. We found that relevant scale-free near-critical dynamics originated only from broad-band high-frequency (> 100 Hz) MEG activity, which has been associated with action potential firing, and therefore links criticality on the macroscopic level of MEG to critical spike avalanches on a microscopic level. Whereas a scale-free dynamics was found under mindfulness meditation and rest, avalanche dynamics shifted towards a critical point during meditation by reduction of neural noise. Together with our finding that during mindfulness meditation avalanches show differences in topography relative to rest, our results show that self-regulated attention as required during meditation can serve as a control parameter of criticality in scale-free brain dynamics.

Neuronal activation in the human centromedian-parafascicular complex predicts cortical responses to behaviorally significant auditory events.

Studies with non-human primates have suggested an excitatory influence of the thalamus on the cerebral cortex, with the centromedian-parafascicular complex (CM-Pf) being particularly involved in processes of sensory event-driven attention and arousal. To define the involvement of the human CM-Pf in bottom-up and top-down auditory attention, we simultaneously recorded cortical EEG activity and intracranial local field potentials (LFPs) via electrodes implanted for deep brain stimulation for the treatment of neuropathic pain. The patients (N â€‹= â€‹6) performed an auditory three-class oddball paradigm with frequent standard stimuli and two types of infrequent deviant stimuli (target and distractor). We found a parietal P3b to targets and a central P3a to distractors at the scalp level. Subcortical recordings in the CM-Pf revealed enhanced activation to targets compared to standards. Interarea-correlation analyses showed that activation in the CM-Pf predicted the generation of longer latency P3b scalp potentials specifically in the target condition. Our results provide first direct human evidence for a functional temporal relationship between target-related activation in the CM-Pf and an enhanced cortical target response. These results corroborate the hypothetical model of a cortico-basal ganglia loop system that switches from top-down to bottom-up mode in response to salient, task-relevant external events that are not predictable.

Deep brain stimulation of the nucleus basalis of Meynert attenuates early EEG components associated with defective sensory gating in patients with Alzheimer disease - a two-case study.

Alzheimer's disease (AD) is associated with deterioration of memory and cognitive function and a degeneration of neurons of the nucleus basalis of Meynert (NBM). The NBM is the major input source of acetylcholine (ACh) to the cortex. The decreasing cholinergic innervation of the cortex due to degeneration of the NBM might be the cause of loss of memory function. NBM-Deep brain stimulation (NBM-DBS) is considered to serve as a potential therapeutic option for patients with AD by supporting residual cholinergic transmission to stabilize oscillatory activity in memory-relevant circuits. However, whether DBS could improve sensory memory functions in patients with AD is not clear. Here, in a passive auditory oddball paradigm, patients with AD (N = 2) listened to repetitive background tones (standard tones) randomly interrupted by frequency deviants in two blocks with NBM-DBS OFF and then NBM-DBS ON, while age-matched healthy controls (N = 6) repeated the experiment twice. The mismatch negativity in NBM-DBS OFF significantly differed from controls in both blocks, but not under NBM-DBS, which was likely due to a pronounced P50 increase overlapping with the N1 in NBM-DBS OFF. This early complex of EEG components recovered under stimulation to a normal level as defined by responses in controls. In this temporal interval, we found in patients with NBM-DBS ON (but not with NBM-DBS OFF) and in controls a strong repetition suppression effect to standard tones - with more attenuated responses to frequently repeated standard tones. This highlights the role of NBM-DBS for sensory gating of familiar auditory information into sensory memory.

Direct Evidence for Prediction Signals in Frontal Cortex Independent of Prediction Error.

Predictive coding (PC) has been suggested as one of the main mechanisms used by brains to interact with complex environments. PC theories posit top-down prediction signals, which are compared with actual outcomes, yielding in turn prediction error (PE) signals, which are used, bottom-up, to modify the ensuing predictions. However, disentangling prediction from PE signals has been challenging. Critically, while many studies found indirect evidence for PC in the form of PE signals, direct evidence for the prediction signal is mostly lacking. Here, we provide clear evidence, obtained from intracranial cortical recordings in human surgical patients, that the human lateral prefrontal cortex evinces prediction signals while anticipating an event. Patients listened to task-irrelevant sequences of repetitive tones including infrequent predictable or unpredictable pitch deviants. The broadband high-frequency amplitude (HFA) was decreased prior to the onset of expected relative to unexpected deviants in the frontal cortex only, and its amplitude was sensitive to the increasing likelihood of deviants following longer trains of standards in the unpredictable condition. Single-trial HFA predicted deviations and correlated with poststimulus response to deviations. These results provide direct evidence for frontal cortex prediction signals independent of PE signals.

A Comparative Study on the Detection of Covert Attention in Event-Related EEG and MEG Signals to Control a BCI.

In brain-computer interface (BCI) applications the detection of neural processing as revealed by event-related potentials (ERPs) is a frequently used approach to regain communication for people unable to interact through any peripheral muscle control. However, the commonly used electroencephalography (EEG) provides signals of low signal-to-noise ratio, making the systems slow and inaccurate. As an alternative noninvasive recording technique, the magnetoencephalography (MEG) could provide more advantageous electrophysiological signals due to a higher number of sensors and the magnetic fields not being influenced by volume conduction. We investigated whether MEG provides higher accuracy in detecting event-related fields (ERFs) compared to detecting ERPs in simultaneously recorded EEG, both evoked by a covert attention task, and whether a combination of the modalities is advantageous. In our approach, a detection algorithm based on spatial filtering is used to identify ERP/ERF components in a data-driven manner. We found that MEG achieves higher decoding accuracy (DA) compared to EEG and that the combination of both further improves the performance significantly. However, MEG data showed poor performance in cross-subject classification, indicating that the algorithm's ability for transfer learning across subjects is better in EEG. Here we show that BCI control by covert attention is feasible with EEG and MEG using a data-driven spatial filter approach with a clear advantage of the MEG regarding DA but with a better transfer learning in EEG.

Perimovement decrease of alpha/beta oscillations in the human nucleus accumbens.

The human nucleus accumbens is thought to play an important role in guiding future action selection via an evaluation of current action outcomes. Here we provide electrophysiological evidence for a more direct, i.e., online, role during action preparation. We recorded local field potentials from the nucleus accumbens in patients with epilepsy undergoing surgery for deep brain stimulation. We found a consistent decrease in the power of alpha/beta oscillations (10-30 Hz) before and around the time of movements. This perimovement alpha/beta desynchronization was observed in seven of eight patients and was present both before instructed movements in a serial reaction time task as well as before self-paced, deliberate choices in a decision making task. A similar beta decrease over sensorimotor cortex and in the subthalamic nucleus has been directly related to movement preparation and execution. Our results support the idea of a direct role of the human nucleus accumbens in action preparation and execution.

Hierarchy of prediction errors for auditory events in human temporal and frontal cortex.

Predictive coding theories posit that neural networks learn statistical regularities in the environment for comparison with actual outcomes, signaling a prediction error (PE) when sensory deviation occurs. PE studies in audition have capitalized on low-frequency event-related potentials (LF-ERPs), such as the mismatch negativity. However, local cortical activity is well-indexed by higher-frequency bands [high-γ band (Hγ): 80-150 Hz]. We compared patterns of human Hγ and LF-ERPs in deviance detection using electrocorticographic recordings from subdural electrodes over frontal and temporal cortices. Patients listened to trains of task-irrelevant tones in two conditions differing in the predictability of a deviation from repetitive background stimuli (fully predictable vs. unpredictable deviants). We found deviance-related responses in both frequency bands over lateral temporal and inferior frontal cortex, with an earlier latency for Hγ than for LF-ERPs. Critically, frontal Hγ activity but not LF-ERPs discriminated between fully predictable and unpredictable changes, with frontal cortex sensitive to unpredictable events. The results highlight the role of frontal cortex and Hγ activity in deviance detection and PE generation.

Sensory Deviancy Detection Measured Directly Within the Human Nucleus Accumbens.

Rapid changes in the environment evoke a comparison between expectancy and actual outcome to inform optimal subsequent behavior. The nucleus accumbens (NAcc), a key interface between the hippocampus and neocortical regions, is a candidate region for mediating this comparison. Here, we report event-related potentials obtained from the NAcc using direct intracranial recordings in 5 human participants while they listened to trains of auditory stimuli differing in their degree of deviation from repetitive background stimuli. NAcc recordings revealed an early mismatch signal (50-220 ms) in response to all deviants. NAcc activity in this time window was also sensitive to the statistics of stimulus deviancy, with larger amplitudes as a function of the level of deviancy. Importantly, this NAcc mismatch signal also predicted generation of longer latency scalp potentials (300-400 ms). The results provide direct human evidence that the NAcc is a key component of a network engaged in encoding statistics of the sensory environmental.

Oscillatory dynamics track motor performance improvement in human cortex.

Improving performance in motor skill acquisition is proposed to be supported by tuning of neural networks. To address this issue we investigated changes of phase-amplitude cross-frequency coupling (paCFC) in neuronal networks during motor performance improvement. We recorded intracranially from subdural electrodes (electrocorticogram; ECoG) from 6 patients who learned 3 distinct motor tasks requiring coordination of finger movements with an external cue (serial response task, auditory motor coordination task, go/no-go). Performance improved in all subjects and all tasks during the first block and plateaued in subsequent blocks. Performance improvement was paralled by increasing neural changes in the trial-to-trial paCFC between theta ([Formula: see text]; 4-8 Hz) phase and high gamma (HG; 80-180 Hz) amplitude. Electrodes showing this covariation pattern (Pearson's r ranging up to .45) were located contralateral to the limb performing the task and were observed predominantly in motor brain regions. We observed stable paCFC when task performance asymptoted. Our results indicate that motor performance improvement is accompanied by adjustments in the dynamics and topology of neuronal network interactions in the [Formula: see text] and HG range. The location of the involved electrodes suggests that oscillatory dynamics in motor cortices support performance improvement with practice.

Phase-amplitude cross-frequency coupling in the human nucleus accumbens tracks action monitoring during cognitive control.

The Nucleus Accumbens (NAcc) is an important structure for the transfer of information between cortical and subcortical structures, especially the prefrontal cortex and the hippocampus. However, the mechanism that allows the NAcc to achieve this integration is not well understood. Phase-amplitude cross-frequency coupling (PAC) of oscillations in different frequency bands has been proposed as an effective mechanism to form functional networks to optimize transfer and integration of information. Here we assess PAC between theta and high gamma oscillations as a potential mechanism that facilitates motor adaptation. To address this issue we recorded intracranial field potentials directly from the bilateral human NAcc in three patients while they performed a motor learning task that varied in the level of cognitive control needed to perform the task. As in rodents, PAC was observable in the human NAcc, transiently occurring contralateral to a movement following the motor response. Importantly, PAC correlated with the level of cognitive control needed to monitor the action performed. This functional relation indicates that the NAcc is engaged in action monitoring and supports the evaluation of motor programs during adaptive behavior by means of PAC.

ERP effects of change localization, change identification, and change blindness.

Change blindness is the failure to detect changes in visual scenes. Changes can elicit phenomenologically different perceptual experiences, possibly relating to different mechanisms: changes may be entirely missed, merely detected, located, or identified. We presented sequences of meaningful objects, one of which could change between the presentations. Changes had to be located and identified. Observers sometimes located the change without knowing which object had changed. However, effects of localization with and without identification were remarkably similar on a sequence of event-related potential components (including change-related positivity and N2pc). Only a late contralateral positivity was found exclusively for identified changes, indicating that change localization and change identification initially rely on a common processing sequence and differ only at later stages.