Alpha-band Suppression Research Articles

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.

Alpha-band EEG suppression as a neural marker of sustained attentional engagement to conditioned threat stimuli.

Attention helps us to be aware of the external world, and this may be especially important when a threat stimulus predicts an aversive outcome. Electroencephalogram (EEG) alpha-band suppression has long been considered as a neural signature of attentional engagement. The present study was designed to test whether attentional engagement, as indexed by alpha-band suppression, is increased in a sustained manner following a conditioned stimulus (CS) that is paired with an aversive (CS+) vs neutral (CS-) outcome. We tested 70 healthy young adults in aversive conditioning and extinction paradigms. One of three colored circles served as the CS+, which was paired in 50% of the trials with a noise burst (unconditioned stimulus, US). The other colored circles (CS-) were never paired with the US. For conditioning, we found greater alpha-band suppression for the CS+ compared to the CS-; this suppression was sustained through the time of the predicted US. This effect was significantly reduced for extinction. These results indicate that conditioned threat stimuli trigger an increase in attentional engagement as subjects monitor the environment for the predicted aversive stimulus. Moreover, this alpha-band suppression effect may be valuable for future studies examining normal or pathological increases in attentional monitoring following threat stimuli.

Electrophysiological evidence of sustained attention to music among conscious participants and unresponsive hospice patients at the end of life

ObjectiveTo characterize electrophysiological activity, and likely neural sources of that activity, associated with listening to music in both healthy participants and in a small group of hospice patients both when responsive and when unresponsive hours before death. MethodsYoung, healthy participants (N = 22) were asked to attend to (Active condition) and to ignore (Passive condition) brief (6 s) music excerpts. A smaller group (N = 13) of hospice patients was asked to attend to the same musical excerpts (Active condition only), both when they were responsive (N = 8) and again when they became unresponsive (N = 4) only hours before death. EEG-derived event-related spectral perturbations (ERSPs) to music stimuli, and their approximate neural sources, were computed for each individual in both groups. ResultsIn the healthy participants, alpha-band ERSP during the music excerpts in a group-level analysis was significantly lower in posterio-parietal brain areas in the Active condition than in the Passive condition (event-related desynchronization, ERD). Moreover, in an analysis of individual ERSP data, most (18 of 22 or 84%) healthy participants showed meaningful sustained (4 or more seconds) alpha-band suppression in one or more posterio-parietal brain areas when they were asked to attend to the music, whereas far fewer healthy participants (only 7 of 19 or 37%) generated the same response when asked to ignore the music, indicating that posterio-parietal alpha-band ERD could be a useful marker of music listening. Similarly, 75% of eight responsive hospice patients, and 100% of four unresponsive hospice patients showed sustained posterio-parietal alpha-band suppression when asked to attend to the music, indicating that they could be listening to the music covertly even when overtly unresponsive. ConclusionsSome (but likely not all, as other patients will vary from those we studied) unresponsive patients at the end of life might be able to listen to music, despite being unable to overtly indicate their awareness. SignificanceMusic stimulation may be a promising way to engage unresponsive patients.

Model-Based Planning Deficits in Compulsivity Are Linked to Faulty Neural Representations of Task Structure.

Compulsive individuals have deficits in model-based planning, but the mechanisms that drive this have not been established. We examined two candidates—that compulsivity is linked to (1) an impaired model of the task environment and/or (2) an inability to engage cognitive control when making choices. To test this, 192 participants performed a two-step reinforcement learning task with concurrent EEG recordings, and we related the neural and behavioral data to their scores on a self-reported transdiagnostic dimension of compulsivity. To examine subjects' internal model of the task, we used established behavioral and neural responses to unexpected events [reaction time (RT) slowing, P300 wave, and parietal-occipital alpha band power] measured when an unexpected transition occurred. To assess cognitive control, we probed theta power at the time of initial choice. As expected, model-based planning was linked to greater behavioral (RT) and neural (alpha power, but not P300) sensitivity to rare transitions. Critically, the sensitivities of both RT and alpha to task structure were weaker in those high in compulsivity. This RT-compulsivity effect was tested and replicated in an independent pre-existing dataset (N = 1413). We also found that mid-frontal theta power at the time of choice was reduced in highly compulsive individuals though its relation to model-based planning was less pronounced. These data suggest that model-based planning deficits in compulsive individuals may arise, at least in part, from having an impaired representation of the environment, specifically how actions lead to future states.SIGNIFICANCE STATEMENT Compulsivity is linked to poorer performance on tasks that require model-based planning, but it is unclear what precise mechanisms underlie this deficit. Do compulsive individuals fail to engage cognitive control at the time of choice? Or do they have difficulty in building and maintaining an accurate representation of their environment, the foundation needed to behave in a goal-directed manner? With reaction time and EEG measures in 192 individuals who performed a two-step decision-making task, we found that compulsive individuals are less sensitive to surprising action–state transitions, where they slow down less and show less alpha band suppression following a rare transition. These findings implicate failures in maintaining an accurate model of the world in model-based planning deficits in compulsivity.

Electrophysiology of the Human Superior Temporal Sulcus during Speech Processing.

The superior temporal sulcus (STS) is a crucial hub for speech perception and can be studied with high spatiotemporal resolution using electrodes targeting mesial temporal structures in epilepsy patients. Goals of the current study were to clarify functional distinctions between the upper (STSU) and the lower (STSL) bank, hemispheric asymmetries, and activity during self-initiated speech. Electrophysiologic properties were characterized using semantic categorization and dialog-based tasks. Gamma-band activity and alpha-band suppression were used as complementary measures of STS activation. Gamma responses to auditory stimuli were weaker in STSL compared with STSU and had longer onset latencies. Activity in anterior STS was larger during speaking than listening; the opposite pattern was observed more posteriorly. Opposite hemispheric asymmetries were found for alpha suppression in STSU and STSL. Alpha suppression in the STS emerged earlier than in core auditory cortex, suggesting feedback signaling within the auditory cortical hierarchy. STSL was the only region where gamma responses to words presented in the semantic categorization tasks were larger in subjects with superior task performance. More pronounced alpha suppression was associated with better task performance in Heschl's gyrus, superior temporal gyrus, and STS. Functional differences between STSU and STSL warrant their separate assessment in future studies.

Stimulus-induced Alpha Suppression Tracks the Difficulty of Attentional Selection, Not Visual Working Memory Storage.

Human alpha-band activity (8-12 Hz) has been proposed to index a variety of mechanisms during visual processing. Here, we distinguished between an account in which alpha suppression indexes selective attention versus an account in which it indexes subsequent working memory storage. We manipulated two aspects of the visual stimuli that perceptual attention is believed to mitigate before working memory storage: the potential interference from distractors and the size of the focus of attention. We found that the magnitude of alpha-band suppression tracked both of these aspects of the visual arrays. Thus, alpha-band activity after stimulus onset is clearly related to how the visual system deploys perceptual attention and appears to be distinct from mechanisms that store target representations in working memory.

Enhanced Theta-Band Coherence Between Midfrontal and Posterior Parietal Areas Reflects Post-feedback Adjustments in the State of Outcome Uncertainty.

Medial frontal cortex is currently viewed as the main hub of the performance monitoring system; upon detection of an error committed, it establishes functional connections with brain regions involved in task performance, thus leading to neural adjustments in them. Previous research has identified targets of such adjustments in the dorsolateral prefrontal cortex, posterior cortical regions, motor cortical areas, and subthalamic nucleus. Yet most of such studies involved visual tasks with relatively moderate cognitive load and strong dependence on motor inhibition – thus highlighting sensory, executive and motor effects while underestimating sensorimotor transformation and related aspects of decision making. Currently there is ample evidence that posterior parietal cortical areas are involved in task-specific neural processes of decision making (including evidence accumulation, sensorimotor transformation, attention, etc.) – yet, to our knowledge, no EEG studies have demonstrated post-error increase in functional connectivity in the theta-band between midfrontal and posterior parietal areas during performance on non-visual tasks. In the present study, we recorded EEG while subjects were performing an auditory version of the cognitively demanding attentional condensation task; this task involves rather non-straightforward stimulus-to-response mapping rules, thus, creating increased load on sensorimotor transformation. We observed strong pre-response alpha-band suppression in the left parietal area, which presumably reflected involvement of the posterior parietal cortex in task-specific decision-making processes. Negative feedback was followed by increased midfrontal theta-band power and increased functional coupling in the theta band between midfrontal and left parietal regions. This could be interpreted as activation of the performance monitoring system and top–down influence of this system on the posterior parietal regions involved in decision making, respectively. This inter-site coupling related to negative feedback was stronger for subjects who tended to commit errors with slower response times. Generally, current findings support the idea that slower errors are related to the state of outcome uncertainty caused by failures of task-specific processes, associated with posterior parietal regions.

Neurophysiology underlying influence of stimulus reliability on audiovisual integration.

We tested the predictions of the dynamic reweighting model (DRM) of audiovisual (AV) speech integration, which posits that spectrotemporally reliable (informative) AV speech stimuli induce a reweighting of processing from low-level to high-level auditory networks. This reweighting decreases sensitivity to acoustic onsets and in turn increases tolerance to AV onset asynchronies (AVOA). EEG was recorded while subjects watched videos of a speaker uttering trisyllabic nonwords that varied in spectrotemporal reliability and asynchrony of the visual and auditory inputs. Subjects judged the stimuli as in-sync or out-of-sync. Results showed that subjects exhibited greater AVOA tolerance for non-blurred than blurred visual speech and for less than more degraded acoustic speech. Increased AVOA tolerance was reflected in reduced amplitude of the P1-P2 auditory evoked potentials, a neurophysiological indication of reduced sensitivity to acoustic onsets and successful AV integration. There was also sustained visual alpha band (8-14Hz) suppression (desynchronization) following acoustic speech onsets for non-blurred vs. blurred visual speech, consistent with continuous engagement of the visual system as the speech unfolds. The current findings suggest that increased spectrotemporal reliability of acoustic and visual speech promotes robust AV integration, partly by suppressing sensitivity to acoustic onsets, in support of the DRM's reweighting mechanism. Increased visual signal reliability also sustains the engagement of the visual system with the auditory system to maintain alignment of information across modalities.

Theta, Alpha and Beta Band Modulations During Auditory Condensation Task Performance

Outcome of a behavioral response can be detected either internally at the time of the response commission, or externally through a feedback signal. In both cases, a number of brain networks that subserve cognitive control are recruited, all networks having certain distinctive signatures in electroencephalographic oscillations. Yet most studies in the field have several limitations. First, typical behavioral tasks depend heavily upon inhibition of prepotent responses – thus they mostly exploit control of the motor threshold rather than the full range of processes related to cognitive control. Second, these studies were conducted in the visual modality, leaving it unclear whether the oscillatory phenomena found in these studies truly relate to cognitive control or they reflect effects specific to the tasks used. Here, we studied outcome-related adjustments by analyzing response-related and feedback-related modulations of theta, alpha, and beta band activity in the auditory version of the condensation task, which bears no inherent dependence upon inhibition of prepotent responses and which is administered in the auditory modality. Frontal midline theta (FMT) activity was enhanced after errors compared with correct trials, and after negative feedback compared with positive feedback. Alpha band suppression in the parieto-occipital region was enhanced in the late post-error interval. Frontal beta oscillatory activity was increased on correct trials during positive feedback onset. These findings indicate that several separate neuronal networks are involved in post-error and post-feedback adjustments: the midfrontal performance monitoring network, the parietal attentional network, and the frontal reward-processing network. Our findings extend the current knowledge concerning the functional role of theta, alpha, and beta band oscillations in cognitive control beyond a limited range of tasks and beyond the visual modality.

Alpha-band rhythm suppression during memory recall reflecting memory performance.

Alpha-band rhythm is thought to be involved in memory processes, similarly to other spontaneous brain rhythms. Ten right-handed healthy volunteers participated in our proposed sequential short-term memory task that provides a serial position effect in accuracy rate. We recorded alpha-band rhythms by magnetoencephalography during performance of the task and observed that the amplitude of the rhythm was suppressed dramatically in the memory recall period. The suppressed region was estimated to be in the occipital lobe, suggesting that alpha-band rhythm is suppressed by activation of the occipital attentional network. Additionally, the alpha-band suppression reflected accuracy rate, that is, the amplitude was suppressed more when recalling items with higher accuracy rate. The sensors with a significant correlation between alpha-band amplitude and accuracy rate were located widely from the frontal to occipital regions mainly in the right hemisphere. The results suggests that alpha-band rhythm is involved in memory recall and can be index of memory performance.

Alpha-Band Oscillations Reflect Altered Multisensory Processing of the McGurk Illusion in Schizophrenia.

The formation of coherent multisensory percepts requires integration of stimuli across the multiple senses. Patients with schizophrenia (ScZ) often experience a loss of coherent perception and hence, they might also show dysfunctional multisensory processing. In this high-density electroencephalography study, we investigated the neural signatures of the McGurk illusion, as a phenomenon of speech-specific multisensory processing. In the McGurk illusion lip movements are paired with incongruent auditory syllables, which can induce a fused percept. In ScZ patients and healthy controls we compared neural oscillations and event-related potentials (ERPs) to congruent audiovisual speech stimuli and McGurk illusion trials, where a visual /ga/ and an auditory /pa/ was often perceived as /ka/. There were no significant group differences in illusion rates. The EEG data analysis revealed larger short latency ERPs to McGurk illusion compared with congruent trials in controls. The reversed effect pattern was found in ScZ patients, indicating an early audiovisual processing deficit. Moreover, we observed stronger suppression of medio-central alpha-band power (8–10 Hz, 550–700 ms) in response to McGurk illusion compared with control trials in the control group. Again, the reversed pattern was found in SCZ patients. Moreover, within groups, alpha-band suppression was negatively correlated with the McGurk illusion rate in ScZ patients, while the correlation tended to be positive in controls. The topography of alpha-band effects indicated an involvement of auditory and/or frontal structures. Our study suggests that short latency ERPs and long latency alpha-band oscillations reflect abnormal multisensory processing of the McGurk illusion in ScZ.

Theta and Alpha Band Modulations Reflect Error-Related Adjustments in the Auditory Condensation Task.

Error commission leads to adaptive adjustments in a number of brain networks that subserve goal-directed behavior, resulting in either enhanced stimulus processing or increased motor threshold depending on the nature of errors committed. Here, we studied these adjustments by analyzing post-error modulations of alpha and theta band activity in the auditory version of the two-choice condensation task, which is highly demanding for sustained attention while involves no inhibition of prepotent responses. Errors were followed by increased frontal midline theta (FMT) activity, as well as by enhanced alpha band suppression in the parietal and the left central regions; parietal alpha suppression correlated with the task performance, left central alpha suppression correlated with the post-error slowing, and FMT increase correlated with both behavioral measures. On post-error correct trials, left-central alpha band suppression started earlier before the response, and the response was followed by weaker FMT activity, as well as by enhanced alpha band suppression distributed over the entire scalp. These findings indicate that several separate neuronal networks are involved in post-error adjustments, including the midfrontal performance monitoring network, the parietal attentional network, and the sensorimotor network. Supposedly, activity within these networks is rapidly modulated after errors, resulting in optimization of their functional state on the subsequent trials, with corresponding changes in behavioral measures.

Oscillatory neural responses evoked by natural vestibular stimuli in humans.

While there have been numerous studies of the vestibular system in mammals, less is known about the brain mechanisms of vestibular processing in humans. In particular, of the studies that have been carried out in humans over the last 30 years, none has investigated how vestibular stimulation (VS) affects cortical oscillations. Here we recorded high-density electroencephalography (EEG) in healthy human subjects and a group of bilateral vestibular loss patients (BVPs) undergoing transient and constant-velocity passive whole body yaw rotations, focusing our analyses on the modulation of cortical oscillations in response to natural VS. The present approach overcame significant technical challenges associated with combining natural VS with human electrophysiology and reveals that both transient and constant-velocity VS are associated with a prominent suppression of alpha power (8-13 Hz). Alpha band suppression was localized over bilateral temporo-parietal scalp regions, and these alpha modulations were significantly smaller in BVPs. We propose that suppression of oscillations in the alpha band over temporo-parietal scalp regions reflects cortical vestibular processing, potentially comparable with alpha and mu oscillations in the visual and sensorimotor systems, respectively, opening the door to the investigation of human cortical processing under various experimental conditions during natural VS.

Alpha-band suppression in the visual word form area as a functional bottleneck to consciousness

The current state of empirical investigations refers to consciousness as an all-or-none phenomenon. However, a recent theoretical account opens up this perspective by proposing a partial level (between nil and full) of conscious perception. In the well-studied case of single-word reading, short-lived exposure can trigger incomplete word-form recognition wherein letters fall short of forming a whole word in one's conscious perception thereby hindering word-meaning access and report. Hence, the processing from incomplete to complete word-form recognition straightforwardly mirrors a transition from partial to full-blown consciousness. We therefore hypothesized that this putative functional bottleneck to consciousness (i.e. the perceptual boundary between partial and full conscious perception) would emerge at a major key hub region for word-form recognition during reading, namely the left occipito-temporal junction. We applied a real-time staircase procedure and titrated subjective reports at the threshold between partial (letters) and full (whole word) conscious perception. This experimental approach allowed us to collect trials with identical physical stimulation, yet reflecting distinct perceptual experience levels. Oscillatory brain activity was monitored with magnetoencephalography and revealed that the transition from partial-to-full word-form perception was accompanied by alpha-band (7-11 Hz) power suppression in the posterior left occipito-temporal cortex. This modulation of rhythmic activity extended anteriorly towards the visual word form area (VWFA), a region whose selectivity for word-forms in perception is highly debated. The current findings provide electrophysiological evidence for a functional bottleneck to consciousness thereby empirically instantiating a recently proposed partial perspective on consciousness. Moreover, the findings provide an entirely new outlook on the functioning of the VWFA as a late bottleneck to full-blown conscious word-form perception.

Oscillatory alpha-band suppression mechanisms during the rapid attentional shifts required to perform an anti-saccade task.

Neuroimaging has demonstrated anatomical overlap between covert and overt attention systems, although behavioral and electrophysiological studies have suggested that the two systems do not rely on entirely identical circuits or mechanisms. In a parallel line of research, topographically-specific modulations of alpha-band power (~8-14 Hz) have been consistently correlated with anticipatory states during tasks requiring covert attention shifts. These tasks, however, typically employ cue-target-interval paradigms where attentional processes are examined across relatively protracted periods of time and not at the rapid timescales implicated during overt attention tasks. The anti-saccade task, where one must first covertly attend for a peripheral target, before executing a rapid overt attention shift (i.e. a saccade) to the opposite side of space, is particularly well-suited for examining the rapid dynamics of overt attentional deployments. Here, we asked whether alpha-band oscillatory mechanisms would also be associated with these very rapid overt shifts, potentially representing a common neural mechanism across overt and covert attention systems. High-density electroencephalography in conjunction with infra-red eye-tracking was recorded while participants engaged in both pro- and anti-saccade task blocks. Alpha power, time-locked to saccade onset, showed three distinct phases of significantly lateralized topographic shifts, all occurring within a period of less than 1s, closely reflecting the temporal dynamics of anti-saccade performance. Only two such phases were observed during the pro-saccade task. These data point to substantially more rapid temporal dynamics of alpha-band suppressive mechanisms than previously established, and implicate oscillatory alpha-band activity as a common mechanism across both overt and covert attentional deployments.

Interactions between posterior gamma and frontal alpha/beta oscillations during imagined actions

Several studies have revealed that posterior parietal and frontal regions support planning of hand movements but far less is known about how these cortical regions interact during the mental simulation of a movement. Here, we have used magnetoencephalography (MEG) to investigate oscillatory interactions between posterior and frontal areas during the performance of a well-established motor imagery task that evokes motor simulation: mental rotation of hands. Motor imagery induced sustained power suppression in the alpha and beta band over the precentral gyrus and a power increase in the gamma band over bilateral occipito-parietal cortex. During motor imagery of left hand movements, there was stronger alpha and beta band suppression over the right precentral gyrus. The duration of these power changes increased, on a trial-by-trial basis, as a function of the motoric complexity of the imagined actions. Crucially, during a specific period of the movement simulation, the power fluctuations of the frontal beta-band oscillations became coupled with the occipito-parietal gamma-band oscillations. Our results provide novel information about the oscillatory brain activity of posterior and frontal regions. The persistent functional coupling between these regions during task performance emphasizes the importance of sustained interactions between frontal and occipito-parietal areas during mental simulation of action.