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.

Localization of deep brain activity with scalp and subdural EEG.

To what extent electrocorticography (ECoG) and electroencephalography (scalp EEG) differ in their capability to locate sources of deep brain activity is far from evident. Compared to EEG, the spatial resolution and signal-to-noise ratio of ECoG is superior but its spatial coverage is more restricted, as is arguably the volume of tissue activity effectively measured from. Moreover, scalp EEG studies are providing evidence of locating activity from deep sources such as the hippocampus using high-density setups during quiet wakefulness. To address this question, we recorded a multimodal dataset from 4 patients with refractory epilepsy during quiet wakefulness. This data comprises simultaneous scalp, subdural and depth EEG electrode recordings. The latter was located in the hippocampus or insula and provided us with our "ground truth" for source localization of deep activity. We applied independent component analysis (ICA) for the purpose of separating the independent sources in theta, alpha and beta frequency band activity. In all patients subdural- and scalp EEG components were observed which had a significant zero-lag correlation with one or more contacts of the depth electrodes. Subsequent dipole modeling of the correlating components revealed dipole locations that were significantly closer to the depth electrodes compared to the dipole location of non-correlating components. These findings support the idea that components found in both recording modalities originate from neural activity in close proximity to the depth electrodes. Sources localized with subdural electrodes were ~70% closer to the depth electrode than sources localized with EEG with an absolute improvement of around ~2cm. In our opinion, this is not a considerable improvement in source localization accuracy given that, for clinical purposes, ECoG electrodes were implanted in close proximity to the depth electrodes. Furthermore, the ECoG grid attenuates the scalp EEG, due to the electrically isolating silastic sheets in which the ECoG electrodes are embedded. Our results on dipole modeling show that the deep source localization accuracy of scalp EEG is comparable to that of ECoG. SIGNIFICANCE STATEMENT: Deep and subcortical regions play an important role in brain function. However, as joint recordings at multiple spatial scales to study brain function in humans are still scarce, it is still unresolved to what extent ECoG and EEG differ in their capability to locate sources of deep brain activity. To the best of our knowledge, this is the first study presenting a dataset of simultaneously recorded EEG, ECoG and depth electrodes in the hippocampus or insula, with a focus on non-epileptiform activity (quiet wakefulness). Furthermore, we are the first study to provide experimental findings on the comparison of source localization of deep cortical structures between invasive and non-invasive brain activity measured from the cortical surface.

Overlapping connectivity patterns during semantic processing of abstract and concrete words revealed with multivariate Granger Causality analysis.

. Abstract, unlike concrete, nouns refer to notions beyond our perception. Even though there is no consensus among linguists as to what exactly constitutes a concrete or abstract word, neuroscientists found clear evidence of a "concreteness" effect. This can, for instance, be seen in patients with language impairments due to brain injury or developmental disorder who are capable of perceiving one category better than another. Even though the results are inconclusive, neuroimaging studies on healthy subjects also provide a spatial and temporal account of differences in the processing of abstract versus concrete words. A description of the neural pathways during abstract word reading, the manner in which the connectivity patterns develop over the different stages of lexical and semantic processing compared to that of concrete word processing are still debated. We conducted a high-density EEG study on 24 healthy young volunteers using an implicit categorization task. From this, we obtained high spatio-temporal resolution data and, by means of source reconstruction, reduced the effect of signal mixing observed on scalp level. A multivariate, time-varying and directional method of analyzing connectivity based on the concept of Granger Causality (Partial Directed Coherence) revealed a dynamic network that transfers information from the right superior occipital lobe along the ventral and dorsal streams towards the anterior temporal and orbitofrontal lobes of both hemispheres. Some regions along these pathways appear to be primarily involved in either receiving or sending information. A clear difference in information transfer of abstract and concrete words was observed during the time window of semantic processing, specifically for information transferred towards the left anterior temporal lobe. Further exploratory analysis confirmed a generally stronger connectivity pattern for processing concrete words. We believe our study could guide future research towards a more refined theory of abstract word processing in the brain.

Semantic and perceptual priming activate partially overlapping brain networks as revealed by direct cortical recordings in humans.

Facilitation of object processing in the brain due to a related context (priming) can be influenced by both semantic connections and perceptual similarity. It is thus important to discern these two when evaluating the spatio-temporal dynamics of primed object processing. The repetition-priming paradigm frequently used to study perceptual priming is, however, unable to differentiate between the mentioned priming effects, possibly leading to confounded results. In the current study, we recorded brain signals from the scalp and cerebral convexity of nine patients with refractory epilepsy in response to related and unrelated image-pairs, all of which shared perceptual features while only related ones had a semantic connection. While previous studies employing a repetition-priming paradigm observed largely overlapping networks between semantic and perceptual priming effects, our results suggest that this overlap is only partial (both temporally and spatially). These findings stress the importance of controlling for perceptual features when studying semantic priming.

Decoding Steady-State Visual Evoked Potentials From Electrocorticography.

We report on a unique electrocorticography (ECoG) experiment in which Steady-State Visual Evoked Potentials (SSVEPs) to frequency- and phase-tagged stimuli were recorded from a large subdural grid covering the entire right occipital cortex of a human subject. The paradigm is popular in EEG-based Brain Computer Interfacing where selectable targets are encoded by different frequency- and/or phase-tagged stimuli. We compare the performance of two state-of-the-art SSVEP decoders on both ECoG- and scalp-recorded EEG signals, and show that ECoG-based decoding is more accurate for very short stimulation lengths (i.e., less than 1 s). Furthermore, whereas the accuracy of scalp-EEG decoding benefits from a multi-electrode approach, to address interfering EEG responses and noise, ECoG decoding enjoys only a marginal improvement as even a single electrode, placed over the posterior part of the primary visual cortex, seems to suffice. This study shows, for the first time, that EEG-based SSVEP decoders can in principle be applied to ECoG, and can be expected to yield faster decoding speeds using less electrodes.

Representation of steady-state visual evoked potentials elicited by luminance flicker in human occipital cortex: An electrocorticography study.

Despite the widespread use of steady-state visual evoked potentials (SSVEPs) elicited by luminance flicker in clinical and research settings, their spatial and temporal representation in the occipital cortex largely remain elusive. We performed intracranial-EEG recordings in response to targets flickering at frequencies from 11 to 15 Hz using a subdural electrode grid covering the entire right occipital cortex of a human subject, and we were able to consistently locate the gazed stimulus frequency at the posterior side of the primary visual cortex (V1). Peripheral flickering, undetectable in scalp-EEG, elicited activations in the interhemispheric fissure at locations consistent with retinotopic maps. Both foveal and peripheral activations spatially coincided with activations in the high gamma band. We detected localized alpha synchronization at the lateral edge of V2 during stimulation and transient post-stimulation theta band activations at the posterior part of the occipital cortex. Scalp-EEG exhibited only a minor occipital post-stimulation theta activation, but a strong transient frontal activation.

Semantic Features Reveal Different Networks During Word Processing: An EEG Source Localization Study.

The neural principles behind semantic category representation are still under debate. Dominant theories mostly focus on distinguishing concrete from abstract concepts but, in such theories, divisions into categories of concrete concepts are more developed than for their abstract counterparts. An encompassing theory on semantic category representation could be within reach when charting the semantic attributes that are capable of describing both concept types. A good candidate are the three semantic dimensions defined by Osgood (potency, valence, arousal). However, to show to what extent they affect semantic processing, specific neuroimaging tools are required. Electroencephalography (EEG) is on par with the temporal resolution of cognitive behavior and source reconstruction. Using high-density set-ups, it is able to yield a spatial resolution in the scale of millimeters, sufficient to identify anatomical brain parcellations that could differentially contribute to semantic category representation. Cognitive neuroscientists traditionally focus on scalp domain analysis and turn to source reconstruction when an effect in the scalp domain has been detected. Traditional methods will potentially miss out on the fine-grained effects of semantic features as they are possibly obscured by the mixing of source activity due to volume conduction. For this reason, we have developed a mass-univariate analysis in the source domain using a mixed linear effect model. Our analyses reveal distinct networks of sources for different semantic features that are active during different stages of lexico-semantic processing of single words. With our method we identified differences in the spatio-temporal activation patterns of abstract and concrete words, high and low potency words, high and low valence words, and high and low arousal words, and in this way shed light on how word categories are represented in the brain.