Donatella Mattia

Combining Brain–Computer Interfaces and Assistive Technologies: State-of-the-Art and Challenges

In recent years, new research has brought the field of electroencephalogram (EEG)-based brain–computer interfacing (BCI) out of its infancy and into a phase of relative maturity through many demonstrated prototypes such as brain-controlled wheelchairs, keyboards, and computer games. With this proof-of-concept phase in the past, the time is now ripe to focus on the development of practical BCI technologies that can be brought out of the lab and into real-world applications. In particular, we focus on the prospect of improving the lives of countless disabled individuals through a combination of BCI technology with existing assistive technologies (AT). In pursuit of more practical BCIs for use outside of the lab, in this paper, we identify four application areas where disabled individuals could greatly benefit from advancements in BCI technology, namely, “Communication and Control”, “Motor Substitution”, “Entertainment”, and “Motor Recovery”. We review the current state of the art and possible future developments, while discussing the main research issues in these four areas. In particular, we expect the most progress in the development of technologies such as hybrid BCI architectures, user–machine adaptation algorithms, the exploitation of users’ mental states for BCI reliability and confidence measures, the incorporation of principles in human–computer interaction (HCI) to improve BCI usability, and the development of novel BCI technology including better EEG devices.

Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function

Nowadays, several types of brain imaging device are available to provide images of the functional activity of the cerebral cortex based on hemodynamic, metabolic, or electromagnetic measurements. However, static images of brain regions activated during particular tasks do not convey the information of how these regions communicate with each other. In this study, advanced methods for the estimation of cortical connectivity from combined high-resolution electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) data are presented. These methods include a subjects multicompartment head model (scalp, skull, dura mater, cortex) constructed from individual magnetic resonance images, multidipole source model, and regularized linear inverse source estimates of cortical current density. Determination of the priors in the resolution of the linear inverse problem was performed with the use of information from the hemodynamic responses of the cortical areas as revealed by block-designed (strength of activated voxels) fMRI. We estimate functional cortical connectivity by computing the directed transfer function (DTF) on the estimated cortical current density waveforms in regions of interest (ROIs) on the modeled cortical mantle. The proposed method was able to unveil the direction of the information flow between the cortical regions of interest, as it is directional in nature. Furthermore, this method allows to detect changes in the time course of information flow between cortical regions in different frequency bands. The reliability of these techniques was further demonstrated by elaboration of high-resolution EEG and fMRI signals collected during visually triggered finger movements in four healthy subjects. Connectivity patterns estimated for this task reveal an involvement of right parietal and bilateral premotor and prefrontal cortical areas. This cortical region involvement resembles that revealed in previous studies where visually triggered finger movements were analyzed with the use of separate EEG or fMRI measurements.

Comparison of different cortical connectivity estimators for high-resolution EEG recordings

The aim of this work is to characterize quantitatively the performance of a body of techniques in the frequency domain for the estimation of cortical connectivity from high‐resolution EEG recordings in different operative conditions commonly encountered in practice. Connectivity pattern estimators investigated are the Directed Transfer Function (DTF), its modification known as direct DTF (dDTF) and the Partial Directed Coherence (PDC). Predefined patterns of cortical connectivity were simulated and then retrieved by the application of the DTF, dDTF, and PDC methods. Signal‐to‐noise ratio (SNR) and length (LENGTH) of EEG epochs were studied as factors affecting the reconstruction of the imposed connectivity patterns. Reconstruction quality and error rate in estimated connectivity patterns were evaluated by means of some indexes of quality for the reconstructed connectivity pattern. The error functions were statistically analyzed with analysis of variance (ANOVA). The whole methodology was then applied to high‐resolution EEG data recorded during the well‐known Stroop paradigm. Simulations indicated that all three methods correctly estimated the simulated connectivity patterns under reasonable conditions. However, performance of the methods differed somewhat as a function of SNR and LENGTH factors. The methods were generally equivalent when applied to the Stroop data. In general, the amount of available EEG affected the accuracy of connectivity pattern estimations. Analysis of 27 s of nonconsecutive recordings with an SNR of 3 or more ensured that the connectivity pattern could be accurately recovered with an error below 7% for the PDC and 5% for the DTF. In conclusion, functional connectivity patterns of cortical activity can be effectively estimated under general conditions met in most EEG recordings by combining high‐resolution EEG techniques, linear inverse estimation of the cortical activity, and frequency domain multivariate methods such as PDC, DTF, and dDTF. Hum. Brain Mapp, 2007.

Seizure‐like discharges recorded in human dysplastic neocortex maintained in vitro

Application of the convulsant drug 4-aminopyridine (50 to 100 μM) induced spontaneous seizure-like discharges (duration = 76.3 ± 46.8 sec, mean ± SD; interval of occurrence = 225.2 ± 87.9 sec) in slices of neocortex obtained from patients with a diagnosis of focal neuronal migration disorders during neurosurgical procedures for relief of drug-resistant seizures. Similar epileptiform discharges could also be elicited in these slices by single-shock stimuli delivered in the underlying white matter or within the gray matter. By contrast, neocortical slices obtained from patients suffering from temporal lobe epilepsy (which is characterized by Ammons horn sclerosis but relatively normal neocortex) did not generate any epileptiform activity during 4-aminopyridine application. Thus, our study is the first to provide experimental evidence for the intrinsic epileptogenicity that characterizes neuronal migration disorders.

Tracking the Time-Varying Cortical Connectivity Patterns by Adaptive Multivariate Estimators

The directed transfer function (DTF) and the partial directed coherence (PDC) are frequency-domain estimators that are able to describe interactions between cortical areas in terms of the concept of Granger causality. However, the classical estimation of these methods is based on the multivariate autoregressive modelling (MVAR) of time series, which requires the stationarity of the signals. In this way, transient pathways of information transfer remains hidden. The objective of this study is to test a time-varying multivariate method for the estimation of rapidly changing connectivity relationships between cortical areas of the human brain, based on DTF/PDC and on the use of adaptive MVAR modelling (AMVAR) and to apply it to a set of real high resolution EEG data. This approach will allow the observation of rapidly changing influences between the cortical areas during the execution of a task. The simulation results indicated that time-varying DTF and PDC are able to estimate correctly the imposed connectivity patterns under reasonable operative conditions of signal-to-noise ratio (SNR) ad number of trials. An SNR of Ave and a number of trials of at least 20 provide a good accuracy in the estimation. After testing the method by the simulation study, we provide an application to the cortical estimations obtained from high resolution EEG data recorded from a group of healthy subject during a combined foot-lips movement and present the time-varying connectivity patterns resulting from the application of both DTF and PDC. Two different cortical networks were detected with the proposed methods, one constant across the task and the other evolving during the preparation of the joint movement.

Brain-computer interface boosts motor imagery practice during stroke recovery

Motor imagery (MI) is assumed to enhance poststroke motor recovery, yet its benefits are debatable. Brain–computer interfaces (BCIs) can provide instantaneous and quantitative measure of cerebral functions modulated by MI. The efficacy of BCI‐monitored MI practice as add‐on intervention to usual rehabilitation care was evaluated in a randomized controlled pilot study in subacute stroke patients.

A Brain-Computer Interface as Input Channel for a Standard Assistive Technology Software

Recently brain-computer interface (BCI) control was integrated into the commercial assistive technology product QualiWORLD (QualiLife Inc., Paradiso-Lugano, CH). Usability of the first prototype was evaluated in terms of effectiveness (accuracy), efficiency (information transfer rate and subjective workload/NASA Task Load Index) and user satisfaction (Quebec User Evaluation of Satisfaction with assistive Technology, QUEST 2.0) by four end-users with severe disabilities. Three assistive technology experts evaluated the device from a third person perspective. The results revealed high performance levels in communication and internet tasks. Users and assistive technology experts were quite satisfied with the device. However, none could imagine using the device in daily life without improvements. Main obstacles were the EEG-cap and low speed.

Epileptiform discharges in the human dysplastic neocortex: In vitro physiology and pharmacology

Field potential and intracellular recordings were made in slices of human neocortical tissue obtained during surgery for the treatment of seizures associated with focal cortical dysplasia. Ictal‐like epileptiform discharges, along with isolated field potentials, were induced by bath application of 4‐aminopyridine (50–100 μM). Some of the isolated field potentials were associated with fast transients representing population spikes. Field potential profile analysis indicated that both types of synchronous activity had maximal negative values at 1,400 to 1,600 μm from the pia. The intracellular counterpart of the ictal‐like discharge was a prolonged membrane depolarization capped by repetitive action potential burst firing. By contrast, the isolated field potentials were mirrored by long‐lasting depolarizations with minimal action potential firing; only when population spikes occurred, the isolated field potentials were associated with epileptiform action potential bursting. Ictal‐like discharges were abolished by either N‐methyl‐D‐aspartate or non–N‐methyl‐D‐aspartate receptor antagonists. In contrast, the isolated field potentials continued to occur synchronously during excitatory transmission blockade (although they lacked fast transients) but were abolished by the γ‐aminobutyric acidA receptor antagonist bicuculline methiodide (n = 2 slices). Our study demonstrates that focal cortical dysplasia tissue maintained in vitro has an intrinsic ability to generate ictal‐like epileptiform events when challenged with 4‐aminopyridine. These discharges depend on excitatory amino acid receptor–mediated mechanisms. Our results also show the presence in focal cortical dysplasia tissue of glutamatergic‐independent synchronous potentials that are mainly contributed by γ‐aminobutyric acidA receptor–mediated conductances.

Assessing cortical functional connectivity by partial directed coherence: simulations and application to real data

The aim of this paper is to test a technique called partial directed coherence (PDC) and its modification (squared PDC; sPDC) for the estimation of human cortical connectivity by means of simulation study, in which both PDC and sPDC were studied by analysis of variance. The statistical analysis performed returned that both PDC and sPDC are able to estimate correctly the imposed connectivity patterns when data exhibit a signal-to-noise ratio of at least 3 and a length of at least 27 s of nonconsecutive recordings at 250 Hz of sampling rate, equivalent, more generally, to 6750 data samples

Cortical Functional Connectivity Networks in Normal and Spinal Cord Injured Patients: Evaluation by Graph Analysis

The present work aims at analyzing the structure of cortical connectivity during the attempt to move a paralyzed limb by a group of spinal cord injured (SCI) patients. Connectivity patterns were obtained by means of the Directed Transfer Function applied to the cortical signals estimated from high resolution EEG recordings. Electrical activity were estimated in normals (Healthy) and SCI patients on twelve regions of interest (ROIs) coincident with Brodmann areas. Degree distributions showed the presence of few cortical regions with a lot of outgoing connections in all the cortical networks estimated irrespectively of the frequency band investigated. For both of the groups (SCI and Healthy), bilateral cingulate motor area (CMA) acts as hub transmitting information flows. The efficiency index, allowed to assert the ordered properties of such estimated cortical networks in both populations. The comparison of such estimated networks with those obtained from random networks, elicited significant differences (P < 0.05, Bonferroni‐corrected for multiple comparisons). A statistical comparison (ANOVA) between SCI patients and healthy subjects showed a significant difference (P < 0.05) between the local efficiency of their respective networks. For three frequency bands (theta 4–7 Hz, alpha 8–12 Hz, and beta 13–29 Hz) the higher value observed in the spinal cord injured population entails a larger level of internal organization and fault tolerance. This fact suggests a sort of compensative mechanism as local response to the alteration in their MIF areas, which is probably due to the indirect effects of the spinal injury. Hum Brain Mapp, 2007.