SSVEP Responses Research Articles

Development of a practical high frequency brain–computer interface based on steady-state visual evoked potentials using a single channel of EEG

Brain–computer interfaces based on steady-state visual evoked potentials have recently gained increasing attention due to high performance and minimal user training. Stimulus frequencies in the range of 4–60Hz have been used in these systems. However, eye fatigue when looking at low-frequency flickering lights, higher risk of induced epileptic seizure for medium-frequency flickers, and low signal amplitude for high-frequency flickers complicate appropriate selection of flickering frequencies. Here, different flicker frequencies were evaluated for development of a brain–computer interface speller that ensures user's comfort as well as the system's efficiency. A frequency detection algorithm was also proposed based on Least Absolute Shrinkage and Selection Operator estimate that provides excellent accuracy using only a single channel of EEG. After evaluation of the SSVEP responses in the range of 6–60Hz, three stimulus frequency sets of 30–35, 35–40 and 40–45Hz were adopted and the system's performance and corresponding eye fatigue were compared. While the accuracy of the asynchronous speller for all three stimulus frequency sets was close to the maximum (average 97.6%), repeated measures ANOVA demonstrated that the typing speed for 30–35Hz (8.09char/min) and 35–40Hz (8.33char/min) are not significantly different, but are significantly higher than for 40–45Hz (6.28char/min). On the other hand, the average eye fatigue scale for 35–40Hz (80%) is comparable to that for 40–45Hz (85%), but very higher than for 30–35Hz (60%). Therefore, 35–40Hz range was proposed for the system which resulted in 99.2% accuracy and 67.1bit/min information transfer rate.

Advancing the detection of steady-state visual evoked potentials in brain–computer interfaces

Objective. Spatial filtering has proved to be a powerful pre-processing step in detection of steady-state visual evoked potentials and boosted typical detection rates both in offline analysis and online SSVEP-based brain–computer interface applications. State-of-the-art detection methods and the spatial filters used thereby share many common foundations as they all build upon the second order statistics of the acquired Electroencephalographic (EEG) data, that is, its spatial autocovariance and cross-covariance with what is assumed to be a pure SSVEP response. The present study aims at highlighting the similarities and differences between these methods. Approach. We consider the canonical correlation analysis (CCA) method as a basis for the theoretical and empirical (with real EEG data) analysis of the state-of-the-art detection methods and the spatial filters used thereby. We build upon the findings of this analysis and prior research and propose a new detection method (CVARS) that combines the power of the canonical variates and that of the autoregressive spectral analysis in estimating the signal and noise power levels. Main results. We found that the multivariate synchronization index method and the maximum contrast combination method are variations of the CCA method. All three methods were found to provide relatively unreliable detections in low signal-to-noise ratio (SNR) regimes. CVARS and the minimum energy combination methods were found to provide better estimates for different SNR levels. Significance. Our theoretical and empirical results demonstrate that the proposed CVARS method outperforms other state-of-the-art detection methods when used in an unsupervised fashion. Furthermore, when used in a supervised fashion, a linear classifier learned from a short training session is able to estimate the hidden user intention, including the idle state (when the user is not attending to any stimulus), rapidly, accurately and reliably.

SSVEP-based Experimental Procedure for Brain-Robot Interaction with Humanoid Robots.

Brain-Robot Interaction (BRI), which provides an innovative communication pathway between human and a robotic device via brain signals, is prospective in helping the disabled in their daily lives. The overall goal of our method is to establish an SSVEP-based experimental procedure by integrating multiple software programs, such as OpenViBE, Choregraph, and Central software as well as user developed programs written in C++ and MATLAB, to enable the study of brain-robot interaction with humanoid robots. This is achieved by first placing EEG electrodes on a human subject to measure the brain responses through an EEG data acquisition system. A user interface is used to elicit SSVEP responses and to display video feedback in the closed-loop control experiments. The second step is to record the EEG signals of first-time subjects, to analyze their SSVEP features offline, and to train the classifier for each subject. Next, the Online Signal Processor and the Robot Controller are configured for the online control of a humanoid robot. As the final step, the subject completes three specific closed-loop control experiments within different environments to evaluate the brain-robot interaction performance. The advantage of this approach is its reliability and flexibility because it is developed by integrating multiple software programs. The results show that using this approach, the subject is capable of interacting with the humanoid robot via brain signals. This allows the mind-controlled humanoid robot to perform typical tasks that are popular in robotic research and are helpful in assisting the disabled.

SSVEP-based Experimental Procedure for Brain-Robot Interaction with Humanoid Robots

Brain-Robot Interaction (BRI), which provides an innovative communication pathway between human and a robotic device via brain signals, is prospective in helping the disabled in their daily lives. The overall goal of our method is to establish an SSVEP-based experimental procedure by integrating multiple software programs, such as OpenViBE, Choregraph, and Central software as well as user developed programs written in C++ and MATLAB, to enable the study of brain-robot interaction with humanoid robots. This is achieved by first placing EEG electrodes on a human subject to measure the brain responses through an EEG data acquisition system. A user interface is used to elicit SSVEP responses and to display video feedback in the closed-loop control experiments. The second step is to record the EEG signals of first-time subjects, to analyze their SSVEP features offline, and to train the classifier for each subject. Next, the Online Signal Processor and the Robot Controller are configured for the online control of a humanoid robot. As the final step, the subject completes three specific closed-loop control experiments within different environments to evaluate the brain-robot interaction performance. The advantage of this approach is its reliability and flexibility because it is developed by integrating multiple software programs. The results show that using this approach, the subject is capable of interacting with the humanoid robot via brain signals. This allows the mind-controlled humanoid robot to perform typical tasks that are popular in robotic research and are helpful in assisting the disabled.

Immersive BCI with SSVEP in VR head-mounted display.

In this paper we present an immersive brain computer interface (BCI) where we use a virtual reality head-mounted display (VRHMD) to invoke SSVEP responses. Compared to visual stimuli in monitor display, we demonstrate that visual stimuli in VRHMD indeed improve the user engagement for BCI. To this end, we validate our method with experiments on a VR maze game, the goal of which is to guide a ball into the destination in a 2D grid map in a 3D space, successively choosing one of four neighboring cells using SSVEP evoked by visual stimuli on neighboring cells. Experiments indicate that the averaged information transfer rate is improved by 10% for VRHMD, compared to the case in monitor display and the users feel easier to play the game with the proposed system.

Suppressed SSVEP strength in stroke patients with unilateral spatial neglect

Event Abstract Back to Event Suppressed SSVEP strength in stroke patients with unilateral spatial neglect Masato Shimura1, Yumie Ono1*, Satoko Omatsu2 and Takanori Tominaga2 1 Meiji University, Department of Electronics and Bioinformatics, Japan 2 Murata Hospital, Department of Rehabilitation, Japan Introduction: Previous studies demonstrated that attention to the visual stimulus enhances the strength of the SSVEP signals in healthy adults, suggesting that the attention-related increase in the SSVEP response may represent the strength of attention oriented to the visual stimulus. We therefore compared the attention-related increase in the SSVEP response among healthy controls, stroke patients with unilateral spatial neglect (USN), and those without USN to better understand the mechanism between attention and primary visual processing in patients with USN. Methods:Ten healthy young adults and 14 stroke patients participated in the experiment. Four out of 14 stroke patients were with USN. EEG was measured from PO7, O1, O2, and PO8 based on the international 10% system. A fixation point was placed at the center position in front of the participants and a flicker stimulus (white LED, 6Hz) was placed on their right or left visual field (45 and 15 degrees in healthy controls and patients, respectively). First, participants watched the fixation point without paying attention to the flicker stimulus. EEG was measured for 30 s for 3 times with each visual field. Second, we conducted the same experiment again except we placed a red LED in the vicinity of the white LED, which blinked randomly 5 or 6 times during the measurement. They were instructed to report the number of the blink of the red LED at the end of the measurement, yielding spontaneous attention of participants to the specific visual field. Results and Discussion: Healthy controls and patients without USN reported correct number (accuracy: 96-100%) of the red LED blinking located at either visual hemifield. Patients with USN reported the number of blinking as correct as other participants (98%) when the red LED was presented to the right visual hemifield but they failed to count more than half number of blinking when it was presented to the left visual hemifield (46%). Wavelet-based time-frequency analysis showed that attention to the visual hemifield robustly enhanced SSVEP strength in the healthy controls. Although patients without USN showed enhanced SSVEP strength by paying attention, the increase in SSVEP response was is smaller than that of healthy controls. The increase of patients with USN in SSVEP response was further smaller than those in patients without USN. Patients with USN showed decreased SSVEP response in case of paying attention to their right side. These results suggest that patients were not able to pay attention than healthy controls. Also, patients with USN could not pay attention to both visual hemifields than those without USN. The pathology of USN even affects the primary visual response of attention-oriented change in SSVEP. Further research would be conducted to study whether the recovery of USN is associated with the recovered strength of SSVEP response in stroke patients. Keywords: SSVEP, Stroke, Unilateral spatial neglect, Visual stimulus, attention-related increase Conference: 2015 International Workshop on Clinical Brain-Machine Interfaces (CBMI2015), Tokyo, Japan, 13 Mar - 15 Mar, 2015. Presentation Type: Poster 1-5 Topic: Clinical Brain-Machine Interfaces Citation: Shimura M, Ono Y, Omatsu S and Tominaga T (2015). Suppressed SSVEP strength in stroke patients with unilateral spatial neglect. Conference Abstract: 2015 International Workshop on Clinical Brain-Machine Interfaces (CBMI2015). doi: 10.3389/conf.fnhum.2015.218.00027 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 23 Apr 2015; Published Online: 29 Apr 2015. * Correspondence: Dr. Yumie Ono, Meiji University, Department of Electronics and Bioinformatics, Tama-ku, Kawasaki, Japan, yumie@meiji.ac.jp Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers Masato Shimura Yumie Ono Satoko Omatsu Takanori Tominaga Google Masato Shimura Yumie Ono Satoko Omatsu Takanori Tominaga Google Scholar Masato Shimura Yumie Ono Satoko Omatsu Takanori Tominaga PubMed Masato Shimura Yumie Ono Satoko Omatsu Takanori Tominaga Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Towards an architecture of a hybrid BCI based on SSVEP-BCI and passive-BCI.

Recent decades have seen BCI applications as a novel and promising new channel of communication, control and entertainment for disabled and healthy people. However, BCI technology can be prone to errors due to the basic emotional state of the user: the performance of reactive and active BCIs decrease when user becomes stressed or bored, for example. Passive-BCI is a recent approach that fuses BCI technology with cognitive monitoring, providing valuable information about the user's intentions, the situational interpretations and mainly the emotional state. In this work, an architecture composed by passive-BCI co-working with SSVEP-BCI is proposed, with the aim of improving the performance of the reactive-BCI. The possibility of adjusting recognition characteristics of SSVEP-BCIs using a passive-BCI output is evaluated. In this sense, two ways to recover the accuracy of SSVEP are presented in this paper: 1) Adjusting of Amplitude of the SSVEP and 2) Adjusting of Frequency of the SSVEP response. The results are promising, because accuracy of SSVEP-BCI can be recovered in the case that it was reduced by the BCI user's emotional state.

A frequency-tagging electrophysiological method to identify central and peripheral visual field deficits.

The aim of this study was to develop a fast and efficient electrophysiological protocol to examine the visual field's integrity, which would be useful in pediatric testing. Steady-state visual-evoked potentials (ssVEPs) to field-specific radial checkerboards flickering at two cycle frequencies (7.5 and 6 Hz for central and peripheral stimulations, respectively) recorded at Oz were collected from 22 participants from 5 to 34 years old and from 5 visually impaired adolescents (12-16 years old). Responses from additional leads (POz, O1, O2), and the impact of gaze deviation on the signals, were also investigated in a subgroup of participants. Steady-state visual-evoked potentials responses were similar at all electrode sites, although the signal from the central stimulation was significantly higher at Oz and was highly sensitive in detecting gaze deviation. No effect of age or sex was found, indicating similar ssVEP responses between adults and healthy children. Visual acuity was related to the central signal when comparing healthy participants with four central visual impaired adolescents. Clinical validation of our electrophysiological protocol was also achieved in a 15-year-old adolescent with a severe peripheral visual deficit, as assessed with Goldmann perimetry. A single electrode over Oz is sufficient to gather both central and peripheral visual signals and also to control for gaze deviation. Our method presents several advantages in evaluating visual fields integrity, as it is fast, reliable, and efficient, and applicable in children as young as 5 years old. However, a larger sample of healthy children should be tested to establish clinical norms.

Phase stability in the SSVEP responses

Phase stability in the SSVEP responses

Temporal characteristic of SSVEP response

Temporal characteristic of SSVEP response

The 6 Hz fundamental stimulation frequency rate for individual face discrimination in the right occipito-temporal cortex

What is the stimulus presentation rate at which the human brain can discriminate each exemplar of a familiar visual category? We presented faces at 14 frequency rates (1.0–16.66Hz) to human observers while recording high-density electroencephalogram (EEG). Different face exemplars elicited a larger steady-state visual evoked (ssVEP) response than when the same face was repeated, but only for stimulation frequencies between 4 and 8.33Hz, with a maximal difference at 5.88Hz (170ms cycle). The effect was confined to the exact stimulation frequency and localized over the right occipito-temporal cortex. At high frequency rates (>10Hz), the response to different and identical exemplars did not differ, suggesting that the fine-grained analysis needed for individual face discrimination cannot be completed before the next face interrupts, or competes, with the processed face. At low rates (<3Hz), repetition suppression could not be identified at the stimulation frequency, suggesting that the neural response to an individual face is temporally dispersed and distributed over different processes. These observations indicate that at a temporal rate of 170ms (6 faces/s) the face perception network is able to fully discriminate between each individual face presented, providing information about the temporal bottleneck of individual face discrimination in humans. These results also have important practical implications for optimizing paradigms that rely on repetition suppression, and open an avenue for investigating complex visual processes at an optimal range of stimulation frequency rates.

Tough doughnuts: affect and the modulation of attention

Positive affect has been associated with improvement in performance in various attentional domains. Negative affect has been associated with narrowing of attention and lowering of performance in attentional tasks. Previous behavioral studies have put forth the diffuse mental state idea as the mechanism of these effects, where attentional resources are more evenly distributed during positive affect and more focused during negative affect. To explore neural correlates of this mechanism, a two-stream rapid serial visual presentation (RSVP) paradigm with centrally presented, overlapping streams was used. Participants attended one of the streams at a time and steady-state visual evoked potentials (ssVEP) in response to the attended and unattended streams were recorded in a positive, negative or neutral affect state. We predicted that in the positive affect condition, ssVEP responses to the attended and the unattended stream would be more alike than in a neutral condition. In the negative affect condition, as an expression of a less diffuse mental state, ssVEP responses were predicted to be more dissimilar. Self-assessments confirmed the effectiveness of the emotional manipulation. In the negative affect condition power was found to be higher than in the neutral condition. However, the modulations in the ssVEP did not reflect the predicted neural correlate of the diffuse mental state mechanism. Thus, the results provide evidence for negative affect modulating attention but suggest that the diffuse mental state is not a spatially oriented phenomenon.

On diversity within operators’ EEG responses to LED-produced alternate stimulus in SSVEP BCI

Abstract This work is an attempt to identify causes of the widely observed fact that performance of Brain-Computer Interface systems based on Steady-State Visual Evoked Potentials varies between different users. The efficient LED-produced alternate stimulus systems are taken into account. The effect of stimulus color and flickering frequency on measured SSVEP response at first and second harmonics is investigated for 10 women and 11 men. The experimental setup is described, measurement procedure, signal processing and analysis algorithms are outlined. The results are presented and discussed. One of the early conclusions drawn from this extensive research is that the promising strategy of SSVEP-based BCI system optimization for best performance can be through stimulus adjustment to each individual user.

A steady-state visual evoked potential approach to individual face perception: Effect of inversion, contrast-reversal and temporal dynamics

Presentation of a face stimulus for several seconds at a periodic frequency rate leads to a right occipito-temporal evoked steady-state visual potential (SSVEP) confined to the stimulation frequency band. According to recent evidence (Rossion and Boremanse, 2011), this face-related SSVEP is largely reduced in amplitude when the exact same face is repeated at every stimulation cycle as compared to the presentation of different individual faces. Here this SSVEP individual face repetition effect was tested in 20 participants stimulated with faces at a 4 Hz rate for 84 s, in 4 conditions: faces upright or inverted, normal or contrast-reversed (2×2 design). To study the temporal dynamics of this effect, all stimulation sequences started with 15s of identical faces, after which, in half of the sequences, different faces were introduced. A larger response to different than identical faces at the fundamental (4 Hz) and second harmonic (8 Hz) components was observed for upright faces over the right occipito-temporal cortex. Weaker effects were found for inverted and contrast-reversed faces, two stimulus manipulations that are known to greatly affect the perception of facial identity. Addition of the two manipulations further decreased the effect. The phase of the fundamental frequency SSVEP response was delayed for inverted and contrast-reversed faces, to the same extent as the latency delay observed at the peak of the face-sensitive N170 component observed at stimulation sequence onset. Time-course analysis of the entire sequence of stimulation showed an immediate increase of 4Hz amplitude at the onset (16th second) of different face presentation, indicating a fast, large and frequency-specific release to individual face adaptation in the human brain. Altogether, these observations increase our understanding of the characteristics of the human steady-state face potential response and provide further support for the interest of this approach in the study of the neurofunctional mechanisms of face perception.

Stability of SSVEP responses to optic flow

Stability of SSVEP responses to optic flow

High-frequency SSVEP responses parametrized by multichannel matching pursuit

Event Abstract Back to Event High-frequency SSVEP responses parametrized by multichannel matching pursuit Piotr Durka1*, Rafal Kus1, Jaroslaw Zygierewicz1, Piotr Milanowski1 and Gary Garcia2 1 University of Warsaw, Poland 2 Philips Research Europe, Netherlands High-frequency stimuli (above 30Hz) are crucial for implementing steady-state-visual-evoked-potential (SSVEP) based brain-computer interfaces (BCIs). Indeed SSVEPs induced by high-frequency stimuli significantly diminish user's fatigue and risk of photosensitive epileptic seizures. However, SSVEPs in the high-frequency range are up to two orders of magnitude weaker than that in the low frequency range. This poses a considerable challenge to the sensitivity of applied signal processing methods. This problem has been addressed by using an optimal linear combination of the electroencephalogram (EEG) channels to maximize the contribution of SSVEP components while minimizing the background EEG and noise [1]. In this abstract we present a novel approach based on multichannel matching pursuit [2], which provides a joint multivariate decomposition of all the EEG channels. In this study we scan all the EEG channels for matching Gabor oscillations, with potentially varying amplitudes and phases. A topographic representation of the response, taken as the amplitude of Gabor atoms fitted between 38.5 and 39.5 Hz, is depicted in Figure 1 (c). It corresponds to the distribution of response's energy across electrodes. In Figure 1 (a), the time-frequency energy density, computed for electrode Oz is represented. This high-resolution estimate, apart from the clear frequency-following response, reveals also two alpha bands with different desynchronization patterns in relation to the stimulus onset. Figure 1 (b) confirms the statistical significance of the observed changes, displaying only the area in the stimulation period where the event-related desynchronization or synchronization in relation to the pre-stimulus period was statistically significant with the false discovery rate set at 5% [3].These preliminary results indicate the potential of high-resolution adaptive time-frequency estimates in the SSVEP research targeted at enhancing BCI operation. While the average reports are primarily of exploratory and research value, we are working towards single-trial detection schemes. Complete software for multivariate matching pursuit can be downloaded via http://bci.fuw.edu.pl/wiki/Matching_pursuit. Acknowledgement:Part of the work presented here has been sponsored by EU-project BRAIN (ICT-2007-224156)

Nonlinear SSVEP responses are sensitive to the perceptual binding of visual hemifields during conventional ‘eye’ rivalry and interocular ‘percept’ rivalry

We conducted behavioral and EEG experiments to identify physiological correlates of perceptual binding during two types of binocular rivalry: (1) conventional ‘eye’ rivalry where perception alternates between the two monocular images presented one to each eye and (2) interocular ‘percept’ rivalry, where perception alternates between percepts formed by grouping complementary hemifields one from each eye. We employed ‘frequency-tagging’ by flickering a grating in each hemifield of each eye at different frequencies to elicit SSVEP responses specific to each hemifield of each eye. When the gratings in complementary visual fields of the two eyes were congruent in color and orientation, robust interocular ‘percept’ rivalry was observed with roughly equal probability to conventional ‘eye’ rivalry. The SSVEPs evoked by the flickering gratings were enhanced by conscious perception at both posterior and frontal electrodes only during conventional ‘eye’ rivalry and not during interocular ‘percept’ rivalry, suggesting that dominance of one eye is the basis of most previous reports of SSVEP modulation by conscious perception. We also observed nonlinear SSVEP responses at the sums of our four fundamental frequencies. These combination responses were only produced by flicker in complementary visual hemifields — in the same eye or across eyes, but never by incongruent flickering gratings that occupy the same visual field across eyes, suggesting that they are related to the binding of the visual hemifields (monocular or interocular) into a coherent percept. These combination responses were modulated by the type of rivalry experienced by the observer, but not by the specific conscious perception. Neural processes related to perceptual binding of both rival percepts take place during binocular rivalry even when only one percept is consciously perceived. This suggests that conventional ‘eye’ and interocular ‘percept’ rivalry both involve competition between percepts.