Steady-state Visual Evoked Potential Responses Research Articles

Steady-State Visually Evoked Potentials and Feature-based Attention: Preregistered Null Results and a Focused Review of Methodological Considerations.

Feature-based attention is the ability to selectively attend to a particular feature (e.g., attend to red but not green items while looking for the ketchup bottle in your refrigerator), and steady-state visually evoked potentials (SSVEPs) measured from the human EEG signal have been used to track the neural deployment of feature-based attention. Although many published studies suggest that we can use trial-by-trial cues to enhance relevant feature information (i.e., greater SSVEP response to the cued color), there is ongoing debate about whether participants may likewise use trial-by-trial cues to voluntarily ignore a particular feature. Here, we report the results of a preregistered study in which participants either were cued to attend or to ignore a color. Counter to prior work, we found no attention-related modulation of the SSVEP response in either cue condition. However, positive control analyses revealed that participants paid some degree of attention to the cued color (i.e., we observed a greater P300 component to targets in the attended vs. the unattended color). In light of these unexpected null results, we conducted a focused review of methodological considerations for studies of feature-based attention using SSVEPs. In the review, we quantify potentially important stimulus parameters that have been used in the past (e.g., stimulation frequency, trial counts) and we discuss the potential importance of these and other task factors (e.g., feature-based priming) for SSVEP studies.

Repeated Contrast Adaptation Does Not Cause Habituation of the Adapter.

Adaptation can optimize information processing by allowing the visual system to always adjust to the environment. However, only a few studies have investigated how the visual system makes adjustments to repeatedly occurring changes in the input, still less about the related neural mechanism. Our previous study found that contrast adaptation attenuated after multiple daily sessions of repeated adaptation, which was explained by the habituation of either the adapter’s effective strength or the adaptation mechanisms. To examine the former hypothesis, in the present study we used the frequency tagging technique to measure the adapter-elicited steady-state visual evoked potential (SSVEP) amplitudes. Participants repeatedly adapted to the same contrast adapter in a top-up manner for six continuous days, which was called training of adaptation. The behavioral adaptation effect and SSVEP response to the trained adapter and an untrained control adapter were measured before and after training. The psychophysical results showed that the effect of adaptation in the trained condition significantly reduced after training, replicating our previous finding. Contradicting the prediction of the hypothesis that repeated adaptation attenuated the effective strength of the adapter, the SSVEP amplitude was unchanged after training, which was further confirmed by an equivalence test. Taken together, the results challenge the account of habituation of adapter in repeated adaptation, while leaving the account of habituation of adaptation mechanism to be tested.

Reinforcement history shapes primary visual cortical responses: An SSVEP study

Efficient learning requires allocating limited attentional resources to meaningful stimuli and away from irrelevant stimuli. This prioritization may occur via covert attention, evident in the activity of the visual cortex. We used steady-state visual evoked potentials (SSVEPs) to assess whether associability-driven changes in stimulus processing were evident in visuocortical responses. Participants were trained on a learned-predictiveness protocol, whereby one stimulus on each trial accurately predicted the correct response for that trial, and the other was irrelevant. In a second phase the task was arranged so that all cues were objectively predictive. Participants’ overt attention (eye gaze) was affected by each cue’s reinforcement history, as was their covert attention (SSVEP responses). These biases persisted into Phase 2 when all stimuli were objectively predictive, thereby demonstrating that learned attentional processes are evident in basic sensory processing, and exert an effect on covert attention above and beyond the effects of overt gaze bias.

Steady-State Visual-Evoked Potentials as a Biomarker for Concussion: A Pilot Study

This study aims to utilize a portable system capable of measuring steady-state visual evoked potentials (SSVEP) to investigate their use as an objective electrophysiologic biomarker for concussion. The most pressing issues in relation to sports related concussion (SRC) involves accurate and timely diagnosis, for a safe return to play criteria. Despite the vast range of tools available to help clinicians assess concussion, most are subjective, non-portable, and therefore non-ideal for unbiased application at the site and time of a suspected injury. This system applied a smartphone housed in a VR-frame delivering a 15-Hz flickering stimulus while a wireless electroencephalography (EEG) headset recorded EEG signals. Sixty-five male amateur rugby athletes (20.9 ± 2.3 years-old) were tested throughout a season and were stratified into healthy, concussed, and recovered groups based on clinical examinations pre- and post-competitive games. Players SSVEP responses was quantified into a signal-to-noise ratio (SNR) and summarized into respective study-groups for comparison of medians with 25th-75th interquartile range. All sixty-five participants completed a baseline evaluation preseason. Twelve participants sustained a diagnosed concussion during the season and were retested within 72 h of injury. Eight concussed players received additional SSVEP testing following a 2-week recovery period. Concussed participants had a significantly lower SNR [2.20 (2.04-2.38)] when compared to their baseline [4.54 (3.79-5.10)]. When clinically recovered, participant SNR [4.82 (4.13-5.18)] was not significantly different to their baseline. Baseline SNR of concussed and non-concussed participants [4.80 (4.07-5.68)] did not significantly differ. This is the first study to show that SSVEPs are significantly attenuated in the presence of concussion in male athletes. Concussed individuals' ability to generate SSVEP appear to recover following clinical recovery. The observations of this study indicate SSVEP have the potential to be a supplemental aid for the assessment and management of concussion at point-of-care.

Single stimulus location for two inputs: A combined brain-computer interface based on Steady-State Visual Evoked Potential (SSVEP).

Brain-computer interfaces (BCI) help severely paralyzed people communicate with the outside world. One type of BCI depends on eye movements and has high information transfer (ITR) but is tiring for users and not applicable to people with eye dyskinesia. Conversely, independent BCIs enable attention shifts across visual stimuli without eye movement, but at the cost of a lower ITR. Steady-state visual evoked potential (SSVEP) is an oscillatory brain response and typically used as BCI signal sources because of high signal-to-noise ratio (SNR). Considering the effect of attentional modulation on the SSVEP, we proposed the novel concept of one-to-two BCI to optimize existing problems, wherein the target and other stimuli shared the same location. Specifically, two spatially overlapping stimuli were displayed in the center-of-view field, as in the independent BCI, and participants were required to divide their attention between the right and left visual fields, as in the dependent BCI. Using three different design schemes in two experiments, we aimed to provide a new framework for BCI design by exploring the feasibility of a combined BCI that can realize a single stimulus location for two inputs. The results strongly demonstrated that, even when the targets and distractors overlapped spatially, the former evoked stronger SSVEP responses. Notably, the BCI scheme based on the object-based attention could achieve a recognition rate as high as 83.2% and an ITR of 12.5 bits per minute. The feasibility of a one-to-two BCI design, which simplified the keyboard layout, reduced the attention shift, and relieved user fatigue, was established.

The Validity of Steady-State Visual Evoked Potentials as Attention Tags and Input Signals: A Critical Perspective of Frequency Allocation and Number of Stimuli.

Steady-state visual evoked potential (SSVEP) is a periodic response to a repetitive visual stimulus at a specific frequency. Currently, SSVEP is widely treated as an attention tag in cognitive activities and is used as an input signal for brain–computer interfaces (BCIs). However, whether SSVEP can be used as a reliable indicator has been a controversial issue. We focused on the independence of SSVEP from frequency allocation and number of stimuli. First, a cue–target paradigm was adopted to examine the interaction between SSVEPs evoked by two stimuli with different frequency allocations under different attention conditions. Second, we explored whether signal strength and the performance of SSVEP-based BCIs were affected by the number of stimuli. The results revealed that no significant interaction of SSVEP responses appeared between attended and unattended stimuli under various frequency allocations, regardless of their appearance in the fundamental or second-order harmonic. The amplitude of SSVEP suffered no significant gain or loss under different numbers of stimuli, but the performance of SSVEP-based BCIs varied along with duration of stimuli; that is, the recognition rate was not affected by the number of stimuli when the duration of stimuli was long enough, while the information transfer rate (ITR) presented the opposite trend. It can be concluded that SSVEP is a reliable tool for marking and monitoring multiple stimuli simultaneously in cognitive studies, but much caution should be taken when choosing a suitable duration and the number of stimuli, in order to achieve optimal utility of BCIs in the future.

Dynamics of Contrast Decrement and Increment Responses in Human Visual Cortex.

PurposeThe goal of the present experiments was to determine whether electrophysiologic response properties of the ON and OFF visual pathways observed in animal experimental models can be observed in humans.MethodsSteady-state visual evoked potentials (SSVEPs) were recorded in response to equivalent magnitude contrast increments and decrements presented within a probe-on-pedestal Westheimer sensitization paradigm. The probes were modulated with sawtooth temporal waveforms at a temporal frequency of 3 or 2.73 Hz. SSVEP response waveforms and response spectra for incremental and decremental stimuli were analyzed as a function of stimulus size and visual field location in 67 healthy adult participants.ResultsSSVEPs recorded at the scalp differ between contrast decrements and increments of equal Weber contrast: SSVEP responses were larger in amplitude and shorter in latency for contrast decrements than for contrast increments. Both increment and decrement responses were larger for displays that were scaled for cortical magnification.ConclusionsIn a fashion that parallels results from the early visual system of cats and monkeys, two key properties of ON versus OFF pathways found in single-unit recordings are recapitulated at the population level of activity that can be observed with scalp electrodes, allowing differential assessment of ON and OFF pathway activity in human.Translational RelevanceAs data from preclinical models of visual pathway dysfunction point to differential damage to subtypes of retinal ganglion cells, this approach may be useful in future work on disease detection and treatment monitoring.

Steady-State Visual Evoked Potentials Elicited from Early Visual Cortex Reflect Both Perceptual Color Space and Cone-Opponent Mechanisms.

Colors are represented in the cone-opponent signals, L-M versus S cones, at least up to the level of inputs to the primary visual cortex. We explored the hue selective responses in early cortical visual areas through recordings of steady-state visual evoked potentials (SSVEPs), elicited by a flickering checkerboard whose color smoothly swept around the hue circle defined in a cone-opponent color space. If cone opponency dominates hue representation in the source of SSVEP signals, SSVEP amplitudes as a function of hue should form a profile that is line-symmetric along the cardinal axes of the cone-opponent color space. Observed SSVEP responses were clearly chromatic ones with increased SSVEP amplitudes and reduced response latencies for higher contrast conditions. The overall elliptic amplitude profile was significantly tilted away from the cardinal axes to have the highest amplitudes in the “lime-magenta” direction, indicating that the hue representation in question is not dominated by cone-opponency. The observed SSVEP amplitude hue profile was better described as a summation of a perceptual response and cone-opponent responses with a larger weight to the former. These results indicate that hue representations in the early visual cortex, measured by the SSVEP technique, are possibly related to perceptual color contrast.

Five-Class SSVEP Response Detection using Common-Spatial Pattern (CSP)-SVM Approach

Brain-computer interface (BCI) technologies significantly facilitate the interaction between physically impaired people and their surroundings. In electroencephalography (EEG) based BCIs, a variety of physiological responses including P300, motor imagery, movement-related potential, steady-state visual evoked potential (SSVEP) and slow cortical potential have been utilized. Because of the superior signal-to-noise ratio (SNR) together with quicker information transfer rate (ITR), the intentness of SSVEP-based BCIs is progressing significantly. This paper represents the feature extraction and classification frameworks to detect five classes EEG-SSVEP responses. The common-spatial pattern (CSP) has been employed to extract the features from SSVEP responses and these features have been classified through the support vector machine (SVM). The proposed architecture has achieved the highest classification accuracy of 88.3%. The experimental result proves that the proposed architecture could be utilized for the detection of SSVEP responses to develop any BCI applications. Keywords: EEG, BCI, SSVEP, CSP, SVM, Machine Learning

Effects of Stimulus Spatial Resolution on SSVEP Responses under Overt and Covert Attention.

Steady-State Visual Evoked Potentials (SSVEP) Brain-Computer Interface (BCI) relies on overt spatial attention to exhibit reliable steady-state responses. There is a promising potential to employ the SSVEP paradigm in with vision research and clinical use, for instance, for visual field assessment. In this study, we investigate the SSVEP characteristics with different spatial attention, the different number of stimuli, and different viewing/visual angles. We collected data from eleven subjects in three experiment sessions, lasting about forty minutes, including the setup and calibration. Our evaluation results show similar SSVEP responses between overt and covert attention in multiple stimuli scenarios in most of the visual angles. We do not find any significant differences in SSVEP responses in visual angles between single and multi stimuli in covert attention. From this study, we found that reliable SSVEP responses can be achieved with covert spatial attention regardless of visual angles and stimulus spatial resolution.

Interaction between steady-state visually evoked potentials at nearby flicker frequencies

Steady-state visually evoked potential (SSVEP) studies routinely employ simultaneous presentation of two temporally modulated stimuli, with SSVEP amplitude modulations serving to index top-down cognitive processes. However, the nature of SSVEP amplitude modulations as a function of competing temporal frequency (TF) has not been systematically studied, especially in relation to the normalization framework which has been extensively used to explain visual responses to multiple stimuli. We recorded spikes and local field potential (LFP) from the primary visual cortex (V1) as well as EEG from two awake macaque monkeys while they passively fixated plaid stimuli with components counterphasing at different TFs. We observed asymmetric SSVEP response suppression by competing TFs (greater suppression for lower TFs), which further depended on the relative orientations of plaid components. A tuned normalization model, adapted to SSVEP responses, provided a good account of the suppression. Our results provide new insights into processing of temporally modulated visual stimuli.

Steady-State Visual-Evoked Potentials as a Biomarker for Concussion: A Pilot Study.

A variety of assessment tools are currently available to help clinicians assess Sports Related Concussion (SRC). Currently, the most widely available tools are neither objective nor portable, and are therefore not ideal for assessment at the site and time of a suspected injury. A portable system was developed to deliver a measurement of the steady-state visual-evoked potential (SSVEP). This system involved a smartphone housed in a Google Cardboard frame, which delivered a 15-Hz flicker visual stimulus while an electroencephalography (EEG) headset recorded EEG signals. Sixty-five rugby union players were tested during their regular season and were stratified into healthy, concussed, and recovered groups based on clinical examination. Their SSVEP response was quantified into a signal-to-noise ratio (SNR). The SNRs of players in each study group were summarized. Additionally, the SNRs of individual players who had baseline, post-injury, and post-recovery readings were analyzed. Sixty-five participants completed a baseline evaluation to measure their SSVEP. Twelve of these participants sustained a medically diagnosed concussion and completed SSVEP re-testing within 72 h. Eight concussed players received follow-up SSVEP testing after recovery. Concussed participants had a lower SNR [2.20 (2.04–2.38)] when compared to their baseline [4.54 (3.79–5.10)]. When clinically recovered, participant SNR was not significantly different to their baseline [4.82 (4.13–5.18)]. The baseline SNRs of the players who experienced a concussion during the season were not different to those of players who did not experience a concussion [4.80 (4.07–5.68)]. This is the first study to identify differences in SSVEP responses in male amateur rugby union players with and without concussion. It is also the first SSVEP demonstration for concussion evaluation at point-of-care. SSVEPs are significantly attenuated in the presence of concussion in these male athletes. Individuals returned to their baseline SSVEP following clinical recovery from the concussive injury. The use of SSVEPs has the potential to be a supplemental aid for the assessment and management of concussion.

Steady-state visual evoked potential (SSVEP)-based brain–computer interface (BCI) of Chinese speller for a patient with amyotrophic lateral sclerosis: A case report

This study applied a steady-state visual evoked potential (SSVEP) based brain–computer interface (BCI) to a patient in lock-in state with amyotrophic lateral sclerosis (ALS) and validated its feasibility for communication. The developed calibration-free and asynchronous spelling system provided a natural and efficient communication experience for the patient, achieving a maximum free-spelling accuracy above 90% and an information transfer rate of over 22.203 bits/min. A set of standard frequency scanning and task spelling data were also acquired to evaluate the patient’s SSVEP response and to facilitate further personalized BCI design. The results demonstrated that the proposed SSVEP-based BCI system was practical and efficient enough to provide daily life communication for ALS patients.

Spatial Attentional Selection Modulates Early Visual Stimulus Processing Independently of Visual Alpha Modulations

The capacity-limited human brain is constantly confronted with a huge amount of sensory information. Selective attention is needed for biasing neural processing towards relevant information and consequently allows meaningful interaction with the environment. Activity in the alpha-band has been proposed to be related to top-down modulation of neural inhibition and could thus represent a viable candidate to control the priority of stimulus processing. It is, however, unknown whether modulations in the alpha-band directly relate to changes in the sensory gain control of the early visual cortex. Here, we used a spatial cueing paradigm while simultaneously measuring ongoing alpha-band oscillations and steady-state visual evoked potentials (SSVEPs) as a marker of continuous early sensory processing in the human visual cortex. Thereby, the effects of spatial attention for both of these signals and their potential interactions were assessed. As expected, spatial attention modulated both alpha-band and SSVEP responses. However, their modulations were independent of each other and the corresponding activity profiles differed across task demands. Thus, our results challenge the view that modulations of alpha-band activity represent a mechanism that directly alters or controls sensory gain. The potential role of alpha-band oscillations beyond sensory processing will be discussed in light of the present results.

Data mining based approach to study the effect of consumption of caffeinated coffee on the generation of the steady-state visual evoked potential signals

The steady-state visual evoked potentials (SSVEP), are elicited at the parieto-occipital region of the cortex when a light source (3.5–75 Hz), flickering at a constant frequency, stimulates the retinal cells. In the last few decades, researchers have reported that caffeine enhances the vigilance and the executive control of visual attention. However, no study has investigated the effect of caffeinated coffee on the SSVEP response, which is used for controlling the brain-computer interface (BCI) devices for rehabilitative applications. The current work proposes a data mining-based approach to gain insight into the alterations in the SSVEP signals after the consumption of caffeinated coffee. Recurrence quantification analysis (RQA) of the electroencephalogram (EEG) signals was employed for this purpose. The EEG signals were acquired at seven frequencies of photic stimuli. The stimuli frequencies were chosen such that they were distributed throughout the EEG frequency bands. The prominent SSVEP signals were identified using the Canonical Correlation Analysis (CCA) method. Several statistical features were extracted from the recurrence plot of the SSVEP signals. Statistical analyses using the t-test and decision tree-based methods helped to select the most relevant features, which were then classified using Automated Neural Network (ANN). The relevant features could be classified with a maximum accuracy of 97%. This supports our hypothesis that the consumption of caffeinated coffee can alter the SSVEP response. In conclusion, utmost care should be taken in selecting the features for designing BCI devices.

An optimized facial stimuli paradigm for hybrid SSVEP+P300 brain computer interface

In this paper, hybrid BCI that merges Event Related Potentials (P300) and Steady State visual Evoked Potentials (SSVEP) simultaneously is proposed to enhance the performance of Four-choice command system. Here we integrate human facial structure in external visual stimulus to evoke stronger cortical responses in hybrid SSVEP+P300 BCI & compare it with non-face stimuli. We also addressed question of feasibility of eliciting one potential by face & other by non-face stimuli. To evoke SSVEP & P300 responses, paradigms with non-face stimuli, neutral face stimuli, and facial expression changes stimuli are proposed. We also projected additional paradigm where SSVEP is elicited by non-face and P300 by flashing different facial expressions. Results proved the last paradigm evoke stronger cortical potentials and thereby improve system accuracy and ITR than other paradigms. Author discussed external stimulus parameters that might affect simultaneous evocation of multiple brain potentials and their deterioration effect on individual potentials.

Designing a Sum of Squared Correlations Framework for Enhancing SSVEP-Based BCIs.

This study illustrates and evaluates a novel subject-specific target detection framework, sum of squared correlations (SSCOR), for improving the performance of steady-state visual evoked potential (SSVEP) based brain-computer interfaces (BCIs). The SSCOR spatial filter learns a common SSVEP representation space through the optimization of the individual SSVEP templates. The projection onto this SSVEP response subspace improves the signal to noise ratio (SNR) of the SSVEP components embedded in the recorded electroencephalographic (EEG) data. To demonstrate the effectiveness of the proposed framework, the target detection performance of the SSCOR method is compared with the state of the art task-related component analysis (TRCA). The evaluation is conducted on a 40 target SSVEP benchmark data collected from 35 subjects. The results of the extensive comparisons of the performance metrics show that the proposed SSCOR method outperforms the TRCA method. The ensemble version of the SSCOR framework provides an offline simulated information transfer rate (ITR) of 387 ± 9 bits/min which is much higher than that of the ensemble TRCA approach (max. ITR 216 ± 27 bits/min). The significant improvement in the detection accuracy and simulated ITR demonstrates the efficacy of the proposed framework for target detection in SSVEP based BCI applications.

Frequency-tagged visual evoked responses track syllable effects in visual word recognition

The processing of syllables in visual word recognition was investigated using a novel paradigm based on steady-state visual evoked potentials (SSVEPs). French words were presented to proficient readers in a delayed naming task. Words were split into two segments, the first of which was flickered at 18.75 Hz and the second at 25 Hz. The first segment either matched (congruent condition) or did not match (incongruent condition) the first syllable. The SSVEP responses in the congruent condition showed increased power compared to the responses in the incongruent condition, providing new evidence that syllables are important sublexical units in visual word recognition and reading aloud. With respect to the neural correlates of the effect, syllables elicited an early activation of a right hemisphere network. This network is typically associated with the programming of complex motor sequences, cognitive control and timing. Subsequently, responses were obtained in left hemisphere areas related to phonological processing.

Shift in lateralization during illusory self‐motion: EEG responses to visual flicker at 10 Hz and frequency‐specific modulation by tACS

Self-motion perception is a key aspect of higher vestibular processing, suggested to rely upon hemispheric lateralization and alpha-band oscillations. The first aim of this study was to test for any lateralization in the EEG alpha band during the illusory sense of self-movement (vection) induced by large optic flow stimuli. Visual stimuli flickered at alpha frequency (approx. 10Hz) in order to produce steady state visually evoked potentials (SSVEPs), a robust EEG measure which allows probing the frequency-specific response of the cortex. The first main result was that differential lateralization of the alpha SSVEP response was found during vection compared with a matched random motion control condition, supporting the idea of lateralization of visual-vestibular function. Additionally, this effect was frequency-specific, not evident with lower frequency SSVEPs. The second aim of this study was to test for a causal role of the right hemisphere in producing this lateralization effect and to explore the possibility of selectively modulating the SSVEP response. Transcranial alternating current stimulation (tACS) was applied over the right hemisphere simultaneously with SSVEP recording, using a novel artefact removal strategy for combined tACS-EEG. The second main result was that tACS enhanced SSVEP amplitudes, and the effect of tACS was not confined to the right hemisphere. Subsequent control experiments showed the effect of tACS requires the flicker frequency and tACS frequency to be closely matched and tACS to be of sufficient intensity. Combined tACS-SSVEPs are a promising method for future investigation into the role of neural oscillations and for optimizing tACS.

Towards a state-space geometry of neural responses to natural scenes: A steady-state approach

Our understanding of information processing by the mammalian visual system has come through a variety of techniques ranging from psychophysics and fMRI to single unit recording and EEG. Each technique provides unique insights into the processing framework of the early visual system. Here, we focus on the nature of the information that is carried by steady state visual evoked potentials (SSVEPs). To study the information provided by SSVEPs, we presented human participants with a population of natural scenes and measured the relative SSVEP response. Rather than focus on particular features of this signal, we focused on the full state-space of possible responses and investigated how the evoked responses are mapped onto this space. Our results show that it is possible to map the relatively high-dimensional signal carried by SSVEPs onto a 2-dimensional space with little loss. We also show that a simple biologically plausible model can account for a high proportion of the explainable variance (~73%) in that space. Finally, we describe a technique for measuring the mutual information that is available about images from SSVEPs. The techniques introduced here represent a new approach to understanding the nature of the information carried by SSVEPs. Crucially, this approach is general and can provide a means of comparing results across different neural recording methods. Altogether, our study sheds light on the encoding principles of early vision and provides a much needed reference point for understanding subsequent transformations of the early visual response space to deeper knowledge structures that link different visual environments.