A proposal for bio-synchronized transmission of EEG/ERP data
© Lopez-Gordo et al. 2016
Received: 20 October 2015
Accepted: 4 February 2016
Published: 19 February 2016
Acquisition of event-related potentials (ERPs) requires a nearly perfect synchronization between the stimulus player and the EEG acquisition unit that clinical systems implement at hardware level by means of a wired link. Out of clinical context, current brain-computer interface technology offers wireless and wearable EEG headsets that provide ubiquitous EEG acquisition. However, they are not adequate for ERPs acquisition since they lack the physical wire with the stimulus player. In this paper, we propose a novel technique devoted to provide a solution to this problem by means of a bio-synchronization approach. This technique adds to the stimulus data, a tagged audio preamble for synchronization (TAP-S) that embeds a synchronization mechanism in its physiological response based on pseudo random sequences. In this way, the EEG data elicited by the preamble and the stimulus are recorded together and the stimulus onset can be directly extracted from the EEG data by preamble detection. TAP-S is tailored to work with any low-cost multimedia player and wireless EEG headsets. Our preliminary results reveal TAP-S as a first, promising, and low-cost approach that, after further improvement, could enable remote processing of ERPs with wireless acquisition with application in telemedicine, ambient assisted living, or brain-computer interfaces.
EEG is a measure of the brain activity caused by populations of neurons that synchronously discharge their action potentials. An event-related potential (ERP) is the electrophysiological response evoked by an external stimulus that appears as positive or negative deflections of the EEG amplitude. In practical terms, ERPs are characterized by the amplitude and the latency with temporal reference to the stimulus onset. They are denoted by a letter P (positive) or N (negative) followed by a number that denotes the latency time in milliseconds since stimulus onset (e.g., P75, N100, and P200). ERP analysis is extensively used in clinical practice because their latencies and amplitudes correlate with well-known cognitive or physiological pathologies or functional impairments (e.g., long list with more than 20 visual abnormalities that includes optic neuropathy, multiple sclerosis, brain injury, and glaucoma [1, 2]). That means that an accurate estimation of the latencies and amplitudes is needed for diagnosis based on ERP analysis. The latter justifies the need of precise synchrony between the stimulus display and the EEG acquisition unit.
Telemonitoring is a key aspect for current e-health systems (see some current studies in [3–5]). Regarding remote EEG/ERP acquisition and testing, we merely mention some studies and cases of mobile and home-based EEG services. This service is gaining adepts among clinicians and users. As a matter of fact, approximately 30 % of Dutch neurologists use EEG recordings for clinical diagnosis . For instance, in , a telemedicine solution for remote video-EEG consultation was tried in La Rioja (Spain). Almost 99 % of patients expressed a high degree of satisfaction with the service. The authors of the paper concluded that users preferred the telemedicine service to in-hospital EEG test because it constitutes an improvement in access to this specialized medical care as well as important financial and time savings. The authors of  proposed a home-based polysomnography system as a cost-effective alternative for obstructive sleep apnea diagnosis. The system was equipped with a WiFi/3G interface for data and video communication via Skype. The authors of  compared the performance of four mobile EEG systems in recording epileptiform discharges. They concluded that most of the patients were satisfied with the service. There are more examples of home-based EEG [9–11] and medical services in general [12, 13]. However, these and other examples of home-based EEG and bio-signal testing do not apply to ERPs because of the nearly perfect synchrony needed between the stimulus player and EEG acquisition unit. Instead they register other long-term and non-related-to-events signals such as epileptic seizures or apnea episodes.
In respect to wireless EEG acquisition, we mention some studies and works related to brain-computer interfaces (BCIs) [14, 15]. In the last years, the technological evolution of BCIs has caused an increase of ambulatory, mobile, and wireless EEG headsets for clinic, entertainment, ambient assisted living, and other personal uses and applications [16–19]. The latest advance consists in low-cost, wearable and dry EEG headsets with wireless transmission (see [20, 21] for reviews) that allows mobile EEG services. These devices offer synchronization by means of proprietary software and protocols but not between the stimulus player and the wireless EEG headset. They are standalone solutions that do not integrate a stimulus player. Then, they are not meant to execute ERP paradigms but are suitable for others in which stimulation is not needed (e.g., self-regulation of low frequency cerebral rhythms , alpha band modulation  or steady-state EEG responses ). Conversely, other wireless EEG designs combine both stimulus player and EEG headset with synchronization [25, 26]. In , the latter attempt, specific clinical hardware for stimulation with a specific SYN port was used (PS33-PLUS, by Grass Technologies); although in terms of usability, we would expect wireless EEG headsets to permit users to use their own stimulus players without addition of extra synchronization hardware.
In summary, event-related paradigms are limited to clinical acquisition due to restrictions in synchrony. In this paper, we propose a technique, in the field of novel bio-inspired and bio-collaborative approaches [27, 28], aimed to address this limitation. Tagged audio preamble for synchronization (TAP-S) adds to the stimulation data a tagged audio preamble that embeds in its physiological response a synchronization mechanism based on pseudo random sequences. Our preliminary results reveal TAP-S as the first, promising, and low-cost approach that could enable recordings of ERPs with wireless EEG headsets and remote processing with application in telemedicine, ambient assisted living, or brain-computer interfaces.
2 TAP-S overview
2.1 The synchronization issue in ERP acquisition
Interactive services: Fig. 3 shows messages flow in a mobile EEG service. In the scenario of Fig. 3, the stimulation server stores the stimulus content. In an online application, it streams both a preamble and stimulation down to the stimulation player. The stimulation player buffers or reproduces it online, thus evoking the corresponding brain response on the user. A wireless EEG headset acquires this brain response and uploads the EEG data to the monitoring and processing server. In an online application, this server analyzes the brain response and immediately takes a decision. This decision modifies the next stimulation to be streamed down to the subject, thus closing the interactive loop.
This type of interactive service could permit online cognitive telerehabilitation, such as neuro-feedback applied to a multitude of pathologies (e.g., attention deficit hyperactivity disorder [30, 31], autism spectrum [32, 33], cerebral palsy , and mental impairment ).
Ubiquitous execution of event-related paradigms: since the synchronization provided by TAP-S is embedded in the EEG data, both the online and the offline execution of event-related paradigms could be performed. As an example, Fig. 4 shows a scenario of use: a volunteer (for instance a female) in a clinical study of vision downloads her video. It is stored in her mobile devices or her stimulus player. Then, during the commuting, she plays it. The wireless EEG headset acquires the brain responses and stores the EEG data. Then, it uploads them to a remote monitoring and processing server when a broadband connection is available (for instance at office). This server detects the stimulus onset of each trial by means of TAP-S and performs ERP analysis.
2.3.1 Physical principles
2.3.2 Preamble design
2.3.3 Preamble detection
We detect the preamble by means of a replica-correlator detector (equivalent to a matched filter detector ). There are two ways to build the replica signal, either by averaging many ERPs during a previous calibration session or synthetically by software. In this study, we decided the second option, thus avoiding calibration sessions and challenging the study under a plug-and-play approach. The replica signal was the expected electrophysiological response to the stimulus signal p 40hz(t) and was synthetically built as the convolution of the m(t) with 3 cycles of a 40-Hz sinusoidal signal. We used receiver operating characteristic (ROC) curves  and area under the curve (AUC) to assess the discrimination capacity of TAP-S. In addition, we estimated the best operating point (BOP).
2.3.4 Encapsulation process
2.4 Operation restrictions
TAP-S has only one restriction for an optimal synchronization. The media player must reproduce the stimulus data stream, including the preamble, in continuous mode. Buffering or playback is permitted, as well as online or offline upload of the EEG data. The only restriction is that both preamble and stimulus must be reproduced together without gaps, that is, without interruptions once the stimulation is started. Uninterrupted reproduction is mandatory because the synchronization process requires a replica signal that matches the response to the signal p 40hz(t).
In this preliminary study, we pursue (i) the assessment of preliminary results of TAP-S as the first bionic synchronization mechanism of data transmission and (ii) the analysis of its practical utility in medical diagnosis. In this experiment, we used a clinical EEG system in an isolated lab with a wired link between the stimulation and the acquisition units (similar to Fig. 1). The onset marks obtained with this configuration was considered the gold standard. Then, we tried the blind detection of the onset marks by means of TAP-S.
3.1 Experimental procedure
Two healthy volunteers participated (both males, 31 and 41 years old). The experiment was undertaken in a room isolated from external disturbances. The study was meant to be completely auditory, so blind volunteers could participate if necessary (see  for a discussion about the controversy in auditory vs. visual BCIs). Then, participants were told to close their eyes during the whole experiment, thus facilitating concentration and avoiding muscular EEG artifacts (e.g., eyes blinking or involuntary gazing). The auditory stimulation was manually adjusted to the comfort level of each participant. They were informed of all aspects of the study and signed the informed consent.
The experiment consisted of 21 trials with the same structure. First, an allocution indicated trial start after key pressing. Once the participant pressed a key, a beep announced the beginning of the trial. After the beep, the preamble was presented to the participant by means of earphones. Finally, a beep sounded and an allocution signaled the end of the trial and the preparation for the next one. The duration of each trial was around 6 s, and the inter-trial resting time was up to the participant (typically 15–25 s). The goal was to avoid cumulative effects along the trials (e.g., fatigue and lack of focus on the experiment).
3.1.2 Preamble header
Some simple rules were adopted to reduce the number of FPs. We excluded the beginning and the end of the EEG signals to avoid electrical artifacts due to electrode impedance measurement, initial calibration of amplifiers, filters setting, etc. The replica-correlator detector found peaks that exceeded the threshold with a minimum separation guard between them. If two peaks were detected within the separation guard, then the one with the highest amplitude was considered as preamble detection. If the separation between peaks was longer than the separation guard, then both were considered two independent detections. The upper limit of the separation guard is the duration of the preamble, namely 6.375 s, because this is minimum time between two consecutive trials without resting time. The minimum separation time is twice the length of a pulse of 3 cycles of the 40-Hz phenomenon, namely 150 ms, because it is the width of its autocorrelation function.
With these two limits, we did some preliminary trials and we estimated that a time guard of 2 s was a flexible choice that keeps balance between a low rate of false positives and a good time resolution for peak scrutiny.
3.1.4 EEG signal preprocessing
To suppress artifacts (e.g., due to muscular movement or induced by electrical glitches), any EEG amplitudes larger than 50 μV were grounded before presented to the replica-correlator detector.
The output of the replica-correlator in the absence of noise is a pass-band signal (a sinc function centered at 40 Hz). Since we preferred a base-band signal to perform detection of peaks of synchrony, we used a simple envelope detector (half-wave rectifier and low-pass filter) to obtain the base-band signal. The width of the main lobe of the sinc function in the frequency domain is the inverse of the duration of the 40-Hz phenomenon, that is, 3 cycles of 40 Hz. Then, the total length corresponds to 75 ms and the inverse is 13.3 Hz. This was the 3-dB cutoff frequency of the low-pass filter. The filter consisted in a second order Butterworth filter that was executed forward and reverse to cancel phase shifts. Note that the net effect is a fourth order filter with 6 dB of loss at the original 3 dB cutoff frequency.
The filtering process explained in this section is applied to the whole EEG acquisition, and the main goal is the detection of the preamble. In a clinical application, the specific processing of trials is typically specified by the clinical protocol.
Statistic at BOP
maxG (dB) 12.6
maxG (dB) 7.7
Stimulus onset (seconds)
Figure 10 contains relevant information about the detection performed at the BOP for subjects 1 and 2. It shows the output of the replica-correlator detector, the onset marks provided by the clinical EEG system, the onset marks detected by TAP-S, and the best detection threshold corresponding to the BOP (dotted horizontal line).
Figure 11 shows the ROC curves for both subjects. The AUC was AUC1 = 0.99 and AUC2 = 0.70 for subjects 1 and 2, respectively. The BOP was considered the detection threshold that maximized (4). These maximum values for each subject, in dB units, were BOP1 = 12.6 dB and BOP2 = 7.7 dB (see Table 1). Assuming perfect synchrony, these values correspond to the maximum improvement in SNR of ERPs after trial averaging with respect to a single trial.
Table 1 shows statistics of the detection at the BOP, namely the TF, FP, accuracy, and confidence intervals of a proportion at a significance level α = 0.05.
Table 2 shows details about the synchrony for the 21 trials in both subjects. The first column of each subject indicates the absolute time of each trial onset referenced to the beginning of the experiment. For instance, the first trial of subject 1 initiated 90.765 s after the experiment started. This first column (real) represents the gold pattern. The second column (TAP-S) indicates the onset time yielded by TAP-S. The last column (err.) computes the difference between the first and second columns, that is, the error in synchrony. Italics indicate trials for which TAP-S was unable to detect a valid preamble. This is the case when the error was longer than 150 ms. They were considered as outliers and not taken into account for the calculation of mean and standard deviation (see bottom rows of Table 2).
Based on the results of Table 2, the example of Fig. 12 illustrates the effects of trial averaging after using TAP-S and with perfect synchrony. For this purpose, synthetic ERPs, namely N100 and P200, were generated and used as patterns (thin lines in the snapshots). The two main plots of Fig. 12 show for subjects 1 and 2 (upper and bottom plots, respectively) the TAP-S-based trial averaging of the synthetic ERPs, assuming as synchrony errors as shown from the values of Table 2 (thick lines). Also, they show perfectly synchronous trial averaging (thin lines). The small snapshots on the upper-right corners correspond to a zoom-in of the central part of each main plot. The errors in synchrony with respect to the N100 and P200 components were less than 1 ms and −11 ms for subjects 1 and 2, respectively. See Section 5.2 for discussion regarding the impact of these error magnitudes.
In this section, we discuss the results in terms of detection performance and medical diagnosis utility. In summary, our preliminary results with two subjects support that TAP-S is capable to provide bio-synchronization by means of the 40-Hz response. However, the dissimilar results between subject 1 and subject 2 suggest that additional testing is required before TAP-S could be considered efficient enough for clinical applications.
5.1 Performance of TAP-S
Figure 10 shows detection performance at BOP for both subjects. The bottom plot shows a much more noisy aspect than the upper plot. We analyzed the EEG raw signals from both subjects, and the ones corresponding to subject 2 presented many more EEG artifacts. It could be due to muscular movements or nervous behavior during the trials (in fact, this subject recognized that this was his very first experience in this type of experiments). In some technologies such BCIs, it is assumed that they do not work for everyone  (i.e., BCI illiteracy). It could be stated that even though BCIs do not work for everyone, evoked potential recording does. That is, auditory potentials evoked by the recommended protocol (clinical instrumentation, setup, number of electrodes and positions, stimuli intensity, number of averages, signal preprocessing, etc.) are reproducible. Our proposal does not follow any clinical protocol since we pursued a simple plug-and-play approach (e.g., only one active electrode, no calibration session, and the use in detection of a generic replica) suitable for future plug-and-play BCI applications. Another justification for the poor performance of subject 2 could be in the stimulus used for the evocation of the 40-Hz response. Under our plug-and-play approach, the design of the stimulus was the same for both subjects. However, many aspects influence the amplitude of the 40-Hz response and, hence, the SNR of the signal to be detected (e.g., the intensity and auditory threshold of each person or the optimal carrier of the tone-pip). In addition, it has been reported that the optimal peaking frequency of the 40-Hz response probably varies (in the range 35–45 Hz) from one person to the next . The latter would lead to variances of the amplitude of the 40-Hz response that could justify the differences in performance between subjects 1 and 2. For sure, a calibration session would have improved the results of both subjects, but at the cost of our plug-and-play approach. Under these circumstances, entire success cannot be expected. This is the cost of the human factor. However, and despite the noisy aspect of the bottom plot, TAP-S was able to filter most of them due to the time guard defined in the methodological section (at BOP, only FP = 43 and TP = 19). It is important to consider that for a high rate in successful detection, some premises were introduced in the detection, namely the initial and end periods and the time guard. Without this information, the number of FPs would have increased. It is important to understand that this prior information only filters out FPs in the scale of seconds (e.g., separation guard was 6.375 s). This is not relevant to TAP-S and does not affect the essence of this experiment because TAP-S concerns synchronization in the millisecond scale. Synchronization in the scale of seconds between the media player and the EEG headset can be easily performed by IP protocols or even manually.
Figure 11 shows the ROC curves for both subjects. A rough guide for classifying the accuracy of a test based on the AUC is the traditional academic point system : 1.0 perfect; 0.90–0.99 excellent; 0.80–0.89 good; 0.70–0.79 fair; 0.60–0.69 poor; 0.50–0.60 worthless. In our study, the detection of preamble was excellent (AUC1 = 0.99) and fair (AUC2 = 0.70) for subjects 1 and 2, respectively. Then, the performance of TAP-S as preamble detector can be considered as excellent and fair for subjects 1 and 2, respectively.
Table 1 shows some details about the detection performance at the BOP. The large difference in accuracy between subject 1 (acc1 = 0.95) and subject 2 (acc2 = 0.31) is justified by the noise at the output of the replica-correlator detector (Fig. 8, bottom). The maximum improvement of SNR after trial averaging is remarkable (see Table 1, last row). It must be interpreted as the denoising capacity of TAP-S in this study. The maximum theoretical capacity, considering 0 FPs and 21 TPs is 13.2 dB by direct application of (4). Then, subject 1 achieved almost the maximum (12.6 dB).
We finalize this section mentioning that the scope of this experiment was not to obtain the highest performance in detection but to show evidence that synchronization in the range of milliseconds can be performed with TAP-S. As stated before, EEG is considered a non-stationary signal with large variations in inter-trials for the same subject and inter-subjects. The ROC curve showed a completely satisfactory performance for one subject. Consequently, it is more than enough to think of TAP-S as a promising technique that deserves to be optimized in future works.
5.2 Usefulness of TAP-S in medical diagnosis
Table 2 shows the numerical results on the detection of the onset marks. An aspect that deserves to be discussed is the large error values in the table (italics). It is obvious that the TAP-S did not work in all trials and some outliers happened. However, the gist of the discussion should orbit around the applicability of TAP-S in medical diagnosis with wireless EEG headset. The question to address are the following: (i) What would happen if some of the trials were detected with large synchronization errors? The immediate answer is that the corresponding EEG data would contain nothing but uncorrelated EEG that do not disturb the detection, except that more number of trials are needed to achieve a certain target SNR; (ii) What would be the effect of small errors around 20–50 ms? Small errors would give rise to a smoother shape but they would have no effect on the latency since negative and positive errors would cancel each other after a sufficient number of averages. Furthermore, results of subject 1 (see Table 2) show a very low number of errors in this time window (only 1 out of the 21 trials). The low number of small errors is justified because FPs are distributed in a large time window (from few milliseconds to seconds) and not only in the 20–50-ms window. Therefore, we expect a relative small number of small errors, thus having a minor impact on the shape. The next question would be, How would it affect the quality of the registered ERPs? In clinical practice, ERPs are estimated by averaging a high number of trials. Averaging of some trials with uncorrelated EEG data would just decrease the SNR of the ERPs, but the latencies and shape of the averaged ERPs would remain unaltered. It is interesting to point out that FPs with errors of several hundreds of milliseconds affect less than those with few milliseconds because the latter contain partial correlated EEG data. Figure 12 is an illustrative example of this with results reported in Table 2. Italics of the table are easily identified because, after trial averaging, they become small and positioned far from the zero lag. The snapshot of subject 1, at the upper-right corner of the main plot, shows with detail that the averaged trials yield N100 and P200 peaks with near zero error in latency with respect to the synthetized ERP. Furthermore, the envelope remains almost the same. This justifies the usability of TAP-S in medical diagnosis with wireless EEG teleservices.
In this paper, we propose a novel technique that provides synchronization for wireless EEG acquisition. TAP-S adds a preamble to the stimulation data that embeds in its neuro-physiological response a synchronization mechanism based on pseudo random sequences.
Despite a promising performance, still many open questions remain. For instance, the impulse response was assumed to be 3 cycles of 40 Hz. It could be optimized by individual basis with a previous calibration session. Also, the type of potential used for the preamble (the mid-latency auditory 40 Hz) could be substituted by others. Nothing prevents the use of visual stimulus instead of auditory. In fact, there are some pioneering studies about time-locking visual stimulus [60, 61]. Another fact is the design of the preamble. A sequence of 255 seemed to be a good trade-off between the detection performance and the overhead added to the stimulus. In our study, this overhead was just 6.375 s, while the recommendation to obtain visual ERPs is longer than 30 s (more than one sweep, each sweep containing 64 stimuli at a rate of two stimuli per second ). Furthermore, the stimulus data could be encapsulated by a header and tail, both for synchronization purposes, thus augmenting detection performance at the cost of overhead increasing.
To the best of our knowledge, this is the first attempt to provide a synchronization mechanism based on brain signals used in wireless ERP acquisition. Our very first design remarkably worked with one subject. This is the most relevant contribution of this work and it proves that TAP-S is a feasible approach that deserves to be improved. After further improvements, the level of synchronization provided by TAP-S would let remote assessment of ERPs and online analysis, thus opening the door to interactive mobile EEG applications.
This work was supported and co-financed by Nicolo Association for the R&D in Neurotechnologies for disability, the research project P11-TIC-7983, Junta of Andalucia (Spain), the Spanish National Grant TIN2015-67020, co-financed by the European Regional Development Fund (ERDF) and the CASIP research group TIC-117. We thank the Bio-engineering Institute of the University of Miguel Hernández of Elche (Spain), where part of this study was undertaken as a research stay.
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