1. Introduction
Wearable electroencephalography (EEG) offers promising application potentials for brain–computer interfaces (BCI) to improve everyday life, for example, in the form of sleep improvement [
1], seizure detection [
2], adaptive hearing aids [
3], or thought-based control of digital or robotic devices [
4,
5]. To realize these innovations, scholars are increasingly turning to miniaturized, and less visible EEG systems (so-called transparent, or concealed EEG) that are still capable of reliably capturing neural activity at the millisecond scale [
6], and that approach usability in everyday life situations [
7,
8,
9]. These researchers use custom-made in- or around-the-ear EEG systems [
2,
9], or, alternatively, ready-to-use flex-printed EEG electrode arrays that can be attached around the ear (“cEEGrids” [
10]). Thereby, they collect high quality EEG signals related to auditory attention, for example to study whether they can detect attentiveness to sounds in everyday situations [
7,
8,
11]. By using these ear-EEG solutions, researchers can overcome some of the major limitations of traditional cap-based EEG, in particular the cumbersome setup procedures (which include repeated hair washing) and the unpleasant aesthetics (who wants to wear a swim cap filled with gel and connected to 32–64 electrodes in everyday life?).
However, while these concealed EEG approaches represent an intriguing development, their use is somewhat limited due to the inherent measurement challenges. As the electrode space is reduced (compared to conventional EEG), the recorded signal amplitudes are also reduced (the effects of interest are on the order of a few microvolts) [
3]. Therefore, the amplifiers used need to show high recording sensitivity to enable data collection with these miniaturized EEG electrode designs. As a result, the amplification systems used to date have mostly been high-end products with high costs [
12]. This high cost, in turn, is a major limitation to the widespread adoption of concealed EEG designs. For this reason, previous research has, for instance, attempted to study whether around-the-ear cEEGrid electrodes can also be used with lower-cost open-source amplification systems, such as the OpenBCI Cyton+Daisy boards [
12]. The authors of [
12] found a general suitability of the OpenBCI amplifiers to collect large-effect neural activity changes in the frequency domain, such as the increase in occipital Alpha frequency power during eye closure (the Berger effect [
13]), or a decrease in Alpha band power with increasing task difficulty [
12] which were in line with previous work using high-end amplifiers [
10,
14]. However, these authors did not directly compare the performance of the OpenBCI amplifiers with that of a high-end amplifier, nor did they evaluate the aforementioned critical performance factors (timing accuracy and signal-to-noise ratio—SNR), which are essential for several applications (e.g., auditory evoked potential detection). Furthermore, previous research has also reported low input-referred noise (~1 µVpp) and low power consumption (5 mW/channel) for the OpenBCI Cyton+Daisy [
15]. In addition, this OpenBCI amplifier has shown a high SNR compared to clinical-grade amplifiers [
16] and the usability of this amplifier for event-related potential (ERP) research with classical cap-EEG [
15,
16]. Nevertheless, it remains to be investigated whether the system can be reliably used for the more challenging recording situation with concealed EEG designs.
In this article, we provide a thorough comparison of the Cyton+Daisy boards (OpenBCI, New York, NY, USA) with a benchmark amplifier, the Smarting Mobi (MBrainTrain, Belgrade, Serbia). To this end, we conducted three studies to assess the temporal accuracy of both systems, their performance in a typical laboratory study design, and finally a direct comparison of signal quality through simultaneous data recording with both amplifiers on the same participant. In doing so, we focus on concealed EEG recordings with the around-the-ear cEEGrid electrodes because they are readily available and don’t require custom fabrication for individual subjects. Initially, with the default settings of both systems, we found large differences in temporal precision, with high timing variation in the OpenBCI Cyton+Daisy, which would greatly reduce the ability to record time-domain features (ERPs). However, by correcting the Bluetooth dongle buffer settings and, most importantly, by developing a timestamp correction algorithm (provided with the article), the temporal precision of this low-cost amplifier was significantly improved, approaching the precision of the Smarting Mobi. In addition to the temporal accuracy, frequency and time domain comparisons of the amplifiers in the two recording setups with human participants show highly comparable recordings. This confirms the applicability of the OpenBCI system for these challenging EEG recordings, a finding that we believe provides a valuable foundation for further advancing research on concealed EEG.
2. Materials and Methods
As reference for a concealed EEG recording method, we use the so-called cEEGrids—a ‘flexible printed Ag/AgCl electrode system consisting of ten electrodes arranged in a c-shape to fit around the ear’ [
10] (see
Figure 1) in this work. While they are not the only available option for concealed EEG (see e.g., [
9,
17,
18] for in-ear EEG approaches), we focus on the around-ear method as the electrodes are readily available, can be used without personalization or customization, and come with multiple electrodes which allows recording signals across a range of positions on the head. Because of these multiple positions, the cEEGrids allow characterizing known EEG phenomena by providing additional information (e.g., the strength of an effect or feature morphologies on different positions around the ear [
3]). At the same time, it should be highlighted, that these cEEGrids—much like other ear-EEG solutions—only capture a subset of neural information when compared to traditional cap EEG [
3]. Specifically, they capture sources close to the ear region well (e.g., from the auditory cortex [
6,
19,
20]). More distant sources (e.g., from anterior or central brain regions) are harder to observe [
3]. The cEEGrids have been repeatedly reported to enable comfortable, high-quality and multiple-hour EEG recordings in field settings [
7,
8,
10,
11]. The recording quality is primarily realized by the possibility of using the cEEGrids with a gel enclosed by the adhesive [
10]. This property is also essential for our signal quality comparisons as dry electrodes are typically much more prone to irregular recording artefacts [
21]. The electrodes’ application around the ear is realized in about five minutes (including light cleaning of the skin with alcohol or an abrasive gel) [
22]. The electrodes can be re-used numerous times after cleaning the gel residue and re-applying a double-sided adhesive. For thorough application instructions we refer the reader to [
22].
The cEEGrids are then connected to the two amplifiers compared in this study: the OpenBCI Cyton+Daisy, and the MBrainTrain Smarting Mobi 24 (see
Figure 2). The OpenBCI amplifier comes in two configurations: either as the standalone Cyton amplifier (with 8 recording channels) or extended to the Cyton+Daisy configuration with 16 recording channels. In the eight-channel configuration, EEG data can be recorded with a sampling frequency of 250 Hz. This temporal resolution is reduced to 125 Hz in the 16-channel version due to limitations in the wireless packet transmission bandwidth. It is possible to also collect data with 250 Hz for the Cyton+Daisy configuration when data is not directly streamed to a recording computer, but instead stored on an SD card. Data from the Cyton+Daisy can be streamed to a computer using an RFDuino Bluetooth 4.0 Low Energy (BLE) radio transceiver. Due to low power consumption and the option to pair the Cyton+Daisy with battery sizes up to 1000 mAh, this amplifier system allows continuous recordings for over 12 h, which enables full-day data collections (e.g., to conveniently monitor neural activity in field study settings that span an entire day). Importantly, all of the OpenBCI components (hardware and software) are open-source and the amplifiers come with a much lower price than high-end systems like the Smarting Mobi. For the higher price, the Smarting Mobi features certain advantages like a higher sampling frequency of 500 Hz, up to 22 recording electrodes, and very low input-referred noise (<1 μVpp). Data from the Smarting Mobi can be streamed to a computer or portable device using a BlueSoleil Bluetooth Dongle Class I (Type BS002) with the Bluetooth v2.1 + EDR transmission protocol. Furthermore, in contrast to the OpenBCI amplifiers, the Smarting Mobi uses an active ground electrode (driven right leg—DRL) configuration. Other than that, the two amplifiers share many similarities like an amplification gain of up to factor 24, and a resolution of 24 bits. Additionally, both amplifiers are fitted with three-axis accelerometer sensors to observe head movement during recordings.
Table 1 summarizes the features of both amplifiers.
While these specifications are available from the respective user manuals, we wanted to put both systems to the test in a challenging EEG recording scenario: concealed ear-EEG where high temporal precision and low noise are essential. Therefore, we pursued three studies that are reported below. All studies used the same technical setup (i.e., the same hardware/software combination). As main recording device, a Microsoft Surface Laptop 3 was used running Windows 10 Home (Version 10.0.19042), NeuroBS Presentation Version 22.1 for the presentation of the audio stimuli, Smarting Streamer Version 3.4.3 for the recording with the Smarting Mobi amplifier, and the OpenBCI LSL Python interface (
https://github.com/openbci-archive/OpenBCI_LSL, accessed on 10 June 2021), executed in JetBrains PyCharm 2020.2 running Python Version 3.6.0. Finally, LabRecorder Version 1.14.0 was used to collect all data streams using the LabStreamingLayer (LSL) protocol (
https://github.com/sccn/labstreaminglayer, accessed on 10 June 2021).
3. Timing Test
As a first step, we decided to test the timing precision of the two amplifiers in a highly controlled setup. By feeding a consistent voltage-modulated signal (i.e., a square wave generated through the integrated sound card of a PC) into the amplifiers repeatedly, the actual timing precision can be assessed by having a clear ground-truth metric without any biological, or behavioral signal contaminations from human study participants. Our timing tests were closely aligned with the procedure in [
23], thereby focusing on the temporal precision between the presentation of a physical stimulus and the recorded event markers.
3.1. Protocol
Using the EEG amplifiers as oscilloscopes, we adapted the protocol from [
23] to a desktop PC, which allowed us to evaluate and quantify the temporal precision of the amplifiers using audio signals. The core part of this timing test protocol is that the signal on the audio jack is fed directly into the EEG amplifiers, whose signals are transmitted through the Bluetooth dongle and recorded by the corresponding desktop PC. This setup can measure the time between the programmatic start of the playback of a sound, marked by a stimulus event marker, and the actual playback onset of the sound, as indicated by the audio jack voltage fluctuations, with EEG sampling rate precision (here: 125 to 500 Hz sampling rate, resulting in 8 ms to 2 ms precision). To prevent possible damage to the amplifier and a clipped signal, the volume is set to a medium level (35%). Additionally, capacitors (ZSU 100 nF 20% 50 V RM2.54) were integrated in the circuit to prevent accidental power surges from damaging the amplifiers.
To record the signal, the stimulus presentation application (NeuroBS Presentation) plays a sound and sends out an LSL marker indicating the intended playback time, which is recorded in the EEG acquisition file. The sound signal is picked up from the headphone jack and is recorded on a single EEG channel using a cable connection. Both amplifiers are connected to the recording PC at the same time (see
Figure 3). The signal data is transmitted to the PC using the respective, proprietary Bluetooth dongles of each device manufacturer. We used the integrated sound card of the PC to produce a periodic square wave signal (10 Hz frequency, 5 ms duration) for the timing tests. This setup allowed us to quantify the delay between the generation of each square wave and its detection by the tested EEG amplifiers. The same number of trials were presented for each recording (~400) in a single block.
Multiple meaningful configurations are possible for comparing the timing in the two amplifiers, which is why we ran the timing test in three configuration pairs.
Configuration 1: First, recordings were collected using the typical recording parameters in each amplifier, as they are used in the physiological evaluation study (i.e., sampling frequencies of 500 Hz for the Smarting Mobi and 125 Hz for the 16-channel Bluetooth recording with the OpenBCI Cyton+Daisy). These data can show how the amplifiers would perform in their default configurations.
Configuration 2: To more directly assess possible timing differences, we collected a set of recordings in which both amplifiers were set to the highest common sampling frequency of 250 Hz. For the Smarting Mobi, this can be set up in the Smarting Streamer Application. For the OpenBCI LSL Python interface, a higher sampling rate can be used when data is only collected using an eight-channel OpenBCI Cyton setup.
Configuration 3: We learned that the regular OpenBCI Dongle configuration is considered insufficiently precise for ERP studies by the manufacturer due to the FTDI buffer latency timer being set to an inadequately long interval (16 ms) by default. Therefore, the manufacturer recommends lowering this setting to 1 ms (
https://docs.openbci.com/Troubleshooting/FTDI_Fix_Windows/, Last accessed on 15 March 2023). The third set of recordings was, therefore, collected after changing this buffer setting, one set with the regular sampling frequencies (Smarting Mobi: 500 Hz and OpenBCI Cyton+Daisy: 125 Hz), and one set with the highest common sampling frequency (250 Hz).
Across all configurations, the cables connecting directly to the reference and first channel pins in each amplifier were switched after every four recordings, to eliminate possible confounding influences in the circuits. Altogether, 32 recordings were made with 400 trials per recording (eight for each configuration). The data and code for these timing tests are available at
https://github.com/MKnierim/openbci-vs-smarting-timing-test.
3.2. Data Processing
3.2.1. Regular Dejitter and Signal Peak Detection
To extract the single trial epochs from the continuous recording of the square wave signal, the recorded data were cut between −200 ms and +800 ms after the stimulus software marker. The timestamp of this software marker was thus set as the timing reference (t
0). Afterwards, the delay between the stimulus marker and the signal amplitude increase (onset) was assessed. In alignment with [
23], the single trial latency was defined as the time between marker onset and the amplitude exceeding the half-maximum of the trial-averaged response. Additionally, latency jitter was defined as the standard deviation of those single trial latencies, and latency lag was defined as the mean of the single trial latencies (see
Figure 4).
It is important to note the inherent presence of a slight jitter in the sample time stamps as the timestamping itself usually does not happen exactly in regular intervals but on a somewhat random schedule (dictated by the perils of the hardware, drivers, and operating systems). To remove this jitter, the XDF file importer (e.g., the Python interface pyxdf which we used here—
https://github.com/xdf-modules/pyxdf, accessed 10 June 2021) uses a robust linear interpolation method (i.e., adjusting the timestamps with a linear model fit in signal segments without gaps). This approach performed as expected for all recordings with single packet transmission (all Smarting Mobi recordings and the OpenBCI recordings in Configuration 3 with 1 ms FTDI buffer settings). In contrast, the observed trial latencies for the default OpenBCI recordings (with 16 ms FTDI buffer—Configuration 1 and 2) showed a highly erratic pattern. These observations led us to further investigate the suitability of alternative dejittering approaches for the OpenBCI data.
3.2.2. Chunk-Dejittering
The default buffer configuration of the OpenBCI Bluetooth dongle leads to an accumulation of data samples in packets that are then received at more or less regular intervals. Thereby, the time structure in this data resembles chunks with low sample-to-sample time difference within chunks, and large differences between the last sample and the following chunk (see
Figure 5A). Importantly, slight variations can be observed in these chunk sizes (59–61 samples for 125 Hz recordings and 119–121 samples for 250 Hz recordings), which explains why the linear XDF interpolation method (regular dejitter) performed poorly with this timestamp structure.
Assuming good temporal accuracy for the chunk reception timestamps, we pursued an alternative dejittering approach for the OpenBCI data that focused on within-chunk (i.e., local) timestamp correction instead of a global timestamp correction. Thereby, the reception of a new chunk is identified by their large sample-to-sample time difference first, and afterwards, the timestamps for each chunk are extrapolated from the first sample (the original chunk reception timestamp) using the underlying sampling frequency. Initially, this approach showed a substantial improvement in jitter metrics, but produced outliers with some trials. Inspecting the sample-to-sample timespans again further highlighted that the previously mentioned irregular chunks now appeared to overlap with previous chunks (and with gaps to following chunks—see
Figure 5B). To further correct this issue, short chunks were shifted in place (i.e., moved to the right by adding the delta value to the chunk timestamps). This process appeared to correct the timestamp information (see
Figure 5C), as can also be seen in the example of a recording from Configuration 1 in
Figure 6. Therefore, this chunk-dejitter algorithm was also used for analyzing the timing performance in the OpenBCI recordings in Configuration 1 and 2. To enable other researchers to utilize this dejitter method, we also integrated the algorithm in a fork of the pyxdf library that is available at:
https://github.com/MKnierim/pyxdf (see
Supplementary Materials).
3.3. Results
The global results of the timing comparisons for all 32 audio marker recordings (runs) are summarized below. The boxplots in
Figure 7 reflect the onset latency distributions based on ~400 presented stimuli per session in the top row, and the average lag and jitter metrics in the mid and bottom rows, respectively. Note that the y-Axis axis range is consistent (showing 150 ms) but the level is much higher for plots B and C (OpenBCI Config 1 and 2).
Across the runs and configurations, the lag was found to be the lowest for the Smarting Mobi (31.3 ms at 500 Hz and 22.64 ms at 250 Hz), and the OpenBCI recordings with the FTDI buffer fix (21.92 ms at 125 Hz and 18.12 ms at 250 Hz). For the OpenBCI recordings with the default buffer settings, the lag was much larger both with the regular dejitter method (337.31 ms at 125 Hz and 328.16 ms at 250 Hz) and the chunk dejitter method (529.52 ms at 125 Hz and 527.07 ms at 250 Hz). This observation implies that the observation of a classical ERP component (e.g., the P300) would be critically skewed in this default buffer configuration, if the lag is not accounted for. This problem is exacerbated by a substantial variation in lag per run that is present with the regular dejitter method. In contrast, the chunk dejitter method eliminates this lag variance. Thus, with the chunk dejitter method, the large lag can easily be accounted for by subtracting the average lag from the EEG signal timestamps in a given run.
More important than this lag is the presence of timing jitter. This variation in timing precision is lowest for the Smarting Mobi (0.59 ms at 500 Hz and 1.17 ms at 250 Hz). Such variation is to be expected for these sampling frequencies. Overall, these results highlight the high and superior temporal precision of the Smarting Mobi amplifier. For the OpenBCI Cyton, the lowest jitter is found with the regular buffer setting and the chunk dejitter method (3.19 ms at 125 Hz and 1.69 ms at 250 Hz), closely followed by the recordings with the FTDI buffer fix (4.36 ms at 125 Hz and 2.10 ms at 250 Hz). These values imply that the OpenBCI Cyton+Daisy can be used reliably for the collection of ERPs with these configurations. The best performance is achieved with the regular buffer setting and the chunk dejitter method, which also showed very high consistency in jitter metrics (only minimally higher than for the Smarting Mobi). We, therefore, decided to use this configuration (default buffer setting + chunk dejitter timestamp correction) for the following amplifier comparisons with human participants.
6. Discussion and Conclusions
In this work, we compared the performance of a high-end (MBrainTrain Smarting Mobi) and a low-cost (OpenBCI Cyton+Daisy) EEG signal amplifier for recording neural activity with around-the-ear (cEEGrid) electrodes. This comparison provides crucial answers for the accessibility and progress of the research on concealed EEG, which can be used in everyday life to enable applications such as adaptive hearing aids [
3], sleep monitoring [
1] or novel human–computer interaction modalities [
4,
5]. Due to the high technical requirements for the recording of ear EEG signals (high temporal precision for ERPs and high SNR for the acquisition of low-amplitude signals [
3]) a comprehensive evaluation of the recording capabilities of a low-cost amplifier alternative is essential. Thereby, our work goes beyond previous comparisons of the OpenBCI Cyton+Daisy amplifier [
15,
32] by documenting temporal precision more systematically and directly comparing ear-EEG signals and features. We adapted a paradigm specifically for this purpose and identified a number of interesting parameters.
First of all, our work shows that it is necessary to determine the desired recording configuration with the OpenBCI Cyton+Daisy and the USB dongle buffer settings. If the system is used with its default settings (“out-of-the-box”), scholars will experience problems with latency and jitter—especially when using the currently available dejittering methods (i.e., those implemented in the XDF interfaces like pyxdf). While the OpenBCI developers are aware of this limitation and recommend the FTDI buffer fix in the amplifier documentation, this step may not be obvious to all users. For example, we were not aware of this aspect when recording the timing test signals. On the other hand, this led us to investigate and develop a fix for the chunky and irregular timestamp patterns in this initial configuration—the chunk dejitter method. This new algorithm not only allowed for the correction of misaligned timestamps, but actually led to improved timing performance (higher precision and consistency), which is why we used (and recommend) it for our ERP study recordings. The improved consistency is the main reason for this recommendation, as the OpenBCI Cyton+Daisy sometimes showed quite high jitter variances. Even with the manufacturer’s recommended FTDI buffer fix, sample transfer timestamps can be quite volatile, which can have a serious impact on ERP analyses. Still, we must emphasize that our recommended recording configuration without the buffer fix will require a one-time shift of the recorded timestamps to provide accurate ERP results due to the high lag of over 500 ms. In summary, with these recommended corrections (using the new chunk dejitter and timestamp shift) OpenBCI Cyton+Daisy users can reliably (i.e., with high temporal precision) and easily (without having to change hardware settings) record ear-EEG time-domain signals that approach the quality of the high-end Smarting Mobi amplifier.
Second, beyond these timing findings, we found comparable performance in human cEEGrid recordings with both amplifiers in two experimental designs: (1) repeated experiments with both amplifiers per participant, and (2) simultaneous amplifier recordings in a single experiment run. Generally, it should be highlighted that our results rely on a relatively small sample size, which poses a limitation for the detection of small effects. However, as we were primarily interested in replicating relatively large and well-known effects—and did so with both amplifiers—we feel that this sample size was acceptable for the purposes of this work. In the first case, comparable signals are found for the frequency-domain and time-domain features, with no discernible patterns that would indicate superior performance of one amplifier over the other. However, since the recorded data in this first experiment showed general limitations with artifacts, we also looked more closely at the concurrent recordings. In this last experiment, we were able to directly assess signal comparability and found very similar signal morphologies and ERP components for both amplifiers. Again, these results lead us to conclude that both amplifiers have similar SNR performance. Because the signals were compared for electrodes in close proximity, but not exactly in the same position, there remain minimal differences that could be further eliminated by building adapters that allow signals from the same electrodes to be recorded simultaneously with both amplifiers. A design for such an adapter (which also limits crosstalk between amplifiers connected to the same electrode) has been documented in [
32]. However, since the author found very similar signals in the OpenBCI Cyton and another high-end EEG amplifier, and since our results have consistently shown similar signal qualities, we believe that the sum of the evidence sufficiently documents the suitability of the OpenBCI Cyton+Daisy amplifier for recording (around-the-ear) EEG signals.
In conclusion, the MBrainTrain Smarting Mobi definitely offers advantages in terms of sampling frequency and temporal precision for the study of neural signals in the ear region. If money is no obstacle, it is probably the preferably option currently. However, if you are on a smaller budget, using the OpenBCI Cyton+Daisy amplifiers is a viable alternative for (around-the-ear) EEG research and prototype development. Given that many of these amplifiers are already distributed around the world (OpenBCI currently lists over 200 publications with their devices, which is only a fraction of the units distributed) this new evidence of additional recording capabilities will hopefully stimulate further growth in the development of concealed EEG [
3], which has the potential to deliver exciting applications and technologies in the near future.