Method Article

Inter-Brain Synchrony in Open-Ended Collaborative Learning: An fNIRS-Hyperscanning Study

DOI:

10.3791/62777

⸱

July 21st, 2021

 ,  , 
1School of Psychology and Cognitive Science, East China Normal University, 2Shanghai Key Laboratory of Mental Health and Crisis Intervention, East China Normal University

In This Article

Summary

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The protocol for conducting fNIRS hyperscanning experiments on collaborative learning dyads in a naturalistic learning environment is outlined. Further, a pipeline to analyze the Inter-Brain Synchrony (IBS) of oxygenated hemoglobin (Oxy-Hb) signals is presented.

Abstract

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fNIRS hyperscanning is widely used to detect the neurobiological underpinnings of social interaction. With this technique, researchers qualify the concurrent brain activity of two or more interactive individuals with a novel index called inter-brain synchrony (IBS) (i.e., phase and/or amplitude alignment of the neuronal or hemodynamic signals across time). A protocol for conducting fNIRS hyperscanning experiments on collaborative learning dyads in a naturalistic learning environment is presented here. Further, a pipeline of analyzing IBS of oxygenated hemoglobin (Oxy-Hb) signal is explained. Specifically, the experimental design, the process of NIRS data recording, data analysis methods, and future directions are all discussed. Overall, implementing a standardized fNIRS hyperscanning pipeline is a fundamental part of second-person neuroscience. Also, this is in line with the call for open-science to aid the reproducibility of research.

Introduction

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Recently, to reveal the concurrent brain activity across the interactive dyads or members of a group, researchers employ the hyperscanning approach1,2. Specifically, electroencephalogram (EEG), functional magnetic resonance imaging (fMRI), and functional near-infrared spectroscopy (fNIRS) are used to record the neural and brain activities from two or more subjects simultaneously3,4,5. Researchers extract a neural index entailing concurrent brain coupling based on this technique, which refers to inter-brain synchrony (IBS) (i.e., phase and/or amplitude alignment of the neuronal or hemodynamic signals across time). A large variety of hyperscanning research found IBS during social interaction between multiple individuals (e.g., player-audience, instructor-learner, and leader-follower)6,7,8. Furthermore, IBS holds specific implications of effective learning and instruction9,10,11,12,13,14. With the surging of hyperscanning research in naturalistic learning scenarios, establishing a standard protocol of hyperscanning experiments and the pipeline of data analysis in this field is necessary.

Thus, this paper provides a protocol for conducting fNIRS-based hyperscanning of collaborative learning dyads and a pipeline for analyzing IBS. fNIRS is an optical imaging tool, which radiates near-infrared light to assess the spectral absorption of hemoglobin indirectly, and then hemodynamic/oxygenation activity is measured15,16,17. Compared with fMRI, fNIRS is less prone to motion artifacts, allowing measurements from subjects who are doing real-life experiments (e.g., imitation, talking, and non-verbal communication)18,7,19. In comparison with EEG, fNIRS holds higher spatial resolution, allowing researchers to detect the location of brain activity20. Thus, these advantages in spatial resolution, logistics, and feasibility qualify fNIRS to conduct hyperscanning measurement1. Using this technology, an emerging research body detects an index term as IBS-the neural alignment of two (or more) people's brain activity-in different forms of naturalistic social settings9,10,11,12,13,14. In those studies, various methods (i.e., Correlation analysis and Wavelet Transform Coherence (WTC) analysis) are applied to calculate this index; meanwhile, a standard pipeline on such analysis is essential but lacking. As a result, a protocol for conducting fNIRS-based hyperscanning and a pipeline using WTC analysis to identify IBS is presented in this work

This study aims to evaluate IBS in collaborative learning dyads using the fNIRS hyperscanning technique. First, a hemodynamic response is recorded simultaneously in each dyads' prefrontal and left temporoparietal regions during a collaborative learning task. These regions have been identified as associated with interactive teaching and learning9,10,11,12,13,14. Second, the IBS is calculated on each corresponding channel. The fNIRS data recording process consists of two parts: resting-state session and collaborative session. The resting-state session lasts for 5 min, during which both the participants (sitting face-to-face, apart from one another by a table (0.8 m)) are required to remain still and relax. This resting-state session is served as the baseline. Then, in the collaborative session, the participants are told to study the entire learning materials together, eliciting understanding, summarizing the rules, and making sure all learning materials are mastered. Here, the specific steps of conducting the experiment and fNIRS data analysis are presented.

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Protocol

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All recruited participants (40 dyads, mean age 22.1 ± 1.2 years; 100% right-handed; normal or corrected-to-normal vision) were healthy. Before the experiment, participants gave informed consent. Participants were financially compensated for their participation. The study was approved by the University Committee of Human Research Protection (HR-0053-2021), East China Normal University.

1. Preparation steps before adopting data

  1. Homemade NIRS caps
    1. Adopt elastic swimming cap to place optode holder grid.
      NOTE: Considering that the head sizes of the participants are different, two sizes of caps are used. Small caps are prepared for participants with a head circumference of 55.4 ± 1.1 cm, and large caps are for the participants with a head circumference of 57.9 ± 1.2 cm.
    2. Anchor the location of the EEG electrodes (inion, Cz, T3, T4, Fpz, and P5) as reference optodes according to the standard international 10-10 system on elastic swimming caps (see Table of Materials).
      1. First, place the standard 10-10 EEG cap (see Table of Materials) on the head mold, and put the elastic swimming cap on the EEG cap. Second, mark reference optodes (inion, Cz, T3, T4, Fpz, and P5) with chalk on each cap. Finally, cut two holes about 15 mm in diameter to place the two reference optodes (i.e., Fpz and P5, Figure 1).
        NOTE: Specifically, a 3 x 5 optode probe set and a 4 x 4 optode probe set are separately placed over the prefrontal area (reference optode is placed at Fpz, Figure 1B) and left temporoparietal regions (reference optode is placed at P5, Figure 1B).
    3. Cut holes to place the other optodes. Arrange a swimming cap with two grid holders directly on the head mold. Then, mark the location of other optodes with chalk. After that, cut the rest holes to make sure the grid holder fits in.
    4. Mount two probe sets (i.e., 3 x 5 and 4 x 4) to the swimming caps (see Table of Materials).
      NOTE: The NIRS measurement system (see Table of Materials) provides these standard probe sets (i.e., 3 x 5 and 4 x 4) with standard holder sockets ensuring the 30 mm optode separation.
    5. Open the probe set monitor window at the NIRS measurement system and select four probe sets arranged in 3 x 5 and 4 x 4 for each person, separately.
      NOTE: The probe arrangements of the two caps should correspond to the structures in the probe set window (i.e., the exact location of the receiver probe numbers and the respective emitter).
  2. Preparation of the experiment
    1. Before recording data, ensure the NIRS system is keeping a stable operating temperature by starting the system for at least 30 min.
      NOTE: The stable operating temperature ranged from 5 °C to 35 °C.
    2. Set the measurement mode to event-related measurement. Ensure the triggers receiver is active (i.e., the RS232 serial input).
      NOTE: The experiment is programmed in commercially available psychology software (see Table of Materials). The absorption of near-infrared light (two wavelengths: 695 and 830 nm) is measured with a sampling rate of 10 Hz.
    3. Prepare the lighted fiber optic probe, which can be used to move hair aside.
    4. Set the experiment environment with one table with two chairs to keep participants' seats face-to-face.

2. Adopting data by instructing participants

  1. Prepare the participants
    1. Instruct the participants, including the details of NIRS measurement methods.
      NOTE: All the participants were healthy and were financially compensated for participation. No participants withdrew from the experiment halfway through. The laser beam of the NIRS may be harmful to the participants' eyes, and they were instructed not to look directly into those laser beams.
    2. Make the participants sit face-to-face (apart from a table (0.8 m)) to make sure they can see each other directly. Adjust the chair-to-table distance (i.e., nearly 0.3 m) to make the participants sit comfortably.
    3. Turn on the laser button, and place the caps with the probe sets on the participants' heads.
      NOTE: The 3 x 5 probe sets cover the forehead of the participants (middle probe of the bottom row is placed on Fpz); the 4 x 4 probe sets cover the left temporoparietal cortex (the third probe of the third row is placed on P5).
    4. Put the four optical fiber bundles loosely on the holder's arms without contact with the participants or chairs.
      NOTE: Here, the NIRS measurement system has four bundles of optical fibers. Additionally, ensure that the participants do not feel too heavy to pull off the caps.
    5. Let the probe tips touch participants' scalp by carefully pushing each spring load probe further into its socket.
    6. Perform signal calibration.
      1. First, check the quality of the signal by clicking the Auto Gain in the probe set monitor window of the fNIRS machine. Then, a channel's poor signal and sufficient signal are marked in yellow and green in the probe set monitor window, respectively.
        NOTE: For a channel with insufficient signals, lighted fiber optic probes are used to move the hair under the probe's tip to one side.
      2. Then, push the probes further into their sockets to get sufficient signals. Repeat this process until all the channels are marked in green in the probe set monitor window of the NIRS measurement system, indicating that the quality of signals is accessible.
  2. Run the experiment
    1. Start the experiment with a 5 min rest state, which serves as the baseline. Then, two participants are required to co-learn the learning materials.
    2. After the experiment, click on Text File Out to export the raw light intensity data and save the data as a text file.
      NOTE: No filters are applied in the NIRS measurement system.
    3. Use the three-dimensional (3D) digitizer (see Table of Materials) to determine the locations of emitters, receivers, and other references (i.e., inion, nasion, Cz, and left and right ears) for each participant.
      1. Obtain the MNI coordinates for the recording channels using the commercially available numeric computing platform21 (see Table of Materials). Supplementary Table S1 shows the corresponding anatomical locations of each channel.
    4. Clean probes and probe holders with ethanol. Wash caps with mild detergent and let the caps air dry.

3. Data analysis

  1. Data preprocessing
    NOTE: Previous research has adopted variable non-commercial software packages (e.g., Homer222, AnalyzIR23, or nirs LAB24) with numeric computing platforms (see Table of Materials) on fNIRS data analysis, and they are all available on the website. Here Homer2 was used to do the preprocessing of the NIRS data. Additionally, both fNIRS recording data collected in the rest and collaborative learning phases share the same preprocessing and analysis pipeline.
    1. Copy the dataset from the fNIRS machine. Convert the original data formation to the proper formation (i.e., convert cvs file to nirs file).
    2. Convert raw data to optical density (OD) data with "hmrIntensity2OD" function provided in the Numeric computing platform (see Table of Materials).
    3. Delete the bad channels. Then average the OD value for each participant on each channel and full sample points, respectively.
      NOTE: Here, 46 averaged OD values are obtained.
      1. Calculate the standard deviation (SD) for each participant.
      2. Mark as unusable and remove the channels with very low or high OD (which exceeded 5 SDs) from the analysis for each participant.
        NOTE: This step can be performed before and/or after fNIRS data preprocessing. In this data analyses pipeline, the bad channels are detected before the fNIRS data preprocessing.
    4. Convert the OD time data into Oxy-Hb, DeOxy-Hb, and combined signal based on the modified Beer-Lambert Law25.
      NOTE: Reference25 says, "All data analysis steps are conducted on Oxy-Hb data, which is an indicator of the change in regional cerebral blood flow having higher signal-to-noise ratio26. Additionally, previous research employed fNIRS hyperscanning in teaching and learning scenarios mainly focused on Oxy-Hb concentration11,12,13,14."
    5. Calibrate Oxy-Hb time series from motion artifacts by the channel-by-channel wavelet-based method.
      NOTE: Specifically, the Daubechies 5 (db5) wavelet with tuning parameter at 0.1 (see details in Homer2 manual)27,28 is adopted in removing motion artifacts.
    6. Apply the band-pass filter (i.e., 0.01-1 Hz) on the calibrated Oxy-Hb data to reduce the high-frequency noise and slow drift.
    7. Conduct principal components analysis (PCA) on the OxyHb signal to remove non-neural global components (e.g., blood pressure, respiration, and blood flow variation)29.
      NOTE: The PCA analysis proposed by Zhang and colleagues29 is adopted here.
      1. First, decompose the signal.
        NOTE: The specific formula of decomposition of fNIRS signal is: H = UΣVT. Here, temporal and spatial patterns of fNIRS data are presented in two matrices (i.e., U and V). U is a 2D (sample point x principal component) matrix. V is also a 2D (principal component x principal component) matrix. The column in V indicates one principal component (PC), and the strength of that PC for a particular channel is estimated in each entry of the column. The relative importance of each PC is represented by the value of the diagonal matrix Σ.
      2. Second, conduct spatial smoothing.
        NOTE: Gaussian kernel convolution is employed to remove localized signals and get the global component.
      3. Third, reconstruct the signal.
        NOTE: To calculate the global component of the fNIRS data, the smoothed spatial pattern matrix V* is plugged back into the decomposition formula: HGlobal = UΣ(V*)T. Then, localized derived neuronal signal can be obtained using original data H to subtract HGlobal : HNeuronal = H - HGlobal.
  2. Inter-brain synchrony
    NOTE: To reveal brain coupling in second-person neuroscience, wavelet transform coherence (WTC) is adopted here. Briefly, WTC measures the correlation between two-time series as a function of frequency and time. The specific formula of wavelet coherence of two-time series x and y is:
    Wavelet Transform Coherence (WTC) formula; mathematical equation for time-frequency analysis.
    ​T and s denote the time and wavelet scale separately, ‹·› indicates a smoothing operation in scale and time. W represents the continuous wavelet transform. Then, a 2D (time x frequency) WTC matrix is generated30. Several toolboxes are used to calculate the WTC value. Here the toolbox created by Grinsted and colleagues was used30.
    1. Adopt the WTC function of the numeric computing platform (see Table of Materials).
      NOTE: Here, the default setting of the mother wavelet (i.e., Generalized Morse Wavelet with its parameters beta and gamma) is used. Mother wavelet converts each time series into the frequency and time domain.
    2. Set the default setting on the other parameters (i.e., MonteCarloCount, representing the number of surrogate data sets in the significance calculation).
    3. Calculate the WTC value for two corresponding channels (the same channel in two participants) in a numeric computing platform (see Table of Materials). Following the same procedure, 46 WTC matrices are generated from 46 channels.
    4. Determine the frequency band of interest (FOI), which is sensitive to collaborative learning.
      NOTE: Here, a cluster-based permutation approach is adopted to detect such FOI31, which offers a solution to multiple comparisons in multi-channel and multi-frequency data.
      1. Perform Time-average of the WTC values in the resting and collaborative learning phases, respectively, for each channel combination. Then, conduct paired sample t-tests along with the entire frequency (frequency range: 0.01-1Hz32) on these time-averaged WTC values (collaborative learning vs. rest). Next, identify frequency bins at which the task effect is significant (collaborative learning > rest, p < 0.05).
      2. Obtain significant frequency neighboring points (≥2) as observed clusters and corresponding T values.
      3. Conduct a series of paired sample t-tests on permuted data to generate the T values for each cluster qualified in step 3.2.4.2 for 1000 times.
        NOTE: For forming permuted data, participants are randomly assigned to form new two-member pairs. As the length of datasets varied across dyads for each random pair, the longer dataset is trimmed to the same length as the shorter one33.
      4. Compare the averaged cluster-based T values from original pairs with the T values of 1000 permutations.
        NOTE: The p values evaluated by this formula34:
        Error function equation, erfc, statistical analysis formula, data distribution evaluation. , where S0 denotes observed averaged-cluster t-value, μp and σp indicate the mean and standard deviation of permutation values.
      5. Average WTC values in the identified FOI in each channel in each dyad. Then, apply fisher z transformation to the WTC values to get a normal distribution of WTC values. Use this value to index the IBS for further statistical analysis.

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Results

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Figure 1 illustrates the experimental protocol and probe location. The fNIRS data recording process consists of two parts: resting-state session (5 min) and collaborative session (15-20 min). The collaborative learning dyads are required to relax and to keep still in the resting-state session. After that, participants are told to co-learning the learning material (Figure 1A). Their prefrontal and left temporoparietal regions are covered by the corresponding prob...

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Discussion

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First, in the present protocol, the specific steps of conducting fNIRS hyperscanning experiments in a collaborative learning scenario are stated. Second, the data analysis pipeline that assesses the IBS of hemodynamic signals in collaborative learning dyads is also presented. The detailed operation on conducting fNIRS hyperscanning experiments would promote the development of open-science. Furthermore, the analysis pipeline is provided here to increase the reproducibility of hyperscanning research. In the following, the ...

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Disclosures

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The authors have nothing to disclose.

Acknowledgements

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This work is supported by the ECNU Academic Innovation Promotion Program for Excellent Doctoral Students (YBNLTS2019-025) and the National Natural Science Foundation of China (31872783 and 71942001).

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Materials

List of materials used in this article
NameCompanyCatalog NumberComments
EEG capsCompumedics Neuroscan,Charlotte,USA64-channel Quik-CapWe choose two sizes of cap(i.e.medium and large).
NIRS measurement system with probe sets and probe holder gridsHitachi Medical Corporation, Tokyo, JapanETG-7100 Optical Topography SystemThe current study protocol requires an optional second adult probe set for 92 channels of measurement in total.
Numeric computing platformThe MathWorks, Inc., Natick, MAMATLAB R2020aServes as base for Psychophysics Toolbox extensions (stimulus presentation), Homer2  (fNIRS preprocess analysis), and "wtc" function(WTC computation).
Psychology softwarepsychology software tools,Sharpsburg, PA,USAE-prime 2.0We apply E-prime to start the fNIRS measurement system and send triggers which marking the rest phase and collaborative learning phase for fNIRS recording data.
Swimming capsZoke corporation,Shanghai,China611503314We first placed the standard 10-20 EEG cap on the head mold, and placed the swimming cap on the EEG cap. Second, we marked (inion, Cz, T3, T4, PFC and P5) with chalk.
Three-dimensional (3-D) digitizerPolhemus, Colchester, VT, USA;Three-dimensional (3-D) digitizerAnatomical locations of optodes in relation to standard head landmarks were determined for each participant using a Patriot 3D Digitizer

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Inter Brain SynchronyCollaborative LearningFNIRS HyperscanningSocial InteractionOxygenated HemoglobinWavelet TransformPrincipal Components AnalysisMotion Artifact RemovalDyad Brain ActivityNaturalistic Learning

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