apps.einstein.brapps.einstein.br/.../artigos/-artigo-8702020623.docx · web viewthey played allegro...
TRANSCRIPT
Interpersonal Synchronization in groups: A Review on Research Techniques and Paradigms
Abstract:
Social interactions are in the base of human cognition processes. It arises when two or more individuals develop joint aleatory actions causing interpersonal synchronization. Studies evidences show physiological, behavioral and neural synchronization underlying these processes. Several studies on real life social interactions and their underlying neural mechanisms use a single person or second person approach. However, naturalistic social interactions are not limited to dyadic/dual exchange. Thus, recent studies have focused on group paradigms. The question remains whether the biological patterns found in dyad interactions will also occur in groups of three or more individuals. Furthermore, will all individuals’ brains react the same way? Is the biological reaction associated with a correspondent psychological and/or behavioral experience? How researchers are developing these studies? We expect to clarify some of these issues in the current review which focus is on IPS studies involving three or more individuals using biological signals such as brain activity, peripheral signs (skin temperature and heart beat), body movement and eye tracking.
Keywords: Interpersonal synchronization; Hyperscanning; Biological signals synchrony; Eye Tracking; Accelerometers; Bio sensing devices.
Sincronização Interpessoal em grupos: Uma Revisão de Técnicas de Pesquisa e Paradigmas
Resumo:As interações sociais estão na base dos processos de cognição humana. Surge quando dois ou mais indivíduos desenvolvem ações aleatórias conjuntas, causando sincronização interpessoal. As evidências dos estudos mostram sincronização fisiológica, comportamental e neural subjacente a esses processos. Vários estudos sobre as interações sociais da vida real e seus mecanismos neurais subjacentes usam uma abordagem de pessoa única ou segunda pessoa. No entanto, as interações sociais naturalistas não se limitam à troca entre apenas dois indivíduos. Assim, estudos recentes se concentraram em paradigmas utilizando grupos de indivíduos. Resta saber se os padrões biológicos encontrados nas interações das díades também ocorrerão em grupos de três ou mais indivíduos. Além disso, o cérebro de todos os indivíduos reagirá da mesma maneira? A reação biológica está associada a uma experiência psicológica e / ou comportamental correspondente? Como os pesquisadores estão desenvolvendo estes estudos? Esperamos esclarecer algumas dessas questões na revisão atual, cujo foco está nos estudos de IPS
envolvendo três ou mais indivíduos usando sinais biológicos, como atividade cerebral, sinais periféricos (temperatura da pele e batimentos cardíacos), movimento corporal e rastreamento ocular.
Keywords: sincronização interpessoal; Hyperscanning; Sincronia de sinais biológicos; Rastreamento Ocular; Acelerômetros; Dispositivos de detecção biológica.
Introduction
The interpersonal interaction (IPI) behavior is a defining feature of the human
bonding process.(1)(2) Actually, as a social species, the quality of our attachments is
determinant for healthy states and well-being.(3)
The IPI behavior arises when two or more individuals are interacting and combine
their own behaviors with others creating joint behaviors.(3)(4) This definition is in line
with recent studies results on human attachment process that show significant
evidence of biobehavioral synchrony among individuals during social interaction.(2)(5)(6)
Although the way humans perceive and interact with each other are in the base of
brain organization, only recently researchers started to study cognition processes
within Interpersonal Synchronization (IPS)(7). IPS, defined as the synchrony among
participants, can occur in different forms and intensity during IPI. It can be interbrain
neural synchrony (INS)(8), as well as biological signals synchrony like skin
temperature, heart rate and movements (9)(10)(11)(12)(13)(14)(15)(16)(17)(18). The interpersonal
attunement is also evident in autonomic and endocrine responses. (6)
Social cognition, largely studied on psychology, focus on how humans process, store
and apply external information (social situations and interactions). Social cognitive
processes are interactive, just like our social lives (2). Through the many possible
experimental designs, social cognitive processes will also differ (3), for instance, using
a third-person approach (social observation using relevant stimuli) instead of a
second-person approach (social interactive context). (19)
Social Neuroscience, at first, used single-brain approaches. The aim of those studies
was to analyze the relationship between social stimulus and neural responses in a
third-person context. This means that the focus of the study was on intra-personal
effects only, neglecting the IPI dynamics (4) .The researches involved in those studies
had a high control of the experiment, data collection and analysis. The paradigms’
tasks included the observation of expressive facial photographs, social context
videos, interaction with a real or a perceived partner. Though they used a constrain
behavioral variance and no real interaction (3), this kind of approach allowed
researchers to understand fundamental interactive social processes and how they
are represented on brain and biological levels.(6)
Sequential dual brain studies are more recent than single brain approaches studies.
This higher complexity method enabled the comparison between two participants’
brain activities, even if they have been collected at different times. This kind of study
allowed researchers to study how influence occurs and eventually to predict one’s
brain activation triggered by the other, how they transfer information between them
and how they build shared representations. Within second-person approaches,
Hyperscanning is a technique that enables data collection from two or more
participants’ brains interacting simultaneously. This technique allows researchers to
compare participants neural activity simultaneously and study the dynamics that
emerge between them in real time. In the first Hyperscanning studies the paradigms
were tasks related to game theory that allowed tight controlled experiments. The aim
was to understand the underlying cognitive processes within an IPS and behavioral
correlates.(19)
The experimental paradigms used in IPS Hyperscanning studies with one or two
participants at a time are mainly divided in six tasks’ categories:(20) Imitation (e.g.
imitation of others’ movements or behaviors); coordination (e.g. movements like
walking or dancing); eye contact (e.g. tasks with and without eye contact); game
theory tasks (e.g. economic games like Trust); cooperation (e.g. cooperative tasks
where you have to achieve a goal with a partner) and competition (e.g. virtual games
with individual scores).
Even with the development of new second-person approach paradigms, many
components of IPI were still not practicable, behavioral components like gaze, for
instance.
Second-person approach studies mostly use IPS as outcome measure. Recently
experimental paradigms focusing on inter-brain coherence search for synchrony
mainly using four different task patterns: a common external stimuli like a movie that
causes synchronization; a unidirectional leader/follower approach; an interactive
leader follower environment; and a group situation. (6)
The studies focus have become increasingly sensitive to the demand for paradigms
that included real social situations. Nowadays we observe the increase of paradigms
that use real-time interactive and ecologically valid research scenarios (that can
duplicate real-life situations) to study cognitive abilities and brain functions in groups. (3)(29)(21)
While researching for this review, we observed that many studies have determined
similar paradigms. But while paradigms may be similar, objectives, methods and
results differ greatly depending on the chosen method and technique. For example,
in the classroom paradigm studies, the focus were on sustained attention processes,
Ko et al (26) used EEG technique while Brockington et al (27) used fNIRS. Although
both are neuroimaging techniques, they differ in terms of advantages, limitations and
therefore, results.
Our main goal is to group INS studies conducted with three or more individuals
simultaneously. Understand the different experimental designs. Understand how
researchers related their objectives to the choice of technique and methodology
employed in their studies. We also aim to study the relationship between paradigms,
outcome measures and results. Finally, our aim is to help new researchers to
compare the limitations and experimental advantages of each methodology and so to
make appropriate choices according to their own study objectives.
Techniques used for group studies
Hyperscanning methods – consist of neuroimaging techniques such as EEG and
fNIRS that can measure simultaneously brain’s activity from two or more subjects.
They allow researchers to study the co-variations of neural activities. Therefore, allow
the study of possible correlations with INS and behavioral/ biological correlations. (28)
fNIRS Hyperscanning -
The functional near-infrared spectroscopy (fNIRS) is a functional neuroimaging
acquisition method. The near-infrared spectroscopy (NIRS) method is grounded on
the fact that human tissues are relatively transparent to light from 650 to 1000 nm
wavelengths in the electromagnetic spectrum. The near infrared (NIR) light is either
absorbed by pigmented compounds (chromophores) or scattered. According to Delpy
and Cope (29) scattering is 100 times more probable than absorption and the relatively
high attenuation of NIR light in the tissue is due to the main chromophore hemoglobin
(the oxygen transport red blood cell protein) located in small vessels of the
microcirculation, such as capillary, arteriolar and venular beds.(30)
Thus, this technique offers the possibility to obtain information on the neurovascular
coupling, neurophysiological fluctuations and cerebral hemodynamics. Over time,
what occurs in the functional NIRS data is the variation of oxyhemoglobin and
deoxyhemoglobin concentrations. Based on the tight coupling of neural activity and
oxygen delivery (31), these variations in concentration are taken as indicators for
cortical activation. The common fNIRS signal observed after neural activation is a
decrease of deoxyhemoglobin accompanied by an increase of oxyhemoglobin
concentrations.(32) Therefore, it allows researchers to make sense of physiological
signals and find neural correlates of cognitive and motor processes.
However, we can only measure the relative variations in oxygenation. Absolute
values are not available, especially taking into account the different brain structures
through which light can cross. For functional hemodynamic measures, it is assumed
that the variations in concentrations are insufficient to disturb the light path through
the human tissue and can be generalized through the Beer-Lambert Law. However,
this equation is only valid in the absence of scattering. As the average light path
depends on the spreading properties of the human tissue, the modified Beer-Lambert
law can be used to take into account the diffusive propagation of light. (33)
In general the major advantages of optical methods are: the biochemical specificity;
high temporal resolution; the potential to measure intracellular/intravascular events
simultaneously; and the ease in which devices can be transported. (30) That allows
participants to have more movement freedom and consequently help researchers to
create ecological settings.(34)(35)
However, it has also limitations such as: the impossibility of investigating deep brain
regions, such as basal ganglia and amygdala; the struggle of separating the NIRS
signals of signals originating from extra-cerebral tissues; the impossibility of providing
information about brain structure for anatomical reference; the attenuation of the NIR
light by the layering and dark color hair.(36)
There are a few hyperscanning studies using fNIRS to evaluate the interaction of
more than two brains throughout different interpersonal situations, such as group
communication (37)(38)(39)(40)(41); coordinated group walking (42); drumming together (43)
and classroom interaction.(27)
Experimental design and implementation of fNIRS studies: fNIRS punctually
measures intracellular/intravascular events simultaneously, so that the researcher
can determine areas of activation over time. However, the exposure time must be
short. The tasks are performed in blocks with maximum intervals of 40 seconds,
normally interspersing rest periods (baseline information), experimental condition and
control condition. Outcome measures are associated with the synchronization of
brain signals between individuals in the group.
EEG Hyperscanning –
Electroencephalography (EEG) is a screening procedure that measures the electric
activity of the brain and so reflects its function. Metal electrodes placed on a cap and
applied to the scalp record the data. (44)
The EEG high temporal resolution allows perceiving the quick changes in neuronal
population electrical dynamics. Therefore it enables an adequate sampling. (45) It is
also a non-expensive and noninvasive technique that is good for ecological settings. (28) Therefore, it is the most commonly used method for Hyperscanning. (45) Besides
that, EEG has a limited spatial resolution which means no precision to perceive the
origin of the neuroelectrial signal. It is also less robust to movement artifacts than the
fNIRS technique.(28)
EEG captures the scalp signals that are propagating electric potential fluctuations
that results mainly from large populations of cortical pyramid cells’ postsynaptic
activity. External stimuli can modulate rhythmic and arrhythmic ongoing brain electric
activities. These oscillations are found in frequency bands (delta, 0.5-4 Hz; theta, 4-8
Hz; alpha, 8-13 Hz; beta, 13-30 HZ and gama, above 30 Hz). Each one of these
bands has its own characteristics in terms of topographic location, stimuli sensibility
and expression in pathologies.(44)
There are also a few Hyperscanning studies using EEG to evaluate the interaction of
more than two brains throughout different social situations, such as classroom
situations (26)(46)(47)(48); musical performance paradigms (17)(20)(49)(50) and more.
Experimental design and implementation of EEG studies: EEG tasks are also
performed in blocks. Initially with a rest period (baseline information), followed by the
experimental condition/ control condition. Exposure time varies from a few minutes to
up to an hour. Outcome measures are associated with synchronizing the oscillation
of brain frequency bands.
Biological markers: Skin temperature, Heart beat, body and eye movement -
Although they are not Hyperscanning techniques, wearable bio-sensing devices
(accelerometers, electrodermal activity (EDA) devices, heart rate (HR) devices) are
used to study physiological synchrony relating it to attentional processes, cognitive
processes, and others during IPI. The advantages are the low cost of the methods,
as well as their high applicability and portability. Although they indicate biological
synchrony and therefore interaction behavior across a group of individuals, they must
be used as complementar instruments to study the cognitive or psychological
processes that underlies social interaction.
Accelerometers are noninvasive and unobtrusive devices or app (installed on
cellphones) that measures body movement.(9)
EDA is the variation of the electrical characteristics of the skin. The sweat gland
activity controls skin’s moisture level that is related to its conductance. Therefore, the
increase in sweat gland activity is related to physiological and psychological arousal.
(16) EDA is also known as Galvanic Skin Response (GSR), Electrodermal Response
(EDR), Psychogalvanic Reflex (PGR), Sympathetic skin Response (SSR) and others.
For measuring EDA researchers use noninvasive unobtrusive wearable devices with
electrodes, like wristbands. They measure the low voltage electrical response of the
skin.
Some of the paradigms where researchers use these devices are: group discussion (14); classroom situation (10)(13)(16)(18)(51)(52)(53); music paradigms(54); movie paradigms(55);
audience paradigms(11); music and dance paradigms.(9)(15)(56)
Figure 1 – Example of paradigms: A- Classroom situation (EEG); B- Club environment
(Accelerometers); C- Group communication (EEG) and D- Musical performance (fNIRS).
Methods
For this review, we searched the following databases: PubMed (2011- 2020), Scopus
(2011- 2020). The following combined terms were searched: IPS, biological signals
synchrony, Galvanic skin response, Accelerometers, Heart beat synchronization,
Hyperscanning, Bio sensing devices, eye tracking. We found no Mesh results and
therefore we researched for text words. We selected 2011 as a cutoff year as it is the
year the first Hyperscanning study involving three or more participants was
published. The selection included only research articles in which the methodological
task included groups of three or more individuals together in collective activities. As
the researched articles presented great differences, regarding the testing protocols
and hypothesis it was not possible to control for severity. We conducted a manual
search on text words, keywords, references and citations in order to identify other
appropriate articles. We also considered review articles for the manual search. For
this review we only considered research articles written in English.
Results
Initially we found 153 studies. We excluded all studies in which the tasks involved
two or less individuals together simultaneously. The six remaining articles were
reviewed and their hypothesis, technical setting, methodology and results were
tabulated ( Table 1). The manual search resulted in other 28 studies. These studies
were also reviewed and their hypothesis, methodology, and results described at
Table 1.
Table – 1 – Studies included in this review – Resume including Paradigms,
Technical Settings, Hypothesis, Outcome measures and main results.
2. List of paradigms employed in group studies:
1) Music Paradigms:
a. Playing Instruments/ performing together
Babiloni et al (49) aimed to develop a methodological approach for acquiring and
storing neurophysiological data, EEG, eletrooculographic (EOG), Electromyographic
(EMG) signals while professional musicians played in ensemble simultaneously as
recording the environmental sounds. They hypothesized that EEG could be used to
identify "on" and "off" states during the performance which would allow the
investigation upon interaction X characteristics of the play. The subjects were a
professional saxophonists’ quartet that played together for 22 years. They played
Allegro (sonata I amoll L 223- from Domenico Sciarrino) that lasted 1.5 min after a 10
minutes training session.
Babiloni et al (50) in this EEG Hyperscanning study hypothesized that activities on
Frontal Brodmann areas were associated with emotional and cognitive empathy in
musicians playing in ensemble. Their sample consisted of 3 quartets of professional
saxophonists. Therefore they created a paradigm that included the execution of a
performance, the observation of their own performance and a control task that
consisted of watching a video in which they turned pages of a score. They played
Allegro (sonata I amoll L 223- from Domenico Sciarrino) that lasted 1.5 min after a 10
minutes training session. The results suggested that the activation of BAs during the
observation task reflects an "emotional" empathic process in musicians.
Duan et al (43) intended to create a “multi brain modeling method”, known as a Cluster
Imaging of multi-brain networks (CIMBN), validated by fNIRS. This CIMBN could
enable the measurement of multiple brains simultaneously in a realistic, face to face
social interaction environment. Therefore, they conducted a nine people drumming
together experiment and recorded the participants brains activities simultaneously.
They were asked to seat in a circle and make their best effort to create a consistent
rhythm, beating all together. The researches target areas were the prefrontal cortex
and the Temporoparietal Junction (TPJ) in a four channels probe fNIRS. The
researches also recorded the drumbeats of all participants using vibration
transducers. They hypothesized that CIMBN would be feasible and this cluster
imaging system would be functional for hyperscanning of multiple participants. The
CIMBN showed 9 brains linked during the drumming task. The results suggested a
diversity of roles played by participants and therefore can be useful to find neural
correlates of group IS and develop affective and social neuroscience.
Muller et al (17) in their experiment recorded EEG signals simultaneously from 4
professional guitarists playing in ensemble. Their goal was to study hyperbrain
networks based on interbrain (lower frequencies e.g.,theta and delta) and intra-brain
(higher frequencies. e.g.,beta) connectivity among them during different musical
situations. They hypothesized that situations that needed a greater musical
coordination would lead to interbrain increased activity, while situations in which the
guitarists would have differential roles would increase the intra-brain connections.
The task was to play two different music pieces that were chosen by a specialist
regarding the hypothesis: Libertango by Astor Piasola and Comme un Tango by
Patrick Roux. The conclusions showed complex interactions between the 4 brains
during the performance and pointed to the existence of mechanisms that support
temporally joint and coordinated actions.
Grecco el al (20), developed and experiment comprising empathy and leadership
towards brain activity using a 4 professional saxophonists quartet playing together
paradigm. Their goal was to study oscillatory brain activity possible synchrony during
the task. The protocol comprised a session where they played a 5 minutes musical
arrangement composed specially for the experiment (with a continuous interchange
of leader roles among the quartet) and a second session where they watched their
own previously recorded performance on a screen while their EEG signals and
electrooculogram were acquired. The results confirmed the hypothesis that the
instrument voice affects the synchrony of oscillatory brain-to-brain activity. Also
showed that Broca’s area is not important to characterize empathy trait and that
leadership can be determined by perceptual rather than empathy or conscious
attention.
b. Singing Situation
Muller et al (25) developed a choral singing paradigm to investigate hyper-frequency
neural network (HFN) arrangement connections using a graph-theoretical approach.
The researchers registered the electrocardiogram (ECG), respiratory movements,
and the vocal audio signals at the same time during a singing situation. Eleven
singers and one conductor engaged in choral singing (aged between 23 and 56
years) volunteered to participate in the experiment that consisted in three
experimental variations. The variations consisted in: singing in unison, singing with
three individual parts at regular intervals with open eyes, and singing with three
individual parts at regular intervals with closed eyes. The chosen song canon was
“Signor Abbate” in B major (by Ludwig van Beethoven) and the task lasted 5 minutes
for each variation type.
The results were reached calculating phase coupling between respiratory, cardiac,
and vocalizing subsystems across ten frequencies of interest. When the entire choir
sang together in unison, graph-theory metrics such as clustering coefficients, local
and global efficiency were lower if compared to singing in parts. However, in the
same comparison, characteristic path lengths were longer. That is an indicator that
the choir network is more separated and, at the same time, more attached when
singing the canon in parts. The results also showed that specific changes in the
network topology of HFN structures happened due to the singing condition.
Moreover, the graph-theory metrics showed up to be related to individual heart rate,
as an indicator of arousal, and to an index of heart rate variability indicated by low
and high ratio frequency. Those metrics also reflected the balance between
sympathetic and parasympathetic activity. Their main conclusion appoints that the
dynamics of the neural connections’ layout provide significant information about
mechanisms of social interaction and is a potential indicator for group social behavior
and group dynamics.
In a previous and similar study, Muller et al (24) made it evident that respiratory and
cardiac subsystems are synchronized to each other while singing and are coupled to
oscillatory vocalizing patterns and to the hand-movement fluctuations of the choir’s
conductor. In addition they found out that the cross-frequency connections of the
singing group is the strongest when singing a canon in parts. Contrariwise, within-
frequency couplings (WFC) are more pronounced when singing the same canon in
unison. To reach these results they analyzed the cross-frequency couplings and the
WFC of respiratory, cardiac, vocalizing, and motor subsystems by describing the
network topography of a singing choir.
In order for these studies to be possible, the same group of research had already
suggested that oscillatory coupling of cardiac and respiratory patterns provide a
physiological basis for interpersonal action coordination.(23) It occurred in an
investigation that was based on ECG and respiration measures of couplings of a
choir. Between their findings at the time were the following topics: phase
synchronization higher when singing in unison than when singing pieces with multiple
voice parts; it increases both in respiration and heart rate variability during singing
relative to a rest condition; directed coupling measures are consistent with the
presence of causal effects of the conductor on the singers at high modulation
frequencies; the individual voices of the choir are reflected in network analyses of
cardiac and respiratory activity based on graph theory.
Both studies were composed of five men and seven women, of whom eleven were
singers and one was a conductor. The canon chosen was also “Signor Abbate” in B
major (by Ludwig van Beethoven) in the same experimental variations as the study
cited earlier in the text.
c. Dancing / Club Environment Paradigm:
Ellamil et al (9) studied group synchrony throughout a dance club paradigm using
accelerometers. Out of a 75 individuals sample they recorded movement data from
46 participants while they listened to the music and danced. (33 female and 13 male
aged 20-49 old). The experiment lasted 31 minutes. The music list included a
sequence of well known discotech tracks. The researchers aim was to study
movement synchrony covariation in according to music, and if the previous
knowledge of the music could improve group synchronization. The researches
collected movement data using an accelerometer app on two mobile phones. They
allocated the phones on a running belt placed at waist level. The results suggest that
well-known music caused greater synchrony of movements and rhythm among the
group.
Solberg and Jensenius (56) also created a club-like setting in order to study social
interactions in relation to body movement and music. The experiment goal was to
investigate how people engage to each other and how musical features affects
individuals and groups. They used a 29 people sample divided in 3 groups. Their
paradigm consisted of dancing 4 different music tracks (electronic music) within a 10-
minutes period. 2 tracks had no structural development, the other 2 were structured
and had a break routine (with and without a bass drum). They hypothesized that
dancing together causes similarity of movements and social closeness; and, also,
that change in music dynamics would affect synchronization. They analyzed the 29
participants horizontal and vertical movement patterns and the overall movement
tendencies, They found out that the use of intensifying sound features and rhythmic
frameworks affects group sensorimotor synchronization. The results suggest that the
musical feature influences our movements but also the way we interact with others.
Chauvigné et al (15) study’s aim was to investigate the mechanisms of group
coordination and cooperation. Therefore, they developed a dancing paradigm and
measured the coordination dynamics of the group towards multisensory coupling -
Auditory, haptic and visual coupling. Their participants were all folk dancers (around
70 years old) and they performed under 4 conditions (as usual, to auditory, holding
hands and with eyes opened) two Greek folk dances with different step level of
complexity. They formed a closed circle with the groups’ teacher in the center. They
hypothesized that sensory coupling plays an important whole on stability of
interpersonal coordination. Their results showed that the group relied mostly on the
haptic information to synchronize movements and that visual and auditory
information are spatio-temporal context-dependent. Their results also suggest that
sensory couplings support multi-person coordination in groups and opens the
possibility of a deep understanding on group dynamics in a naturalistic context.
d. Listening to music
Auditory Paradigm: Jaimovich et al (54) study is about emotional contagion. Therefore,
they investigated the influence of music performers emotional and mental states on
an audience and vice-versa. The hypothesis was that emotional responses can be
triggered during a performance. They carried out the experiment in live performance
environments and recorded data from two different 9 subject groups each and 3
performers. The musical program included a piano performance (12 min) an
interactive electronic piece (12min) and an electroacoustic piece (25min). The
researchers collected HR and GSR data and found that there is a correlation
between the biosignals of the audience and the momentum/music characteristics of
the pieces. They also found a correlation between biosignals of performers and
audience. Although emotional contagion´s mechanisms are still undefined, this study
presented a novel approach to its study.
Rhythm paradigm: Ikeda et al (42) also used rhythm as outcome measure in their
fNIRS study. They hypothesized that INS variation would be dependent on the
modulation of coordination related to cognitive processes, therefore, a steady beat
sound would facilitate INS and coordinate a group walking. They experimented a 4
group of 24 or 25 participants each. The task was to perform a walking in circles
experiment, with and without a metronome´s steady beat sound. Each group
performed two 4 minutes blocks, one walking, one stepping (control condition) and
three 30’ resting blocks. The researches target area was the frontopolar region in a
two channels probe. The researchers found that steady beat sound increased INS
and improved the walking flow what suggests the diffuse nature of group
coordination.
2) Classroom Paradigms :
MacNeal et al (16) investigated the relationship between emotional state and
engagement in a classroom environment. They used the GSR methodology in 17
subjects of a 24 undergraduate students’ introductory environmental geology course.
The course was focused on environmental issues related to climate change and was
composed of different learning approaches such as lectures, movies, students’
presentations and discussions. They expected differences of class engagement
measured by skin conductance response due to the pedagogical approach. The
researchers’ hypothesis was that active learning approaches would cause increase
of in-class engagement reflected on skin conductance data. They also hypothesized
the increase of students’ knowledge about the matter. The study suggests that active
learning such as move viewing and dialogue are more engaging than passive
learning approaches such as lectures.
Wang and Cesar (51) had also investigated students’ engagement. Their aim was to
measure engagement in a distributed learning environment, students on classroom
and remote location students at the same time. The experimental design consisted of
34 students, 17 students in a lecture classroom and 17 in a remote classroom
watching a normal scheduled class on Structured Query Language before an exam.
They hypothesized that students in remote class would be less engaged than
students in real classroom and this would reflect differences in bio-signals. The study
resulted in non-engaging learning experiences with different recording patterns of
other studies with engaged students. The results suggested that GSR sensors can
be used to measure engagement.
Senthil et Wong (18) studied the correlation between students’ heart rate and their
engagement during lectures. They have chosen a 30-student second semester class
in an Indian university. Previously they collected baseline data from each participant
(resting and stimulated heart rate), then they chose a random student to have the bio
signals recorded during a one-hour lecture class. Their hypothesis was that there
would be significant differences between heart rates from students academically
performed and those who did not. Researchers concluded that due to the confirmed
correlation of heart rate and engagement, this study can be useful to pedagogy as an
instrument for developing more engaging teaching methods.
Ko et al (26) developed a classroom environment sustained attention paradigm using
EEG Hyperscanning technique. They wanted to investigate possible relations
between activities that causes impaired behavioral performance and brain activity.
They had an 18 university students’ sample (11 males, 7 females) during lectures on
a regular academic semester. Their outcome measure was the level of visual
alertness. They created a visual targets recognition task in which geometric objects
(triangle, square, circle and star), where shown on screen during the lecture (one
object per minute - randomized intervals). When participants noticed the stimulus
they were asked to press the correspondent smartphone button. The response time
was determined as the time between appearance of stimuli and button pressing.
Their hypothesis was a correlation between variation in EEG spectral dynamics and
performing attention related tasks. The results confirmed their hypothesis.
Dikker et al (46), aim was to study brain synchrony during a face to face interaction.
They leaded an EEG study with 12 high school students over 11 regular classes.
Their outcome measure was brain to brain synchrony of neural activities. The
experiment was developed to investigate whether neural synchrony could be
considered a marker for social dynamics and classroom engagement, both of them
critical for the learning process. They started the semester with a course in
neuroscience, after that, along the regular semester, the students developed
research projects and their brains were recorded. In this study teaching styles,
personality traits, affinity and empathy were considered while investigating synchrony
across the group: student-to-group, student-to-student. The researchers concluded
that groups social dynamics and classroom engagement could be predicted by
students’ neural synchrony.
Brockington’s et al (27) fNIRS study aim was to investigate students learning
processes while attending a classroom lecture. They hypothesized neural synchrony
would occur “whenever similar attentional and arousal states were attained during
the lecture” (p.3), and time would be a key factor for sustained attention process. The
longer the lecture, the harder it would be for the students to sustain attention. They
also hypothesized that visual contact and engagement were related in INS. They
experimented it in a four students’ group, the target area was the frontal cortex and
used a probe 4X4 set (8 channels). The researchers confirmed their hypothesis and
results suggests that teacher-students eye contact during classes are important to
the students attentional and learning process.
Bevilacqua et al (47) EEG technique experiment is about 12 senior students and their
biology teacher during their regular classes in a New York high school. The
researchers aim was to study the relationship between classroom learning and
students-teacher, and students-group relationships. Therefore, they focused on
attentional processes and the underlying neural activity of social interaction to
develop a paradigm. The procedure lasted six classroom sessions (80 minutes each)
on a three-month period. They also applied questionnaires. They developed 3
baseline conditions (2minutes each), facing the wall, facing a partner and facing the
group. They recorded the baseline conditions of all participants before recording the
lesson, in which the data was collected simultaneously. After the lessons, students
were tested about the lesson content. Researchers outcome measure was brain to
brain synchrony. Their results showed that there’s a higher engagement for video
classes compared to lectures. Teaching styles and teacher’s likeability also affects
lesson content retention.
Pijeira-Diaz et al (13) focused on collaborative learning, their study goal was to
investigate the dynamics of this teaching method in the classroom. They used the
synchrony of sympathetic arousal as an outcome measure for engagement in 8
Finnish high school students’ triads. The paradigm was watching an 18-75-minutes
classes Advanced Physics course. The lessons had a theoretical part followed by a
group collaborative practical part. They hypothesized that triad members would have
synchronic moments, that there would be a difference of biosignals among
influencers and influenced students and that Eda can predict arousal contagion. The
results showed that only during small percentage of the lessons the triads were
simultaneously in a state of activation. Contagion occurred not for all, and not at the
same time on triads. They concluded that collaborative work is not an automatic
result of group work and that EDA can be used to study collaborative processes.
Di Lascio et al (10) wanted to measure students’ emotional engagement towards
classroom situation. Therefore, they used EDA sensors to monitor 24 students and 9
teachers’ physiological parameters over 41 lessons in a 3 weeks’ time period. Their
paradigm included a set of features to represent three observable physiological data
phenomena that indicates emotional engagement (general arousal; teacher/student
physiological synchronicity and momentary engagement). They hypothesized that it
is possible to define methods that capture students’ engagement during classes.
Their aim was to allow students to self-monitor themselves and increase their scholar
performance, as well as permitting teachers to benefit from the non-engaged
students’ information.
Gashi et al (52), using previous data from Dilascio et al (10) studied emotional climate in
a classroom paradigm throughout the physiological synchrony (PS) of 24 students
during 42 lectures. Their hypothesis was that PS can be an indicator of emotional
climate among students in classroom. They found an increment on students’ OS that
is reflected on their EDA.
Zhang et al (12) in their study collected EDA and HR signals (with a wristband) from
100 seven graded students during two weeks of math and Chinese classes. Students
were from 3 different classrooms. There was a total of 72 classes (40 minute
sessions) for each group of students, 36 math classes and 36 Chinese classes. They
also collected self-reports from students in each lecture and used the student’s final
exam scores to measure academic performance. Their goal was to verify whether
physiological data could be compared to self-reported data on academic
performance variation matter. They found correlations between students EDA
responses and academic performance.
Davidesco et al (48) hypothesized that brain-to-brain synchrony could predict individual
outcomes such as memory retention. In this EEG study their sample was composed
of 11 groups - 4 students each and a teacher groups in a laboratory classroom. Their
paradigm consisted of 4 teacher led lectures, preceded by a brief pre lecture or no
activity, when they could interact with the group freely. The students were tested
about content knowledge of that session 1 week early, after the lecture and 1 week
following. The student/teacher brain-to-brain synchrony was not considered. They
concluded that INS among students (listeners) can predict delayed memory
retention. They also concluded that synchrony can predict immediate and delayed
memory retention. And the variations could discriminate the achieved and not
achieved information by the students.
3) Communication Paradigms :
Jiang et al (37) intended to investigate the role of INS in human communication.
Therefore, they developed a fNIRS paradigm focused on the emergence of
leadership through INS in eleven triads. They were sat in triangles and the task was
to perform a “leaderless group discussion”. They were asked to discuss about a
theme for five minutes and then elect a leader to talk about their conclusions. Their
target regions were left frontal, temporal and parietal cortices, specifically TJP and
Inferior Frontal Gyrus (IFG). They used a probe of ten channels. All the experiment
was filmed by two cameras and the behavior and nonverbal communication was
analyzed. They hypothesized that there would be differences on interpersonal neural
communication between leader-follower (LF) pairs and between follower-follower
(FF) pairs. INS between LF pairs would be higher than INS between FF pairs and
that the INS in LF pairs would activate the social mentalizing and language related
areas. Actually, differences of activation were found between the LF and FF pairs.
For the LF pairs there was an increase of the INS at the left TJP. The study suggests
a correspondence of the emergence of leadership in people that have the ability of
saying the right thing at the right time.
Nozawa et al (38) created a cooperative fNIRS paradigm to study communication and
neural synchrony. They used twelve groups of four participants that were acquainted
to each other. The task was a cooperative word chain game where the participant
says a word, then the next participant uses the last two syllables of that word to say
another word. The paradigm was developed in two sessions of three blocks, two of
them were the communication task and the other one was resting state. The
researches target area was the frontopolar region in a two channels fNIRS probe.
They hypothesized that cooperative and unstructured verbal communication
enhances frontopolar INS and that there is a timescale dependency in the INS
modulation. Their results confirmed the enhance of frontopolar INS and the timescale
dependency in the INS modulation. This study also set parameters and technical
basis for new hyperscanning studies involving groups and communication.
Zhang et al (53), decided to study leadership in a group communication paradigm
using EEG. Their aim was to evaluate brain activities of the group members
perceiving differences in leader/followers activations during group discussions. For
that they developed a 4 blocks task. In the first block participants received a topic
and had a 20 minutes free discussion. After the discussion they elected a leader to
report the results. The second block was a leader established discussion. The third
block was a building block game task in which participants had to simultaneously
construct the same building and discuss the process. The fourth one consisted on
the same task but the leader was elected by the group. Their results showed that the
left hemisphere activation of the leader was much higher than the followers. They
also concluded that there's an indication that followers summarize consciously and
unconsciously the tasks and leader’s orders, and leaders can understand other’s
thoughts fastly and adapt the speech to satisfy their expectations.
Dai et al (39) study was based on the investigation of INS in a noisy multi speaker
situation in 21 same gender adult triads. Participants were sat in a triangle. One was
randomly named the listener. Two tasks were developed. On the first one, only one
speaker would talk to the listener. Then the two speakers would talk simultaneously,
and the listener should pay attention to only one of them. The task was performed in
a face to face condition and in a back to back condition. The experiment was made in
three blocks, one of them, a resting pause and the other two, different tasks. The
researches target areas were the left frontal, temporal, and parietal cortices in a ten
channels fNIRS probe. Their hypothesis was that in a multi speaker situation the INS
is a neural mechanism for selective processing of the target information. Their results
showed a selective enhancement of TJP-TJP INS for listener-attended pairs in all
conditions and the increase of INS between the listeners’ posterior superior temporal
cortex and the attended speaker’s TJP.
Lu and Hao (40), studied INS during a collaborative fNIRS task using the cooperative
interaction hypothesis and the similar task hypothesis. 44 participants in dyads that
did not know each other before, were randomly assigned to interact with a
confederate (a fake participant, an experimental assistant). They were asked to
discuss a topic for 5 minutes in collaborative brainstorming task. The rules were to
answer one at a time in a clockwise order. The researchers target area was the
prefrontal cortex and they developed a 22 channels probe set. Behavior and
cooperation index were also measured. The researchers hypothesized differences of
neural synchrony between different dyads in the groups due to the use of cooperative
or similar tasks. They found different individual engagement, a high INS among real
participants and low INS among participants and confederate.
Lu et al (41) in this fNIRS study intended to evaluate how different feedbacks should
affect creative performance in a brainstorming group. 59 dyads that did not know
each other before, were randomly assigned to interact with a fake participant (an
experimental assistant that acted as an evaluator). They were randomly assigned for
one of the three conditions: positive feedback (20 dyads), negative feedback (19
dyads) and control condition (20 dyads). They were asked to discuss a topic for 5
minutes in a brainstorming task and the feedback was given by the evaluator. The
researchers target areas were frontopolar and bilateral dorsolateral in the prefrontal
cortex. They developed a 22 channels probe 3 X 5 set. Behavior and cooperation
index were also measured. They hypothesized that social interaction affects group
creative performance and different types of feedback will generate differences on
INS. In their results they found that INS showed up to be higher when feedback was
positive rather than negative. The conclusion was that creativity showed to be
suppressed when the group received a negative feedback.
Capozzi et al (14) used eye tracking methods to study leadership in group interactions.
They hypothesized that social gaze behavior is a marker for leadership during social
interaction. They used a 64 people sample (16 groups of 4 strangers each). In each
group one participant was designated the leader. And within a limited period of time
they had to solve a survival task. The participants sat on equidistant chairs in a circle
and had four video cameras recording the experiment. They created 4 leadership
settings according to democratic and autocratic leadership styles or situational
condition (low and high pressure situation). The results suggest that social gaze
behavior can be used to identify leaders in a group.
4) Audience Paradigms:
Wang and Cesar (55) tested the efficiency of GSR sensors to evaluate audience
experiences towards different commercials. They used a 15 people sample in a video
watching paradigm. The subjects were exposed to audio tracks of a Starbucks'
commercial under three conditions, a mute condition, the video with an up-tempo
music audio and the video with a ballad music audio. The differences found in GSR
data analysis in comparison to surveys showed that the use of GSR can be specific
on delivering audience attentional level data and therefore, GSR can be useful to
publicity market since it can report the users' experience more precisely than
surveys.
Gashi et al (11), developed a field study. They used EDA sensors to collect data from
17 presenters and 6 listeners in an auditory environment during a 2 days conference
on Energy Informatics. They also collected IBI traces and applied questionnaires to
investigate the relation between physiological synchrony and attentional processes
among presenter and audience. Their aim was to compare signals between audience
and presenters and study satisfaction, immersion and engagement. Their results
suggest that physiological synchronicity can be used as a proxy to measure
engagement and satisfaction and therefore is a good method to provide audience
feedback in lectures, conferences, classroom, etc.
Future Directions
The study field of neural and behavioral mechanisms related to group interaction is
still novelty and a promising research area. Hyperscanning techniques such as fNIRS
and EEG, as well as the use of eye tracking and other measuring devices for
biological signals have allowed more ecological settings and therefore more freely
forming group interactions. This improvement enriched researchers’ ability to study
neural mechanisms and behavior within IPI. However, most of Hyperscanning
studies have as an outcome measures of synchronicity and mirroring-based analysis,
which occurs not necessarily due to IPI and are just possible biological signatures of
the dynamic process of interaction.
Due to technical limitations tasks and set-ups are still constrained, so that to fully
understand the emergence of interpersonal dynamics we still have to develop more
portable, affordable and integrated devices. We also have to look forward to more
robust analysis tools and processing algorithms, as well as signals and data
processing and artefacts removal, making them more replicable and scalable for
other studies.
The future signalizes for multidimensional approaches. With the development of
Hyperscanning techniques that are able to capture spatial and temporal data at the
same time, therefore allowing researchers to study similarities and differences across
individual brains during a free social interaction, characterizing inter-brain
organization from interpersonal behavioural, reciprocal influence process and the
construction of joint representations.
Also, the functional implication of synchrony will be better understood and delineated
in an integrative approach of techniques that study inter-brain coherence with
biobehavioral synchronicity devices.
Acknowledgements
References
1) Decety J, Lamm C. Human empathy through the lens of social neuroscience. ScientificWorldJournal. 2006; 6:1146–1163. doi:10.1100/tsw.2006.221.
2) Feldman R. The Neurobiology of Human Attachments. Trends Cogn Sci. 2017;21(2):80–99. doi:10.1016/j.tics.2016.11.007.
3) Reader, A.T. and Holmes, N.P. Examining ecological validity in social interaction: problems of visual fidelity, gaze, and social potential. Cult. Brain (2016) 4:134–146. Doi: 10.1007/s40167-016-0041-8.
4) Konvalinka I., Roepstorff A. The two-brain approach: how can mutually interacting brains teach us something about social interaction?. Front Hum Neurosci. 2012;6:215. doi:10.3389/fnhum.2012.00215.
5) Hove, M.J., & Eisen, J.L. It´s all in the timing: Interpersonal Synchrony increases affiliation. Social Cognition. 2009, 27(6), 949-961. doi: 10.1521/soco.2009.27.6.949.
6) Long, M., Verbeke, W., Ein-Dor, T., & Vrtička, P. (2020). A functional neuro-anatomical model of human attachment (NAMA): Insights from first-and second-person social neuroscience. cortex. 2020; V.126.p.281-321. Doi: 10.1016/j.cortex.2020.01.010.
7) Schilbach L, Timmermans B, Reddy V, et al. Toward a second-person neuroscience. Behav Brain Sci. 2013;36(4):393–414. doi:10.1017/S0140525X12000660.
8) Gvirts, H. Z., & Perlmutter, R. What Guides Us to Neurally and Behaviorally Align With Anyone Specific? A Neurobiological Model Based on fNIRS Hyperscanning Studies. The Neuroscientist. 2020; 26(2), 108–116. doi.org/10.1177/1073858419861912.
9) Ellamil M, Berson J, Wong J, Buckley L, Margulies DS. One in the Dance: Musical Correlates of Group Synchrony in a Real-World Club Environment. PLoSONE. 2016;11(10):e0164783. Doi: 10.1371/journal.pone.0164783
10)Di Lascio, Elena; Gashi, Shkurta & Santini, Silvia. Unobtrusive Assessment of Students' Emotional Engagement during Lectures Using Electrodermal Activity Sensors. Proc.ACM Interact.Mob. Wearable Ubiquitous Technol. 2018; 2. 1-21. Doi: 10.1145/3264913.
11) Gashi, Shkurta and Di Lascio, Elena and Santini, Silvia. Using Unobtrusive Wearable Sensors to Measure the Physiological Synchrony Between Presenters and Audience Members. Proc.ACM Interact.Mob. Wearable Ubiquitous Technol. 2019; 13 (1) 1-19. Doi: 10.1145/3314400.
12) Zhang Yu, Qin Fei, Liu Bo, Qi Xuan, Zhao Yingying, Zhang Dan. Wearable Neurophysiological Recordings in Middle-School Classroom Correlate With Students’ Academic Performance. Frontiers in Human Neuroscience.2018; V.12. Doi:10.3389/fnhum.2018.00457.
13) Pijeira-Diaz HJ, Drachsler H, Järvelä S, Kirschner PA. Sympathetic arousal commonalities and arousal contagion during collaborative learning: How attuned are triad members? Computers in Human Behavior. 2019 Mar;92:188 - 197. https://doi.org/10.1016/j.chb.2018.11.008.
14) Capozzi, Francesca; Beyan, Cigdem; Pierro,Antonio; Koul, Atesh; Murino, Vittorio; Livi, Stefano; Bayliss, Andrew P.; Ristic, Jelena and Becchio Cristina. Tracking the leader: Gaze Behavior in Group Interactions. iScience. 2019; 16: 242-249. Doi: 10.1016/j.isci.2019.05.035.
15) Chauvigné, Lea A.; Walton, Ashley; Richardson, Michael J. and Brown, Steven. Multi-person and multisensory synchronization during group dancing. Human Movement Science.2019; V.63: 199-209. Doi: 10.1016/j.humov.2018.12.005.
16) Karen S. McNeal, Jacob M. Spry, Ritayan Mitra & Jamie L. Tipton. Measuring Student Engagement, Knowledge, and Perceptions of Climate Change in an Introductory Environmental Geology Course. Journal of Geoscience Education.2014; 62:4, 655-667, DOI: 10.5408/13-111.1.
17) MUELLER, Viktor, SAENGER, Johanna, LINDENBERGER, Ulman. Hyperbrain network properties of guitarists playing in quartet. Annals of the New York academy of sciences. 2018; V. 1423, No. 1, pp. 198-210 . Doi: 10.1111/nyas.13656.
18) Senthil, S., & Lin, W. M. (2017, August). Measuring students' engagement using wireless heart rate sensors. SmartTechCon. 2017; 699-704. (Presented
at 2017 International Conference On Smart Technologies For Smart Nation (SmartTechCon) (pp. 699-704). IEEE.
19) Redcay, E., & Schilbach, L. Using second-person neuroscience to elucidate the mechanisms of social interaction. Nature Reviews Neuroscience.2019; 20(8), 495-505. Doi: 10.1038/s41583-019-0179-4.
20) Wang, M. Y., Luan, P., Zhang, J., Xiang, Y. T., Niu, H., & Yuan, Z. Concurrent mapping of brain activation from multiple subjects during social interaction by hyperscanning: a mini-review. Quantitative imaging in medicine and surgery.2018; 8(8), 819. Doi: 10.21037/qims.2018.09.07.
21) Volpe, G., D'Ausilio, A., Badino, L., Camurri, A., & Fadiga, L. Measuring social interaction in music ensembles. Philosophical Transactions of the Royal Society B: Biological Sciences. 2016; 371(1693), 20150377.
22) Greco A, Spada D, Rossi S, Perani D, Valenza G, Scilingo EP. EEG Hyperconnectivity Study on Saxophone Quartet Playing in Ensemble. Conf Proc IEEE Eng Med Biol Soc. 2018;2018:1015‐1018. doi:10.1109/EMBC.2018.8512409. Presented at the 40th Annual International Conference of the IEEE Engineering in Medicine and Biology Society (EMBC) (pp. 1015-1018). IEEE.
23) Müller V, Lindenberger U. Cardiac and respiratory patterns synchronize between persons during choir singing. PLoS One. 2011;6(9):e24893. doi:10.1371/journal.pone.0024893.
24) Müller, V., Delius, J., & Lindenberger, U. Complex networks emerging during choir singing. Annals of the New York Academy of Sciences. 2018; 1431(1), 85–101. https://doi.org/10.1111/nyas.13940
25) Müller, V., Delius, J., & Lindenberger, U. Hyper-Frequency Network Topology Changes During Choral Singing. Frontiers in physiology.2019; 10, 207. https://doi.org/10.3389/fphys.2019.00207.
26) Ko, L. W., Komarov, O., Hairston, W. D., Jung, T. P., & Lin, C. T. Sustained attention in real classroom settings: An EEG study. Frontiers in human neuroscience. 2017; 11, 388.
27) Brockington, G., Balardin, J. B., Zimeo Morais, G. A., Malheiros, A., Lent, R., Moura, L. M., & Sato, J. R. From the Laboratory to the Classroom: The Potential of Functional Near-Infrared Spectroscopy in Educational Neuroscience. Frontiers in psychology. 2018; 9, 1840.
28) Mu, Y., Cerritos, C., & Khan, F. Neural mechanisms underlying interpersonal coordination: A review of hyperscanning research. Social and Personality Psychology Compass. 2018; 12(11), e12421.
29) Delpy, D.T., Cope, M. Quantification in tissue near-infrared spectroscopy.
Philos. Trans. R. Soc. Lond. B Biol. Sci.1997; 352, 649–659
30) Ferrari, M., & Quaresima, V. A brief review on the history of human functional
near-infrared spectroscopy (fNIRS) development and fields of application.
NeuroImage. 2012; 63(2), 921–935. doi:10.1016/j.neuroimage.2012.03.049.
31) Logothetis, N.K., Wandell, B.A.. Interpreting the BOLD signal. Annu. Rev.
Physiol.2004; 66, 735 – 769.
32) Plichta, M. M., Herrmann, M. J., Baehne, C. G., Ehlis, A.-C., Richter, M. M.,
Pauli, P., & Fallgatter, A. J. Event-related functional near-infrared
spectroscopy \(fNIRS): Are the measurements reliable? NeuroImage. 2006;
31(1), 116–124. doi:10.1016/j.neuroimage.2005.12.008.
33) Mesquita, Rickson C., and Roberto JM Covolan. Estudo funcional do cérebro
através de NIRS e tomografia óptica de difusao. Neurociências e epilepsia.
2008; 147.
34) Balardin, J. B., Zimeo Morais, G. A., Furucho, R. A., Trambaiolli, L., Vanzella,
P., Biazoli Jr, C., & Sato, J. R. Imaging brain function with functional near-
infrared spectroscopy in unconstrained environments. Frontiers in human
neuroscience.2017; 11, 258.
35) Babiloni, F., & Astolfi, L. Social neuroscience and hyperscanning techniques:
past, present and future. Neuroscience & Biobehavioral Reviews. 2014; 44,
76-93.
36) Quaresima, V., Bisconti, S., & Ferrari, M. A brief review on the use of
functional near-infrared spectroscopy (fNIRS) for language imaging studies in
human newborns and adults. Brain and Language 2012; 121(2), 79–89.
doi:10.1016/j.bandl.2011.03.009.
37) Jiang, J., Chen, C., Dai, B., Shi, G., Ding, G., Liu, L., & Lu, C. Leader
emergence through interpersonal neural synchronization. Proceedings of the
National Academy of Sciences. 2015; 112(14), 4274-4279.
38) Nozawa, T., Sasaki, Y., Sakaki, K., Yokoyama, R., & Kawashima, R.
Interpersonal frontopolar neural synchronization in group communication: an
exploration toward fNIRS hyperscanning of natural interactions. Neuroimage,
2016; 133, 484-497.
39) Dai, B., Chen, C., Long, Y., Zheng, L., Zhao, H., Bai, X., ... & Ding, G. Neural
mechanisms for selectively tuning in to the target speaker in a naturalistic
noisy situation. Nature communications. 2018; 9(1), 1-12.
40) Lu, K., & Hao, N. When do we fall in neural synchrony with others?. Social
cognitive and affective neuroscience. 2019; 14(3), 253-261.
41) Lu, K., Qiao, X., & Hao, N. Praising or keeping silent on partner’s ideas:
leading brainstorming in particular ways. Neuropsychologia. 2019; 124, 19-30.
42) Ikeda, S., Nozawa, T., Yokoyama, R., Miyazaki, A., Sasaki, Y., Sakaki, K., &
Kawashima, R. Steady beat sound facilitates both coordinated group walking
and inter-subject neural synchrony. Frontiers in human neuroscience. 2017;
11, 147.
43) Duan, L., Dai, R., Xiao, X., Sun, P., Li, Z., & Zhu, C. Cluster imaging of multi-
brain networks (CIMBN): a general framework for hyperscanning and
modeling a group of interacting brains. Frontiers in neuroscience. 2015; 9,
267.
44) Aminoff, M. J. Electroencephalography: general principles and clinical
applications. Electrodiagnosis in Clinical Neurology. 2012; 6th ed.; Aminoff,
MJ, Ed, 37-84.
45) Abreu, R., Leal, A., & Figueiredo, P. EEG-informed fMRI: a review of data
analysis methods. Frontiers in human neuroscience. 2018; 12, 29.
46) Dikker, S., Wan, L., Davidesco, I., Kaggen, L., Oostrik, M., McClintock, J., ...
& Poeppel, D. Brain-to-brain synchrony tracks real-world dynamic group
interactions in the classroom. Current Biology. 2017; 27(9), 1375-1380.
47) Bevilacqua, D., Davidesco, I., Wan, L., Chaloner, K., Rowland, J., Ding, M., ...
& Dikker, S. Brain-to-brain synchrony and learning outcomes vary by student–
teacher dynamics: Evidence from a real-world classroom
electroencephalography study. Journal of cognitive neuroscience. 2019; 31(3),
401-411.
48) Davidesco, I., Laurent, E., Valk, H., West, T., Dikker, S., Milne, C., & Poeppel,
D. Brain-to-brain synchrony predicts long-term memory retention more
accurately than individual brain measures. bioRxiv.2019; 644047.
49) Babiloni, C., Vecchio, F., Infarinato, F., Buffo, P., Marzano, N., Spada, D., ...
& Perani, D. Simultaneous recording of electroencephalographic data in
musicians playing in ensemble. Cortex. 2011; 47(9), 1082-1090.
50) Babiloni, C., Buffo, P., Vecchio, F., Marzano, N., Del Percio, C., Spada, D., ...
& Perani, D. Brains “in concert”: frontal oscillatory alpha rhythms and empathy
in professional musicians. Neuroimage. 2012; 60(1), 105-116.
51) Wang, C., & Cesar, P. Physiological Measurement on Students' Engagement
in a Distributed Learning Environment. PhyCS. 2015; 10, 0005229101490156.
52) Gashi, S., Di Lascio, E., & Santini, S. Using Students' Physiological
Synchrony to Quantify the Classroom Emotional Climate. ACM. 2018; P698-
701. ISBN:9781450359665. Doi.org/10.1145/3267305.3267693. (Presented at
the 2018 ACM International Joint Conference and 2018 International
Symposium on Pervasive and Ubiquitous Computing and Wearable
Computers;2018. NY. USA).
53) Zhang, J., & Zhou, Z. (2017, July). Multiple Human EEG Synchronous
Analysis in Group Interaction-Prediction Model for Group Involvement and
Individual Leadership.Lecture BI. 2017: pp.99-108. (Presented at the
International Conference on Augmented Cognition . Springer, Cham. 2017
Nov; Beijing, China).
54) Jaimovich, J., Coghlan, N., & Knapp, R. B. (2010). Contagion of physiological
correlates of emotion between performer and audience: An exploratory study.
In J. Kim & P. Karjalainen (Eds.), Proceedings of B-INTERFACE 2010, 1st
International Workshop on Bio-inspired Human-Machine Interfaces and
Healthcare Applications (pp. 67-74). Valencia, Spain: INSTICC Press.
55) Wang, C., & Cesar, P. Measuring Audience Responses of Video
Advertisements using Physiological Sensors. In ImmersiveME@ ACM
Multimedia. 2015; pp. 37-40.
56) Solberg, R. T., & Jensenius, A. R. Group behaviour and interpersonal
synchronization to electronic dance music. Musicae Scientiae, 2019; 23(1),
111-134.