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PsyCh Journal (2014):


DOI: 10.1002/pchj.56

A new research trend in social neuroscience: Towards an


interactive-brain neuroscience
Tao Liu1 and Matthew Pelowski1,2
1

Department of Cognitive Informatics, Graduate School of Information Science, Nagoya University,

Nagoya, Japan, 2Copenhagen University, Department of Psychology


Abstract: The ability to flexibly modulate our behaviors in social contexts and to successfully interact with other persons is a fundamental,
but pivotal, requirement for human survival. Although previous social neuroscience research with single individuals has contributed greatly
to our understanding of the basic mechanisms underlying social perception and social emotions, much of the dynamic nature of interactions
between persons remains beyond the reach of single-brain studies. This has led to a growing argument for a shift to the simultaneous
measurement of the brain activity of two or more individuals in realistic social interactionsan approach termed hyperscanning. Although
this approach offers important promise in unlocking the brains role in truly social situations, there are multiple procedural and theoretical
questions that require review and analysis. In this paper we discuss this research trend from four aspects: hyperscanning apparatus,
experimental task, quantification method, and theoretical interpretation. We also give four suggestions for future research: (a) electroencephalography and near-infrared spectroscopy are useful tools by which to explore the interactive brain in more ecological settings; (b)
games are an appropriate method to simulate daily life interactions; (c) transfer entropy may be an important method by which to quantify
directed exchange of information between brains; and (d) more explanation is needed of the results of interbrain synchronization itself.
Keywords: electroencephalography (EEG); game; hyperscanning; interactive-brain; near-infrared spectroscopy (NIRS); social
neuroscience; transfer entropy
Correspondence: Dr. Tao Liu, Department of Cognitive Informatics, Graduate School of Information Science, Nagoya University,
Furo-cho, Chikusa-ku, Nagoya 464-8601, Japan. Email: luomayisima@gmail.com
Received 14 August 2013. Accepted 4 February 2014.

Human beings are social by nature. As an African proverb


puts it, a human becomes a human because of other
humans (Narayan, 1999, p. 3). From an evolutionary viewpoint, our social brains are shaped by natural selection
because being social enhances survival (Cozolino, 2006, p.
12). Recently, the focus on social aspects of humans has led
to discussion of the biological functioning of our brains.
Cognitive neuroscience, perhaps the most cutting edge
approach to human cognition and behavior, has demonstrated that, in the words of Goleman (2006, p. 113), our
brains very design makes it sociable, inexorably drawn into
an intimate brain-to-brain linkup whenever we engage with
another person. This neural bridge lets us affect the
brainand the bodyof everyone we interact with
(Goleman, 2006, p. 4). Therefore, a complete understanding

of the cognitive processes underlying human behavior


cannot be achieved without examining the dynamic interactions among persons (Hari, Himberg, Nummenmaa,
Hmlinen, & Parkkonen, 2013; Hari & Kujala, 2009;
Hasson, Ghazanfar, Galantucci, Garrod, & Keysers, 2012).
Although the social nature of humans has long been
evident, the field of social neuroscienceidentifying the
human brain systems involved in social situationsis both
very new and marked by current deficiencies in its approach.
Figure 1 illustrates the present research topics in the field,
which only came into predominance in the last decade (for a
review see Luo, Gu, Chen, & Huang, 2008; Ochsner &
Lieberman, 2001). As can be seen in this figure, because of
the methodological difficulties related to the complex
dynamics of interpersonal interactions, most social

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Towards an interactive-brain neuroscience

Figure 1. Research topics in social neuroscience. The arrow of each axis indicates the
areas of the landscapes that leave more unexplored questions in social neuroscience. The
gray and black cubes represent a new research
trend in social neuroscience: two or multibrain measurement during daily life interactions.

neuroscience studies are largely concerned with social perception and social interaction during artificial tasks, and with
a single individual. This may omit the most unique aspects of
social processing, which come through the dyadic interactions between persons (for a review see Adolphs, 2003; Hari
& Kujala, 2009; Hasson et al., 2012).
Researchers have therefore argued that it is important and
timely to shift from single-brain neuroscience to a twoperson neuroscience (Hari et al., 2013; Hari & Kujala,
2009) or to a second-person neuroscience (Schilbach
et al., 2013). Accordingly, a new technique named
hyperscanning (Montague et al., 2002), which does enable
simultaneous acquisition of cerebral data from two or more
participants, has led to growing efforts to examine interbrain
processing across persons during interpersonal interactions
(e.g., Babiloni & Astolfi, 2012; Jiang et al., 2012;
Konvalinka & Roepstorff, 2012; Liu, Saito, Oi, Pelowski,
et al., 2013; Liu, Saito, & Oi, 2013). This technique offers
important new possibilities for unlocking the mechanisms of
brain-to-brain functioning as well as the unique architecture
of our social brain.
However, as hyperscanning expands within social neuroscience, it also raises many questions that require a review
and discussion. These include four main aspects, regarding:
(a) hyperscanning apparatus: how to measure two brains
simultaneously; (b) experimental task: what findings have
been revealed from previous hyperscanning research, and
how to design studies to capture the brains social interactions; (c) quantification method: how to assess or quantify
the neural relationships across persons; and (d) theoretical
interpretation of results: how to denote that interbrain synchronization has actually occurred. This paper will review

the present literature and related questions on these topics


and give suggestions to provide a reference for future
research in two-person neuroscience.

Hyperscanning apparatus
The first topic of importance for hyperscanning is the apparatus. One of the reasons for the current lack of progress in
studies on interactive-brain measurement stems from the
limitations of neuroimaging techniques such as positron
emission tomography (PET) and functional magnetic resonance imaging (fMRI), which constrain participants to lying
in a motionless and solitary position (Cui, Bryant, & Reiss,
2012). As a result, the hyperscanning technique and its name
came from Montague et al. (2002), who developed the first
fMRI hyperscanning system to overcome the methodological constraints limiting analysis to one person.
fMRI hyperscanning
Figure 2A illustrates Montague et al.s (2002) original fMRI
hyperscanning system. Two fMRI devices located in different rooms are connected by a local area network (LAN) and
used to scan two participants simultaneously. To solve the
synchronization problem of different machines, a computer
server is employed to generate triggers for both fMRI
devices. During the experiment, the two participants lie still
in the scanners separately and interact with each other
through computer interfaces.
The use of fMRI hyperscanning provides the possibility
for simultaneous acquisition of data from two persons
brains with high spatial resolution, and is suitable for investigation of the interbrain processing underlying social

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PsyCh Journal

Figure 2. The functional resonance magnetic imaging (fMRI) hyperscanning systems. (a) The original dual fMRI system developed by Montague et al.
(2002). (b) A new fMRI hyperscanning system with dual-head volume coil in a single fMRI device (adopted from Lee et al., 2012).

perceptions (e.g., Anders, Heinzle, Weiskopf, Ethofer, &


Haynes, 2011) and social decisions from the viewpoint of an
observer (e.g., King-Casas et al., 2005). However, it is
unable to offer a natural environment for face-to-face interactions (Konvalinka & Roepstorff, 2012). In addition, the
requirement for multiple MRIs means that the experimental
cost is high (Cui et al., 2012). Recently, Lee, Dai, and Jones
(2012) attempted to develop a low-cost fMRI hyperscanning
system using a single machine (Figure 2B). They adopted a
novel MRI dual-head volume coil to acquire dyadic fMRI
signals from two brains in one scanner. Although this new
device reduces cost and relatively improves ecological validity, dynamic mutual interactions involving for example
motor movements are still out of reach.
Electroencephalography (EEG) hyperscanning
In contrast, Babiloni et al. (2006) proposed a hyperscanning system using EEG in order to solve many of the
above problems. EEG offers the merits of portability, high
temporal resolution, low cost, and few physical constraints
(Michel & Murray, 2012), and hence enables measurement
of multiple individuals brains in real social interactions
(Konvalinka & Roepstorff, 2012). Figure 3 shows an
example of EEG hyperscanning architecture. Different
EEG devices are normally used to simultaneously acquire
neuroelectric signals from two or more participants brains
in the same laboratory. The issue of synchronization and
sensitivity among the EEG devices can be adjusted by
inducing an external trigger signal with fixed amplitude,
which allows the calibration of all of the machines
(Babiloni & Astolfi, 2012). Due to these advantages, an

increasing number of studies have explored interbrain connectivity between interacting individuals using EEG
hyperscanning (Astolfi et al., 2010, Dumas, Lachat,
Martinerie, Nadel, & George, 2011).
However, EEG hyperscanning also has some weaknesses,
primarily poor spatial and anatomical resolution (Corbetta,
2012; Lieberman, 2010), that is, the inability to precisely
localize the origin of the neuroelectric signals (Cui et al.,
2012; Huster, Debener, Eichele, & Herrmann, 2012). This
limitation is a major obstacle to understanding the brain-tobrain coupling mechanisms of social interaction at the level
of specific brain systems.
Near-infrared spectroscopy (NIRS) hyperscanning
Finally, another brain-imaging technique, NIRS, has also
attracted increasing interest among neuroscientists (Boas,
Elwell, Ferrari, & Taga, 2014), and has been proven to be
a suitable tool to investigate the neural correlates underlying human social behaviors in more ecological situations
(Cui et al., 2012; Holper, Scholkmann, & Wolf, 2012;
Jiang et al., 2012). NIRS is a noninvasive method for
studying functional activation by measuring changes in the
hemodynamic properties of the brain. Unlike fMRI, NIRS
has few physical constraints and is more tolerant to motion
artifacts permitting serial assessments of tasks in less
restricted conditions (for a review of NIRS see
Scholkmann et al., 2014). Although NIRS has a low spatial
resolution of 2030 mm and cannot measure deep brain
structures, several brain regions involved in social interactions, such as the prefrontal cortex (PFC), the inferior
frontal gyrus (IFG), and the inferior parietal lobule (IPL),

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Figure 3.

Towards an interactive-brain neuroscience

A typical electroencephalography (EEG) hyperscanning system (adopted from Babiloni et al., 2011).

are located in close proximity to scalp tissue and are thus


readily accessible (Liu, Saito, & Oi, 2012b; Liu, Saito, Oi,
& Pelowski, 2012a, 2012b).
This technique was pioneered for hyperscanning by
Funane et al. (2011). Figure 4 shows the experimental settings in four NIRS hyperscanning studies. There are typically two types of architecture. One uses a multichannel
NIRS device to measure two brains, with half of the channels
for each participant (Figure 4AC). The advantage of this
architecture is that there is no issue of synchronization
between devices. However, it restricts participants body
movement to some extent. The other type of architecture
uses different wireless NIRS devices, much like EEG
hyperscanning, to simultaneously measure multiple persons
brains (Figure 4D). Although the wireless NIRS machine

normally has few channels, and in turn cannot cover


multiple neural networks in one experiment, it allows participants to move freely (Piper et al., 2014).
Summary of different hyperscanning approaches
Taken together, each hyperscanning technique (fMRI, EEG,
and NIRS) possesses some advantages as well as weaknesses. Among these, fMRI hyperscanning is more suitable
for examining the functional mechanisms involved in social
perception and social decisions from the perspective of an
observer. Both EEG and NIRS are useful for investigating
mutual interactions in natural situations from the perspective
of a participant. Specifically, the high temporal resolution of
EEG hyperscanning makes it particularly appropriate for
detecting the moment-to-moment dynamic changes during

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PsyCh Journal

Figure 4. Samples of the experimental settings in near-infrared spectroscopy hyperscanning studies. (A) Liu, Saito, and Oi (2013); (B) Duan et al. (2013);
(C) Jiang et al. (2012); (D) Liu, Saito, Oi, Pelowski, et al. (2013).

interaction itself. In contrast, NIRS hyperscanning has


relatively higher spatial resolution than EEG and may assess
the functional connectivity across persons in specific brain
regions.

interaction that requires continuous, moment-to-moment


exchange of information between persons. The other is a
turn-based interaction, in which people need to behave in a
turn-taking style with a certain time-delay between actions
of the interactants.

Experimental task
The discussion of methodology in turn leads to the second
key question for hyperscanning research: the specific task
one wishes to assess. The main research interest of twoperson neuroscience is social interaction (Hari et al., 2013),
which is defined as an individuals simultaneous or sequential actions that affect the immediate and future outcomes
of another individual involved in the situation (Johnson &
Johnson, 2005). Accordingly, interactive tasks can primarily be categorized into two types. One is a mutual

Continuously mutual interaction


Table 1 summarizes tasks and results from previous
hyperscanning studies published after 2011 (for review on
hyperscanning studies published before 2011, see Babiloni
& Astolfi, 2012). The existing tasks of continuously mutual
interaction include key-press tasks (Cui et al., 2012; Funane
et al., 2011), finger-movement/tapping tasks (Holper et al.,
2012; Naeem, Prasad, Watson, & Kelso, 2012; Yun,
Watanabe, & Shimojo, 2012) and music-playing tasks
(Babiloni et al., 2012). In key-press tasks, pairs of

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NIRS (2 persons)

EEG (4 persons)

NIRS (2 persons)

NIRS (2 persons)

NIRS (2 persons)

NIRS (2 persons)

EEG (2 persons)

EEG (2 persons)

EEG (2 persons)

Funane et al. (2011)

Babiloni et al. (2012)

Cui et al. (2012)

Dommer et al. (2012)

Holper et al. (2012)

Jiang et al. (2012)

Naeem et al. (2012)

Yun et al. (2012)

Kawasaki et al. (2013)

Inter-brain analysis

Results

Region of interest

Classification analysis
Senders brain activity predicted perceivers brain Temporal, parietal, insular
(similar to a
activity with time-delay (08 s).
and frontal brain
k-nearest-neighbor
regions
classification)
Prisoners dilemma
Partial directed coherence Activity (theta): defect > cooperation Inter-brain Bilateral anterial PFC,
synchronization: defect < cooperation.
ACC, cingulate motor
areas and parietal
cortex
Concurrent key-press
Covariance
Higher inter-brain synchronization is associated
PFC
(cooperation)
with better cooperative performance.
Music playing
Spearman correlation
Higher empathy, higher alpha (812 Hz)
IFG
(saxophone)
desynchronization during observation, but not
during execution/control conditions.
Concurrent key-press
Wavelet transform
Inter-brain coherence increased during
Right superior frontal
(cooperation + competition) coherence
cooperation, but not during competition.
cortices
Higher coherece, better cooperative
performance.
Dual n-back task
Wavelet transform
Inter-brain coherence increased during joint task PFC
coherence
performance compared with baseline task.
Finger-tapping (imitation)
Wavelet transform
Inter-brain synchronization increased during
Premotor
coherence; Granger
imitation, but not during independent
causality
condition.
Verbal communication
Wavelet transform
Inter-brain coherence increased during faceLeft IFG
coherence
to-face dialog, but not during face-to-face
monologue and back-to-back.
dialog/monologue
Finger movement
Correlation
Positive correlation: Right: in-phase Left:
Centro-parietal regions
coordination
anti-phase.
Finger movement
Time-varying
Inter-brain synchronization increased during
IFG, ACC,
(implicit)
phase-locking value
implicit body movement synchrony (theta and
parahippocampal gyrus
beta).
and postcentral gyrus
Speech rhythm
Cross-correlation
Theta/alpha (612 Hz) amplitudes synchronized
Temporal, lateral-parietal
in human-human tasks, and in observation of
regions
human-machine tasks.

Facial communication

Task

Note. ACC = anterior cingulate cortex; EEG =electroencephalography; fMRI = functional resonance magnetic imaging; IFG = inferior frontal gyrus; NIRS = near-infrared spectroscopy; PFC = prefrontal cortex.

EEG (2 persons)

fMRI (2 persons)

Apparatus

Astolfi et al. (2011)

Anders et al. (2011)

Author

Table 1
Summary of Selected Hyperscanning Studies Published after 2011

6
Towards an interactive-brain neuroscience

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PsyCh Journal

participants are normally asked to press two keys at the same


time (cooperation condition) or as fast as possible (competition condition). Using NIRS hyperscanning during a keypress task, Funane et al. (2011) revealed that higher
interbrain synchronization in the PFC is associated with
better cooperative performance. Cui et al. (2012) later confirmed increased coherence in the prefrontal activations of
the paired participants during cooperation, and demonstrated
further that there was no interbrain synchronization during
competition.
The finger-movement tasks consist of two experimental
structures depending on the relationship (leader or follower)
between interacting participants. In the leader-follower
structure, one participant is instructed to move a finger freely
as a leader, while the other participant follows the leaders
finger movement (Holper et al., 2012; Yun et al., 2012). The
hyperscanning results revealed increased interbrain synchronization in the leader-follower pairs fronto-parietal network
during their finger movement synchrony. In the structure of
coleadership, where neither participant is leading or following, two participants are asked to synchronize with their
partners finger movement (Naeem et al., 2012). Correspondingly, the right centro-parietal regions have been
shown to be involved in integrating the mutual information
between dyad members that enables the dynamics of social
interaction to unfold in time.
The interbrain synchronization reported in both key-press
and finger-movement tasks may reflect the neurophysiological substrates of behavioral synchrony across interactants.
Although behavioral synchrony is critical for group performances such as dancing or music playing, without synchronized empathic responses across people, alone it is not
enough for harmonized behavior. To examine the neural
correlates of shared emotion, Babiloni et al. (2012) used
EEG hyperscanning to measure simultaneously the brain
activity of four musicians when they played saxophone in an
ensemble. The result demonstrated a positive correlation
between the empathy score and alpha desynchronization in
their IFG.
Turn-based interaction
The turn-based interactions consist of communication tasks
(Anders et al., 2011; Jiang et al., 2012; Kawasaki, Yamada,
Ushiku, Miyauchi, & Yamaguchi, 2013) and other game
tasks (Astolfi et al., 2010; Liu, Saito, & Oi, 2012a; Liu,
Saito, & Oi, 2013). Depending on the research interests,
the experimental settings of communication tasks can be

classified into two types. To examine the information flow


from sender to receiver during communication, pairs of participants (sender-receiver) are scanned separately in a single
fMRI machine, and the functional connectivity between the
sender-receiver pairs is analyzed offline after the experiment
(for a review see Hasson et al., 2012). Previous studies have
revealed sender-receiver coupling in their fronto-parietal
regions during verbal communication (Stephens, Silbert, &
Hasson, 2010), gesture communication (Schippers,
Roebroeck, Renken, Nanetti, & Keysers, 2010), and facial
communication (Anders et al., 2011). The results suggest
that interbrain synchronization may serve as a mechanism by
which brains convey information across people, creating
shared understanding.
This experimental structure, however, could only examine
the unidirectional interactions where one person receives a
message from another, but cannot assess an ongoing twoperson (or bidirectional) exchange of information during
communication. Using NIRS hyperscanning, Jiang et al.
(2012) investigated the neural mechanisms of mutual communication in face-to-face situations. They demonstrated
that interbrain coherence in the left IFG increased during
face-to-face dialog, but not during face-to-face monolog or
back-to-back dialog/monolog, suggesting that neural synchronization between speaker-listener pairs may underlie
successful communication.
Besides communication, most of our daily life interactions involve behavioral responses. Astolfi et al. (2010)
simultaneously measured four participants brain activity
using EEG during a card game similar to the international
game of Bridge. The results suggested that a winning team
consists of people who are able to imagine their companions cards, and that this imagination elicits higher interbrain synchronization in their PFC. In another NIRS
hyperscanning study, Liu, Saito, and Oi (2013) presented
pairs of participants with a block-building game task. One
participant was instructed to make a copy of a target pattern
by placing blocks on a monitor (i.e., builder), while the other
participant helped or disrupted the builders progress (i.e.,
companion). The results demonstrated that the buildercompanion pairs showed significant positive interbrain correlations in their mirror neuron system during cooperation.
Specifically, the positive interbrain correlation in the IFG
may be involved in coordinating their concrete actions, while
the positive interbrain correlation in the right IPL may be
involved in maintaining a common goal for the final purpose
of cooperation.

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Towards an interactive-brain neuroscience

Another popular task-set comes from game theory, such


as Prisoners Dilemma (PD; Astolfi et al., 2011; De Vico
Fallani et al., 2010), which is useful to investigate neural
substrates of cooperation. In the PD game, participants are
instructed to cooperate with or betray their opponent
(defect). If both participants cooperate, they both win; if
only one participant cooperates, the advantage is given to
the defector; and if both participants defect, they both
lose. Using a PD game, De Vico Fallani et al. (2010)
demonstrated that brain-to-brain couplings in the PFC
and the anterior cingulate cortex occur during the cooperation condition, but are almost absent in the defect
condition.
Bringing daily interactions into the laboratory
The aim of social neuroscience is to understand the neural
mechanisms underlying human behavior in our daily life,
which contains rich stimuli and requires various cognitive
processes (Cacioppo & Decety, 2011; Matsuda & Hiraki,
2006). To simplify the complex behaviors and avoid the
confounding effects of irrelevant stimuli, most neuroscience
studies have mainly pursued an ideally well-controlled
experiment and adopted novel or unfamiliar tasks for participants (Hari & Kujala, 2009). Although the refined
approach is highly appropriate for research of primary
sensory functions, and brain activity during daily operations
can be inferred partially by accumulating established fundamental evidence, the dynamic changes in real-life interactions cannot be assessed and fully understood using limited
stimuli and tasks. Therefore, a review of the current research
makes clear that studying brain activity in everyday operations is necessary for further development (Hasson & Honey,
2012). To emphasize the importance of daily interactions,
this paper refers to two-person neuroscience as interactivebrain neuroscience.
In fact, playing with others (via both communication and
action) is one of the first social activities of childhood. For
adults, playing with peers also represents an important part
of daily life and interaction (Babiloni & Astolfi, 2012).
Ample hyperscanning studies have demonstrated the validity of games for generating interbrain synchronization in
the fronto-parietal networks underlying interactive (both
mutual interactive and turn-based interactive) behaviors.
Thus, as the first stepshifting from the artificial task
to out-of-door everyday operationsgames could be
appropriate tasks by which to simulate daily life
interactions.

Quantification method
The third important question that needs to be considered is
how to assess or quantify the neural relationships across
interactants. Specifically, this touches a major issue of
hyperscanning research: How do we actually evaluate or
document the synchronization and the causality among interacting brains?
Five quantification methods have typically been used in
previous studies, depending on the nature of the multibrain
data. For neuroelectric data (EEG), partial directed coherence (PDC; Astolfi et al., 2011; De Vico Fallani et al., 2010)
and phase-locking value (PLV; Yun et al., 2012) approaches
have been employed. PDC is a frequency-domain approach
to quantifying the directed influences (i.e., causality)
between multivariate time series (Baccal & Sameshima,
2001). PLV is normally used to assess frequency-specific
synchronization between two neuroelectric signals occurring
in the brains of two individuals (Lachaux, Rodriguez,
Martinerie, & Varela, 1999).
For hemodynamic data (fMRI and NIRS), correlation
(Liu, Saito, & Oi, 2012a; Liu, Saito, & Oi, 2013; Saito et al.,
2010), wavelet transform coherence (WTC; Cui et al., 2012;
Dommer, Jger, Scholkmann, Wolf, & Holper, 2012; Holper
et al., 2012; Jiang et al., 2012) and Granger causality
(Holper et al., 2012; Schippers et al., 2010) have been
employed. The correlation assessment considers the similarity between any given pair of signals. This can then be used
by researchers over a time course to show activation synchrony across two brains. WTC is a method for evaluating
the matching of trends or patterns of activation (i.e., synchronization) between individuals brains (Torrence &
Compo, 1998). Granger causality, in contrast, is used to
measure the causality relationship between two hemodynamic time series (Roebroeck, Formisano, & Goebel, 2005).
Although these methods have been proven effective for
assessing interbrain relationships, most are based on specific
linear models (Vicente, Wibral, Lindner, & Pipa, 2011).
However, a complex system such as the brain actually shows
strong nonlinearities between its parts and across different
brains of individuals (Lindner, Vicente, Priesemann, &
Wibral, 2011). The use of the above methods might lead to
overly simplistic results and/or omit the most dynamic
nature of brain interaction.
Transfer entropy (TE) is a model-free, nonlinear method
used to quantify the directed exchange of information
between two systems (Ito et al., 2011). It is an information

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PsyCh Journal

theoretic measure derived by Schreiber (2000). With


minimal assumptions about the nature of the data from different sources, TE enables quantification of the amount of
information transfer from one variable to the other, separately for both directions. A number of neuroscience studies
have demonstrated that TE performs better at identifying
effective connectivity in complex systems than other
methods such as cross-correlation (Garofalo, Nieus,
Massobrio, & Martinoia, 2009). It is also superior in terms
of stability and accuracy when applied to time series from
both linear and nonlinear models with unidirectional and
bidirectional coupling (Lungarella, Pegors, Bulwinkle, &
Sporns, 2005). Because of these advantages, TE has received
much attention in neuroscience and is gaining wide acceptance (Buehlmann & Deco, 2010; Lungarella & Sporns,
2006). Hence, it could also be an important tool to quantify
the interbrain relationships between persons in interactivebrain neuroscience.

Theoretical interpretation
Finally, there is the question of the interpretation of results.
As reviewed above, numerous studies have identified activation similarities between interacting brains with various
tasks. However, it is difficult to explain the meaning of the
synchronized activity given our lack of conceptual understanding of brain processes. It is noteworthy that as the
complexity and/or open-endedness (including how realitylike the task is) increases, the interpretability of the results
can be expected to decrease. In general, interbrain synchronization may imply three possibilities: one concerns functional similarities between two participants engaged in the
same task in a shared environment; the second relates to the
unique brain-to-brain coupling mechanisms underlying
social interaction that cannot be detected merely in solitary
performance. The third possibility, which must be considered in order to truly advance this study, is that the interbrain
synchronization obtained during social activities may be
only a coincidence.
For instance, in a recent study by our own team, Liu, Saito,
Oi, Pelowski, et al. (2013) measured simultaneously the
paired players and observers (friends) prefrontal activations
during a driving video game using two sets of wireless NIRS
devices. Low-proficiency players showed continuously
decreasing prefrontal activation throughout the driving,
whereas high-proficiency players showed increasing prefrontal activation. Interestingly, regardless of the players game

proficiency, the co-present observers generally showed


decreasing prefrontal activation. In this study, positive interbrain correlations were obtained between low-proficiency
players and their co-present observers. It would be hasty,
however, to conclude that interbrain synchronization reflects
their shared attention and/or shared emotion (Astolfi et al.,
2010; Jskelinen et al., 2008).
Although low-proficiency players and their co-present
observers showed similar decreasing activation during the
driving, the observers of both low- and high-proficiency
players also showed a positive correlation in their prefrontal
activation. These results may imply that the decreased activation in both observers and players may represent different
components, even if the activation of observers is related to
the players. The decreasing prefrontal activation in observers
may reflect a general trend due to habituation of the players
performance, while the decreasing prefrontal activation in
players may reflect tension reduction induced by the presence of a friend. Therefore, we need both to carefully explain
the results of interbrain synchronization in interactive-brain
neuroscience, as well as to move beyond the simple assumptions that social and/or shared activation comes from the
mere presence of another person.
Furthermore, to differentiate the brain processes that are
specifically engaged in social interaction from processes that
are merely engaged by the execution of the same task in a
shared environment, future study calls for assessment of
both intrabrain activation and interbrain relationships during
interpersonal interactions with a control condition. The most
obvious solution might be a blind design involving both a
real and a pseudo human with which a participant would
interact. In the real human condition, two participants
perform an interactive task in face-to-face situations. In the
pseudo human condition (i.e., the control condition), a single
participant could be instructed to engage in the task with a
computer program via a screen (in reality the computer
could be a human experimenter). After the experiment, we
might then verify whether the single participants believed
their partner was a computer or not and what strategy they
used during the task. If the intrabrain activations in the
paired (human-human) participants compare with the
human-computer condition, and the single participants also
show synchronized activations with the computer (i.e., the
experimenter), then the interbrain synchronization obtained
during interpersonal interaction may only reflect the functional similarity induced by the shared task/environment.
If the intrabrain activations in both paired and single

2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd

10

Towards an interactive-brain neuroscience

participants increase significantly, but there is no interbrain


synchronization between the single participants and the
experimenter, the synchronized activation across paired participants may subserve interpersonal interaction. If both significant functional activation and interbrain synchronization
are obtained in the paired participants, but not in the single
participants and the experimenter, the activation synchrony
may represent the specific processing underlying social
interactions. If interbrain synchronization across the paired
participants occurs without any significant functional activation, more attention must be paid to the interpretation of the
results.

Conclusion
This paper discussed a new research trend in social
neuroscienceshifting from a single-brain towards a two- or
multibrain paradigm. Our brain is constitutionally social. As
Cozolino (2006) notes, the human brain is an organ of
adaptation that builds its structures through interactions with
others (p. 6). The individual neuron or single human brain
does not exist in nature. Without mutually stimulating interactions, people and neurons wither and die (Cozolino,
2006, p. 11). To reach a full understanding of human cognition and behavior, it is beneficial and important to explore
interbrain processing during daily life interactions, that is,
we need to move towards research of the interactive brain.
This paper concludes with four suggestions: (a) EEG and
NIRS are useful tools by which to explore the interactive
brain in more ecological environments; (b) games are appropriate methods by which to simulate daily life interactions;
(c) transfer entropy may be an important method by which to
quantify the directed exchange of information across brains;
and (d) more careful explanation is needed of the results of
interbrain synchronization, as it may reflect one of three
possibilities: functional similarity induced by shared task/
environment between participants; unique interbrain
processing underlying social interaction; or only a
coincidence.

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