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2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
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
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
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
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).
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),
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
Figure 3.
A typical electroencephalography (EEG) hyperscanning system (adopted from Babiloni et al., 2011).
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
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).
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
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
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)
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
Author
Table 1
Summary of Selected Hyperscanning Studies Published after 2011
6
Towards an interactive-brain neuroscience
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
PsyCh Journal
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
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
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
PsyCh Journal
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
2014 The Institute of Psychology, Chinese Academy of Sciences and Wiley Publishing Asia Pty Ltd
10
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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