FIGURE 4. The comparisons of inter-regional couplings.(a) The coherence spectra between
rTPJseed-rTPJp and (b) The
rTPJseed-rSTG in the conditions of the within-group
interacting pairs (WIP), within-group non-interacting pairs (WNP),
within-group permuted pairs (WPP), and between-group permuted pairs
(BPP). The brain maps show the seed (left) and the target (right)
regions on the 36th frequency bin (out of 324/2 = 162 bins, or the
target frequency 0.0556 Hz, or 1/18 s), under the coherence threshold of
0.215 and the cluster threshold of 40 voxels (FWE p <
.05 corr.). This bin corresponds to the average trial frequency, or the
concatenated event frequency (beta series built by combining 9 betas,
every 2 s/ 1 TR, after the trial feedback time). The spectra of the WIPs
are shown in green, WNPs in yellow, and the BPPs in black. The
independent two-sample t-tests are applied among every possible pair at
the 36th frequency bin. (c) The rTPJseed to
whole-brain coherence maps of the WIP and WNP in the two stages of
feedback periods, respectively. In the first stage of feedback (planning
stage), the WIP and WNP have bilateral Lingual Gyri linked to processing
vision and episodic memory. In the second feedback (decision stage),
more couplings with the rTPJ can be observed in the WIP, while the
rTPJ-STG coupling of the WNP outstands, compared to the WNP map in Stage
1. (d) When the reciprocal pairs are interacting with each
other, their left TPJ and right IFG are coupled with the
rTPJseed in the second feedback. (e) The
non-reciprocal pairs yield rTPJ- amygdala and –left IFG couplings when
interacting together.
Discussion
Collaboration through reciprocity is evident in many social contexts, as
humans share and connect with each other from interactions. In the
present study, we investigated whether brain circuitry was identified as
relevant for reciprocal collaborations through social learning in a
coordination game. First, our behavioral results showed that successful
collaboration was correlated with reciprocity, and the reciprocal
participants and pairs earned the most reward. This reflects that the
utmost successful interaction of the present study lies in reciprocity.
Second, in the neural level, the MNS and the MS involving coordination-,
reward-, and decision-related regions known for cooperation tasks were
identified. Many abovementioned regions were both found in our
time-domain (i.e., GLM and PPI) and frequency-domain (i.e., coherence)
analyses. Furthermore, the rTPJ was suggested to play its dual roles in
social interaction with the brain regions related to other/self-concern
(intrapersonally) and meaning-emergence (interpersonally). In sum, given
its critical placement in mentalizing, the rTPJ is likely to participate
in multiple functions through the present three-person hyperscanning.
‘ Our GLM results confirmed that significant activity in the mirror
neuron related regions, including the Precentral Gyrus, the Posterior
Cingulate, the IFG, and the TPJ when successful coordination was
achieved. The MNS has been known for imitating actions as shared
communication (Schmidt et al., 2021). In previous review studies,
activity in the MNS is often significantly recruited in joint action (Mu
et al., 2018; Pacherie & Dokic, 2006; Sebanz & Knoblich, 2009). In
human social cognition, the MNS plays its crucial role of understanding
of action and intentional agency (Gallese et al., 1996; Rizzolatti,
2005; Rizzolatti et al., 2001) and the emergence of language (Arbib &
Bota, 2003; Arbib, 2002; Mu et al., 2018; Rizzolatti & Arbib, 1998). In
addition, regions related to execution and observation of actions, such
as the IFG, the Middle Frontal Gyrus, and the Medial Frontal Gyrus
(Molenberghs et al., 2012; Takeuchi et al., 2013), were also involved in
succeeding reciprocity. Since our task is a revised coordination game,
far more complicated than merely imitating actions, successful dyadic
interactions lie in careful decision-related processes. One study also
suggests that the mirror neuron system may not just help participant
mirror actions but process intentionally complementary or opposing
actions (Campbell et al., 2018). In order to achieve reciprocity for
final utmost reward, previous trial interactions should be observed and
taken into consideration for the following trial. In particular, the
role of the left IFG in action understanding and processing intention is
examined (Pobric & Hamilton, 2006) as a necessity in making a
perceptual judgment about people’s actions. This may result in the
recruited activity of the IFG, especially, found in all of our three
analyses. Lastly, activity associated with reward/reinforcement in the
Caudate increased as the dyads were mutually benefited in a row. This
explains how the pairs commonly reacted to reward when the successful
results were revealed during the second feedback stage and continued to
follow reciprocal interaction. We further ran correlations between the
[successful trials > failed trials] condition and the
three indices (i.e., reward, greed, and reciprocity), and the right
Sub-gyral in the motor cortex was strongly correlated with an
individual’s reciprocity. The Sub-gyral has been suggested for its role
in coordination (Swinnen et al., 2010; Ullén et al., 2003). Not
surprisingly, a person’s successful interaction with the other, which
often leads to reciprocity in the present experiment, lies in good
coordination in this motor-related area.
Our PPI analyses indicated individual differences in successful and
failed reciprocity trials in functional connectivity between the rTPJ
(seed region) and the other regions, which are similar to our GLM
results. Interestingly, lower functional connectivity was found with the
rTPJ, which is known for a role in theory of mind for mentalizing
others’ intentions (Saxe & Kanwisher, 2003). Our results may elucidate
how the rTPJ interacts with other regions associated with the MNS and
MS. One hypothesis is that the rTPJ may fire more strongly and thus
suppress the other self-related regions. Findings of the previous
studies on the MNS and MS suggest a complementary or collaborative role
of the two networks during social exchanges (Sperduti et al., 2014; Van
Overwalle & Baetens, 2009; Wang et al., 2018), while Frith and Frith
(2006) concluded that the MS is superior to the MNS for communicative
intent. In our coordination game, the task is not simply about winning
cooperatively, but reciprocally. Pairs do not just imitate each other’s
behavior. They have to figure out how to reach mutual benefits and
meanwhile how to gain more reward for themselves. This mentalizing
process may recruit more activity of the rTPJ and less activity of
self-related regions. One cannot be too greedy or too generous (or
submissive), for both of the strategies result in less amount of final
reward than acting reciprocal. This may explain why regions related to
self-related aspects of experience, including the Precuneus, insula and
IPL (Cabanis et al., 2013; Chiao et al., 2009; Harada et al., 2020; Ray
et al., 2010; Shi et al., 2021), exhibited negative correlations with
the rTPJ.
Further PPI analyses were conducted to investigate the relationship
between the functional connectivity and the total reward of individuals.
Regions associated with coordination/MNS (the rPG), attention
reorientation, and self-perception (the rAG and rIPL) (Corbetta et al.,
2008; Igelström & Graziano, 2017; Mitchell, 2008) were shown lower
functional connectivity with the rTPJseed when an
individual’s total reward increased in the contrast of successful trials
versus failed trials. In other words, the bigger the contrast between
the rTPJ and the ROIs mentioned above exhibits, the less total reward
one earns. As discussed above, the rPG for imitation in the MNS and the
IPL for self-other differentiation may be more suppressed when the rTPJ
needs to be more resource-allocated for mentalizing for others to
achieve reciprocity. Moreover, the AG and IPL are activated especially
in predicting valid cues (Corbetta et al., 2002; Vossel et al., 2006),
which results in less effort in successful trials for the cues as
predicted. A gradient descent functional connectivity between these ROIs
and the rTPJ negatively correlated with the total reward was also found
among the dynamics of the subgroups (submissive > dominant
> reciprocal) (see Figure 3f and the Supplementary Figure
S3). That is, a bigger ROI-rTPJ contrast but a smaller amount of the
total reward was yielded among the submissive participants. This can be
interpreted that those who acted submissive might be less coordinated
and less attentive than the reciprocal participants, and suppressing
their desire in reward might exhaust their mind when they were
fulfilling others (higher activity of the rTPJ in mentalizing others).
Regarding our frequency-domain results, two neural couplings of
interest, the rTPJ-rTPJ and rTPJ-rSTG, were found highly consistent with
social interactions. The first connectivity of the rTPJ-rTPJ emerging in
the interacting pairs can be seen to draw on constant tracking of the
other’s intention, mentalizing, and continuous communications for
achieving success in collaboration. This coupling also implies common
operation with attention (Igelström & Graziano, 2017) and social
attributions (Saxe & Kanwisher, 2003). Recently, the rTPJ has been
suggested to act as an interface of self- and other-related or external-
or internal-triggered information processing (Bzdok et al., 2013). In
particular, the rTPJp is associated with social
reasoning in a theory-of-mind experiment design (Krall et al., 2015;
Kubit & Jack, 2013). Previous experiments invoking face-to-face joint
attention with one participant in autism spectrum disorder (Redcay et
al., 2012), and in gaze-following of monkeys (Kamphuis et al., 2009) and
humans (Laube et al., 2011), or two participants (Abe et al., 2019;
Bilek et al., 2015; Koike et al., 2019), have shown activation of the
rTPJp for extra attention to track social cues. In the
present study, this rTPJ-rTPJp neural synchrony based on
social information integration and social behavior formation is in line
with the literature regarding the coordination of self- and
other-behavior (Carter & Huettel, 2013; Corbetta et al., 2008; Geng &
Vossel, 2013). We further compared this feedback in the decision stage
(Stage 2 Feedback) to that in the planning stage (Stage 1 Feedback). The
results again strongly support our original and previous results that
the rTPJ-rTPJ and -rSTG couplings can be found only in the
second/decision/final feedback, not in the feedback in the planning
stage. Another interesting result is that similar couplings (the rTPJ
coupled with the bilateral Lingual Gyri, linked to processing vision and
episodic memory) were found among the pairs who were interacting (WIPs)
and those who were doing the same task in the same group as the WIP but
with other partners (WNPs). In addition, the right Precuneus, involved
in self-referential processing, imagery, and memory, was identified in
sync with the rTPJ only in the WIP in the planning stage, compared with
the WNP also in the planning stage and the WIP in the decision stage.
Our results of the rSTG’s roles in social cognition and perception are
in good agreement with the existing knowledge. A few hyperscanning fMRI
studies, which also implemented the interpersonal coherence measures,
reported similar findings. For example, Wang et al. (2023) demonstrated
the similar rTPJ-rTPJp coupling when participants
competed for the whole reward (i.e., thus highly attentive), the
rTPJ-rSTG coupling when participants collaborated and split the reward
(97.5% trusting the partner, thus less attention demand required). In
the Token-Coordination task (Stolk et al., 2014), similar rSTG-rSTG
coherence between highly collaborative pairs, implicates such coupling
as the foundation of meaning (Stolk et al., 2016). In the present study,
being able to compute among three pairing groups (i.e., interacting,
non-interacting, and permuted), we would like to propose the idea of
decontextualization of the rTPJ-rSTG coupling as the shared meaning for
the common good. When pairs are in the context of interacting, their
rTPJs synchronize to mentalize each other. While they are interacting
with their pairmates, the rTPJs of theirs are coupled with the rSTGs of
the other two groupmates who are interacting with their pairmates at the
same time. The shift of the rTPJ-rTPJ coupling between pairmates (while
interacting with each other) and the rTPJ-rSTG coupling between
groupmates (while interacting with another in the same group), compared
to the baseline (the permuted results), highlights the formation of
decontextualization in the rTPJ-rSTG coupling. As trials go on, the
rTPJ-rSTG coupling can only be explained to be for shared goal
orientation, or simply understanding the game rules. While more
resources may be allocated in the rTPJ for thinking about the real
interacting partner, the interpersonal rTPJ-rSTG coupling is found in
sync between groupmates despite the same coordination game and the
simultaneous interacting time among all of them. In short, we would like
to refer to the rTPJ-rSTG coupling as the understanding of the shared
meaning. Here the interpretation of this coupling can be referred as to
the meaning of the common good, which is that ‘reciprocity leads to
better individual and group gain.’ This neural substrate serves as a
mutual understanding of abstraction, which is relevant to how human
languages were formed and shared among a group of people as human beings
are the symbolic species (Deacon, 1997).
By using the behavioral data, we classified subjects into three types
(reciprocal, dominant, and submissive). We further calculated the
differences in coherence values when subjects of different types were
paired or when subjects of uniform type were paired. This may help to
understand the mental processing of different types of subjects yielding
different oscillation synchronization. The TPJ was found between the
reciprocal pairs, and the IFG was identified among the reciprocal pairs
and the non-reciprocal types (dominant and/or submissive). These brain
regions are often associated with for action understanding and
processing intention as we discussed a lot above. Compared with the
reciprocal pairs, the non-reciprocal pairs had negative emotion arousal
in their right amygdala in sync with the rTPJ. This is an interesting
finding which echoes our real-life scenario that there may be bad blood
or hard feelings between the non-reciprocal pairs.
To date, the analysis for spatio-temporal dynamics of hyperscanning data
does not have standard computational models to follow (Kelsen et al.,
2022). Still, we tested if the evoked neural responses in the frequency
domain were temporally coherent. The results were all found
insignificant, suggesting that the effect size of frequency-domain
coherence is relatively miniscule, rendering the transformation into the
time domain almost non-existent. Small or null temporal effects in the
ROIs were derived from the analyses of the frequency domain. For
example, in the interacting pairs, the
rTPJseed-rTPJp time-course correlation
was 0.039 and its beta correlation was 0.005. Besides more
spatio-temporal analysis comparisons, we suggest that interpersonal
connectivities may be better for frequency-domain analysis, while the
time domain analysis is better for intra-personal correlations.
Moreover, two implications are concluded: 1) publication bias and 2)
future methodological requirements for more than two brains. First, due
to different temporal and spatial resolution of tools (e.g., EEG and
fMRI), analyses vary. Take the fMRI studies for example. Most studies
adopt time domain analyses, such as GLM, PPI, and multivariate pattern
analysis because of fMRI’s poor temporal resolution for frequency domain
analysis (e.g., coherence). Comparisons with temporal-spatial analysis
are barely tested, not to mention being reported, for its unfavorable
insignificant results. Some may propose to collect two kinds of data
from EEG-fMRI or MEG-fMRI. Again, the scanner thresheld within 3 mm head
motion flexibility may result in the ecological setting issue.
Therefore, it still remains incomplete but explorable between
spatio-temporal methods. Second, our limitation here is that the triad
data were not analyzed in a triad method. Instead, the contrasts and
connectivities between pairs were employed. We acknowledge that we have
not been able to come up with new analyses to test the correlations and
connectivities among three participants. As we all know, there will be a
long way to validate the three- or even four-way hyperscanning results
by adopting more than pairwise correlations. In fact, even though dyadic
fMRI hyperscanning has been adopted for more than two decades, the
methods are still diverse and debatable. Besides, previous studies
employed EEG and fNIRS with multiple participants interacting in sync
and also adopted pairwise methods, such as coherence. Interpersonal
couplings are always averaged across pairs; there is no difference
statistically to average across triads. For future possibilities,
analyses can be run by three or more brains simultaneously, as the
results can support more for interpreting multi-brain interactions
(Babiloni & Astolfi, 2014; Hamilton, 2021).
Aside from individual’s mind and brain states to characterize social
neuroscience in the past, the burgeoning works of such hyperscanning,
both in implementation and analysis perspectives, provide novel insights
into this much needed (in both theory and applications) field of study.
Reviewing histories and looking ahead, we are constantly reminded that
the future of human races, facing the challenges of global crises in
environment, welfare, resource management and so forth, will only be
solved by collective actions. The prerequisites of collaborations among
organizations of various scales, from families to countries, are
assurances of mutual attitudes throughout the processes. In cases where
any sign of disconfirming evidence arises, the social reciprocity might
fall and collapse along a downward spiral. This is why in addition to
the protection from supervising organizations or sound policies,
players’ mutual guarantee through trust and reciprocity plays a vital
role in long-term social mutual benefits.