Increased or Decreased Interpersonal Neural Synchronization in - 2022 - NeuroIm
Increased or Decreased Interpersonal Neural Synchronization in - 2022 - NeuroIm
Increased or Decreased Interpersonal Neural Synchronization in - 2022 - NeuroIm
NeuroImage
journal homepage: www.elsevier.com/locate/neuroimage
a r t i c l e i n f o a b s t r a c t
Keywords: Group creation is the process by which group members collaborate to produce novel and useful ideas or products,
Group creation including ideas generation and evaluation. However, the interpersonal neural mechanism of group creation dur-
Hyperscanning ing natural communication remains unclear. In this study, two groups of same-sex dyads with similar individual
fNIRS
creativity collaborated to complete the Product Improvement Task (creative condition) and the Item Purchase
Interpersonal neural synchronization
Plan Task (control condition), respectively. Functional near-infrared spectroscopy (fNIRS) was used to record both
members’ neural activity in the left prefrontal (lPFC) and right temporal-parietal junction (rTPJ) regions during
the task. Considering that the role asymmetry of group members may have an impact on interpersonal neural pat-
terns, we identified leaders and followers in the dyads based on participant performance. The results showed that
leaders and followers in the creative condition had significantly lower interpersonal neural synchronization (INS)
in the right superior temporal gyrus-left superior frontal gyrus, right supramarginal gyrus-left superior frontal
gyrus, and right supramarginal gyrus-left middle frontal gyrus than in the control condition. Partial multivariate
Granger causality analyses revealed the influence between dyads was bidirectional but was significantly stronger
from the leaders to the followers than the other direction. In addition, in the creative task, the INS was signifi-
cantly associated with novelty, appropriateness, and conflict of views. All these findings suggest that the ideas
generation and ideas evaluation process in group creation have poor interpersonal neural activity coupling due
to factors such as the difficulty of understanding novel ideas. However, performances may be improved when
groups can better integrate views and reach collective understanding, intentions, and goals. Furthermore, we
found that there are differences in the dynamics of INS in different brain regions. The INS related to the novelty
of the group creation decreased in the early stages, while the INS related to the appropriateness decreased in
the middle stages. Our findings reveal a unique interpersonal neural pattern of group creation processes in the
context of natural communication.
∗
Corresponding authors at: School of Psychology, Central China Normal University, Wuhan, 430079, China.
∗∗
Corresponding author at: School of Psychology, Jiangxi Normal University, Nanchang 330022, China.
E-mail addresses: [email protected] (Q. Zhao), [email protected] (F. Huang), [email protected] (Q. Yu), [email protected] (Z.
Zhou).
1
The first three authors contribute equally.
https://doi.org/10.1016/j.neuroimage.2022.119448.
Received 29 October 2021; Received in revised form 1 July 2022; Accepted 3 July 2022
Available online 14 July 2022.
1053-8119/© 2022 The Author(s). Published by Elsevier Inc. This is an open access article under the CC BY-NC-ND license
(http://creativecommons.org/licenses/by-nc-nd/4.0/)
Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
interaction process of group creativity. Groups tend to emerge with indi- To better understand the interactions that occur naturally in the
viduals who are good at generating novel ideas and individuals who are group creativity process and the characteristics of its interpersonal neu-
willing to understand and coordinate with others (Bolinger et al., 2009). ral mechanism, Mayseless et al. (2019) explored the INS difference be-
The former usually gain status in the group and may become leaders who tween creative tasks (open product design) and control tasks (prescribed
lead ideas. The latter, as followers, exert less influence on others but are 3D model building) in the context of natural communication and its rela-
also important in promoting creativity (Bolinger et al., 2009). This pat- tionship with behavioral indices of creativity. The result suggested that
tern of collaboration may be relatively stable throughout the process dyads’ INS in anterior prefrontal cortex (aPFC)-posterior superior tem-
of group creativity (Mayseless et al., 2019). Similarly, in the leader- poral gyrus (pSTG) and aPFC-TPJ in the creative task was significantly
less group discussions, many studies have also found that individuals greater than in the control task. However, it should be noted that while
may spontaneously form a “leader-follower” relationship (i.e. one per- the creative design task includes the idea generation and idea evalua-
son lead the task and the other one follow) in interactions (Jiang et al., tion, the 3D model building task as the control condition is quite differ-
2015; Konvalinka et al., 2014; Selten and Warglien, 2007). This spon- ent from it. For example, the 3D model building task requires advanced
taneous asymmetrical interpersonal relationship may be beneficial to manual dexterity and spatial skill. However, this interactive process may
group performance (Selten and Warglien, 2007; Wallot et al., 2016). For involve less verbal communication and less complex processing of lan-
the creative process, group creativity involves both divergent and con- guage and emotions (Li et al., 2021), which may affect the strength of
vergent thinking, which is similar to individual creativity (Tan, 2015; INS (Hasson et al., 2012).
Ulrich, 2018). The interacting members not only generate ideas (related Although the above two studies found higher INS in group cre-
to divergent thinking) but also evaluate the ideas (related to convergent ation, there is also some evidence that the INS of group creation tasks
thinking) of others (Chen et al., 2017; Paulus and Yang, 2000; Ray and may be lower than the general tasks. First, the shared neural response
Romano, 2013), with the two stages being constantly recursive and it- may reflect similar representation or thinking (Cetron et al., 2019;
erative (Harvey, 2014; Harvey and Kou, 2013). The former is expected Meshulam et al., 2021; Nguyen et al., 2021; Wass et al., 2020). To gener-
to improve the novelty of ideas and the latter is expected to improve the ate novel ideas, group members often need to inhibit dominant and con-
appropriateness of the group’s creative ideas (Paletz and Schunn, 2010; sensus representations, engage in mental representational change, break
Singh and Fleming, 2010). In addition, due to cognitive diversity and dif- the thinking impasses and diverge in different directions (Huang et al.,
ficulty in understanding the intentions of others’ views, members may 2019). As a result, the INS of group creation tasks may decrease. Sec-
have a conflict of views during interactions, but creativity tends to de- ond, due to the heterogeneity of knowledge, skills, and experience,
velop better when teams are better able to integrate members’ views group members in the process of idea evaluation may have difficulty
(Harvey, 2014; Kohn et al., 2011; Ristic et al., 2016; Xue et al., 2018). understanding each other’s novel ideas and intentions, resulting in dis-
Since group creation depends on interpersonal interaction, in re- agreements or conflicts (Bodla et al., 2018), which may lead to the
cent years, researchers have used functional near-infrared spectroscopy INS of group creation tasks lower than general tasks (Fishburn et al.,
(fNIRS) based hyperscanning technique to understand the interaction 2018; Lu et al., 2021; van Baar et al., 2021). Finally, Mayseless et al.
of creative groups (e.g., Duan et al., 2020; Lu et al., 2019a, 2019b, (2019) found that the originality score in the creative task showed a
2020b; Lu and Hao, 2019; Mayseless et al., 2019). Compared with trend level negative correlation with the INS increase of inferior frontal
single-brain studies, hyperscanning aims to measure the brain activity gyrus (IFG)-pSTG. This seems to imply that the INS may decrease when
of multiple brains simultaneously to meet the needs of studying the in- the interacting members generate some creative responses (Shamay-
terbrain activity patterns of interactive participants (see (Kelsen et al., Tsoory et al., 2019).
2020; Redcay and Schilbach, 2019; Wang et al., 2018) for further de- The present study used a Product (umbrella) Improvement task as
tails). Because fNIRS has high temporal and spatial resolution, and high the group creation task (Torrance, 1966). Participants were required
tolerance for physical activity, it has been widely used as a brain sig- to eventually generate a novel and appropriate solution. This process
nal acquisition modality in hyperscanning studies (Brockington et al., involved both idea generation and evaluation. The item (umbrella) pur-
2018). By analyzing the synchrony of group members’ neural activ- chase plan task, which requires a similar interaction pattern but does
ity during the interaction, termed interpersonal neural synchronization not demand creativity, was used as a general task for control. The simi-
(INS), researchers mainly focused on the influencing factors of the pro- larity of the experimental materials used and interaction patterns in the
cess of group creation. Recent evidence suggests that INS in the process two tasks better reduced the differences in INS due to excessive differ-
of group creation is related to romantic relationships (Duan et al., 2020), ences between experimental tasks. Given the advantages of fNIRS-based
communication mode (Lu et al., 2020b), cooperation (Xue et al., 2018), hyperscanning techniques, this study used fNIRS to continuously record
feedback (Lu et al., 2019a). And the stronger INS may indicate better changes in the cerebral activity of dyads during the interaction. We fo-
team performance. However, the above-mentioned influencing factors cused on the rTPJ and lDLPFC to explore the interpersonal neural mod-
on INS have also been found in other hyperscanning studies of interper- els between the individuals involved in group creation. The reasons are
sonal interaction (Cui et al., 2012; Liu et al., 2019; Long et al., 2021; as follows. First, the rTPJ and lDLPFC have been considered to be key
Zhu et al., 2021). brain regions for cognitive processing in creative tasks (Huang et al.,
To identify the interpersonal neural models specific to group creativ- 2021). The rTPJ as a component of the default-mode network (DMN)
ity, a direct comparison of group creativity tasks with general tasks (i.e. was considered to be related to the generation of creative ideas, while
non-creative tasks) may be needed. Lu et al. (2019b) compared the INS the lDLPFC as a component of the executive control network (ECN) was
difference between the alternative uses task (AUT, demanding divergent considered to be related to the evaluation of creative ideas (Huang et al.,
thinking) and the object characteristic task (OCT, not demanding diver- 2021; Kleinmintz et al., 2019). Moreover, in the context of social inter-
gent thinking) under the conditions of cooperation. They found that the action, the TPJ and PFC regions are also considered to be components
dyads’ INS of right dorsolateral prefrontal cortex (rDLPFC) and right of the mentalizing system (MS), which is responsible for mentalizing,
temporal-parietal junction (rTPJ) in the AUT task was stronger than in theory of mind, and other social cognition. The coupling between the
the OCT task. However, in this study, participants were only asked to two may reflect the state of interaction between individuals (Lu et al.,
continuously generate novel ideas in the turn taking without eventually 2021). In addition, previous hyperscanning studies of group creativity
forming an integrated proposal. So the study focused more on idea gen- have also shown that the lDLPFC and rTPJ are recruited (Lu et al., 2019a;
eration and less involved idea evaluation in group creativity. In addition, Lu and Hao, 2019).
unlike natural communication, turn taking itself is already a cooperative Role asymmetry has been neglected in previous studies on interper-
process that may affect interpersonal neural models related to creativity sonal neural mechanisms of group creativity, and members’ roles are
(Mayseless et al., 2019). considered to be equal and symmetrical. The INS of different brain areas
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Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
was calculated as the average across all group members in any given con- ment of interest in the task (see Supplementary Material S3 for ques-
dition. For example, the INS between lDLPFC and rTPJ was calculated tionnaires).
from the average of the INS between lDLPFC (Participant 1) and rTPJ
(Participant 2) and the INS between rTPJ (Participant 1) and lDLPFC 2.3.2. General experimental procedure
(Participant 2) (Li et al., 2021). Because role differentiation already ex- The general experimental procedure consisted of an 8 min resting-
hibits unique interpersonal neural characteristics early in natural com- state session, 2 min instruction session, and a 20 min task session (see
munication (Jiang et al., 2015), this calculation method of INS may ob- Fig. 1C).
scure some important information. In the present study, we assessed Participants were asked to sit face to face (see Fig. 1B), and the ini-
individual roles (leader or follower) based on dyads’ interactions before tial 8 min resting-state session served as a baseline. During this session,
data analysis. Then INS was calculated between each channel of the participants were asked to remain as still as possible, with their eyes
leaders and all channels of the followers in each dyad and was not aver- closed and their minds relaxed, and don’t think about specific problems
aged. This study examined the differences and dynamics of INS between or fall asleep (Lu et al., 2019b). Next, in the instruction session, the
creative condition and control condition, the information flow between task and requirements were introduced. Then, during the task session,
roles, and the relationship between INS and behavior indicators. group members cooperated to complete the corresponding experimental
tasks through natural communication. This process was recorded with a
2. Methods video camera with audio. fNIRS data were simultaneously collected dur-
ing both the resting-state session and task session. To ensure the validity
2.1. Participants of the data, the participants were asked to avoid large-scale movement
as much as possible during the experiment. After the discussion, the par-
One hundred and twenty-seven college students were recruited. They ticipants were asked to write down the plan together, and individually
were asked to complete an AUT task through an online questionnaire be- rated the degree of conflict of views during the discussion session from
fore the experiment. The novelty scores of the answers generated by the 1 (not at all) to 5 (very much) points.
participants were used as a measure of individual creativity (Runco and
Acar, 2012) (see details in the supplementary materials S1). 2.3.3. Task performance evaluation and role division
To avoid the influence of gender and creativity level on group cre- Eight graduate students, who were blind to the group assignment,
ation (Cheng et al., 2015; Xue et al., 2018), the dyads were made up of used the consensus assessment technique (Amabile, 1983) to evaluate
two people with the same level of creativity and the same gender (see the novelty and appropriateness of the problem solution on a Likert scale
details in the supplementary materials S1). After excluding participants ranging from 1 (not at all) to 5 (extremely). Four of them evaluated
who disobeyed the experimental instructions (see details in the supple- the creative product improvement task and the other four evaluated
mentary materials S1), there were 17 dyads (6 dyads of men and 11 the purchase plan task. The average of the four scores across two items
dyads of women) under each experimental condition, for a total of 68 was used as the final score for group performance. All the inter-rater
participants (mean age: 20.01 ± 1.91 years old). agreements were satisfactory (ICCs > 0.82).
The members of each dyad did not know each other before the ex- In addition, three graduate students were invited to watch the video
periment. All the participants were right-handed, had no brain disease and evaluate the role of each member of the dyad (leader: who always
or mental illness, and had normal or corrected-to-normal vision. They takes the lead, follower: who more or less follows the other) based on the
were paid a standard experiment participation fee and provided signed naturally emerging discussion. One member was identified as a leader
informed consent before participation. All experimental protocols were if two or more raters marked him or her as a leader. The other member
approved by the Ethics Institute Review Board of Central China Normal of the dyad was marked as a follower. Another four graduate students
University. counted the number of expressed views per individual in each dyad. All
graduate students were blind to the purpose of the experiment.
2.2. Experimental tasks
2.4. fNIRS data acquisition
In the creative condition, dyads were asked to complete the “Prod-
uct Improvement Task”. This task is an item on the Torrance Tests of NIRScout (NIRx Medical Technologies, New York) was used to
Creative Thinking (TTCT), which is typically used to measure individ- record changes in each participant’s oxy-hemoglobin (HbO) and deoxy-
ual creativity (Wei et al., 2014). We slightly changed the task for use in hemoglobin (HbR) concentrations during the experimental task. There
the dyadic context. To make the task relevant to daily life, we replaced were 4 probe sets. Of these, 2 probes had 3 emitters and 4 detectors to
the elephant, the object of the original creative product improvement form a 3∗ 4 probe set, forming a total of 8 measurement channels. The
task, with an umbrella (see Fig. 1A). These dyads were asked to discuss other 2 probe sets had 5 emitters and 4 detectors to form a 5∗ 4 probe set,
form a novel and appropriate improvement plan for the umbrella. In forming a total of 12 measurement channels. Thus, there were a total of
the control condition, dyads were asked to complete a general task of 20 measurement channels. The distance between each channel was up
“Item Purchase Plan”. Compared with the creative task, the general task to 3 cm (fixed with a 3 cm fixing piece).
required little creativity. These dyads were asked to discuss to form an In dyads, each participant had two probe sets on the head: a 3∗ 4
appropriate purchase plan for the umbrella (see supplementary mate- probe set on the left forehead and a 5∗ 4 probe set on the right temporal-
rials S2 for task instructions). After the discussion, the team ultimately parietal joint area. The probe was placed according to the 10-20 inter-
needed to reach a consensus on the improvement plan or purchase plan national system. The emitters on the left forehead covered FP1, AF3,
and then write down the plan together. and F5, with detectors located at FPz, AFz, AF7, and F3. The emitters
on the right temporal-parietal joint area were located at P8, T8, CP6,
2.3. Experimental procedure P4, and C4, with detectors at TP8, P6, C6, and CP4. The positions of
the probes are shown in Fig. 1D. The brain region corresponding to the
2.3.1. Subjective measurement channel was positioned using a three-dimensional locator (NIRx Medi-
Before the general experimental procedure, participants were asked cal Technologies, New York), which to determine the Nz, Cz, Iz, AL, AR
to complete assessments of cooperative preference, the familiarity with points and probe positions. The probabilistic registration method was
umbrellas, and the degree of demand for umbrellas. After the general used to register the fNIRS channel position with the Montreal Neuro-
experimental procedure, participants were asked to complete an assess- logical Institute (MNI) space coordinates to obtain the corresponding
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Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
relationship with the Brodmann area and automatic anatomical labels and the five extraneous variables at the pair level (continuous variables)
(AAL) area (Tsuzuki et al., 2012). were covariates.
The absorption of near-infrared light at two wavelengths (785 and
830 nm) was measured with a sampling rate of 7.8125 Hz. Based on the
modified Beer-Lambert law, changes in the HbO and HbR concentrations 2.6. fNIRS data analysis
were obtained by measuring changes in absorption of fNIRS light after
its transmission through the tissue. Previous studies have shown that 2.6.1. Pair-level analysis
HbO was a sensitive indicator of change in regional cerebral blood flow The fNIRS data collected during the rest session and task session were
(Zheng et al., 2018). Thus, this study focused on the HbO concentrations analyzed. Data from the first 60 s and last 60 s were deleted during pre-
only. processing. Thus, data within the period of steady state were analyzed.
During preprocessing, no filtering or detrending procedures were ap-
plied (Cui et al., 2012). In addition, we did not perform any artifact
2.5. Behavioral data analysis
corrections at the single-subject level, as wavelet transform coherence
(WTC) normalizes the amplitude of the signal according to each time
2.5.1. Correctness check of role division
window and thus was not vulnerable to the transient spikes induced by
Since the leaders may express more views (Wickham and
movements (Nozawa et al., 2016).
Walther, 2007), we conducted a 2 (between-group variable: Task Type:
We employed WTC analysis to estimate INS. A Matlab package was
creative task vs. general task) ∗ 2 (within-group variable: Role: leader
used to perform WTC (Grinsted et al., 2004) as a way to assess the
vs. follower) mixed ANOVA on the number of expressed views to ver-
cross-correlation between the two fNIRS time series generated by each
ify the correctness of the role division. In addition, the communication
pair of participants as a function of frequency and time (Torrence and
skills and competence of members were further evaluated to ensure the
Compo, 1998). For the two participants in one dyad, HbO values were
correctness of the role division (see Supplementary material S4 for de-
obtained in two time series of equal length and aligned. Then, WTC was
tails).
applied to these two aligned time series to find regions in the time fre-
quency space where the two time series co-varied. For more thorough in-
2.5.2. Task performance formation about wavelet coherence, please see Grinsted et al. (2004) and
Before conducting a comparison of task performance between the Chang and Glover (2010). Because there were 20 measurement channels
two tasks, we first tested the control of extraneous variables in the ex- for each participant (leader or follower), 400 (20∗ 20) pairs of time series
periment. A 2 (between-group variable: Task Type: creative task vs. gen- were generated for each dyad, and WTC was thus conducted 400 times
eral task) ∗ 2 (within-group variable: Role: leader vs. follower) mixed (Zheng et al., 2020, 2018). The coherence values were time-averaged
ANOVA was conducted for each of the following dependent variables: across the rest and discussion periods, and converted into Fisher z-
individual creativity, cooperative preference, familiarity with umbrel- values.
las, the degree of demand for umbrellas, and interest in the task. Consistent with previous studies (Dai et al., 2018; Jiang et al., 2012),
As extraneous variables obtained by subjective measurement might we focus on the relative enhancement of INS during the task session
have affected task performance, one-way ANCOVA was conducted to ex- compared to the resting-state session. Thus, we subtracted the coherence
clude possible effects of extraneous variables on task performance. We value of the resting-state session from that of the task session to obtain
separately averaged the five extraneous variables in dyads. For that anal- an index of time-aligned INS increase (Grinsted et al., 2004). At this
ysis, the Task Type (a categorical variable) was an independent variable stage, no specific frequency ranges were selected.
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Since the group creativity process requires members to continuously conditions, we conducted a time accumulation INS analysis to signifi-
generate and evaluate ideas through verbal communication, this process cant CH combinations respectively (Liu et al., 2019). First, we normal-
involves neurocognitive processing of members’ mutual understanding. ized the discussion session of each dyad into 200 epochs. For each dyad,
The neural coupling between two persons in verbal interaction may not the time-cumulative INS at epoch n was calculated as the sum of the INS
be limited to time alignment. Previous studies have shown that in the ranging from the first epoch to the nth epoch. Second, we performed in-
process of information comprehension, listeners’ neural response may dependent samples t-tests at 200 epochs to compare the difference of
lag behind speakers, resulting in a time-lag INS (Jiang et al., 2021; INS increase between the two conditions. Finally, the resulting p values
Liu et al., 2017; Stephens et al., 2010). Therefore, we added various were FDR corrected.
time-lags to the computation of INS increases to obtain the time-lagged
INS increases (Long et al., 2021; Zheng et al., 2018). For the selection 2.6.2.5. Coupling directionality. We further estimate the magnitude of
of time windows, we referred to previous interpersonal neural studies bidirectional information flow between the leaders and the followers
on verbal comprehension (Jiang et al., 2021; Liu et al., 2020, 2017; in the two tasks by conducting partial multivariate Granger causality
Stephens et al., 2010). Specifically, the time course of the leaders’ brain analyses (PMGCA). Tradition Granger causality analysis (GCA) uses vec-
activity (i.e., HbO) was shifted forward or backward relative to that of tor autoregressive models to measure the causal relationship between
the followers’ brain activity by 1–6 s (step = 1 s). time series in brain data. Since the Granger causality value may indi-
cate the strength of the interpersonal influence during the social inter-
2.6.2. Group-level analysis (time-aligned INS) action (Cheng et al., 2019), it provides a neurobiological suggestion of
2.6.2.1. Task type-related differences in time-aligned INS. The following coupling directionality, i.e., which individual was more actively driving
analyses were conducted to identify the difference in the INS increase another (Barnett and Seth, 2014). However, the exogenous and endoge-
between the two tasks. First, to identify the frequency ranges that were nous influences such as common external stimulus-induced neural re-
specifically associated with the task style, independent sample t-tests sponses or similar intrinsic neural responses may confound the Granger
were conducted on the time averaged coherence value of each CH (chan- causality between individuals and lead to spurious causal inference
nel) combination (400 in total) along the full frequency range (0.01–0.7 (Guo et al., 2008; Roelstraete and Rosseel, 2012; Youssofzadeh et al.,
Hz). Following previous studies (Dai et al., 2018; Jiang et al., 2012), data 2016). PMGCA can better mitigate potentially confounding effects on
above 0.7 Hz were not included to avoid aliasing of higher frequency causal inference by modifying the traditional GCA by adding terms
physiological noise, such as cardiac activity (0.8–2.5 Hz). Data below based on residual correlations between the predicted and the condi-
0.01 Hz were also not used, to remove very low frequency fluctuations. tional variables (see more details in (Guo et al., 2008; Roelstraete and
Finally, data within the frequency range of respiratory activity (0.15– Rosseel, 2012, 2011).
0.3 Hz) were not considered. The t-test results were threshold at p < Consistent with previous studies (Hou et al., 2020; Pan et al., 2021,
0.0005. No further corrections were applied because this analysis was 2018), our PMGCA was based on normalized HbO signals of signifi-
used to identify the pattern along the frequency range rather than to cant CH combinations during the discussion periods. The main steps
obtain the final results (Zheng et al., 2018). It was finally found that the of the PMGCA are as follows: First, in each channel, we converted the
frequency range of interest was 0.315–0.445 Hz, and the coherence val- HbO signals of the task session into z-scores using the mean and the
ues within this frequency range were averaged. Independent samples t- standard deviation of the signals recorded during the resting-state ses-
tests (creative task vs. general task) were performed on the time-aligned sion (Chen et al., 2020; Cheng et al., 2019; Pan et al., 2021). Second,
INS increase of all channels in this band, and FDR correction was per- for each individual, the z-scored time series of significant channels in
formed (Zheng et al., 2020, 2018). The channel combinations exhibit- the same brain regions were averaged. Third, to mitigate the impact
ing significant condition-related INS increase differences were defined of exogenous or latent variables, the time series of the leader corre-
as significant CH combinations. sponding follower’s significant channel and the time series of the fol-
lower corresponding leader’s significant channel were used as moderat-
ing variables (see 3.2.5 for details). Fourth, an R package (FIAR; down-
2.6.2.2. Validation of the INS differences between task types through a per-
load from https://github.com/cran/FIAR) was used to calculate the par-
mutation test. To verify that the group difference in INS increase was
tial multivariate Granger causalities in two directions (Roelstraete and
specific to the original pairing of the leaders and followers, a valida-
Rosseel, 2011): from the leaders to the followers and from the followers
tion approach (i.e., a permutation test) was used (Lu et al., 2020b). For
to the leaders. Finally, we used a one-sample t-test to compare the dif-
each condition, all participants were randomly assigned to new dyads
ferences between each direction and zero in each condition, and then
to recompute the INS and perform a series of independent sample t-tests
the effect of Task Type and Direction was examined by mixed ANOVA.
on the newly formed two sets of data. This permutation process was re-
peated 1000 times to yield a distribution (t value) of all CHs, which was
2.6.3. Group-level analysis (time-lagged INS)
then compared with the original pairing data.
2.6.3.1. Task type-related differences in time-lagged INS. To examine
whether there are differences in time-lagged INS between the two tasks,
2.6.2.3. Linking task performances with time-aligned INS. To determine a series of independent samples t-tests (creative task vs. general task)
the behavioral significance of leader-follower neural coupling, we ex- was applied to each time lag (i.e., -6s (follower precede) to +6s (leader
amined the correlation between INS increase of significant CH com- precede)) in 0.315–0.445 Hz frequency range, and FDR correction was
binations and the task performances, separately, under different con- performed (Long et al., 2021; Zheng et al., 2020).
ditions. Since creativity level, cooperative preference, and interest in
the task may affect the correlation between INS and task performance 2.6.3.2. Linking conflict of views with time-lagged INS. Since the level of
(Kelsen et al., 2020; Lu et al., 2019b; Xue et al., 2018; Zhu et al., 2019), time-lagged INS was considered to represent the degree of individual
we separately averaged the three extraneous variables in dyads. Then, understanding of information in the communication (Jiang et al., 2021;
a Pearson’s partial correlation analysis was applied, which controlled Liu et al., 2017; Stephens et al., 2010), it might be related to the conflict
for the potential effect of the three extraneous variables (creativity, co- of views perceived by the individual during the task (Harvey, 2014). To
operative preference, and interest in the task), and FDR correction was test this hypothesis, we averaged the degree of conflict of views in dyads,
performed. then a Pearson’s correlation analysis was adopted to analyze the rela-
tionships between the degree of conflict of views and the time-lagged
2.6.2.4. Dynamics of the time-cumulative time-aligned INS analysis. To INS of significant CH combinations, separately, under different task con-
identify the earliest time-point where the INS increase differed among ditions, and FDR correction was performed.
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Table 1
Specific brain areas involved in the INS between leaders and followers.
CH3-CH14 right Superior temporal gyrus (rSTG) left Superior frontal gyrus (lSFG)
CH3-CH15 right Superior temporal gyrus (rSTG) left Superior frontal gyrus (lSFG)
CH3-CH16 right Superior temporal gyrus (rSTG) left Superior frontal gyrus (lSFG)
CH7-CH16 right Supramarginal gyrus (rSMG) left Superior frontal gyrus (lSFG)
CH7-CH18 right Supramarginal gyrus (rSMG) left Middle frontal gyrus (lMFG)
CH15-CH20 left Superior frontal gyrus (lSFG) left Middle frontal gyrus (lMFG)
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Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
Fig. 2. Time-aligned INS result. (A) Time-aligned INS matrix at 0.315–0.445 HZ. The color indicates the t value. The significantly different CH combinations are
marked by the red frames. (B) The location of significant CH combinations on the cerebral cortex. (C) The distribution of the t value was calculated by 1000 random
dyads for the significant CH combinations. The dotted lines denote the positions of the t values on the actual dyads. (D) The partial correlation between time-aligned
INS increase of CH3-CH16 and novel score. (E) The partial correlation between time-aligned INS increase of CH7-CH18 and appropriateness score.
ever, we did not find a significant interaction effect, F (1, 32) = 0.01, 3.3.2. Relationship between conflict of views and time-lagged INS
p = 0.914. When the brain activity of the leaders precedes the followers, the
correlation analysis found that the INS increase of the CH3-CH14 at 1s
3.3. Time-lagged INS result and 2s time lags was significantly negatively correlated with the degree
of conflict of views in the creative condition (1-s time lag: rCH3-CH14 = -
3.3.1. Task type-related differences in time-lagged INS 0.73, corrected pCH3-CH14 = 0.002; 2-s time lag: rCH3-CH14 = -0.71, cor-
The time-lag results showed that the INS increase of CH3-CH14 (t rected pCH3-CH14 = 0.002) (see Fig. 5E, 5F). The correlation between
(32) = -4.70, corrected p = 0.019, Cohen’s d =1.66) and CH15-CH20 (t time-lagged INS increase and conflict of views was not found in CH15-
(32) = -4.22, corrected p = 0.038, Cohen’s d = 1.49) were significantly CH20 or the general task (corrected ps > 0.05).
lower in the creative condition than in the control condition when the
leaders’ brain activity preceded that of the followers by 1s. In addition, 4. Discussion
when the leaders’ brain activity preceded that of the followers by 2s, the
INS increase of CH3-CH14 (t (32) = -4.42, corrected p = 0.043, Cohen’s The present study explored the difference between the group creativ-
d = 1.56) was significantly lower in the creative condition than in the ity task and the general task and unveiled the underlying interpersonal
general task condition. See Table 1 for specific brain areas involved in neural correlates, using the fNIRS-based hyperscanning technique.
the CH3-CH14 and CH15-CH20. No significant results were found when Our findings first confirm that the “leader-follower” role asymmetry
the followers’ brain activity preceded that of the leaders at any time- occurred spontaneously in groups during natural communication. Lead-
lags, at any CH combinations (corrected p > 0.05) (see Fig. 5A-5D). ers expressed more views, and there was a greater information flow
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Fig. 3. The dynamics of the time-cumulative INS. The time-cumulative INS increase of 200 normalized epochs in the creative condition and control condition. The
red and blue shaded areas denote the standard error at each epoch. The yellow color indicates the INS significant difference between these two conditions, ∗ p < 0.05,
FDR corrected.
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Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
Fig. 5. Time-lagged INS result. (A) Time course of the INS increase of CH3-CH14 and CH15-CH20 from -6s (follower precede) to +6s (leader precede). The y-axis
shows the t value (i.e., independent sample t-tests on the INS increase, two-tailed), ∗ p < 0.05. (B) The location of significant CH combinations on the cerebral cortex.
(C, D) Time-lagged INS matrix at 0.315–0.445 HZ, when the leaders’ brain activity preceded that of the followers by 1s and 2s. The color indicates the t value. The
significantly different CH combinations are marked by the red frames. (E) The correlation between INS increase of CH3-CH14 at 1s time lags and conflict of view
score. (F) The correlation between INS increase of CH3-CH14 at 2s time lags and conflict of view score.
ate solutions, while the latter only required dyads to end up with appro- uation of ideas (Ellamil et al., 2012; Huang et al., 2021). These results
priate solutions. After controlling for extraneous factors, the behavioral may reflect a unique pattern of synergistic activation between DMN and
results showed that the novelty score of the creative task was signif- ECN among leaders and followers during group creation (Li et al., 2021).
icantly higher than the general task, while the appropriateness score Compared with the traditional single-brain functional connectiv-
was not significantly different between the two tasks. This result is con- ity analysis, the functional correlations between subjects (e.g., INS)
sistent with the performance characteristics of both creative and general have a higher signal-to-noise ratio and interpersonal interaction sen-
tasks and demonstrates the validity of our experimental manipulation. sitivity (Pan et al., 2020). According to the cross-brain functional in-
The fNIRS results showed significant differences in the time-aligned tegration hypothesis of INS, INS may ‘reflect a reciprocal and dy-
INS of rSTG-lSFG, rSMG-lSFG, and rSMG-lMFG between the creative namic interplay between the neural states of socially interacting con-
condition and control condition. The STG and SMG belong to the DMN specifics’ (Holroyd, 2022). This hypothesis holds that multiple brains
(Abe et al., 2019; Marron et al., 2018), which are considered to be can come together to act jointly as a functional unit, much like mod-
the core brain regions for creativity and are related to novel associ- ules within a single brain can coordinate their activities to accomplish
ation, idea generation, and divergent thinking (Benedek et al., 2014; tasks (Holroyd, 2022; Valencia and Froese, 2020). The coupling between
Huang et al., 2021; Kleibeuker et al., 2017; Wei et al., 2014; Wu et al., DMN and ECN has been widely found in the study of individual creativ-
2016). The lSFG and lMFG are located in lDLPFC (Kikinis et al., 2010), a ity (Beaty et al., 2016, 2015; Ellamil et al., 2012; Kleinmintz et al., 2019;
key node in the ECN (Huang et al., 2021). The lDLPFC is associated with Pinho et al., 2015), which seems to reflect that the ECN can top-down
working memory and verbal comprehension (Klaus and Schutter, 2018; monitor and direct the DMN’s idea generation process in the form of idea
Kleinmintz et al., 2019), and was found to be recruited during the eval- evaluation to meet the task goals (Beaty et al., 2016). Thus, when the
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Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
ideas generation and ideas evaluation of individual creation is mapped negatively correlated with the conflict degree of views in the creative
to group creation, it may manifest as the interpersonal coupling of DMN condition.
and ECN. We did not find significant results of time-lagged INS when the fol-
Unlike previous studies, we found that the INS of the creative con- lower’s brain activity preceded that of the leaders. The results suggest
dition was significantly lower than the control condition. One possible that the leaders played a dominant role in the interaction during group
explanation for the results may be that the ideas generated by the lead- creation. In this case, the brain activity of the leaders might always be
ers in the creative tasks were more novel and unique than the general ahead of the followers in time (Jiang et al., 2015).
tasks, and it might be difficult for the followers with different knowledge
and experience to understand their intentions or form shared represen- 4.3. Temporal dynamics of INS in group creation
tation. And many group creation studies have indeed found that group
members may react negatively when evaluating the novel ideas of oth- The INS may not be temporal stationarity during measurements
ers (Harvey, 2014; Harvey and Kou, 2013; Mueller et al., 2012). The (Li et al., 2021). We examined the INS dynamics of the creative task.
above factors might lead to the difficulty of good cooperation between Since cumulative INS may be a better dynamic indicator than moment-
the DMN and ECN in dyads, resulting in lower INS (Fishburn et al., to-moment INS (Jiang et al., 2015), we used cumulative INS to assess
2018; Jiang et al., 2021). In addition, the PMGCA results show that the the time point at which INS differences emerged between the creative
G-causalities of creative tasks are also significantly lower than the con- and control conditions. The results of the time-course analysis showed
trol condition, which seems to indicate that the interpersonal influence that about half a minute after the beginning of the problem-solving pro-
between leader and follower is lower in the creative task than in the cess, the difference in time cumulative INS of rSTG and lSFG between
general task for the above reasons (Cheng et al., 2019). the two conditions became significant and persisted until the end of the
However, there are other possible explanations (not necessarily al- interactive process. However, the stable difference in the time cumu-
ternative) for the above results. Although we consider the STG and SMG lative INS of rSMG-lSFG and rSMG-lMFG between the two conditions
as being in the DMN and the SFG and MFG as being within the ECN, it appeared later, about 5–6 minutes after the beginning of the problem-
does not imply in any way that these regions contribute exclusively to solving process.
those networks. For example, STG and SMG are also subcomponents of Our results found that the INS of rSTG-lSFG was related to nov-
rTPJ, which is related to social cognitive processes such as perspective elty and the INS of rSMG-lMFG was related to appropriateness. The
taking, mentalization, and theory of mind (Lu et al., 2020). The rTPJ difference in the temporal dynamics of INS may reflect the character-
and the dlPFC (i.e., where SFG and MFG are located) together form istics of the group creation process. In the early stages of group cre-
the MS. This system can help individuals understand others’ intentions ation, unconstrained divergent thinking is a key factor of group cre-
based on gestures, behaviors, and facial expressions (Mayseless et al., ativity (Rosing et al., 2018). Since the group has not yet determined
2019; Wang et al., 2018). Thus, another possible explanation for these the direction of a novel solution, members can explore a variety of dif-
results is that because of the novelty of the ideas talked about in the ferent approaches and directions. The group tends to generate more
creative task, it may be more difficult for group members to figure out unique and original ideas during this process, and these initial nov-
each other’s intentions. elty ideas generated often influence the novelty of the final solution
Consistent with previous research (Duan et al., 2020; Lu et al., (Puccio et al., 2020). Therefore, the novelty-related INS (e.g., rSTG-
2019a), we also found that INS in group creation was positively cor- lSFG) showed inter-condition differences earlier. As the discussion pro-
related with final task performance (i.e., novelty and appropriateness). gresses, beginning in the middle to late stages of group creation, mem-
Due to factors such as the heterogeneous structure of the group and bers may gradually begin to consider the implementation of creative so-
cognitive diversity, groups may generate different views during the cre- lutions, focusing on their feasibility (Rosing et al., 2018). At this point,
ation process. The dialectical model of group creativity argues that when the group may consider whether the solution is appropriate when devel-
groups are able to actively process the ideas of others and creatively oping its ideas. Therefore, the appropriateness-related INS (e.g., rSMG-
synthesize opposing views, they may have the opportunity to achieve lMFG) showed inter-condition differences later.
high-quality creative solutions (Harvey, 2014). The integration of views
emphasized by this theory is a process of building similarities within 4.4. Limitations
different perspectives and shaping collective attention and collective
understanding, which may improve INS (Cirelli, 2018; Fishburn et al., The study has several limitations. First, gender may affect interper-
2018; Gvirts and Perlmutter, 2020). Therefore, if leaders and follow- sonal interaction (Cheng et al., 2015), and the participants in this study
ers integrate their views into a shared view in a cyclical generation- were all same-sex dyads. In the future, researchers should consider ex-
evaluation process, the DMN and ECN between the two may be better ploring the cooperation mechanism in group creation of opposite-sex
coupled, which will help the group develop a good goal directed and im- members, as leadership and cooperation with the group may vary by
prove task performance (Harvey, 2014; Huang et al., 2021; Paulus et al., gender (Lu et al., 2020a; Mu et al., 2018). Second, in addition to the
2012; Paulus and Brown, 2007). generation and evaluation of novel ideas, DMNs and ECNs have multi-
Previous hyperscanning studies have found that the brain activ- ple functions. For example, the DMN also has the role of making social
ity of listeners tends to lag behind that of speakers (Liu et al., 2020; predictions in interpersonal interactions (Barrett, 2016). This implies
Stephens et al., 2010; Zheng et al., 2018). This delay phenomenon of that there may not be only one interpretation for our findings and fur-
INS is explained by the fact that interactive speech processing between ther detailed exploration is needed in the future. Third, the interper-
individuals takes a certain amount of time to reach mutual understand- sonal neural activity of group creativity may not be limited to rTPJ and
ing, and the strength of the time-lagged INS is also considered as the lDLPFC, and future research should study more brain areas.
level of understanding (Jiang et al., 2021). Our results found that the
time-lagged INS of rSTG-lSFG was significantly lower in the creative 5. Conclusion
condition than in the control condition when the leaders’ brain ac-
tivity was preceded by 1s or 2s to the followers. This may indicate In the present study, we identified the roles in the leaderless group
that followers had difficulty understanding when evaluating the novel discussion and found that leaders expressed more views and influenced
ideas generated by the leaders. Interpersonal incomprehension has long followers more. Compared with the control condition, the interpersonal
been considered an important factor in the generation of conflict in influence between leaders and followers in the creative condition was
group creation (Hu et al., 2017). This view is also confirmed by our weaker, and the time-aligned INS between leaders’ DMN and followers’
findings that the time-lagged INS of rSTG-lSFG was significantly and ECN was lower. However, when these two brain regions of the dyads
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Z. Liang, S. Li, S. Zhou et al. NeuroImage 260 (2022) 119448
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