Abstract
Unselfishness is one of the admired facilitators for human group endeavors, especially in times of urgent calls for global collaboration. Despite its importance, the neural dynamics behind its formation is scarcely understood. With 26 triads interacting as turn-taking pairs in a coordination game, we investigated reciprocal interactions in this tri-fMRI hyperscanning experiment. The critical role of the right temporal-parietal junction (rTPJ) was examined by adopting both time- and frequency-domain analyses. For the former, in the successful versus failed “reciprocity” contrast, brain regions associated with the mirror neuron system (MNS) and the mentalizing system (MS) were identified. In addition, the differences of connectivity between the rTPJ (seed region) and the abovementioned network areas (e.g., the right Inferior Parietal Lobule, rIPL) were negatively correlated with the individual reward. These results both verified the experimental design, which favored ‘reciprocal’ participants/triads with larger gains, and supported the opposition of rTPJ (other-) vs. rIPL (self-concerned) areas during successful social exchanges. Furthermore, the cerebral synchronization of the rTPJs emerged between the interacting pairs, and the coupling between the rTPJ and the right Superior Temporal Gyrus (rSTG) was found between those interacting simultaneously with others of the same group. These coherence findings not only echoed our previous findings, but also reinforced the hypotheses of the rTPJ-rTPJ coupling underpinning simultaneous collaboration and the rTPJ-rSTG coupling for decontextualized shared meaning emergence. Taken together, these results support two of the multi-functions (other-concerning and decontextualizing) subserved by the rTPJ, and highlight its interaction with other self-concerning brain areas in reaching co-benefits.
Keywords: fMRI hyperscanning, Psychophysiological Interactions (PPI), coherence, collaboration, reciprocity
INTRODUCTION
Imagine you are in class and four people are arranged as a group to complete a task. You start to talk with the one next to you, and then maybe the one sitting facing you. After a run of talking, you may find yourself having better interactions with certain partners; meanwhile it is just too hard to keep your conversation flowing with someone. Somehow, each of your partners makes you feel something, and this leaves an impression of how you decide to react to them later on. Normally, the better interaction you have, the more willing you are to help with the task. By the definition of ‘help,’ it actually means you give and take in achieving an end, mutually. Phenomena of mutual interaction, experienced or expressed by each of two or more people or groups about the other, are ubiquitous. Social scientists may wonder if there is a difference that can be observed between pairs who are doing the same task at the same time but interacting with others. If yes, what is the neural difference between the partner who is sitting in front of you and talking to you, and the one who is sitting next to you and talking to another? How does your brain react to ‘good’ partners and ‘bad’ partners? As for neuroscientists, investigating social interactions in various contexts and revealing their neural correlates has never been more profound and implicative enough. In the present study, we are attempting to answer these questions regarding social interaction with three brains communicating pairwisely.
Hyperscanning, simultaneously measuring the brain activity of multiple brains, allows the investigation of intra- and inter-brain neural relations in real-time dynamics (Czeszumski et al., 2020; Hari & Kujala, 2009; Scholkmann et al., 2013). Social neuroscience has developed research designs in hyperscanning in modalities other than fMRI, such as magnetoencephalography (MEG) (Holmes et al., 2023; Mayseless et al., 2019), electroencephalography (EEG) (Haresign et al., 2022; Turk et al., 2022), and functional near-infrared spectroscopy (fNIRS) (Nguyen et al., 2021; Zhang et al., 2023). Despite multiple brains interacting in sync, dyadic interactions and computations retain their fundamental roles in methodology and in research on the brain processes of social science. To progress toward real-life interactions, recent neuroscientific fMRI hyperscanning studies are mostly with dyads interacting with close-by or internet-connected scanners. Tasks to capture the emergent dynamics of simultaneous dual brain interactions include face-to-face interactions (such as gaze behavior) (Koike et al., 2019; Miyata et al., 2021), joint grips (Abe et al., 2019), coordination games (Goelman et al., 2019; Špiláková et al., 2019; Stolk et al., 2014; Wang et al., 2023; Yoshioka et al., 2021), natural events such as movie viewing (Schmälzle & Grall, 2020), and reciprocity in the ultimatum game (Shaw et al., 2018; Sperduti et al., 2014). Both the mirror neuron system (MNS) (Iacoboni & Dapretto, 2006) and the mentalizing system (MS) (Frith & Frith, 2006; Saxe, 2006) are indicated as playing vital roles in social interactions, especially in collaboration (Wang et al., 2018). For example, the Superior Temporal Gyrus (STG), the Inferior Parietal Lobule (IPL), the Inferior frontal gyrus (IFG), and the Precentral Gyrus, are among the brain networks during imitation (Heyes, 2001; Rizzolatti, 2005), an indispensable ingredients in positive rippling effects (Akgün et al., 2015; Barry, 2009); the TPJ and Precuneus are part of a mentalizing and default-mode network for interpreting cues of others (Hyatt et al., 2015; Li et al., 2014; Mars et al., 2012). Yet, as an old saying goes, “two’s company, three’s a crowd,” tri-MRI hyperscanning provides an unprecedented opportunity into the intricacies of group dynamics, given its varieties of three bi-directional, or even tri-directional, communications among group members.
Despite dyadic hyperscanning’s early onset (Montague et al., 2002), it was not until 2020 that we saw the first three-person fMRI hyperscanning study (Xie et al., 2020). In it, twelve triads engaged in a drawing task with collaborative and independent phases. Both GLM and intersubject correlation analyses (Hasson et al., 2004; Nummenmaa et al., 2018) indicated the critical role of rTPJ in the triadic collaborative interaction. As a likely second, in the present study we adopt both the time-domain, including GLM contrasts and Psychophysiological Interactions, or PPI, (O’Reilly et al., 2012), and frequency-domain coherence analysis (Wang et al., 2023) to reveal neural substrates of triadic social interactions. For the former, the aim is to investigate the neural differences between successful and failed reciprocity. We then adopted the successful and failed trials with reciprocity in the second stage of feedback time as our target trials. For the latter, we extend our prior work (Wang et al., 2023), a frequency-domain coherence analysis, into a 3-person internet-based hyperscanning (with the 4th sitting outside doing the same behavioral task) context (Sebanz et al., 2006; Vesper et al., 2016). Here, we focus on the stage of revealing whether the collaboration is successful (i.e., Stage 2 Feedback) because it is the shared period when the pairs check the results, build up the trust, and plan for the following trials. Note that there might be some nuances regarding unsuccessful, but not a failure to try to cooperate, and thus, may be underwritten by cooperative brain processes. This is not within the scope of the present study. Additionally, pairs win in two formats: the dyads could be kept in one dominant and the other submissive, or they could reciprocate with each other, which wins most in the end according to the experimental design. Lastly, when the inter-brain coherences were reported in the hyperscanning literature, the control conditions were mostly done by permuting individuals from different pairs (because of the exclusive within-pair interactions in dyads). In the present tri-fMRI study, however, the analyses of interpersonal coherence can be separated into several pairing combinations (see Methods for details), rendering at least three possible interpersonal couplings, thereby yielding multiple constraints of possible explanations.
What neural substrates, alone or together, contribute to meaningful interaction/coordination still holds scientists’ interest. From one brain to three, questions regarding subtle differences in mutual interaction can be empirically better understood. In summary, besides the technical advances in the tri-MRI implementation, reciprocity in collaboration and its meaning shared among dyads are elucidated in three analyses. These results generally suggest brain areas related to two essential networks in social interaction, the MNS and the MS. The present study plays an important contributor to the neuroscientific understanding of group collaboration, with implications for structuring co-benefits.
METHODS
Participants
Twenty-six triads of fMRI participants (NMale = 42; NFemale = 36) were recruited from National Cheng Kung University (NCKU), National Taiwan University (NTU), and National Chengchi University (NCCU). NCKU is situated in southern Taiwan (Tainan), and NTU and NCCU in northern Taiwan (Taipei). All participants are native Taiwanese speakers, with normal or corrected-to-normal vision, and no history of psychiatric or neurological disorders. Participants gave informed consent and adhered to the guidelines and regulations approved by the NCKU Governance Framework for Human Research Ethics https://rec.chass.ncku.edu.tw/en, with the case number 106-254.
Experimental task
The experimental task was a revised coordination game (Farrell, 1988). Four players were playing at the same time, three inside the scanners and one outside for the behavior data only (Figure 1a). The participants took random turns playing with each other as a pair. The player roles, such as Player A, were fixed. Within a run, there were three 6-trial blocks, e.g., Block 1: A&B/C&D, Block 2: A&C/B&D, and Block 3: A&D/B&C. (Figure 1b), in which any assigned pair (e.g., Block 1: A&B/C&D) completed 6 trials in a row. There were 6 runs of such 3 (blocks) x 6 (trials) combinations, with the random order of pairings as 3! = 6 (e.g., 123, 132, 213, 231, 312, and 321; one order for each run). Each run took about 7 to 8 minutes.
Each trial lasted about 19 seconds, containing two stages: the possible decision stage (preplay) and the actual decision stage (Figure 1c). Before each trial started, the screen showed with whom they would be interacting, e.g., “Interacting with Player B.” Next came the first, or communication, stage (Stage 1 Decision) , where any given participant told the other player his/her choice by clicking the leftmost (‘1’) or the second leftmost key (‘2’), representing X and Y. The reward combination of (X, Y) was (1, 6), (6, 1), or (0, 0), suggesting that either one would choose the reward, 1 (or 6), and the other chooses 6 (or 1), or neither of them would get any reward. About 6 seconds later, the possible choices of both players were shown on the screen (Stage 1 Feedback) . What they chose would be framed with a dotted rectangle, with one’s own choice in white and the other’s in another color. It is important to note that the possible/communicating choice in Stage 1 did not predicate the later actual choice. Participants in the second stage (Stage 2 Decision) , after making their final decisions, would see their responses framed with a solid lined rectangle, with one’s own choice in white and the other’s in another color (Stage 2 Feedback) , for up to 3 seconds. Three combinations to run statistics were Within-group Interacting Pairs (WIPs), Within-group Non-interacting Pairs (WNPs), and Between-group Permuted Pairs (BPPs) (Figure 1d).