Neural Basis for Social Competence


Studies were conducted to assess the hypothesis that social competence and prosocial behavior originate from self–other equivalence and develop as a result of intersubjectively shared learning. Specifically, neural substrates associated with the following were analyzed using fMRI: (1) sense of agency and social contingency, (2) mutual gazing and joint attention, (3) sarcasm, (4) humor processing, (5) empathy, and (6) the role of intrinsic motivation in learning. In addition, experimental research showed that (7) social interactions are intrinsically rewarding. Moreover, studies identified the neural substrates for (8) self-esteem (a key element of wellbeing) and (9) subjective sense of happiness.



(1) Neural Similarities Between Social Contingency and Sense of Agency 

(Sasaki et al., in press)

Detecting the relationship between one’s actions and subsequent responses from others (social action-outcome contingency) is an important aspect of social behavior. Because one’s actions differ from others' in terms of action kinematics, body identity, and feedback timing, the detection of social contingency requires comparison and integration of these three components. According to developmental psychology, a sense of agency is acquired during the early stages of development through acknowledgment of the temporal contiguity between one’s actions and sensory feedback. Sense of agency also serves as the basis for subsequent awareness of social contingency, which is characterized by delayed feedback from others following one’s actions. This fMRI study investigated the neural basis for the sense of agency and social contingency. Healthy volunteers were asked to perform finger gestures with their dominant hand following spoken instructions. On a projector screen, the participants were shown either their real-time or prerecorded finger movements as visual feedback. The visual feedback represented differences in identity of the agent (self/other), action kinematics (concordant/discordant), and feedback timing (delay/no-delay). The results showed that the left inferior and middle frontal gyrus was strongly activated when the hand movements of the participants were fed back in real time or when gestures performed by others were displayed after a short delay. By contrast, the extrastriate body area was sensitive to the concordance of action kinematics, regardless of the identity of agent or feedback timing. The interaction between the identity of agent and feedback timing activated the superior parietal lobule. The three tested variables modulated the connections from the occipital cortex to the left inferior and middle frontal gyrus via the extrastriate body area and superior parietal lobule. These results suggested that both social contingency and the sense of agency are achieved by hierarchical processing that begins with simple concordance coding in the left extrastriate body area, leading to the complex coding of social relevance in the left inferior and middle frontal gyrus.


(2) Mutual Gazing and Joint Attention

(Koike et al., 2016)

Two individuals can share visual attention through gazing. Infants start to make mutual eye contact with other people at 6 to 12 months of age. Eye contact modulates development of the ability to reason about the intentions and desires of others (theory of mind) and is a prerequisite for language learning. The absence of eye contact is an early sign of autism. Joint attention coordinates an awareness of objects or events between partners connected by eye contact. Low levels of initiating joint attention to attract others’ visual focus are a late sign of autism. In order to identify the neural basis for human interactions and understand the process by which two persons develop the sense of “we-ness” through gazing, it is necessary to simultaneously record and analyze the neural activities of visually interacting dyads. Using two sets of MRI scans, neural activities were monitored in pairs of participants engaged in joint attention and eye contact. Specifically, same-sex pairs of participants who met their partners for the first time on the day of the experiment were instructed to gaze at their partner’s face, which was projected onto the screen for several minutes; as they did so, their brain activities were recorded. Eye blinking was hypothesized as an avenue of communication. Eye blinks are often synchronized between persons in face-to-face interactions and disengage visual attention. Eye blinks were video-recorded and analyzed. Inter-individual neural synchronization was investigated using methods similar to those previously reported (Saito et al., 2010; Tanabe et al., 201). The results showed that mutual gazing between unknown partners enhanced neural synchronization in the right middle temporal gyrus, although no explicit eye-blink synchronization occurred.

After this experiment, participants executed joint attention tasks for approximately one hour on Day 1. On Day 2, participants were paired with the same partner as on Day 1, and again performed the real-time mutual gaze task. Brain activity correlations were noted not only in the right middle temporal gyrus but also in the right inferior frontal gyrus. In contrast to the previous day, significant eye-blink synchronization was noted on Day 2 In addition, enhancement of inter-individual neural synchronization was positively correlated with eye-blink synchronization. The different experimental conditions of this study showed that neural synchronization was pair-specific and dependent on the experience of joint attention.

This study suggested that (i) participants repeatedly experienced joint attention by engaging in the joint attention task, (ii) shared attention was unconsciously achieved by synchronized eye blinking, which represents interruption of visual attention, and (iii) learned shared attention was represented by neural synchronization in the right inferior frontal gyrus. At present, efforts are being made to expand the experimental system of this study and develop a method for quantifying dyad interactions based on real-time fMRI and electrophysiological measurements of joint attention–related neural activity.


(3) The Role of Prosody in Sarcasm Comprehension

(Matsui et al., 2016)

Human beings’ pragmatic competence, particularly the ability to understand the unspoken intention, expectation, or feeling of the speaker, may involve the medical prefrontal cortex, right hemisphere, and subcortical regions, in addition to the typical neural substrates for language processing. However, there is no expert consensus about this topic. Prosody (tone of voice) in conversation plays an important role in the expression of sarcasm. As a result of experiments using tasks that involved affective prosody and sarcastic utterance, incongruity between the semantic content of the statement (praise) and negative affective prosody (critical tone of voice) activated the anterior cingulate cortex and bilateral anterior insula, and the left rostro-ventral inferior frontal gyrus (Brodmann area [BA]47) was correlated with sarcasm comprehension. This indicates that BA47, which is involved in semantic processing, participates in integration of discourse context, semantic content of the statement, and affective prosody in the comprehension of sarcasm. The mentalizing network, which is involved in written sarcasm tasks with no auditory input, was not activated during these verbal tasks, suggesting that verbal sarcastic statements are processed by neural substrates other than those involved in mentalizing.


(4) Humor Comprehension

(Nakamura et al., 2017; Sumiya et al., 2017)

From the perspective of clarifying the association between cognitive and affective aspects in human verbal communication, two fMRI studies were carried out to investigate the neural basis for humor comprehension. First, activation of the left amygdala was observed in association with a positive emotional valence in humor processing (Nakamura et al., 2017). This means that the amygdala participates in the evaluation of verbally transmitted affective valence, indicating that the amygdala is the linkage node between cognitive and emotional components. In the other study, the participants’ striatal reward system exhibited greater activation when they elicited positive response (laughter) from the listeners than when others did (Sumiya et al., 2017). In addition, this study demonstrated that activation of the medial prefrontal cortex, which is implicated in self-related processing, modulated the functional connectivity between the auditory cortex and striatum. Detection of contingency between one’s action (telling a funny joke) and the listener’s positive response (laughter) gave rise to subjective pleasure (self-efficacy). These results revealed part of the neural basis for verbally communicated affective valence (self-relevance), suggesting that self-relevance is a major component of the intrinsic reward system that triggers social interactions.


(5) Integration of Affective Social Signals From Others

(Takahashi et al., 2015)

The ability to infer other people’s emotions plays an important role in social life. A fMRI study was conducted to identify the brain regions contributing to the integration of multiple social signals received from another person to infer his or her affective state. Specifically, the brain activities corresponding to their integration and emotional inference were investigated using emotional tears and sad facial images as visual social signals. The results revealed that medial prefrontal cortex and precuneus/posterior cingulate cortex were involved. These regions are the core mentalizing network involved in the theory of mind. This study suggested that these nodes integrate distinct visual social signals to speculate about others’ affective state.


(6) Intrinsic Motivation

(Miura et al., 2017)

When people acknowledge intrinsic value in an action, they find it enjoyable even if it produces no explicit positive consequences. Intrinsic motivation prompts a person to make a particular behavior according to its perceived value. Previous research has suggested that a valuation mechanism within the reward network is responsible for the perception of intrinsic values and external rewards. However, how the intrinsic value of an action is neurally represented remained elusive.

This fMRI study employed a stopwatch game task to test the hypothesis that the intrinsic value of an action is acknowledged when an action–outcome contingency (i.e., operational controllability and feedback) is present. This study administered four versions of the stopwatch game, with or without controllability (presence or absence of the condition where participants could freely manipulate the stopwatch according to their will) and with or without outcome feedback (presence or absence of a signal showing the participants the results of their maneuver). The ventral striatum and midbrain were activated only when action–outcome contingency was present. After the fMRI tasks, a free-choice experiment was administered to explore preference levels for each game. Participants preferred the game with controllability and outcome feedback to other versions (intrinsic motivation). These findings led to the conclusion that the intrinsic value of an action is represented by an increase in ventral striatal and midbrain activation.


(7) Social Interactions and Rewards

(Kawamichi et al., 2016)

Positive social interactions allow individuals to feel that their life is meaningful, motivating them to build social connections according to their personal preferences. This fMRI study was performed to test the hypothesis that social interactions per se activate the reward system. Participants played a virtual ball-toss game in which they received either a similar number of tosses to other players (normal frequency) or a larger number (high frequency). Participants reported greater-than-anticipated enjoyment under the high-frequency condition, and the high-frequency condition strongly activated the ventral striatum, a key node of the reward system. The high-frequency condition also yielded a potent precuneus activation, which was likely to represent positive self-esteem. This study showed that an elevated frequency of positive social interaction represents a social reward.


(8) State Self-Esteem

(Kawamichi et al., 2018)

Self-esteem comprises both enduring personal characteristics (“trait” self-esteem) and short-term variations influenced by others’ appraisal (“state” self-esteem). Previously, the neural substrates underpinning the mechanisms by which others’ appraisal alters the state self-esteem remained unknown. The purpose of this study was to examine the hypothesis that changes in state self-esteem are represented by the mentalizing network, which is modulated by interactions with regions involved in the subjective interpretation of others’ appraisal. For this purpose, task-based and resting-state fMRI measurements were carried out.

Following repeated presentation of their reputations, participants rated their pleasantness and reported their state self-esteem. To evaluate the degree of change in state self-esteem based on pleasantness (i.e., the subjective interpretation of reputation), evaluation sensitivity was defined as the rate of change in state self-esteem per unit pleasantness. Evaluation sensitivity varied across participants, and was positively correlated with precuneus activity evoked by reputation rating. Evaluation sensitivity was positively correlated with functional connectivity between the precuneus and the areas activated by negative reputation, but negatively correlated with functional connectivity between the precuneus and the areas activated by positive reputation. Thus, the precuneus, a key node of the mentalizing system, serves as a gateway for translating the subjective interpretation of reputation into state self-esteem.


(9) Subjective Happiness

(Matsunaga et al., 2016)

Happiness typically involves two dimensions: a short-term, positive affective state (“state” happiness) and a trait-like long-term sense of wellbeing (“trait” happiness). Psychological studies have shown that these two dimensions are interrelated. Individuals with trait happiness are more apt to experience state happiness than those without, and people who experience state happiness more frequently develop higher levels of trait happiness. However, the neural basis for the interrelation between these two dimensions of happiness was unknown. MRI-based functional and structural analyses of the brain showed that trait happiness was positively correlated with the gray matter density of the rostral anterior cingulate cortex (rACC) and the rACC activity was positively correlated with experimentally induced temporal sense of happiness. These results showed that state happiness and trait happiness have a common neural substrate (rACC), which serves as the locus for their interaction.