Coexistence of sensory qualities and value representations in human orbitofrontal cortex.

Despite the multiple regions and neural networks associated with value-based decision-making, the orbitofrontal cortex (OFC) is possible a particularly important one. Although the role of the OFC in reinforcer devaluation tasks, which assess the ability to represent identity, sensory qualities, and subjective values of the expected outcomes, has been established, the specific aspect represented in this area remains unclear. In this study, using functional magnetic resonance imaging, wherein participants rated the palatability of 128 food items using photographs, we investigated whether the human OFC represents object identity, sensory qualities, or value. Employing many items helped us dissociate object identity from sensory qualities and values; the inferred sensory qualities of identical items were manipulated by a change in metabolic state. Moreover, value differences between items were analytically controlled by employing a technique similar to age adjustment. The palatability ratings for food items significantly decreased after a meal. Using representational similarity analysis, we confirmed that the OFC represents value. Moreover, identical items were represented similarly in the lateral OFC in a given metabolic state; however, these representations were altered post-feeding. Importantly, this change was not explained by subjective value, suggesting that the OFC represents sensory quality and value, but not object identity.

Frequency-specific task modulation of human brain functional networks: A fast fMRI study.

How coherent neural oscillations are involved in task execution is a fundamental question in neuroscience. Although several electrophysiological studies have tackled this issue, the brain-wide task modulation of neural coherence remains uncharacterized. Here, with a fast fMRI technique, we studied shifts of brain-wide neural coherence across different task states in the ultraslow frequency range (0.01-0.7 Hz). First, we examined whether the shifts of the brain-wide neural coherence occur in a frequency-dependent manner. We quantified the shift of a region's average neural coherence by the inter-state variance of the mean coherence between the region and the rest of the brain. A clustering analysis based on the variance's spatial correlation between frequency components revealed four frequency bands (0.01-0.15 Hz, 0.15-0.37 Hz, 0.37-0.53 Hz, and 0.53-0.7 Hz) showing band-specific shifts of the brain-wide neural coherence. Next, we investigated the similarity of the inter-state variance's spectra between all pairs of regions. We found that regions showing similar spectra correspond to those forming functional modules of the brain network. Then, we investigated the relationship between identified frequency bands and modules' inter-state variances. We found that modules showing the highest variance are those made up of parieto-occipital regions at 0.01-0.15 Hz, while it is replaced with another consisting of frontal regions above 0.15 Hz. Furthermore, these modules showed specific shifting patterns of the mean coherence across states at 0.01-0.15 Hz and above 0.15 Hz, suggesting that identified frequency bands differentially contribute to neural interactions during task execution. Our results highlight that usage of the fast fMRI enables brain-wide investigation of neural coherence up to 0.7 Hz, which opens a promising track for assessment of the large-scale neural interactions in the ultraslow frequency range.

Role of the right anterior insular cortex in joint attention-related identification with a partner.

Understanding others as intentional agents is critical in social interactions. We perceive others' intentions through identification, a categorical judgment that others should work like oneself. The most primitive form of understanding others' intentions is joint attention (JA). During JA, an initiator selects a shared object through gaze (initiative joint attention, IJA), and the responder follows the direction of the initiator's gaze (reactive joint attention, RJA). Therefore, both participants share the intention of object selection. However, the neural underpinning of shared intention through JA remains unknown. In this study, we hypothesized that JA is represented by inter-individual neural synchronization of the intention-related activity. Additionally, JA requires eye contact that activates the limbic mirror system; therefore, we hypothesized that this system is involved in shared attention through JA. To test these hypotheses, participants underwent hyperscanning fMRI while performing JA tasks. We found that IJA-related activation of the right anterior insular cortex of participants was positively correlated with RJA-related activation of homologous regions in their partners. This area was activated by volitional selection of the target during IJA. Therefore, identification with others by JA is likely accomplished by the shared intentionality of target selection represented by inter-individual synchronization of the right anterior insular cortex.

Brain networks underlying conscious tactile perception of textures as revealed using the velvet hand illusion.

Humans are adept at perceiving textures through touch. Previous neuroimaging studies have identified a distributed network of brain regions involved in the tactile perception of texture. However, it remains unclear how nodes in this network contribute to the tactile awareness of texture. To examine the hypothesis that such awareness involves the interaction of the primary somatosensory cortex with higher order cortices, we conducted a functional magnetic resonance imaging (fMRI) study utilizing the velvet hand illusion, in which an illusory velvet-like surface is perceived between the hands. Healthy participants were subjected to a strong illusion, a weak illusion, and tactile perception of real velvet. The strong illusion induced greater activation in the primary somatosensory cortex (S1) than the weak illusion, and increases in such activation were positively correlated with the strength of the illusion. Furthermore, both actual and illusory perception of velvet induced common activation in S1. Psychophysiological interaction (PPI) analysis revealed that the strength of the illusion modulated the functional connectivity of S1 with each of the following regions: the parietal operculum, superior parietal lobule, precentral gyrus, insula, and cerebellum. The present results indicate that S1 is associated with the conscious tactile perception of textures, which may be achieved via interactions with higher order somatosensory areas.

Qualitative differences in offline improvement of procedural memory by daytime napping and overnight sleep: An fMRI study.

Daytime napping offers various benefits for healthy adults, including enhancement of motor skill learning. It remains controversial whether napping can provide the same enhancement as overnight sleep, and if so, whether the same neural underpinning is recruited. To investigate this issue, we conducted functional MRI during motor skill learning, before and after a short day-nap, in 13 participants, and compared them with a larger group (n=47) who were tested following regular overnight sleep. Training in a sequential finger-tapping task required participants to press a keyboard in the MRI scanner with their non-dominant left hand as quickly and accurately as possible. The nap group slept for 60min in the scanner after the training run, and the previously trained skill was subsequently re-tested. The whole-night sleep group went home after the training, and was tested the next day. Offline improvement of speed was observed in both groups, whereas accuracy was significantly improved only in the whole-night sleep group. Correspondingly, the offline increment in task-related activation was significant in the putamen of the whole-night group. This finding reveals a qualitative difference in the offline improvement effect between daytime napping and overnight sleep.

Structural and functional associations of the rostral anterior cingulate cortex with subjective happiness.

Happiness is one of the most fundamental human goals, which has led researchers to examine the source of individual happiness. Happiness has usually been discussed regarding two aspects (a temporary positive emotion and a trait-like long-term sense of being happy) that are interrelated; for example, individuals with a high level of trait-like subjective happiness tend to rate events as more pleasant. In this study, we hypothesized that the interaction between the two aspects of happiness could be explained by the interaction between structure and function in certain brain regions. Thus, we first assessed the association between gray matter density (GMD) of healthy participants and trait-like subjective happiness using voxel-based morphometry (VBM). Further, to assess the association between the GMD and brain function, we conducted functional magnetic resonance imaging (MRI) using the task of positive emotion induction (imagination of several emotional life events). VBM indicated that the subjective happiness was positively correlated with the GMD of the rostral anterior cingulate cortex (rACC). Functional MRI demonstrated that experimentally induced temporal happy feelings were positively correlated with subjective happiness level and rACC activity. The rACC response to positive events was also positively correlated with its GMD. These results provide convergent structural and functional evidence that the rACC is related to happiness and suggest that the interaction between structure and function in the rACC may explain the trait-state interaction in happiness.

Neural substrates of shared attention as social memory: A hyperscanning functional magnetic resonance imaging study.

During a dyadic social interaction, two individuals can share visual attention through gaze, directed to each other (mutual gaze) or to a third person or an object (joint attention). Shared attention is fundamental to dyadic face-to-face interaction, but how attention is shared, retained, and neutrally represented in a pair-specific manner has not been well studied. Here, we conducted a two-day hyperscanning functional magnetic resonance imaging study in which pairs of participants performed a real-time mutual gaze task followed by a joint attention task on the first day, and mutual gaze tasks several days later. The joint attention task enhanced eye-blink synchronization, which is believed to be a behavioral index of shared attention. When the same participant pairs underwent mutual gaze without joint attention on the second day, enhanced eye-blink synchronization persisted, and this was positively correlated with inter-individual neural synchronization within the right inferior frontal gyrus. Neural synchronization was also positively correlated with enhanced eye-blink synchronization during the previous joint attention task session. Consistent with the Hebbian association hypothesis, the right inferior frontal gyrus had been activated both by initiating and responding to joint attention. These results indicate that shared attention is represented and retained by pair-specific neural synchronization that cannot be reduced to the individual level.

Unintentional Interpersonal Synchronization Represented as a Reciprocal Visuo-Postural Feedback System: A Multivariate Autoregressive Modeling Approach.

People's behaviors synchronize. It is difficult, however, to determine whether synchronized behaviors occur in a mutual direction--two individuals influencing one another--or in one direction--one individual leading the other, and what the underlying mechanism for synchronization is. To answer these questions, we hypothesized a non-leader-follower postural sway synchronization, caused by a reciprocal visuo-postural feedback system operating on pairs of individuals, and tested that hypothesis both experimentally and via simulation. In the behavioral experiment, 22 participant pairs stood face to face either 20 or 70 cm away from each other wearing glasses with or without vision blocking lenses. The existence and direction of visual information exchanged between pairs of participants were systematically manipulated. The time series data for the postural sway of these pairs were recorded and analyzed with cross correlation and causality. Results of cross correlation showed that postural sway of paired participants was synchronized, with a shorter time lag when participant pairs could see one another's head motion than when one of the participants was blindfolded. In addition, there was less of a time lag in the observed synchronization when the distance between participant pairs was smaller. As for the causality analysis, noise contribution ratio (NCR), the measure of influence using a multivariate autoregressive model, was also computed to identify the degree to which one's postural sway is explained by that of the other's and how visual information (sighted vs. blindfolded) interacts with paired participants' postural sway. It was found that for synchronization to take place, it is crucial that paired participants be sighted and exert equal influence on one another by simultaneously exchanging visual information. Furthermore, a simulation for the proposed system with a wider range of visual input showed a pattern of results similar to the behavioral results.

Brain networks of affective mentalizing revealed by the tear effect: The integrative role of the medial prefrontal cortex and precuneus.

Affective mentalizing involves the integration of various social signals in order to infer the affective states of others. Previous neuroimaging studies have shown that the medial prefrontal cortex, the precuneus/posterior cingulate cortex, and the temporo-parietal junction constitute the core affective mentalizing network. However, the relative contributions of these regions to affective mentalizing remain unclear. We used functional magnetic resonance imaging to investigate which of these nodes are involved in the integration of two social signals: emotional tears and facial expressions. We assumed that this integration would produce a supra-additive effect, indicated by greater activity than the sum of the effects of the individual social signals. Female subjects rated the sadness of faces with either tears or tear-like circles, and either sad or neutral expressions. We observed the supra-additive effect in the medial prefrontal cortex and precuneus/posterior cingulate cortex but not in the temporo-parietal junction. These results indicate that the medial prefrontal cortex and precuneus/posterior cingulate cortex play an important role in integrating tears and facial expressions during affective mentalizing.

Interpersonal touch suppresses visual processing of aversive stimuli.

Social contact is essential for survival in human society. A previous study demonstrated that interpersonal contact alleviates pain-related distress by suppressing the activity of its underlying neural network. One explanation for this is that attention is shifted from the cause of distress to interpersonal contact. To test this hypothesis, we conducted a functional MRI (fMRI) study wherein eight pairs of close female friends rated the aversiveness of aversive and non-aversive visual stimuli under two conditions: joining hands either with a rubber model (rubber-hand condition) or with a close friend (human-hand condition). Subsequently, participants rated the overall comfortableness of each condition. The rating result after fMRI indicated that participants experienced greater comfortableness during the human-hand compared to the rubber-hand condition, whereas aversiveness ratings during fMRI were comparable across conditions. The fMRI results showed that the two conditions commonly produced aversive-related activation in both sides of the visual cortex (including V1, V2, and V5). An interaction between aversiveness and hand type showed rubber-hand-specific activation for (aversive > non-aversive) in other visual areas (including V1, V2, V3, and V4v). The effect of interpersonal contact on the processing of aversive stimuli was negatively correlated with the increment of attentional focus to aversiveness measured by a pain-catastrophizing scale. These results suggest that interpersonal touch suppresses the processing of aversive visual stimuli in the occipital cortex. This effect covaried with aversiveness-insensitivity, such that aversive-insensitive individuals might require a lesser degree of attentional capture to aversive-stimulus processing. As joining hands did not influence the subjective ratings of aversiveness, interpersonal touch may operate by redirecting excessive attention away from aversive characteristics of the stimuli.

Medial prefrontal cortex activation is commonly invoked by reputation of self and romantic partners.

The reputation of others influences partner selection in human cooperative behaviors through verbal reputation representation. Although the way in which humans represent the verbal reputations of others is a pivotal issue for social neuroscience, the neural correlates underlying the representation of verbal reputations of others are unclear. Humans primarily depend on self-evaluation when assessing reputation of self. Likewise, humans might primarily depend on self-evaluation of others when representing their reputation. As interaction promotes the formation of more nuanced, individualized impressions of an interaction partner, humans tend to form self-evaluations of persons with whom they are intimate in their daily life. Thus, we hypothesized that the representation of reputation of others is modulated by intimacy due to one's own evaluation formation of that person. To test this hypothesis, we conducted a functional magnetic resonance imaging experiment with 11 pairs of romantic partners while they viewed an evaluation of a target person (self, partner [intimate other], or stranger [non-intimate other]), made by other evaluators. When compared with strangers, viewing evaluations of self and partner activated overlapping regions in the medial prefrontal cortex. Verbal reputation of self-specific activation was found in the precuneus, which represents self-related processing. The data suggest that midline structures represent reputation of self. In addition, intimacy-modulated activation in the medial prefrontal cortex suggests that the verbal reputation of intimate others is represented similarly to reputation of self. These results suggest that the reputation representation in the medial prefrontal cortex is engaged by verbal reputation of self and intimate others stemming from both own and other evaluators' judgments.

Activation of the reward system during sympathetic concern is mediated by two types of empathy in a familiarity-dependent manner.

Humans work to improve the situation of others through sympathetic concern. The empathic joy hypothesis proposes that the urge to help is stimulated by enhanced sensitivity to vicarious joy achieved through helping a recipient to meet their needs. We further hypothesized that the positive feeling-related brain activation that occurs in the striatum during sympathetic concern is enhanced by empathy in a familiarity-dependent manner. To test this, we conducted behavioral and functional magnetic resonance imaging experiments in which two participants simultaneously played a virtual ball-toss game where either the subjects' partner or an unfamiliar player was isolated by the other players. The subjects showed sympathetic behavior by tossing the ball to the isolated player and reported enhancement of self-positive feelings and anticipation of feeling improvements of the isolated player during sympathetic behaviors. Activation in the bilateral dorsal striatum became more prominent during the behaviors, supporting the empathic joy hypothesis. Dorsal striatal activity when helping a romantic partner positively correlated with affective empathic traits toward that partner, whereas the activity measured when helping a stranger positively correlated with perspective-taking traits. The correlation results further revealed a familiarity-dependent empathic enhancement of positive feelings. Therefore, sympathetic concern is invoked through empathic positive feeling.