Interoception is associated with the impact of eye contact on spontaneous facial mimicry.

Interoception (perception of one's own physiological state) has been suggested to underpin social cognition, although the mechanisms underlying this association remain unclear. The current study aimed to elucidate the relationship between interoception and two factors underlying social cognition: self-other boundary and sensitivity to social cues. We measured performance in a heartbeat perception task as an index of interoceptive accuracy (IAc), the frequency of spontaneous facial mimicry (SFM) as an index of self-other boundary, and the degree of the effect of eye contact on SFM (difference in SFM between conditions in which models' eyes were directed to and averted from participants) as an index of social-cue sensitivity, and tested correlations among these measures. The results revealed that IAc and SFM were positively correlated only in the direct gaze condition. The extent of the effect of eye contact on SFM (difference in frequency between direct vs. averted conditions) was positively correlated with IAc. These overall findings were also observed in separate analyses of male and female participant groups, supporting the robustness of the findings. The results suggest that interoception is related to sensitivity to social cues, and may also be related to the self-other boundary with modulation by social context.

Behavioral evidence of delayed prediction signals during agency attribution in patients with schizophrenia.

Self-disturbance, a core feature of schizophrenia, recently has been explained from the standpoint of an abnormal sense of agency (SoA). Previous studies showed that aberrant SoA in schizophrenia arise from imprecise predictions about the sensory consequences of actions. However, the nature of the malfunctioning predictions remains unclear. We examined the temporally "delayed" nature of inadequate predictions. We studied 30 patients with schizophrenia and 30 healthy controls. Our original SoA task evaluates explicit experience of the temporal causal relationship between an intentional action and an effect on a computer screen under the presence of temporal biases. We introduced an adaptation with a "trial-by-trial" method that prolonged or shortened the temporal biases. We hypothesized that delayed prediction signals in schizophrenia could lead to a match in timing between predictions and actual outcomes, resulting in self-agency. The adjustment courses to changing temporal biases were evaluated. Patients with schizophrenia continued to feel self-agency even when the adjusted temporal bias was longer than 1000ms. This result indicated that patient's prediction would be delayed in each trial. Our study empirically showed behavioral evidence for "delayed" prediction signals in a SoA paradigm for the first time.

Mothers' multimodal information processing is modulated by multimodal interactions with their infants.

Social learning in infancy is known to be facilitated by multimodal (e.g., visual, tactile, and verbal) cues provided by caregivers. In parallel with infants' development, recent research has revealed that maternal neural activity is altered through interaction with infants, for instance, to be sensitive to infant-directed speech (IDS). The present study investigated the effect of mother- infant multimodal interaction on maternal neural activity. Event-related potentials (ERPs) of mothers were compared to non-mothers during perception of tactile-related words primed by tactile cues. Only mothers showed ERP modulation when tactile cues were incongruent with the subsequent words, and only when the words were delivered with IDS prosody. Furthermore, the frequency of mothers' use of those words was correlated with the magnitude of ERP differentiation between congruent and incongruent stimuli presentations. These results suggest that mother-infant daily interactions enhance multimodal integration of the maternal brain in parenting contexts.

Neural correlates of error processing reflect individual differences in interoceptive sensitivity.

Although self-monitoring is an important process for adaptive behaviors in multiple domains, the exact relationship among different internal monitoring systems is unclear. Here, we aimed to determine whether and how physiological monitoring (interoception) and behavioral monitoring (error processing) are related to each other. To this end we examined within-subject correlations among measures representing each function. Score on the heartbeat counting task (HCT) was used as a measure of interoceptive awareness. The amplitude of two event-related potentials (error-related negativity [ERN] and error-positivity [Pe]) elicited in error trials of a choice-reaction task (Simon task) were used as measures of error processing. The Simon task presented three types of stimuli (objects, faces showing disgust, and happy faces) to further examine how emotional context might affect inter-domain associations. Results showed that HCT score was robustly correlated with Pe amplitude (the later portion of error-related neural activity), irrespective of stimulus condition. In contrast, HCT score was correlated with ERN amplitude (the early component) only when participants were presented with disgust-faces as stimuli, which may have automatically elicited a physiological response. Behavioral data showed that HCT score was associated with the degree to which reaction times slowed after committing errors in the object condition. Cardiac activity measures indicated that vigilance level would not explain these correlations. These results suggest a relationship between physiological and behavioral monitoring. Furthermore, the degree to which behavioral monitoring relies on physiological monitoring appears to be flexible and depend on the situation.

Neural substrates for judgment of self-agency in ambiguous situations.

The sense of agency is the attribution of oneself as the cause of one's own actions and their effects. Accurate agency judgments are essential for adaptive behaviors in dynamic environments, especially in conditions of uncertainty. However, it is unclear how agency judgments are made in ambiguous situations where self-agency and non-self-agency are both possible. Agency attribution is thus thought to require higher-order neurocognitive processes that integrate several possibilities. Furthermore, neural activity specific to self-attribution, as compared with non-self-attribution, may reflect higher-order critical operations that contribute to constructions of self-consciousness. Based on these assumptions, the present study focused on agency judgments under ambiguous conditions and examined the neural correlates of this operation with functional magnetic resonance imaging. Participants performed a simple but demanding agency-judgment task, which required them to report on whether they attributed their own action as the cause of a visual stimulus change. The temporal discrepancy between the participant's action and the visual events was adaptively set to be maximally ambiguous for each individual on a trial-by-trial basis. Comparison with results for a control condition revealed that the judgment of agency was associated with activity in lateral temporo-parietal areas, medial frontal areas, the dorsolateral prefrontal area, and frontal operculum/insula regions. However, most of these areas did not differentiate between self- and non-self-attribution. Instead, self-attribution was associated with activity in posterior midline areas, including the precuneus and posterior cingulate cortex. These results suggest that deliberate self-attribution of an external event is principally associated with activity in posterior midline structures, which is imperative for self-consciousness.

Brain response to affective pictures in the chimpanzee.

Advancement of non-invasive brain imaging techniques has allowed us to examine details of neural activities involved in affective processing in humans; however, no comparative data are available for chimpanzees, the closest living relatives of humans. In the present study, we measured event-related brain potentials in a fully awake adult chimpanzee as she looked at affective and neutral pictures. The results revealed a differential brain potential appearing 210 ms after presentation of an affective picture, a pattern similar to that in humans. This suggests that at least a part of the affective process is similar between humans and chimpanzees. The results have implications for the evolutionary foundations of emotional phenomena, such as emotional contagion and empathy.

Neural representation of face familiarity in an awake chimpanzee.

Evaluating the familiarity of faces is critical for social animals as it is the basis of individual recognition. In the present study, we examined how face familiarity is reflected in neural activities in our closest living relative, the chimpanzee. Skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of familiar and unfamiliar chimpanzee faces (Experiment 1) and human faces (Experiment 2). The ERPs evoked by chimpanzee faces differentiated unfamiliar individuals from familiar ones around midline areas centered on vertex sites at approximately 200 ms after the stimulus onset. In addition, the ERP response to the image of the subject's own face did not significantly diverge from those evoked by familiar chimpanzees, suggesting that the subject's brain at a minimum remembered the image of her own face. The ERPs evoked by human faces were not influenced by the familiarity of target individuals. These results indicate that chimpanzee neural representations are more sensitive to the familiarity of conspecific than allospecific faces.

How does interoceptive awareness interact with the subjective experience of emotion? An fMRI study.

Recent studies in cognitive neuroscience have suggested that the integration of information about the internal bodily state and the external environment is crucial for the experience of emotion. Extensive overlap between the neural mechanisms underlying the subjective emotion and those involved in interoception (perception of that which is arising from inside the body) has been identified. However, the mechanisms of interaction between the neural substrates of interoception and emotional experience remain unclear. We examined the common and distinct features of the neural activity underlying evaluation of emotional and bodily state using functional magnetic resonance imaging (fMRI). The right anterior insular cortex and ventromedial prefrontal cortex (VMPFC) were identified as commonly activated areas. As both of these areas are considered critical for interoceptive awareness, these results suggest that attending to the bodily state underlies awareness of one's emotional state. Uniquely activated areas involved in the evaluation of emotional state included the temporal pole, posterior and anterior cingulate cortex, medial frontal gyrus, and inferior frontal gyrus. Also the precuneus was functionally associated with activity of the right anterior insular cortex and VMPFC when evaluating emotional state. Our findings indicate that activation in these areas and the precuneus are functionally associated for accessing interoceptive information and underpinning subjective experience of the emotional state. Thus, awareness of one's own emotional state appears to involve the integration of interoceptive information with an interpretation of the current situation.

Event-related potentials in response to subjects' own names: A comparison between humans and a chimpanzee.

The sound of one's own name is one of the most salient auditory environmental stimuli. Several studies of human brain potentials have revealed some characteristic waveforms when we hear our own names. In a recent work, we investigated event-related potentials (ERPs) in a female chimpanzee and demonstrated that the ERP pattern generated when she heard her own name differed from that generated when she heard other sounds. However, her ERPs did not exhibit a prominent positive shift around 300 ms (P3) in response to her own name, as has been repeatedly shown in studies of human ERPs. The present study collected comparative data for adult humans using basically the same procedure as that used in our previous study of the chimpanzee. These results also revealed no prominent P3 to the human subjects' own names. The lack of increased P3 is therefore likely due to our experimental protocol, in which we presented the subject's own name relatively frequently. In contrast, our results revealed prominent negativity to the subject's own name at around 500 ms in the chimpanzee and around 200 ms in human subjects. This may indicate that initial orientation to the sound of one's own name is delayed in the chimpanzee.

Association between interoception and empathy: evidence from heartbeat-evoked brain potential.

Physiological bodily states play an important role in affective experiences. This study investigated whether the neural processing of internal body state (interoception) is associated with empathy, the understanding of the affective states of others. We used the 'heartbeat-evoked potential' (HEP), a surface electroencephalography (EEG) pattern, as a neural index of interoceptive processing. The HEP is contingent on the most prominent peak (R-wave) of the electrocardiogram (ECG) and is thought to reflect cortical processing of cardiac afferent input. Twenty-one healthy adults performed empathy and control tasks while EEG and ECG were recorded, where they made judgments based on either the affective or physical aspects of images of human eyes. HEP, ECG and heart rate in each task block were calculated and compared. Results showed that cardiac activity was not significantly different between tasks. In contrast, HEP showed a significant task difference, exhibited as an increased negativity during the empathy task over frontocentral sites at a latency of approximately 250-430 ms. Furthermore, a self-reported measure of empathy was associated with mean HEP amplitude during the period of task-related differentiation. These results suggest that afferent feedback from visceral activity may contribute to inferences about the affective state of others.

Neural correlates of face and object perception in an awake chimpanzee (Pan troglodytes) examined by scalp-surface event-related potentials.

BACKGROUND: The neural system of our closest living relative, the chimpanzee, is a topic of increasing research interest. However, electrophysiological examinations of neural activity during visual processing in awake chimpanzees are currently lacking. METHODOLOGY/PRINCIPAL FINDINGS: In the present report, skin-surface event-related brain potentials (ERPs) were measured while a fully awake chimpanzee observed photographs of faces and objects in two experiments. In Experiment 1, human faces and stimuli composed of scrambled face images were displayed. In Experiment 2, three types of pictures (faces, flowers, and cars) were presented. The waveforms evoked by face stimuli were distinguished from other stimulus types, as reflected by an enhanced early positivity appearing before 200 ms post stimulus, and an enhanced late negativity after 200 ms, around posterior and occipito-temporal sites. Face-sensitive activity was clearly observed in both experiments. However, in contrast to the robustly observed face-evoked N170 component in humans, we found that faces did not elicit a peak in the latency range of 150-200 ms in either experiment. CONCLUSIONS/SIGNIFICANCE: Although this pilot study examined a single subject and requires further examination, the observed scalp voltage patterns suggest that selective processing of faces in the chimpanzee brain can be detected by recording surface ERPs. In addition, this non-invasive method for examining an awake chimpanzee can be used to extend our knowledge of the characteristics of visual cognition in other primate species.

Brain activity in an awake chimpanzee in response to the sound of her own name.

The brain activity of a fully awake chimpanzee being presented with her name was investigated. Event-related potentials (ERPs) were measured for each of the following auditory stimuli: the vocal sound of the subject's own name (SON), the vocal sound of a familiar name of another group member, the vocal sound of an unfamiliar name and a non-vocal sound. Some differences in ERP waveforms were detected between kinds of stimuli at latencies at which P3 and Nc components are typically observed in humans. Following stimulus onset, an Nc-like negative shift at approximately 500 ms latency was observed, particularly in response to SON. Such specific ERP patterns suggest that the chimpanzee processes her name differently from other sounds.

Whose loss is it? Human electrophysiological correlates of non-self reward processing.

To recognize whether another person's action results in a good or bad outcome is imperative for social learning, as well as for understanding the behavior of others in a broad context. Recent studies have reported that a scalp-surface event-related potential (ERP) called medial-frontal negativity (MFN), considered to be an index of negative reward processing, is generated when perceiving not only one's own losses, but also those of others. This suggests that the same neural mechanisms operate in monitoring one's own actions and in perceiving the consequences of the actions of others. To further elucidate the properties of this "observational" MFN, this study examined whether its amplitude differs with different observational targets. In a gambling task, participants observed the performances of non-self agents: a human friend and PC programs. The outcomes of the decisions of these agents were not associated with the participants' own benefits. ERP results showed that the MFN-like pattern was significantly elicited only when observing the outcomes of decisions made by human agents. Furthermore, self-reported measures of empathy were positively associated with the magnitude of the observational MFN. These findings suggest that the neural activity in non-self reward processing reflects a socioemotional state generated by the target of observation, as well as an empathetic trait of the individual.

Salivary alpha-amylase levels and hyperbolic discounting in male humans.

OBJECTIVE: Little is known regarding the role of the sympathetic-adrenal-medullary (SAM) system in self-control and impulsivity in intertemporal choice (delay discounting), although the roles of dopaminergic and serotonergic systems have been extensively examined. This study was aimed to examine the relationships between salivary alpha-amylase (sAA, a non-invasive biological marker of adrenergic/SAM activities) levels and hyperbolic discounting, which is of interest in psychoneuroendocrinology and neuroeconomics. METHODS: We assessed degrees to which delayed monetary gains were discounted (hyperbolic discount rates) in healthy male students. Participants' sAA were also assessed. RESULTS: We observed negative relationships between sAA and hyperbolic discounting of small, medium, and large monetary gains. CONCLUSIONS: The results indicate that subjects with low sAA are impulsive in intertemporal choice. Implications for the roles of adrenergic and SAM systems in self-control in intertemporal choice are discussed.

Perceiving an opponent's loss: gender-related differences in the medial-frontal negativity.

Along with expanding the understanding of the human 'social brain', a new challenge for neuroscience is to elucidate the nature of individual differences in social competence. Here we report a neural index of gender difference in empathy-related processing in a complex social situation. Using electroencephalography, we measured the neural activity of perceptions to one's own and another's monetary gain or loss, while individuals played a 'competitive' two-person gambling game, in which one's monetary gain resulted in the other's loss. The medial-frontal negativity (MFN), a component within 300 ms latency reflecting an emotional categorization of the event, showed a significant gender difference in perceiving an opponent's, but not a self-performed outcome. When females perceive the opponent's outcomes, the MFN was elicited, indicating that another's loss was categorized as negative, even though it resulted in a benefit to them. On the contrary, the males did not elicit discernable MFN to the opponent's outcomes. Together with the fact that the affect score has a negative linear correlation with the MFN, this indicated that the MFN was sensitive to socio-emotional processing. These results suggest that individual differences in complex social behavior result from rapid neural activity in response to external stimuli.

Active processing of biological motion perception: an ERP study.

The purpose of this study was to measure event-related potentials (ERPs) to clarify how attention affects neural activity during the visual perception of biological motion (BM). Thirteen healthy subjects observed BM or scrambled motion (SM). For SM, each point had the same velocity vector as in BM, but the initial starting positions were randomized. Each BM and SM was overlaid with ten noise dots and four rectangles. For the rectangles, one was or was not rotated 90 degrees relative to the others. Subjects were required to undertake two kinds of visual tasks. For the attention-to-motion condition, subjects directed their attention to the type of motion. For the attention-to-rectangle condition, subjects directed their attention to the rotational angle of the overlaid rectangles. As in our earlier study, the ERP response to the perception of BM had two negative components at approximately 200 ms (N200) and approximately 330 ms (N330) in both attentional conditions. Our analysis focused on the amplitude of the second negative component, which was sensitive to BM. There was a significant interaction between attention and the type of motion regarding the amplitude of N330. Specifically, the amplitude of N330 in response to BM was greater in the attention-to-motion condition than in the attention-to-rectangle condition, and was greater than the amplitude of the response to SM in the attention-to-motion condition. These results suggest that in this experimental design, processing of BM is modulated by attention.

Neural dynamics in human imitation revealed by ERP surface topography.

To clarify the neural dynamics in human motor imitation, we examined event-related potentials (ERP) for a reaction time task that required responses to an actor's finger motions with identical motions. Compared with a control task (reaction to an LED illumination), the ERP surface topography in the imitative reaction was differentiated at around 120-200 ms post-cueing, showing an early sensitivity to the response hand over the pre-central region. This result suggested that activities around the motor areas were facilitated in the imitative reaction, which is consistent with recent neuroimaging studies. However, taken together with that there were no differences in reaction times, the early ERP latency of conditional divergence indicated that neural activities related to imitation are visual responses and do not directly lead to motor acceleration.

An event-related potentials study of biological motion perception in humans.

In order to clarify the neural dynamics involved in the perception of biological motion, we recorded event-related potentials from 12 subjects. The subjects were shown biological motion or scrambled motion as a control stimulus. In the scrambled motion, each point had the same velocity vector as in the biological motion, but the initial starting positions were randomized. The perception of both biological and scrambled motion elicited negative peaks at around 200 (N200) and 240 ms (N240). Furthermore, both negative peaks were significantly larger in the biological motion condition than in the scrambled motion condition over the right occipitotemporal region. In light of previous human neuroimaging studies, we speculate that component N200 is generated near the extrastriate cortex area and N240 is generated from the superior temporal sulcus region.