Differences in the neural networks of thermal sensation with and without evaluation process.

Several neuroimaging studies have analyzed the neural networks involved in thermal sensation. In some of these studies, participants were instructed to evaluate and report the thermal sensation using a point scale, visual analog scale, or other psychophysical rating tool while the imaging data were obtained. Therefore, the imaging data may reflect signals involved in the processes of both sensation and evaluation. The present study aimed to discriminate the neural networks involved in identifying different temperature stimuli and the two different processes by using functional magnetic resonance imaging (fMRI). We applied four different thermal stimuli ("hot," 40C; "warm," 36 °C, "cool," 27 °C; and "cold," 22 °C) to the left forearm using Peltier apparatus. During the stimuli, participants were instructed to either evaluate (evaluation task) or not evaluate (no-evaluation task) and report the thermal sensation. We found brain activation in the medial prefrontal cortex/anterior cingulate gyrus, inferior frontal gyrus, bilateral insula, and posterior parietal cortex during the four thermal stimuli both with and without the evaluation task. Additionally, the stimuli with the evaluation task induced stronger and broader activation, including the right fronto-parietal and anterior insula regions. These results indicate that thermal stimulation activates the common neural networks, independent of the thermal conditions and evaluation process. Moreover, the evaluation process may increase the attention to the thermal stimuli, resulting in the activation of the right lateralized ventral attentional network.

Neural basis for anxiety and anxiety-related physiological responses during a driving situation: an fMRI study.

Although the exteroceptive and interoceptive prediction of a negative event increases a person's anxiety in daily life situations, the relationship between the brain mechanism of anxiety and the anxiety-related autonomic response has not been fully understood. In this functional magnetic resonance imaging (fMRI) study, we examined the neural basis of anxiety and anxiety-related autonomic responses in a daily driving situation. Participants viewed a driving video clip in the first-person perspective. During the video clip, participants were presented with a cue to indicate whether a subsequent crash could occur (attention condition) or not (safe condition). Enhanced activities in the anterior insula, bed nucleus of the stria terminalis, thalamus, and periaqueductal gray, and higher sympathetic nerve responses (pupil dilation and peripheral arterial stiffness) were triggered by the attention condition but not with the safe condition. Autonomic response-related functional connectivity was detected in the visual cortex, cerebellum, brainstem, and MCC/PCC with the right anterior insula and its adjacent regions as seed regions. Thus, the right anterior insula and adjacent regions, in collaboration with other regions play a role in eliciting anxiety based on the prediction of negative events, by mediating anxiety-related autonomic responses according to interoceptive information.

Neural substrates of accurate perception of time duration: A functional magnetic resonance imaging study.

Time duration, an essential feature of the physical world, is perceived and cognitively interpreted subjectively. While this perception is deeply connected with arousal and interoceptive signals, the underlying neural mechanisms remain elusive. As the insula is critical for integrating information from the external world with the organism's inner state, we hypothesized that it might have a central role in the perception of time duration and contribute to its estimation accuracy. We conducted a functional magnetic resonance imaging study with 27 healthy participants performing temporal duration and pitch bisection tasks that used the same stimuli. By comparison with two referents with short and long duration in the time range of 1 s (close to the heart rate period), or low and high pitch, participants had to decide whether target stimuli were closer in duration or pitch to the referent stimuli. The temporal bisection point between short and long duration perception was obtained through a psychometric response curve analysis for each participant. The deviation between the bisection point and the average of reference stimuli durations was used as a marker of duration accuracy. Duration discrimination-specific activation, contrasted to pitch discrimination, was found in the dorsomedial prefrontal cortex, bilateral cerebellum, and right anterior insular cortex (AIC), extending to the inferior frontal gyrus (IFG), inferior parietal lobule, and frontal pole. The activity in the right AIC and IFG was positively correlated with the accuracy of duration discrimination. The right AIC is known to be related to the reproduction of duration, whereas the right IFG is involved in categorical decisions. Thus, the comparison between the referent durations reproduced in the AIC and the target duration may occur in the right IFG. We conclude that the right AIC and IFG contribute to the accurate perception of temporal duration.

Neural substrates for sharing intention in action during face-to-face imitation.

Face-to-face imitation is a unique social interaction wherein a shared action is executed based on the feedback of the partner. Imitation by the partner is the feedback to the imitatee's action, resulting in sharing actions. The neural mechanisms of the shared representation of action during face-to-face imitation, the core of inter-subjectivity, are not well-known. Here, based on the predictive coding account, we hypothesized that the pair-specific forward internal model is the shared representation of action which is represented by the inter-individual synchronization of some portion of the mirror neuron system. Hyperscanning functional magnetic resonance imaging was conducted during face-to-face interaction in 16 pairs of participants who completed an immediate imitation task of facial expressions. Paired participants were alternately assigned to either an imitator or an imitatee who was prompted to express a happy, sad, or non-emotional face. While neural activation elicited by imitating and being imitated were distinct with little overlap, on-line imitative interaction enhanced inter-brain synchronization in the right inferior parietal lobule that correlated with the similarity in facial movement kinematic profile. This finding indicates a critical role of the right inferior parietal lobule in sharing representation of action as a pair-specific forward internal model through imitative interaction.

Cultural influences on neural systems of intergroup emotion perception: An fMRI study.

Cultural factors, such as cultural group membership, have been shown to affect neural bases of face and emotion perception. However, little is known about how cultural factors influence neural processing of emotional faces expressed by in-group and out-group members. In this study, we examined cultural influences on neural activation during the intergroup perception of negative emotional faces. We used functional magnetic resonance imaging to compare neural activation during intergroup emotion processing across cultures in three participants groups; two monocultural groups (i.e. Caucasian-Americans and native Japanese) and a bicultural group (i.e. Japanese-Americans). During scanning, the participants completed an emotional match-to-sample task consisting of negative facial expressions of Japanese and Caucasians. Our results show cultural modulation of neural response in the bilateral amygdala as a function of in-group biases and collectivistic values. Additionally, bicultural Japanese-Americans showed enhanced neural responses in the ventral medial prefrontal and posterior cingulate cortices, which had been related to self-related processing, during the perception of negative facial expression of Japanese. Neural activation in the ventral and posterior cingulate cortices reflected individuals' collectivistic tendencies only in the Japanese-American group, possibly due to greater sensitivity to ingroup biases in bicultural individuals. Our results demonstrate the influence of culture on neural responses during the perception of intergroup emotion from faces.

Cross-cultural similarity in relationship-specific social touching.

Many species use touching for reinforcing social structures, and particularly, non-human primates use social grooming for managing their social networks. However, it is still unclear how social touch contributes to the maintenance and reinforcement of human social networks. Human studies in Western cultures suggest that the body locations where touch is allowed are associated with the strength of the emotional bond between the person touched and the toucher. However, it is unknown to what extent this relationship is culturally universal and generalizes to non-Western cultures. Here, we compared relationship-specific, bodily touch allowance maps across one Western ( N = 386, UK) and one East Asian ( N = 255, Japan) country. In both cultures, the strength of the emotional bond was linearly associated with permissible touch area. However, Western participants experienced social touching as more pleasurable than Asian participants. These results indicate a similarity of emotional bonding via social touch between East Asian and Western cultures.

Assessment of brain mechanisms involved in the processes of thermal sensation, pleasantness/unpleasantness, and evaluation.

The conscious perception of thermal stimuli is divided into two categories: thermal sensation (i.e., discriminative component) and pleasantness/unpleasantness (i.e., hedonic component). There have been very few studies which clearly dissociated the two components. The aim of the present study was 1) to identify brain regions involved in perception of thermal stimuli per se, dissociating those related to the two components, and additionally 2) to examine brain regions of the explicit evaluation processes for the two components. Sixteen participants received local thermal stimuli of either 41.5 °C or 18.0 °C during whole-body thermal stimuli of 47.0 °C, 32.0 °C, or 17.0 °C. The local stimuli were delivered to the right forearm with the Peltier device. The whole-body stimuli delivered through a water-perfusion suit was aimed to modulate thermal pleasantness/unpleasantness to the local stimulus. The local stimulation at the same temperature was conducted five times with 30-s intervals. Brain activation was assessed by functional magnetic resonance imaging (fMRI), and the participants were asked to report their ratings of thermal sensation and pleasantness/unpleasantness following the cessation of each local stimulus. Local thermal stimulation activated specific brain regions such as the anterior cingulate cortex, insula, and inferior parietal lobe, irrespective of the temperature of local and whole-body stimuli; however, no specific activation for hot or cold sensation was observed. Different brain regions were associated with pleasantness and unpleasantness; the caudate nucleus and frontal regions for pleasantness, and the medial frontal and anterior cingulate cortex for unpleasantness. In addition, the explicit evaluation process for the discriminative and hedonic components immediately following the cessation of local stimulus involved different brain regions; the medial prefrontal cortex extending to the anterior cingulate cortex, insula, middle frontal cortex, and parietal lobes during the explicit evaluation of thermal sensation, and the medial prefrontal cortex, posterior cingulate cortex, and inferior parietal lobes during that of pleasantness/unpleasantness.

The role of the amygdala in incongruity resolution: the case of humor comprehension.

A dominant theory of humor comprehension suggests that people understand humor by first perceiving some incongruity in an expression and then resolving it. This is called "the incongruity-resolution theory." Experimental studies have investigated the neural basis of humor comprehension, and multiple neural substrates have been proposed; however, the specific substrate for incongruity resolution is still unknown. The reason may be that the resolution phase, despite its importance in humor comprehension, has not been successfully distinguished from the perception phase because both phases occur almost simultaneously. To reveal the substrate, we conducted a functional magnetic resonance study using 51 healthy participants. We used a humor-producing frame of "Given A, I'd say B, because C" so as to focus on the resolution phase independently by suspending humor processing just after the perception phase. This frame allowed us to separate the two phases. Based on our results, incongruity resolution evoked positive emotion and activated the left amygdala, which is known to be related to positive emotion. On the basis of these findings, we argue that the amygdala plays an important role in humor comprehension, considering its functional role in emotional evaluation, particularly the relevance detection for incoming stimuli.

Neural evidence for the intrinsic value of action as motivation for behavior.

The intrinsic value of an action refers to the inherent sense that experiencing a behavior is enjoyable even if it has no explicit outcome. Previous research has suggested that a common valuation mechanism within the reward network may be responsible for processing the intrinsic value of achieving both the outcome and external rewards. However, how the intrinsic value of action is neurally represented remains unknown. We hypothesized that the intrinsic value of action is determined by an action-outcome contingency indicating the behavior is controllable and that the outcome of the action can be evaluated by this feedback. Consequently, the reward network should be activated, reflecting the generation of the intrinsic value of action. To test this hypothesis, we conducted a functional magnetic resonance imaging (fMRI) investigation of a stopwatch game in which the action-outcome contingency was manipulated. This experiment involved 36 healthy volunteers and four versions of a stopwatch game that manipulated controllability (the feeling that participants were controlling the stopwatch themselves) and outcome (a signal allowing participants to see the result of their action). A free-choice experiment was administered after the fMRI to explore preference levels for each game. The results showed that the stopwatch game with the action-outcome contingency evoked a greater degree of enjoyment because the participants chose this condition over those that lacked such a contingency. The ventral striatum and midbrain were activated only when action-outcome contingency was present. Thus, the intrinsic value of action was represented by an increase in ventral striatal and midbrain activation.

Cultural influences on neural basis of inhibitory control.

Research on neural basis of inhibitory control has been extensively conducted in various parts of the world. It is often implicitly assumed that neural basis of inhibitory control is universally similar across cultures. Here, we investigated the extent to which culture modulated inhibitory-control brain activity at both cultural-group and cultural-value levels of analysis. During fMRI scanning, participants from different cultural groups (including Caucasian-Americans and Japanese-Americans living in the United States and native Japanese living in Japan) performed a Go/No-Go task. They also completed behavioral surveys assessing cultural values of behavioral consistency, or the extent to which one's behaviors in daily life are consistent across situations. Across participants, the Go/No-Go task elicited stronger neural activity in several inhibitory-control areas, such as the inferior frontal gyrus (IFG) and anterior cingulate cortex (ACC). Importantly, at the cultural-group level, we found variation in left IFG (L-IFG) activity that was explained by a cultural region where participants lived in (as opposed to race). Specifically, L-IFG activity was stronger for native Japanese compared to Caucasian- and Japanese-Americans, while there was no systematic difference in L-IFG activity between Japanese- and Caucasian-Americans. At the cultural-value level, we found that participants who valued being "themselves" across situations (i.e., having high endorsement of behavioral consistency) elicited stronger rostral ACC activity during the Go/No-Go task. Altogether, our findings provide novel insight into how culture modulates the neural basis of inhibitory control.

The role of prosody and context in sarcasm comprehension: Behavioral and fMRI evidence.

A hearer's perception of an utterance as sarcastic depends on integration of the heard statement, the discourse context, and the prosody of the utterance, as well as evaluation of the incongruity among these aspects. The effect of prosody in sarcasm comprehension is evident in everyday conversation, but little is known about its underlying mechanism or neural substrates. To elucidate the neural underpinnings of sarcasm comprehension in the auditory modality, we conducted a functional MRI experiment with 21 adult participants. The participants were provided with a short vignette in which a child had done either a good or bad deed, about which a parent made a positive comment. The participants were required to judge the degree of the sarcasm in the parent's positive comment (praise), which was accompanied by either positive or negative affective prosody. The behavioral data revealed that an incongruent combination of utterance and the context (i.e., the parent's positive comment on a bad deed by the child) induced perception of sarcasm. There was a significant interaction between context and prosody: sarcasm perception was enhanced when positive prosody was used in the context of a bad deed or, vice versa, when negative prosody was used in the context of a good deed. The corresponding interaction effect was observed in the rostro-ventral portion of the left inferior frontal gyrus corresponding to Brodmann's Area (BA) 47. Negative prosody incongruent with a positive utterance (praise) activated the bilateral insula extending to the right inferior frontal gyrus, anterior cingulate cortex, and brainstem. Our findings provide evidence that the left inferior frontal gyrus, particularly BA 47, is involved in integration of discourse context and utterance with affective prosody in the comprehension of sarcasm.

Pharmacological and Expectancy Effects of a Low Amount of Alcohol Drinking on Outcome Valuation and Risk Perception in Males and Females.

The high-dose, alcohol-induced influences on risk perception and loss aversion depend on sex. On the other hand, low-dose alcohol has less effect on risky behavior. However, the effect of low-dose alcohol on subjective valuation of gain or loss and also the effect of placebo (expectancy of alcohol) on risk perception have not been fully investigated. We investigated the effects of low-dose alcohol (0.02 g/100 ml blood alcohol concentration) and placebo effects on subjective risk perception and subjective valuation of uncertain gain and loss in females and males. Participants in the control group and the placebo group were served alcohol-free, wine-flavored beverage and participants of alcohol group were served wine (14% alcohol). The placebo group was not informed that the drink was not alcohol but the control group was informed. Then paper-pencil tasks for subjective risk perception and valuation of gain or loss were performed 45 min after drinking the beverage. The participants were asked to draw the line on a 180 mm scale for each question. The placebo effects as well as the low-dose alcohol effects were observed in subjective valuations of gain or loss. Except for effect of beverages, a gender difference was also observed for subjective likelihood. The females estimated a low-probability loss as more likely and estimated a high-probability gain as less likely than did the males. From the Stevens' law fitting analysis, the placebo, not alcohol, significantly induced the psychophysical effect of the subjective valuation of gain or loss. These results indicate that the psychological effects of expectancy of alcohol (placebo) could be a major factor in changing the subjective valuation of gain or loss over the pharmacological effects of a small amount of alcohol (like a glass of wine). Furthermore, these results also indicate that gender differences should be taken into account when investigating pharmacological or psychological effect on decision-making.

Overlapping neural response to the pain or harm of people, animals, and nature.

Interpersonal pain perception is a fundamental and evolutionarily beneficial social process. While critical for navigating the social world, whether or not people rely on similar processes to perceive and respond to the harm of the non-human biological world remains largely unknown. Here we investigate whether neural reactivity toward the suffering of other people is distinct from or overlapping with the neural response to pain and harm inflicted upon non-human entities, specifically animals and nature. We used fMRI to measure neural activity while participants (n=15) perceived and reported how badly they felt for the pain or harm of humans, animals, and nature, relative to neutral situations. Neural regions associated with perceiving the pain of other people (e.g. dorsal anterior cingulate cortex, bilateral anterior insula) were similarly recruited when perceiving and responding to painful scenes across people, animals, and nature. These results suggest that similar brain responses are relied upon when perceiving the harm of social and non-social biological entities, broadly construed, and that activity within the dorsal anterior cingulate cortex and bilateral anterior insula in response to pain-relevant stimuli is not uniquely specific to humans.

Correction: Time Adaptation Shows Duration Selectivity in the Human Parietal Cortex.

[This corrects the article DOI: 10.1371/journal.pbio.1002262.].

Time Adaptation Shows Duration Selectivity in the Human Parietal Cortex.

Although psychological and computational models of time estimation have postulated the existence of neural representations tuned for specific durations, empirical evidence of this notion has been lacking. Here, using a functional magnetic resonance imaging (fMRI) adaptation paradigm, we show that the inferior parietal lobule (IPL) (corresponding to the supramarginal gyrus) exhibited reduction in neural activity due to adaptation when a visual stimulus of the same duration was repeatedly presented. Adaptation was strongest when stimuli of identical durations were repeated, and it gradually decreased as the difference between the reference and test durations increased. This tuning property generalized across a broad range of durations, indicating the presence of general time-representation mechanisms in the IPL. Furthermore, adaptation was observed irrespective of the subject's attention to time. Repetition of a nontemporal aspect of the stimulus (i.e., shape) did not produce neural adaptation in the IPL. These results provide neural evidence for duration-tuned representations in the human brain.

False memory for face in short-term memory and neural activity in human amygdala.

Human memory is often inaccurate. Similar to words and figures, new faces are often recognized as seen or studied items in long- and short-term memory tests; however, the neural mechanisms underlying this false memory remain elusive. In a previous fMRI study using morphed faces and a standard false memory paradigm, we found that there was a U-shaped response curve of the amygdala to old, new, and lure items. This indicates that the amygdala is more active in response to items that are salient (hit and correct rejection) compared to items that are less salient (false alarm), in terms of memory retrieval. In the present fMRI study, we determined whether the false memory for faces occurs within the short-term memory range (a few seconds), and assessed which neural correlates are involved in veridical and illusory memories. Nineteen healthy participants were scanned by 3T MRI during a short-term memory task using morphed faces. The behavioral results indicated that the occurrence of false memories was within the short-term range. We found that the amygdala displayed a U-shaped response curve to memory items, similar to those observed in our previous study. These results suggest that the amygdala plays a common role in both long- and short-term false memory for faces. We made the following conclusions: First, the amygdala is involved in detecting the saliency of items, in addition to fear, and supports goal-oriented behavior by modulating memory. Second, amygdala activity and response time might be related with a subject's response criterion for similar faces.

Cultural modulation of the neural correlates of emotional pain perception: the role of other-focusedness.

Cultures vary in the extent to which they emphasize group members to habitually attend to the needs, perspectives, and internal experiences of others compared to the self. Here we examined the influence that collectivistic and individualistic cultural environments may play on the engagement of the neurobiological processes that underlie the perception and processing of emotional pain. Using cross-cultural fMRI, Korean and Caucasian-American participants passively viewed scenes of others in situations of emotional pain and distress. Regression analyses revealed that the value of other-focusedness was associated with heightened neural response within the affective pain matrix (i.e. anterior cingulate cortex and insula) to a greater extent for Korean relative to Caucasian-American participants. These findings suggest that mindsets promoting attunement to the subjective experience of others may be especially critical for pain-related and potentially empathic processing within collectivistic relative to individualistic cultural environments.

Functional connectivity between amygdala and facial regions involved in recognition of facial threat.

The recognition of threatening faces is important for making social judgments. For example, threatening facial features of defendants could affect the decisions of jurors during a trial. Previous neuroimaging studies using faces of members of the general public have identified a pivotal role of the amygdala in perceiving threat. This functional magnetic resonance imaging study used face photographs of male prisoners who had been convicted of first-degree murder (MUR) as threatening facial stimuli. We compared the subjective ratings of MUR faces with those of control (CON) faces and examined how they were related to brain activation, particularly, the modulation of the functional connectivity between the amygdala and other brain regions. The MUR faces were perceived to be more threatening than the CON faces. The bilateral amygdala was shown to respond to both MUR and CON faces, but subtraction analysis revealed no significant difference between the two. Functional connectivity analysis indicated that the extent of connectivity between the left amygdala and the face-related regions (i.e. the superior temporal sulcus, inferior temporal gyrus and fusiform gyrus) was correlated with the subjective threat rating for the faces. We have demonstrated that the functional connectivity is modulated by vigilance for threatening facial features.

Neuroanatomical substrates involved in true and false memories for face.

We often mistake an unknown person for a familiar person because of the similarities in facial features. This phenomenon, known as false memory, has been investigated mainly using words, pictures, and shapes. Previous neuroimaging studies on false memory have shown that both true and false memories trigger a similar activation in the medial temporal lobe, suggesting that it plays a common role in both. However, no study to date has investigated neural substrates of false memories for faces. In the present fMRI study, we applied a modified version of the standard false memory paradigm, using morphed pictures of faces, to induce false memory in an MRI environment. We found that activity in the amygdala and orbital cortices was associated with the degree of familiarity of items. In particular, false responses to "lure" items evoked a level of activity in the amygdala between that evoked for correct or incorrect responses to "true" items. This indicates a possible role of the amygdala in false memory. A specific region in the anterior cingulate cortex was involved in false recognition; the activity being correlated to reaction times for the response types. These results suggest that the amygdala is involved in determining the relevance of items; therefore, ambiguousness of lure items in terms of familiarity and novelty may be related to decreased activity in the amygdala. The anterior cingulate activity in false memory may be caused not only by increased effort and motor demand but also by higher mnemonic processing of lure items.

Distinct human face representations in the perirhinal cortex and fusiform gyrus.

Face representation, which is believed to be processed in the temporal visual pathway, has been extensively investigated in humans and monkeys through neuroimaging and electroneurophysiology. Lesion studies in monkeys indicate that simple facial features are processed in the caudal regions, and that the combined and integrated features of the face are stored in the perirhinal cortex (PRC). However, this hypothesis still lacks experimental evidence in normal human subjects; therefore, we conducted 2 functional magnetic resonance imaging experiments to investigate whether the function of the PRC differs from that of conventional face-related areas during face recognition tests. In experiment 1, normal subjects learned 6 facial identity-figure associations before scanning, and their brain activity was measured during recognition testing of correct and incorrect face-figure pairs in 3 different angles. The degree of activation in the PRC differed among the facial angles, and activation in response to frontal views was greater than that to other views. In experiment 2, where face angle, but not identity, was paired with an abstract figure, activation was significantly greater in response to the frontal view than that to other views. In contrast, the degree of activation in conventional face-related areas, i.e., the fusiform gyrus, did not differ among viewing angles in both experiments. The results indicate that the function of face representation in the PRC differs from that in the conventional face-related areas, and that a frontal view of the face plays a role in the activation of face representation stored in the PRC.