Hirokata Fukushima

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 ones 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 ones own emotional state appears to involve the integration of interoceptive information with an interpretation of the current situation. Hum Brain Mapp, 2013.

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.

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

Abstract To recognize whether another persons 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 ones own losses, but also those of others. This suggests that the same neural mechanisms operate in monitoring ones 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.

Auditory ERPs to Stimulus Deviance in an Awake Chimpanzee ( Pan troglodytes ): Towards Hominid Cognitive Neurosciences

Background For decades, the chimpanzee, phylogenetically closest to humans, has been analyzed intensively in comparative cognitive studies. Other than the accumulation of behavioral data, the neural basis for cognitive processing in the chimpanzee remains to be clarified. To increase our knowledge on the evolutionary and neural basis of human cognition, comparative neurophysiological studies exploring endogenous neural activities in the awake state are needed. However, to date, such studies have rarely been reported in non-human hominid species, due to the practical difficulties in conducting non-invasive measurements on awake individuals. Methodology/Principal Findings We measured auditory event-related potentials (ERPs) of a fully awake chimpanzee, with reference to a well-documented component of human studies, namely mismatch negativity (MMN). In response to infrequent, deviant tones that were delivered in a uniform sound stream, a comparable ERP component could be detected as negative deflections in early latencies. Conclusions/Significance The present study reports the MMN-like component in a chimpanzee for the first time. In human studies, various ERP components, including MMN, are well-documented indicators of cognitive and neural processing. The results of the present study validate the use of non-invasive ERP measurements for studies on cognitive and neural processing in chimpanzees, and open the way for future studies comparing endogenous neural activities between humans and chimpanzees. This signifies an essential step in hominid cognitive neurosciences.

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 subjects 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.

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 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 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.

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.

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.