Hemodynamic and electrophysiological responses of the human amygdala during face imitation-a study using functional MRI and intracranial EEG.

The involvement of the human amygdala in facial mimicry remains a matter of debate. We investigated neural activity in the human amygdala during a task in which an imitation task was separated in time from an observation task involving facial expressions. Neural activity in the amygdala was measured using functional magnetic resonance imaging in 18 healthy individuals and using intracranial electroencephalogram in six medically refractory patients with epilepsy. The results of functional magnetic resonance imaging experiment showed that mimicry of negative and positive expressions activated the amygdala more than mimicry of non-emotional facial movements. In intracranial electroencephalogram experiment and time-frequency analysis, emotion-related activity of the amygdala during mimicry was observed as a significant neural oscillation in the high gamma band range. Furthermore, spectral event analysis of individual trial intracranial electroencephalogram data revealed that sustained oscillation of gamma band activity originated from an increased number and longer duration of neural events in the amygdala. Based on these findings, we conclude that during facial mimicry, visual information of expressions and feedback from facial movements are combined in the amygdalar nuclei. Considering the time difference of information approaching the amygdala, responses to facial movements are likely to modulate rather than initiate affective processing in human participants.

One out of ten independent components shows flipped polarity with poorer data quality: EEG database study.

Independent component analysis (ICA) is widely used today for scalp-recorded EEG analysis. One of the limitations of ICA-based analysis is polarity indeterminacy. It is not easy to find detailed documentations that explains engineering solutions of how the polarity indeterminacy is addressed in a given implementation. We investigated how it is implemented in the case of EEGLAB and also the relation between the outcome of the polarity determination and classification of independent components (ICs) in terms of the estimated nature of the sources (brain, muscle, eye, etc.) using an open database of n = 212 EEG dataset of resting state recordings. We found that (1) about 91% of ICs showed positive-dominant IC scalp topographies; (2) positive-dominant ICs were more associated with brain-originated signals; (3) positive-dominant ICs showed more radial (peaked at 10-30 degrees deviations from the radial axis) dipolar projection pattern with less residual variance from fitting the equivalent current dipole. In conclusion, using the EEGLAB's default ICA algorithm, one out of 10 ICs results in flipping its polarity to negative, which is associated with non-radial dipole orientation with higher residual variance. Thus, we determined EEGLAB biases toward positive polarity in decomposing high-quality brain ICs.

Emotion-related cerebral blood flow changes in the ventral medial prefrontal cortex: An NIRS study.

The current study examined whether cerebral blood flow (CBF) changes in the anterior ventral medial prefrontal cortex (VMPFC) represent responses to emotional stimuli instead of cognitive control of emotion during distraction tasks, as suggested by our previous near-infrared spectroscopy (NIRS) study. The functional distinction of MPFC regions is occasionally difficult due to their multiple functions. Here, we addressed some remaining concerns from our previous distraction studies, and employed the distraction paradigm, in which negative or neutral images are presented as emotional stimuli; a rest period is included in one condition and working memory (distraction) tasks in the other. To extract the components of CBF changes associated with responses to negative emotional stimuli (defined as emotion-related CBF changes), we subtracted the CBF changes obtained in the neutral condition from those in the negative condition. We found that emotion-related CBF changes in the anterior left VMPFC were significantly greater in the rest condition than in the distraction task condition. These findings imply that the distraction task decreased unnecessary brain activities, resulting in decrease in the emotion-related CBF changes. They support our previous findings, indicating that CBF changes in anterior VMPFC regions, measured using NIRS, are specifically associated with responses to emotional stimuli.

Affective auditory stimulus database: An expanded version of the International Affective Digitized Sounds (IADS-E).

Using appropriate stimuli to evoke emotions is especially important for researching emotion. Psychologists have provided several standardized affective stimulus databases-such as the International Affective Picture System (IAPS) and the Nencki Affective Picture System (NAPS) as visual stimulus databases, as well as the International Affective Digitized Sounds (IADS) and the Montreal Affective Voices as auditory stimulus databases for emotional experiments. However, considering the limitations of the existing auditory stimulus database studies, research using auditory stimuli is relatively limited compared with the studies using visual stimuli. First, the number of sample sounds is limited, making it difficult to equate across emotional conditions and semantic categories. Second, some artificially created materials (music or human voice) may fail to accurately drive the intended emotional processes. Our principal aim was to expand existing auditory affective sample database to sufficiently cover natural sounds. We asked 207 participants to rate 935 sounds (including the sounds from the IADS-2) using the Self-Assessment Manikin (SAM) and three basic-emotion rating scales. The results showed that emotions in sounds can be distinguished on the affective rating scales, and the stability of the evaluations of sounds revealed that we have successfully provided a larger corpus of natural, emotionally evocative auditory stimuli, covering a wide range of semantic categories. Our expanded, standardized sound sample database may promote a wide range of research in auditory systems and the possible interactions with other sensory modalities, encouraging direct reliable comparisons of outcomes from different researchers in the field of psychology.

Causal Dynamics of Scalp Electroencephalography Oscillation During the Rubber Hand Illusion.

Rubber hand illusion (RHI) is an important phenomenon for the investigation of body ownership and self/other distinction. The illusion is promoted by the spatial and temporal contingencies of visual inputs near a fake hand and physical touches to the real hand. The neural basis of this phenomenon is not fully understood. We hypothesized that the RHI is associated with a fronto-parietal circuit, and the goal of this study was to determine the dynamics of neural oscillation associated with this phenomenon. We measured electroencephalography while delivering spatially congruent/incongruent visuo-tactile stimulations to fake and real hands. We applied time-frequency analyses and calculated renormalized partial directed coherence (rPDC) to examine cortical dynamics during the bodily illusion. When visuo-tactile stimulation was spatially congruent, and the fake and real hands were aligned, we observed a reduced causal relationship from the medial frontal to the parietal regions with respect to baseline, around 200 ms post-stimulus. This change in rPDC was negatively correlated with a subjective report of the RHI intensity. Moreover, we observed a link between the proprioceptive drift and an increased causal relationship from the parietal cortex to the right somatosensory cortex during a relatively late period (550-750 ms post-stimulus). These findings suggest a two-stage process in which (1) reduced influence from the medial frontal regions over the parietal areas unlocks the mechanisms that preserve body integrity, allowing RHI to emerge; and (2) information processed at the parietal cortex is back-projected to the somatosensory cortex contralateral to the real hand, inducing proprioceptive drift.

Tuning of temporo-occipital activity by frontal oscillations during virtual mirror exposure causes erroneous self-recognition.

Self-face recognition, a hallmark of self-awareness, depends on 'off-line' stored information about one's face and 'on-line' multisensory-motor face-related cues. The brain mechanisms of how on-line sensory-motor processes affect off-line neural self-face representations are unknown. This study used 3D virtual reality to create a 'virtual mirror' in which participants saw an avatar's face moving synchronously with their own face movements. Electroencephalographic (EEG) analysis during virtual mirror exposure revealed mu oscillations in sensory-motor cortex signalling on-line congruency between the avatar's and participants' movements. After such exposure and compatible with a change in their off-line self-face representation, participants were more prone to recognize the avatar's face as their own, and this was also reflected in the activation of face-specific regions in the inferotemporal cortex. Further EEG analysis showed that the on-line sensory-motor effects during virtual mirror exposure caused these off-line visual effects, revealing the brain mechanisms that maintain a coherent self-representation, despite our continuously changing appearance.

Cardiac cycle affects risky decision-making.

This study investigates whether decision-making under uncertainty is influenced by the cardiac cycle. To test this hypothesis, we examined the influence of the cardiac cycle on an individual's decision-making process in a gambling experiment. Participants were asked to choose one option with a sure payout or uncertain option with varying degrees of winning probability, ambiguity, and monetary amounts. The onset of presentation of the options is timed to coincide with either cardiac ventricular systole or diastole. The results show that, for most participants, the risk aversion score was lower in the systole trial than in the diastole trial. Model-based exploratory analysis revealed that the higher propensity to take risks in the systole trial compared with that in the diastole trial could be captured better by the change in the gambling bias against the utility of the risky options, rather than by a change in risk attitude. The results provide evidence that the natural fluctuation of cardiac afferent signals can affect risky decision-making.

Top down influence on visuo-tactile interaction modulates neural oscillatory responses.

Multisensory integration involves bottom-up as well as top-down processes. We investigated the influences of top-down control on the neural responses to multisensory stimulation using EEG recording and time-frequency analyses. Participants were stimulated at the index or thumb of the left hand, using tactile vibrators mounted on a foam cube. Simultaneously they received a visual distractor from a light emitting diode adjacent to the active vibrator (spatially congruent trial) or adjacent to the inactive vibrator (spatially incongruent trial). The task was to respond to the elevation of the tactile stimulus (upper or lower), while ignoring the simultaneous visual distractor. To manipulate top-down control on this multisensory stimulation, the proportion of spatially congruent (vs. incongruent) trials was changed across blocks. Our results reveal that the behavioral cost of responding to incongruent than congruent trials (i.e., the crossmodal congruency effect) was modulated by the proportion of congruent trials. Most importantly, the EEG gamma band response and the gamma-theta coupling were also affected by this modulation of top-down control, whereas the late theta band response related to the congruency effect was not. These findings suggest that gamma band response is more than a marker of multisensory binding, being also sensitive to the correspondence between expected and actual multisensory stimulation. By contrast, theta band response was affected by congruency but appears to be largely immune to stimulation expectancy.

Cardiac Cycle Affects the Asymmetric Value Updating in Instrumental Reward Learning.

This study aimed to investigate whether instrumental reward learning is affected by the cardiac cycle. To this end, we examined the effects of the cardiac cycle (systole or diastole) on the computational processes underlying the participants' choices in the instrumental learning task. In the instrumental learning task, participants were required to select one of two discriminative stimuli (neutral visual stimuli) and immediately receive reward/punishment feedback depending on the probability assigned to the chosen stimuli. To manipulate the cardiac cycle, the presentation of discriminative stimuli was timed to coincide with either cardiac systole or diastole. We fitted the participants' choices in the task with reinforcement learning (RL) models and estimated parameters involving instrumental learning (i.e., learning rate and inverse temperature) separately in the systole and diastole trials. Model-based analysis revealed that the learning rate for positive prediction errors was higher than that for negative prediction errors in the systole trials; however, learning rates did not differ between positive and negative prediction errors in the diastole trials. These results demonstrate that the natural fluctuation of cardiac afferent signals can affect asymmetric value updating in instrumental reward learning.

Virtual reality alters cortical oscillations related to visuo-tactile integration during rubber hand illusion.

Virtual reality (VR) enables the fast, free, and highly controllable setting of experimental body images. Illusions pertaining to a body, such as the rubber hand illusion (RHI), can be easily conducted in VR settings, and some phenomena, such as full-body illusions, are only realized in virtual environments. However, the multisensory-integration process in VR is not yet fully understood. Thus, it remains to be clarified if specific phenomena that occur under VR settings manifest in real life as well. One useful investigative approach is measuring brain activities during a psychological experiment. Electroencephalography (EEG) oscillatory activities provide insight into the human multisensory integration process. Nevertheless, EEG data can be vulnerable to VR noise, which causes measurement and analytical difficulties for EEG data recorded in VR environments. Here, we achieve an experimental RHI setting using a head-mounted display that provides a VR visual space and VR dummy hand along with EEG measurements. We compared EEG data collected in both real and VR environments and observed the gamma and theta band oscillatory activities. Ultimately, we observed statistically significant differences between congruent (RHI) and incongruent (not RHI) conditions in the real environment, which is consistent with previous studies. Differences in the VR condition were observed only on the late theta band oscillation, suggesting that the VR setting itself altered the perceptual and sensory integration mechanisms. Thus, we must model this difference between real and VR settings whenever we use VR to investigate our bodily self-perception.

Modulation of Bodily Self-Consciousness by Self and External Touch.

The full body illusion (FBI) is a bodily illusion based on the application of multisensory conflicts that induce changes in bodily self-consciousness (BSC). This has been used to study cognitive brain mechanisms underlying body ownership and related aspects of self-consciousness. Typically, such paradigms employ external passive multisensory stimulation, thus neglecting the possible contributions of self-generated action and haptic cues to body ownership. In this article, the effects of both external and voluntary self-touch on BSC were examined with a robotics-based FBI paradigm. We compared the effects of classical passive visuotactile stimulation and active self-touch (in which experimental participants had a sense of agency over the tactile stimulation) on the FBI. We evaluated these effects using a questionnaire, crossmodal congruency task, and measurements of changes in self-location. The results indicated that both synchronous passive visuotactile stimulation and synchronous active self-touch induced illusory ownership over a virtual body, without significant differences in their magnitudes. However, the FBI induced by active self-touch was associated with a larger drift in self-location towards the virtual body. These results show that movement-related signals arising from self-touch impact the BSC not only for hand ownership but also for torso-centered body ownership and related aspects of BSC.

Transient neural activation in human amygdala involved in aversive conditioning of face and voice.

Elucidating the neural mechanisms involved in aversive conditioning helps find effective treatments for psychiatric disorders such as anxiety disorder and phobia. Previous studies using fMRI and human subjects have reported that the amygdala plays a role in this phenomenon. However, the noxious stimuli that were used as unconditioned stimuli in previous studies (e.g., electric shock) might have been ecologically invalid because we seldom encounter such stimuli in daily life. Therefore, we investigated whether a face stimulus could be conditioned by using a voice that had negative emotional valence and was collected from a real-life environment. A skin conductance response showed that healthy subjects were conditioned by using these stimuli. In an fMRI study, there was greater amygdala activation in response to the faces that had been paired with the voice than to those that had not. The right amygdala showed transient activity in the early stage of acquisition. A psychophysiological interaction analysis indicated that the subcortical pathway from the medial geniculate body to the amygdala played a role in conditioning. Modulation of the subcortical pathway by voice stimuli preceded the transient activity in the amygdala. The finding that an ecologically valid stimulus elicited the conditioning and amygdala response suggests that our brain is automatically processing unpleasant stimuli in daily life.

EEG evidence of face-specific visual self-representation.

Cognitive science has regarded an individual's face as a form of representative stimuli to engage self-representation. The domain-generality of self-representation has been assumed in several reports, but was recently refuted in a functional magnetic resonance imaging study (Sugiura et al., 2008). The general validity of this study's criticism should be tested by other measures to compensate for the limitation of the time resolution of the blood-oxygen-level-dependent (BOLD) signal. In this article, we report an EEG study on the domain-generality of visual self-representation. Domain-general self-representation was operationally defined as the self-relevance common to one's own Face and Cup; three levels of familiarity, Self, Familiar, and Unfamiliar, were prepared for each. There was another condition, Visual Field, that manipulated visual hemifield during stimulus presentation, but it was collapsed because it produced no interaction with stimulus familiarity. Our results confirmed comparable phase resetting in both domains in response to familiarity manipulation, which occurred within the medial frontal area during 270-390 ms poststimulus and in the theta band. However, self-specific dissociation was observed only for Face. The results here support the conclusion that visual self-representation is domain-specific and that the oscillatory responses observed suggest evidence of face-specific visual self-representation. Results also revealed an inter-trial phase coherency decrease specifically for Self-Face within the right fusiform area during 170-290 ms poststimulus and in the alpha and theta band, suggesting reduced functional demand for Self-Face represented by sharpened networks.

Brain and autonomic association accompanying stochastic decision-making.

To examine the functional association between brain and autonomic activities accompanying decision-making, we simultaneously recorded regional cerebral blood flow using (15)O-water positron emission tomography and event-related brain potentials (ERPs) time-locked to feedback of reward and punishment, as well as cardiovascular parameters, during a stochastic decision-making task. We manipulated the uncertainty of outcomes in the task; specifically, we compared a condition with high predictability of reward/punishment (contingent-reward condition) and a condition with low predictability of reward/punishment (random-reward condition). The anterior cingulate cortex (ACC) was commonly activated in both conditions. Compared with the contingent-reward condition, the orbitofrontal and right dorsolateral prefrontal cortices and dorsal striatum were activated in the random-reward condition, where subjects had to continue to seek contingency between stimuli and reward/punishment. Activation of these brain regions correlated with a positive component of ERPs locked to feedback signals (feedback-related positivity), which showed an association with behavioral decision-making in the contingent-reward condition. Furthermore, cardiovascular responses were attenuated in the random-reward condition, where continuous attention and contingency monitoring were needed, and such attenuation of cardiovascular responses was mediated by vagal activity that was governed by the rostral ACC. These findings suggest that the prefrontal-striatal network provides a neural basis for decision-making and modulation over the peripheral autonomic activity accompanying decision-making.

Corrigendum: The Shape of Water Stream Induces Differences in P300 and Alpha Oscillation.

[This corrects the article DOI: 10.3389/fnhum.2019.00460.].

Quantification of anticipation of excitement with a three-axial model of emotion with EEG.

OBJECTIVE: Multiple facets of human emotion underlie diverse and sparse neural mechanisms. Among the many existing models of emotion, the two-dimensional circumplex model of emotion is an important theory. The use of the circumplex model allows us to model variable aspects of emotion; however, such momentary expressions of one's internal mental state still lacks a notion of the third dimension of time. Here, we report an exploratory attempt to build a three-axis model of human emotion to model our sense of anticipatory excitement, 'Waku-Waku' (in Japanese), in which people predictively code upcoming emotional events. APPROACH: Electroencephalography (EEG) data were recorded from 28 young adult participants while they mentalized upcoming emotional pictures. Three auditory tones were used as indicative cues, predicting the likelihood of the valence of an upcoming picture: positive, negative, or unknown. While seeing an image, the participants judged its emotional valence during the task and subsequently rated their subjective experiences on valence, arousal, expectation, and Waku-Waku immediately after the experiment. The collected EEG data were then analyzed to identify contributory neural signatures for each of the three axes. MAIN RESULTS: A three-axis model was built to quantify Waku-Waku. As expected, this model revealed the considerable contribution of the third dimension over the classical two-dimensional model. Distinctive EEG components were identified. Furthermore, a novel brain-emotion interface was proposed and validated within the scope of limitations. SIGNIFICANCE: The proposed notion may shed new light on the theories of emotion and support multiplex dimensions of emotion. With the introduction of the cognitive domain for a brain-computer interface, we propose a novel brain-emotion interface. Limitations of the study and potential applications of this interface are discussed.

Polymorphism of the serotonin transporter gene modulates brain and physiological responses to acute stress in Japanese men.

A short (S) variant, compared to a long (L) variant, of the promoter region of the serotonin transporter gene-linked polymorphic region (5HTTLPR) has been related to emotional hyper-reactivity. We tested whether the 5HTTLPR could modulate acute stress responses in the brain and, the cardiovascular and neuroendocrine systems. Ten Japanese male participants carrying double copies of the S alleles and 10 Japanese males carrying S and L alleles conducted a mental arithmetic task, and their regional cerebral blood flow by (15)O positron emission tomography and cardiovascular and neuroendocrine parameters were measured. During the acute stress task, the participants with the SS alleles showed stronger reactivity in blood pressure and secretion of epinephrine, compared to the participants with the SL and LL alleles. Furthermore, the SS carriers showed greater activation in stress-related brain regions such as the hypothalamus, cerebellum, midbrain, and pulvinar compared to the SL and LL carriers during the acute stress task. The present findings indicated that the S allele of the 5HTTLPR is associated with greater brain and physiological reactivity to acute stress in Japanese men.

The role of gamma band oscillations and synchrony on rubber hand illusion and crossmodal integration.

The rubber hand illusion represents an illusory experience during the mislocalization of own hand when correlated visuotactile stimuli are presented to the actual and fake hands. The visuotactile integration process appears to cause this illusion; the corresponding brain activity was revealed in many studies. In this study, we investigated the effect of the rubber hand illusion on the crossmodal integration process by measuring EEG. The participants who experienced less intensive illusion showed greater congruency effect on reaction time (RT), greater power increase at the parietal zero electrode (Pz) and smaller interelectrode synchrony of the gamma band activity. On the other hand, the participants who experienced more intense illusion showed greater interelectrode synchrony. The results suggested that the gamma band activity in the parietal area reflects the visuotactile integration process and that its synchrony causes the illusory intensity.

The Shape of Water Stream Induces Differences in P300 and Alpha Oscillation.

Touching is a fundamental human behavior used to evaluate objects in the external world. Many previous studies have used tactile stimulation to conduct psychological and psychophysiological experiments. However, most of these studies used solid material, not water stream, as an experimental stimulus. To investigate water perception, or to easily control the temperature of an experimental stimulus, it is important to be able to control the water stimulus. In this study, we investigated the usability of water as an experimental stimulus for electroencephalography (EEG) experiments and report the basic EEG response to water stimulus. We developed a tactile stimulation device using a water stream to study EEG responses, with the ability to control the stimulus onset timing. As stimuli, we selected two types of water stream, normal and soft, based on a psychological experiment to confirm a difference of subjective feeling induced by these water streams. We conducted a typical oddball task using the two different water streams and recorded EEG waveforms from 64 electrodes while participants touched the water streams. We calculated P300 at the Pz electrode, alpha asymmetry at the frontal electrodes, and alpha suppression at the parietal area. As a result, we observed typical P300 differentiation based on the stimulus proportion (target 20% and standard 80%). We observed a weaker alpha suppression when participants touched the soft water stream compared to the normal shower. These results demonstrate the usability of water stream in psychophysiological studies and suggested that alpha suppression could be a candidate to evaluate comfort of water stream.

Controlled emotional tactile stimulation during functional magnetic resonance imaging and electroencephalography.

BACKGROUND: Tactile stimulation used to induce emotional responses is often not well-controlled. Replicating the same tactile stimulations across studies is difficult, compared to replicating visual and auditory modalities, which have standardized stimulus sets. Standardizing a stimulation method by replicating stimuli across studies is necessary to further elucidate emotional responses in neuroscience research using tactile stimulation. THE NEW METHOD: We developed a tactile stimulation device. The device's ultrasonic motor and optical force sensor have the following criteria: (1) controls the physical property of stimuli, pressure, and stroking speed; (2) measures actual touch timing; (3) is safe to use in a magnetic resonance imaging (MRI) scanner; and (4) produces low noise in electroencephalography (EEG) and MRI. RESULTS: The noise level of the device's drive was sufficiently low. For the EEG experiment, we successfully used signal processing to diminish the commercial power supply noise. For functional MRI (fMRI) scans, we found <5% signal loss occurred during device rotation. COMPARISON WITH EXISTING METHOD(S): We found no previous report about the noise level of a tactile stimulation device used to induce emotional responses during EEG and fMRI recordings. The signal loss rate was comparable with that of other robotic devices used in MRI scanners. Emotional feelings induced by this stimulation method were comparable with those elicited in other sensory modalities. CONCLUSIONS: The developed device could be used for cognitive-affective neuroscience research when conducting EEG and fMRI scans. The device should aid in standardizing affective tactile stimulation for research in psychology and cognitive neuroscience.