Interoceptive rhythms in the brain.

Sensing internal bodily signals, or interoception, is fundamental to maintain life. However, interoception should not be viewed as an isolated domain, as it interacts with exteroception, cognition and action to ensure the integrity of the organism. Focusing on cardiac, respiratory and gastric rhythms, we review evidence that interoception is anatomically and functionally intertwined with the processing of signals from the external environment. Interactions arise at all stages, from the peripheral transduction of interoceptive signals to sensory processing and cortical integration, in a network that extends beyond core interoceptive regions. Interoceptive rhythms contribute to functions ranging from perceptual detection up to sense of self, or conversely compete with external inputs. Renewed interest in interoception revives long-standing issues on how the brain integrates and coordinates information in distributed regions, by means of oscillatory synchrony, predictive coding or multisensory integration. Considering interoception and exteroception in the same framework paves the way for biological modes of information processing specific to living organisms.

Piecing together the puzzle of emotional consciousness.

The search for neural correlates of emotional consciousness has gained momentum in the last decades. Nonetheless, disagreements concerning the mechanisms that determine the experiential qualities of emotional consciousness-the "what is it like" to feel an emotion-as well as on their neural correlates have far-reaching consequences on how researchers study and measure emotion, sometimes leading to seemingly irresolvable impasses. The current paper lays out in a balanced way the viewpoint of both cognitive and precognitive approaches to emotional consciousness on the basis of commonalities and differences between the claims of some relevant theories of emotions. We examine the sufficiency of the existing evidence in support of the proposed theories of emotional consciousness by going through the methodological specificity of the study of emotional consciousness and its unique challenges and highlighting what can and cannot be imported by advances in research on perceptual consciousness. We propose that there are three key experimental contrasts that are each equally necessary in the search for the neural correlates of emotional consciousness and each contrast alone coming with its own limitations. We conclude by acknowledging some of the most promising avenues in the field, which may help go beyond the current limitations and collaboratively piece together the puzzle of emotional consciousness.

Whose emotion is it? Perspective matters to understand brain-body interactions in emotions.

Feeling happy, or judging whether someone else is feeling happy are two distinct facets of emotions that nevertheless rely on similar physiological and neural activity. Differentiating between these two states, also called Self/Other distinction, is an essential aspect of empathy, but how exactly is it implemented? In non-emotional cognition, the transient neural response evoked at each heartbeat, or heartbeat evoked response (HER), indexes the self and signals Self/Other distinction. Here, using electroencephalography (n = 32), we probe whether HERs' role in Self/Other distinction extends also to emotion - a domain where brain-body interactions are particularly relevant. We asked participants to rate independently validated affective scenes, reporting either their own emotion (Self) or the emotion expressed by people in the scene (Other). During the visual cue indicating to adopt the Self or Other perspective, before the affective scene, HERs distinguished between the two conditions, in visual cortices as well as in the right frontal operculum. Physiological reactivity (facial electromyogram, skin conductance, heart rate) during affective scene co-varied as expected with valence and arousal ratings, but also with the Self- or Other- perspective adopted. Finally, HERs contributed to the subjective experience of valence in the Self condition, in addition to and independently from physiological reactivity. We thus show that HERs represent a trans-domain marker of Self/Other distinction, here specifically contributing to experienced valence. We propose that HERs represent a form of evidence related to the 'I' part of the judgement 'To which extent do I feel happy'. The 'I' related evidence would be combined with the affective evidence collected during affective scene presentation, accounting at least partly for the difference between feeling an emotion and identifying it in someone else.

Reduced Fading of Visual Afterimages after Transcranial Magnetic Stimulation over Early Visual Cortex.

In the complete absence of small transients in visual inputs (e.g., by experimentally stabilizing an image on the retina or in everyday life during intent staring), information perceived by the eyes will fade from the perceptual experience. Although the mechanisms of visual fading remain poorly understood, one possibility is that higher level brain regions actively suppress the stable visual signals via targeted feedback onto early visual cortex (EVC). Here, we used positive afterimages and multisensory conflict to induce gestalt-like fading of participants' own hands. In two separate experiments, participants rated the perceived quality of their hands both before and after transcranial magnetic stimulation (TMS) was applied over EVC. In a first experiment, triple-pulse TMS was able to make a faded hand appear less faded after the pulses were applied, compared with placebo pulses. A second experiment demonstrated that this was because triple-pulse TMS slowed down fading of the removed hand that otherwise occurs naturally over time. Interestingly, TMS similarly affected the left and right hands, despite being applied only over the right EVC. Together, our results suggest that TMS over EVC attenuates the effects of visual fading in positive afterimages, and it might do so by crossing transcollosal connections or via multimodal integration sites in which both hands are represented.

Influence of continuous flash suppression mask frequency on stimulus visibility.

The continuous flash suppression (CFS) paradigm is increasingly used in consciousness research, but its mechanisms are still not fully understood. To better understand its temporal properties, we presented the CFS masks at 9 frequencies, and examined their influence on stimuli visibility, while taking into account the inter-individual variability and the change of CFS suppression as the experiment progressed. The frequencies consisted of fundamental frequencies of 3, 4 and 5 Hz, and their 2nd and 3rd harmonics, which included the 10 Hz frequency typically used in most of the CFS studies. We found that the suppression of stimulus awareness was stronger under 4, 6 and 8 Hz than 10 Hz. After controlling for inter-individual variability with mixed-effects analysis, we found that the number of seen trials was lower for the 4 Hz-basis frequencies than the 5 Hz ones, and was lower for the 2nd than 3rd harmonic. We propose that this may be caused by an interaction between the CFS masks and the ongoing sampling of the attentional mechanism. Examining individual data, we also found a habituation effect that the participants saw significantly more stimuli as the experiment progressed. Our results suggest that these factors need to be taken care of in future CFS studies in order to achieve optimal visual awareness suppression and ensure the generalizability of results.

The Influence of Conscious and Unconscious Body Threat Expressions on Motor Evoked Potentials Studied With Continuous Flash Suppression.

The observation of threatening expression in others is a strong cue for triggering an action response. One method of capturing such action responses is by measuring the amplitude of motor evoked potentials (MEPs) elicited with single pulse TMS over the primary motor cortex. Indeed, it has been shown that viewing whole body expressions of threat modulate the size of MEP amplitude. Furthermore, emotional cues have been shown to act on certain brain areas even outside of conscious awareness. In the current study, we explored if the influence of viewing whole body expressions of threat extends to stimuli that are presented outside of conscious awareness in healthy participants. To accomplish this, we combined the measurement of MEPs with a continuous flash suppression task. In experiment 1, participants were presented with images of neutral bodies, fearful bodies, or objects that were either perceived consciously or unconsciously, while single pulses of TMS were applied at different times after stimulus onset (200, 500, or 700 ms). In experiment 2 stimuli consisted of neutral bodies, angry bodies or objects, and pulses were applied at either 200 or 400 ms post stimulus onset. In experiment 1, there was a general effect of the time of stimulation, but no condition specific effects were evident. In experiment 2 there were no significant main effects, nor any significant interactions. Future studies need to look into earlier effects of MEP modulation by emotion body stimuli, specifically when presented outside of conscious awareness, as well as an exploration of other outcome measures such as intracortical facilitation.

Dynamic Interactions between Emotion Perception and Action Preparation for Reacting to Social Threat: A Combined cTBS-fMRI Study.

Expressions of emotion are powerful triggers for situation-appropriate responses by the observer. Of particular interest regarding the preparation of such adaptive actions are parietal and premotor cortices, given their potential for interaction with the amygdala (AMG), which is known to play a crucial role in the processing of affective information and in motor response. We set out to disentangle the respective roles of the inferior parietal lobule (IPL) and ventral premotor cortex (PMv) in humans in the processing of emotional body expressions by assessing remote effects of continuous theta burst stimulation (cTBS) in the action network and in AMG. Participants were presented with blocks of short videos showing either angry or neutral whole-body actions. The experiment consisted of three fMRI sessions: two sessions were preceded by stimulation of either right IPL (rIPL) or right PMv (rPMv); and a third session assessed baseline activity. Interestingly, whereas at baseline the left AMG did not differentiate between neutral and angry body postures, a significant difference between these conditions emerged after stimulation of either rIPL or rPMv, with much larger responses to angry than to neutral stimuli. In addition, the effects of cTBS stimulation and emotion were also observed in two other action-relevant areas, the supplementary motor area and the superior parietal cortex. Together, these results show how areas involved in action and emotion perception and in action preparation interact dynamically.

Phase of beta-frequency tACS over primary motor cortex modulates corticospinal excitability.

The assessment of corticospinal excitability by means of transcranial magnetic stimulation-induced motor evoked potentials is an established diagnostic tool in neurophysiology and a widely used procedure in fundamental brain research. However, concern about low reliability of these measures has grown recently. One possible cause of high variability of MEPs under identical acquisition conditions could be the influence of oscillatory neuronal activity on corticospinal excitability. Based on research showing that transcranial alternating current stimulation can entrain neuronal oscillations we here test whether alpha or beta frequency tACS can influence corticospinal excitability in a phase-dependent manner. We applied tACS at individually calibrated alpha- and beta-band oscillation frequencies, or we applied sham tACS. Simultaneous single TMS pulses time locked to eight equidistant phases of the ongoing tACS signal evoked MEPs. To evaluate offline effects of stimulation frequency, MEP amplitudes were measured before and after tACS. To evaluate whether tACS influences MEP amplitude, we fitted one-cycle sinusoids to the average MEPs elicited at the different phase conditions of each tACS frequency. We found no frequency-specific offline effects of tACS. However, beta-frequency tACS modulation of MEPs was phase-dependent. Post hoc analyses suggested that this effect was specific to participants with low (<19 Hz) intrinsic beta frequency. In conclusion, by showing that beta tACS influences MEP amplitude in a phase-dependent manner, our results support a potential role attributed to neuronal oscillations in regulating corticospinal excitability. Moreover, our findings may be useful for the development of TMS protocols that improve the reliability of MEPs as a meaningful tool for research applications or for clinical monitoring and diagnosis.

Looking at the face and seeing the whole body. Neural basis of combined face and body expressions.

In the natural world, faces are not isolated objects but are rather encountered in the context of the whole body. Previous work has studied the perception of combined faces and bodies using behavioural and electrophysiological measurements, but the neural correlates of emotional face-body perception still remain unexplored. Here, we combined happy and fearful faces and bodies to investigate the influence of body expressions on the neural processing of the face, the effect of emotional ambiguity between the two and the role of the amygdala in this process. Our functional magnetic resonance imaging analyses showed that the activity in motor, prefrontal and visual areas increases when facial expressions are presented together with bodies rather than in isolation, consistent with the notion that seeing body expressions triggers both emotional and action-related processes. In contrast, psychophysiological interaction analyses revealed that amygdala modulatory activity increases after the presentation of isolated faces when compared to combined faces and bodies. Furthermore, a facial expression combined with a congruent body enhanced both cortical activity and amygdala functional connectivity when compared to an incongruent face-body compound. Finally, the results showed that emotional body postures influence the processing of facial expressions, especially when the emotion conveyed by the body implies danger.

Affective vocalizations influence body ownership as measured in the rubber hand illusion.

Emotional signals, like threatening sounds, automatically ready the perceiver to prepare an appropriate defense behavior. Conjecturing that this would manifest itself in extending the safety zone around the body we used the rubber hand illusion (RHI) to test this prediction. The RHI is a perceptual illusion in which body ownership is manipulated by synchronously stroking a rubber hand and real hand occluded from view. Many factors, both internal and external, have been shown to influence the strength of the illusion, yet the effect of emotion perception on body ownership remains unexplored. We predicted that listening to affective vocalizations would influence how strongly participants experience the RHI. In the first experiment four groups were tested that listened either to affective sounds (angry or happy vocalizations), non-vocal sounds or no sound while undergoing synchronous or asynchronous stroking of the real and rubber hand. In a second experiment three groups were tested comparing angry or neutral vocalizations and no sound condition. There was a significantly larger drift towards the rubber hand in the emotion versus the no emotion conditions. We interpret these results in the framework that the spatial increase in the RHI indicates that under threat the body has the capacity to extend its safety zone.

A causal role for inferior parietal lobule in emotion body perception.

Recent investigations of emotion body perception have established that perceiving fearful body expressions critically triggers activity in dorsal stream structures related to action preparation. However, the causal contributions of these areas remain unclear. In the current experiment, we addressed this issue using online transcranial magnetic stimulation (TMS) of the inferior parietal lobule (IPL) in the dorsal stream and visual areas (extrastriate body area - EBA in the ventral stream and early visual cortex - EVC). Participants performed a delayed-match-to-sample task requiring detection of a change in posture of body expressions that were either neutral or fearful. Results revealed a significant interaction between the stimulation site and the emotional valence of stimuli, indicating that processing of emotional versus neutral bodies is affected differentially by stimulation of different central areas in body processing. IPL stimulation specifically enhanced fearful body processing. These findings relate emotion processing to separate processing streams, and moreover provide the first evidence that IPL plays a causal role in processing of fearful bodies.