Attention to cardiac sensations enhances the heartbeat-evoked potential during exhalation.

Respiration and cardiac activity intricately interact through complex physiological mechanisms. The heartbeat-evoked potential (HEP) is an EEG fluctuation reflecting the cortical processing of cardiac signals. We recently found higher HEP amplitude during exhalation than inhalation during a task involving attention to cardiac sensations. This may have been due to reduced cardiac perception during inhalation and heightened perception during exhalation through attentional mechanisms. To investigate relationships between HEP, attention, and respiration, we introduced an experimental setup that included tasks related to cardiac and respiratory interoceptive and exteroceptive attention. Results revealed HEP amplitude increases during the interoceptive tasks over fronto-central electrodes. When respiratory phases were taken into account, HEP increases were primarily driven by heartbeats recorded during exhalation, specifically during the cardiac interoceptive task, while inhalation had minimal impact. These findings emphasize the role of respiration in cardiac interoceptive attention and could have implications for respiratory interventions to fine-tune cardiac interoception.

When the heart inhibits the brain: Cardiac phases modulate short-interval intracortical inhibition.

The phasic cardiovascular activity influences the central nervous system through the systolic baroreceptor inputs, inducing widespread inhibitory effects on behavior. Through transcranial magnetic stimulation (TMS) delivered during resting-state over the left primary motor cortex and across the different cardiac phases, we measured corticospinal excitability (CSE) and distinct indices of intracortical motor inhibition: short (SICI) and long (LICI) interval, corresponding to GABAA and GABAB neurotransmission, respectively. We found a significant effect of the cardiac phase on short-intracortical inhibition, without any influence on LICI. Specifically, SICI was stronger at systole compared to diastole. These results show a tight relationship between the cardiac cycle and the inhibitory neurotransmission within M1, and in particular with GABAA-ergic-mediated motor inhibition. We hypothesize that this process requires greater motor control via the gating mechanism and that this, in turn, needs to be recalibrated through the modulation of intracortical inhibition.

Heart is deceitful above all things: Threat expectancy induces the illusory perception of increased heartrate.

It has been suggested that our perception of the internal milieu, or the body's internal state, is shaped by our beliefs and previous knowledge about the body's expected state, rather than being solely based on actual interoceptive experiences. This study investigated whether heartbeat perception could be illusorily distorted towards prior subjective beliefs, such that threat expectations suffice to induce a misperception of heartbeat frequency. Participants were instructed to focus on their cardiac activity and report their heartbeat, either tapping along to it (Experiment 1) or silently counting (Experiment 2) while ECG was recorded. While completing this task, different cues provided valid predictive information about the intensity of an upcoming cutaneous stimulation (high- vs. low- pain). Results showed that participants expected a heart rate increase over the anticipation of high- vs. low-pain stimuli and that this belief was perceptually instantiated, as suggested by their interoceptive reports. Importantly, the perceived increase was not mirrored by the real heart rate. Perceptual modulations were absent when participants executed the same task but with an exteroceptive stimulus (Experiment 3). The findings reveal, for the first time, an interoceptive illusion of increased heartbeats elicited by threat expectancy and shed new light on interoceptive processes through the lenses of Bayesian predictive processes, providing tantalizing insights into how such illusory phenomena may intersect with the recognition and regulation of people's internal states.

Beyond peripersonal boundaries: insights from crossmodal interactions.

We experience our self as a body located in space. However, how information about self-location is integrated into multisensory processes underlying the representation of the peripersonal space (PPS), is still unclear. Prior studies showed that the presence of visual information related to oneself modulates the multisensory processes underlying PPS. Here, we used the crossmodal congruency effect (CCE) to test whether this top-down modulation depends on the spatial location of the body-related visual information. Participants responded to tactile events on their bodies while trying to ignore a visual distractor presented on the mirror reflection of their body (Self) either in the peripersonal space (Near) or in the extrapersonal space (Far). We found larger CCE when visual events were presented on the mirror reflection in the peripersonal space, as compared to the extrapersonal space. These results suggest that top-down modulation of the multisensory bodily self is only possible within the PPS.

The impact of cardiac phases on multisensory integration.

The brain continuously processes information coming from both the external environment and visceral signals generated by the body. This constant information exchange between the body and the brain allows signals originating from the oscillatory activity of the heart, among others, to influence perception. Here, we investigated how the cardiac phase modulates multisensory integration, which is the process that allows information from multiple senses to combine non-linearly to reduce environmental uncertainty. Forty healthy participants completed a Simple Detection Task with unimodal (Auditory, Visual, Tactile) and bimodal (Audio-Tactile, Audio-Visual, Visuo-Tactile) stimuli presented 250 ms and 500 ms after the R-peak of the electrocardiogram, that is, systole and diastole, respectively. First, we found a nonspecific effect of the cardiac cycle phases on detection of both unimodal and bimodal stimuli. Reaction times were faster for stimuli presented during diastole, compared to systole. Then, applying the Race Model Inequality approach to quantify multisensory integration, Audio-Tactile and Visuo-Tactile, but not Audio-Visual stimuli, showed higher integration when presented during diastole than during systole. These findings indicate that the impact of the cardiac phase on multisensory integration may be specific for stimuli including somatosensory (i.e., tactile) inputs. This suggests that the heartbeat-related noise, which according to the interoceptive predictive coding theory suppresses somatosensory inputs, also affects multisensory integration during systole. In conclusion, our data extend the interoceptive predictive coding theory to the multisensory domain. From a more mechanistic view, they may reflect a reduced optimization of neural oscillations orchestrating multisensory integration during systole.

Temporal dynamics of the Rubber Hand Illusion.

It is widely accepted that the representation of the body is not fixed and immutable, but rather flexible and constantly updated based on a continuous stream of multisensory information. This mechanism can be very useful to adapt to several situations, but it would not be adaptive if the body representation was too malleable or if it wasn't capable of restoring its integrity after a transient modification. Here we used the Rubber Hand Illusion (RHI) to investigate how quickly the body representation can be modified. Previous studies have investigated the timing of the onset and offset of the illusion, however, they did not assess a fine temporal resolution. Here, we used a potentiometer to record a moment-by-moment rating of the feeling of owning the RH for two minutes during the visuo-tactile stimulation and two minutes following the stimulation. Our results suggest that the feeling of Ownership is already established during the first 19 s of stimulation then it continues to grow, but at a much slower pace. The feeling of Ownership disappears within 66 s from the end of the stimulation. This work sheds new light on the temporal dynamics of the RHI and the malleability of the body self-consciousness.

Multisensory integration in humans with spinal cord injury.

Although multisensory integration (MSI) has been extensively studied, the underlying mechanisms remain a topic of ongoing debate. Here we investigate these mechanisms by comparing MSI in healthy controls to a clinical population with spinal cord injury (SCI). Deafferentation following SCI induces sensorimotor impairment, which may alter the ability to synthesize cross-modal information. We applied mathematical and computational modeling to reaction time data recorded in response to temporally congruent cross-modal stimuli. We found that MSI in both SCI and healthy controls is best explained by cross-modal perceptual competition, highlighting a common competition mechanism. Relative to controls, MSI impairments in SCI participants were better explained by reduced stimulus salience leading to increased cross-modal competition. By combining traditional analyses with model-based approaches, we examine how MSI is realized during normal function, and how it is compromised in a clinical population. Our findings support future investigations identifying and rehabilitating MSI deficits in clinical disorders.

Brain-heart interactions are modulated across the respiratory cycle via interoceptive attention.

Respiration and heartbeat continuously interact within the living organism at many different levels, representing two of the main oscillatory rhythms of the body and providing major sources of interoceptive information to the brain. Despite the modulatory effect of respiration on exteroception and cognition has been recently established in humans, its role in shaping interoceptive perception has been scarcely investigated so far. In two independent studies, we investigated the effect of spontaneous breathing on cardiac interoception by assessing the Heartbeat Evoked Potential (HEP) in healthy humans. In Study 1, we compared HEP activity for heartbeats occurred during inhalation and exhalation in 40 volunteers at rest. We found higher HEP amplitude during exhalation, compared to inhalation, over fronto-centro-parietal areas. This suggests increased brain-heart interactions and improved cortical processing of the heartbeats during exhalation. Further analyses revealed that this effect was moderated by heart rate changes. In Study 2, we tested the respiratory phase-dependent modulation of HEP activity in 20 volunteers during Exteroceptive and Interoceptive conditions of the Heartbeat Detection (HBD) task. In these conditions, participants were requested to tap at each heartbeat, either listened to or felt, respectively. Results showed higher HEP activity and higher detection accuracy at exhalation than inhalation in the Interoceptive condition only. Direct comparisons of Interoceptive and Exteroceptive conditions confirmed stronger respiratory phase-dependent modulation of HEP and accuracy when attention was directed towards the interoceptive stimuli. Moreover, HEP changes during the Interoceptive condition were independent of heart physiology, but were positively correlated with higher detection accuracy at exhalation than inhalation. This suggests a link between optimization of cortical processing of cardiac signals and detection of heartbeats across the respiratory cycle. Overall, we provide data showing that respiration shapes cardiac interoception at the neurophysiological and behavioural levels. Specifically, exhalation may allow attentional shift towards the internal bodily states.

Body structural representation in schizotypy.

A deficient sense of self, typically observed in schizophrenia spectrum disorders, is often accompanied by abnormalities in bodily perception and awareness. These abnormalities are seemingly among the most powerful predictive factors for the onset of schizophrenic illnesses. According to the hypothesis of the psychosis continuum, high schizotypal traits in the general population may be characterized by a progressive sense of detachment from one's lived body. Building upon previous research that found an abnormal Body Structural Representation (BSR) in individuals with schizophrenia, this study aims to extend these findings to schizotypy. To investigate this, we utilized the Finger Localization Task (FLT), in which participants must identify the finger touched by the experimenter, and the In Between Task (IBT), in which two fingers are touched and participants must specify the number of fingers in between the two stimulated fingers. We found that individuals with high schizotypy were significantly less accurate than individuals with low schizotypy in determining the spatial configuration of their own fingers relative to each other. Most significantly, performances on both tasks were negatively correlated with the score on the Dissociative Experiences Scale (DES). These findings support the hypothesis that the progressive loss of one's sense of self is associated with abnormal bodily experiences and dissociative symptomatology which may represent a potential marker for schizophrenia proneness.

Maladaptive reorganization following SCI: The role of body representation and multisensory integration.

In this review we focus on maladaptive brain reorganization after spinal cord injury (SCI), including the development of neuropathic pain, and its relationship with impairments in body representation and multisensory integration. We will discuss the implications of altered sensorimotor interactions after SCI with and without neuropathic pain and possible deficits in multisensory integration and body representation. Within this framework we will examine published research findings focused on the use of bodily illusions to manipulate multisensory body representation to induce analgesic effects in heterogeneous chronic pain populations and in SCI-related neuropathic pain. We propose that the development and intensification of neuropathic pain after SCI is partly dependent on brain reorganization associated with dysfunctional multisensory integration processes and distorted body representation. We conclude this review by suggesting future research avenues that may lead to a better understanding of the complex mechanisms underlying the sense of the body after SCI, with a focus on cortical changes.

Frontal and parietal background connectivity and their dynamic changes account for individual differences in the multisensory representation of peripersonal space.

Functional connectivity (FC) of brain networks dynamically fluctuates during both rest and task execution. Individual differences in dynamic FC have been associated with several cognitive and behavioral traits. However, whether dynamic FC also contributes to sensorimotor representations guiding body-environment interactions, such as the representation of peripersonal space (PPS), is currently unknown. PPS is the space immediately surrounding the body and acts as a multisensory interface between the individual and the environment. We used an audio-tactile task with approaching sounds to map the individual PPS extension, and fMRI to estimate the background FC. Specifically, we analyzed FC values for each stimulus type (near and far space) and its across-trial variability. FC was evaluated between task-relevant nodes of two fronto-parietal networks (the Dorsal Attention Network, DAN, and the Fronto-Parietal Network, FPN) and a key PPS region in the premotor cortex (PM). PM was significantly connected to specific task-relevant nodes of the DAN and the FPN during the audio-tactile task, and FC was stronger while processing near space, as compared to far space. At the individual level, less PPS extension was associated with stronger premotor-parietal FC during processing of near space, while the across-trial variability of premotor-parietal and premotor-frontal FC was higher during the processing of far space. Notably, only across-trial FC variability captured the near-far modulation of space processing. Our findings indicate that PM connectivity with task-relevant frontal and parietal regions and its dynamic changes participate in the mechanisms that enable PPS representation, in agreement with the idea that neural variability plays a crucial role in plastic and dynamic sensorimotor representations.

Temporal binding window and sense of agency are related processes modifiable via occipital tACS.

The temporal binding window refers to the time frame within which temporal grouping of sensory information takes place. Sense of agency is the feeling of being in control of one's actions, and their associated outcomes. While previous research has shown that temporal cues and multisensory integration play a role in sense of agency, no studies have directly assessed whether individual differences in the temporal binding window and sense of agency are associated. In all three experiments, to assess sense of agency, participants pressed a button triggering, after a varying delay, the appearance of the circle, and reported their sense of agency over the effect. To assess the temporal binding window a simultaneity judgment task (Experiment 1) and a double-flash illusion task (Experiment 2 and 3) was also performed. As expected, the temporal binding window correlated with the sense of agency window. In Experiment 3, these processes were modulated by applying occipital tACS at either 14Hz or 8Hz. We found 14Hz tACS stimulation was associated with narrower temporal biding window and sense of agency window. Our results suggest the temporal binding window and the time window of sense of agency are related. They also point towards a possible underlying neural mechanism (alpha peak frequency) for this association.

Cortical silent period reflects individual differences in action stopping performance.

Inhibitory control is the ability to suppress inappropriate movements and unwanted actions, allowing to regulate impulses and responses. This ability can be measured via the Stop Signal Task, which provides a temporal index of response inhibition, namely the stop signal reaction time (SSRT). At the neural level, Transcranial Magnetic Stimulation (TMS) allows to investigate motor inhibition within the primary motor cortex (M1), such as the cortical silent period (CSP) which is an index of GABAB-mediated intracortical inhibition within M1. Although there is strong evidence that intracortical inhibition varies during action stopping, it is still not clear whether differences in the neurophysiological markers of intracortical inhibition contribute to behavioral differences in actual inhibitory capacities. Hence, here we explored the relationship between intracortical inhibition within M1 and behavioral response inhibition. GABABergic-mediated inhibition in M1 was determined by the duration of CSP, while behavioral inhibition was assessed by the SSRT. We found a significant positive correlation between CSP's duration and SSRT, namely that individuals with greater levels of GABABergic-mediated inhibition seem to perform overall worse in inhibiting behavioral responses. These results support the assumption that individual differences in intracortical inhibition are mirrored by individual differences in action stopping abilities.

Colors and Handles: How Action Primes Perception.

How deeply does action influence perception? Does action performance affect the perception of object features directly related to action only? Or does it concern also object features such as colors, which are not held to directly afford action? The present study aimed at answering these questions. We asked participants to repeatedly grasp a handled mug hidden from their view before judging whether a visually presented mug was blue rather than cyan. The motor training impacted on their perceptual judgments, by speeding participants' responses, when the handle of the presented mug was spatially aligned with the trained hand. The priming effect did not occur when participants were trained to merely touch the mug with their hand closed in a fist. This indicates that action performance may shape the perceptual judgment on object features, even when these features are colors and do not afford any action. How we act on surrounding objects is therefore not without consequence for how we experience them.

Phase-coupling of neural oscillations contributes to individual differences in peripersonal space.

The peripersonal space (PPS) is a multisensory and sensorimotor interface between our body and the environment. The location of PPS boundary is not fixed. Rather, it adapts to the environmental context and differs greatly across individuals. Recent studies have started to unveil the neural correlates of individual differences in PPS extension; however, this picture is not clear yet. Here, we used approaching auditory stimuli and magnetoencephalography to capture the individual boundary of PPS and examine its neural underpinnings. In particular, building upon previous studies from our own group, we investigated the possible contribution of an intrinsic feature of the brain, that is the "resting state" functional connectivity, to the individual differences in PPS extension and the frequency specificity of this contribution. Specifically, we focused on the activity synchronized to the premotor cortex, where multisensory neurons encoding PPS have been described. Results showed that the stronger the connectivity between left premotor cortex (lPM) and a set of fronto-parietal, sensorimotor regions in the right and left hemisphere, the wider the extension of the PPS. Strikingly, such a correlation was observed only in the beta-frequency band. Overall, our results suggest that the individual extension of the PPS is coded in spatially- and spectrally-specific resting state functional links.

Body-environment integration: Temporal processing of tactile and auditory inputs along the schizophrenia continuum.

According to the dimensional approach to psychosis, there is a continuum from low schizotypy to schizophrenia patients. The temporal aspect of sensory processing seems to be compromised across such continuum, as suggested by different studies separately investigating unisensory or multisensory domains. Most of these studies have so far focused primarily on the temporal processing of visual and auditory stimuli, either in schizotypy or schizophrenia, while leaving the tactile domain and the integration of touch with other senses mostly unexplored. Given the relevance of body-related perceptual abnormalities for psychosis proneness, we aimed at filling this gap in the literature across two studies. We asked participants with increasing levels of schizotypy (study 1) and schizophrenia patients (study 2) to perform three simultaneity judgement tasks: a unimodal tactile task, a unimodal auditory task and a bimodal audio-tactile task. Each task allowed estimating a simultaneity range (SR), as a proxy of the individual tolerance to asynchronies in the tactile, auditory and audio-tactile domains, respectively. Results showed larger SRs as the level of schizotypy increases. Specifically, the linear effect of schizotypy levels on the audio-tactile task was stronger than on the auditory task, which in turn was greater than the effect on the tactile task (study 1). Differently, schizophrenia patients showed larger SRs than controls in all the three tasks (study 2). The current study is the first empirical investigation across the continuum from low schizotypy to schizophrenia of the tolerance to asynchronies in the processing of external (auditory) and body-related (tactile) inputs.

Visual similarity and psychological closeness are neurally dissociable in the brain response to vicarious pain.

Personal and vicarious experience of pain activate partially overlapping brain networks. This brain activity is further modulated by low- and high-order factors, e.g., the perceived intensity of the model's pain and the model's similarity with the onlooker, respectively. We investigated which specific aspect of similarity modulates such empathic reactivity, focusing on the potential differentiation between visual similarity and psychological closeness between the onlooker and different types of models. To this aim, we recorded fMRI data in neurotypical participants who observed painful and tactile stimuli delivered to an adult human hand, a baby human hand, a puppy dog paw, and an anthropomorphic robotic hand. The interaction between type of vicarious experience (pain, touch) and nature of model (adult, baby, dog, robot) showed that the right supramarginal gyrus (rSMG) was selectively active for visual similarity (more active during vicarious pain for the adult and baby models), while the anterior cingulate cortex (ACC) was more sensitive to psychological closeness (specifically linked to vicarious pain for the baby model). These findings indicate that visual similarity and psychological closeness between onlooker and model differentially affect the activity of brain regions specifically implied in encoding interindividual sharing of sensorimotor and affective aspects of vicarious pain, respectively.

Affordance matching predictively shapes the perceptual representation of others' ongoing actions.

Predictive processing accounts of social perception argue that action observation is a predictive process, in which inferences about others' goals are tested against the perceptual input, inducing a subtle perceptual confirmation bias that distorts observed action kinematics toward the inferred goals. Here we test whether such biases are induced even when goals are not explicitly given but have to be derived from the unfolding action kinematics. In 2 experiments, participants briefly saw an actor reach ambiguously toward a large object and a small object, with either a whole-hand power grip or an index-finger and thumb precision grip. During its course, the hand suddenly disappeared, and participants reported its last seen position on a touch-screen. As predicted, judgments were consistently biased toward apparent action targets, such that power grips were perceived closer to large objects and precision grips closer to small objects, even if the reach kinematics were identical. Strikingly, these biases were independent of participants' explicit goal judgments. They were of equal size when action goals had to be explicitly derived in each trial (Experiment 1) or not (Experiment 2) and, across trials and across participants, explicit judgments and perceptual biases were uncorrelated. This provides evidence, for the first time, that people make online adjustments of observed actions based on the match between hand grip and object goals, distorting their perceptual representation toward implied goals. These distortions may not reflect high-level goal assumptions, but emerge from relatively low-level processing of kinematic features within the perceptual system. (PsycInfo Database Record (c) 2020 APA, all rights reserved).

Body representations and basic symptoms in schizophrenia.

Patients with schizophrenia report a wide range of anomalous body experiences. According to the basic symptom model of schizophrenia, disturbances of body perception and awareness are among the most powerful predictors of the changes in the subjective experience of the self in schizophrenia. In this study we first investigated the body structural representation (BSR), a specific aspect of body awareness, and its association to basic symptoms in patients with schizophrenia. Using a finger localization task, we found that patients are significantly less accurate than healthy controls when asked to identify pairs of fingers touched by the experimenter, when the hand is hidden from view. Most importantly, patients' performance at the finger localization task was negatively associated to basic symptoms: the worse the individual accuracy, the higher the SPI-A total score. Moreover, the accuracy at the finger localization task was also negatively correlated with the malleability of the sense of body ownership: the less the individual ability to localize fingers, the stronger the rubber hand illusion. These results are in agreement with the idea that self-disorders in schizophrenia reveal a disconnectedness that can be regarded as a problem of disembodiment and traced back to abnormal body experiences.