Interoception: the sense of the physiological condition of the body

Converging evidence indicates that primates have a distinct cortical image of homeostatic afferent activity that reflects all aspects of the physiological condition of all tissues of the body. This interoceptive system, associated with autonomic motor control, is distinct from the exteroceptive system (cutaneous mechanoreception and proprioception) that guides somatic motor activity. The primary interoceptive representation in the dorsal posterior insula engenders distinct highly resolved feelings from the body that include pain, temperature, itch, sensual touch, muscular and visceral sensations, vasomotor activity, hunger, thirst, and 'air hunger'. In humans, a meta-representation of the primary interoceptive activity is engendered in the right anterior insula, which seems to provide the basis for the subjective image of the material self as a feeling (sentient) entity, that is, emotional awareness.     

Perception of Body Ownership Is Driven by Bayesian Sensory Inference

Recent studies have shown that human perception of body ownership is highly malleable. A well-known example is the rubber hand illusion (RHI) wherein ownership over a dummy hand is experienced, and is generally believed to require synchronized stroking of real and dummy hands. Our goal was to elucidate the computational principles governing this phenomenon. We adopted the Bayesian causal inference model of multisensory perception and applied it to visual, proprioceptive, and tactile stimuli. The model reproduced the RHI, predicted that it can occur without tactile stimulation, and that synchronous stroking would enhance it. Various measures of ownership across two experiments confirmed the predictions: a large percentage of individuals experienced the illusion in the absence of any tactile stimulation, and synchronous stroking strengthened the illusion. Altogether, these findings suggest that perception of body ownership is governed by Bayesian causal inference—i.e., the same rule that appears to govern the perception of outside world.     

Disturbances in body ownership in schizophrenia: evidence from the rubber hand illusion and case study of a spontaneous out-of-body experience

Background

A weakened sense of self may contribute to psychotic experiences. Body ownership, one component of self-awareness, can be studied with the rubber hand illusion (RHI). Watching a rubber hand being stroked while one''s unseen hand is stroked synchronously can lead to a sense of ownership over the rubber hand, a shift in perceived position of the real hand, and a limb-specific drop in stimulated hand temperature. We aimed to assess the RHI in schizophrenia using quantifiable measures: proprioceptive drift and stimulation-dependent changes in hand temperature.

Methods

The RHI was elicited in 24 schizophrenia patients and 21 matched controls by placing their unseen hand adjacent to a visible rubber hand and brushing real and rubber hands synchronously or asynchronously. Perceived finger location was measured before and after stimulation. Hand temperature was taken before and during stimulation. Subjective strength of the illusion was assessed by a questionnaire.

Results

Across groups, the RHI was stronger during synchronous stimulation, indicated by self-report and proprioceptive drift. Patients reported a stronger RHI than controls. Self-reported strength of RHI was associated with schizotypy in controls Proprioceptive drift was larger in patients, but only following synchronous stimulation. Further, we observed stimulation-dependent changes in skin temperature. During right hand stimulation, temperature dropped in the stimulated hand and rose in the unstimulated hand. Interestingly, induction of RHI led to an out-of-body experience in one patient, linking body disownership and psychotic experiences.

Conclusions

The RHI is quantitatively and qualitatively stronger in schizophrenia. These findings suggest that patients have a more flexible body representation and weakened sense of self, and potentially indicate abnormalities in temporo-parietal networks implicated in body ownership. Further, results suggest that these body ownership disturbances might be at the heart of a subset of the pathognomonic delusions of passivity.     

Interoceptive Focus Shapes the Experience of Time

The perception of time is a fundamental part of human experience. Recent research suggests that the experience of time emerges from emotional and interoceptive (bodily) states as processed in the insular cortex. Whether there is an interaction between the conscious awareness of interoceptive states and time distortions induced by emotions has rarely been investigated so far. We aimed to address this question by the use of a retrospective time estimation task comparing two groups of participants. One group had a focus on interoceptive states and one had a focus on exteroceptive information while watching film clips depicting fear, amusement and neutral content. Main results were that attention to interoceptive processes significantly affected subjective time experience. Fear was accompanied with subjective time dilation that was more pronounced in the group with interoceptive focus, while amusement led to a quicker passage of time which was also increased by interoceptive focus. We conclude that retrospective temporal distortions are directly influenced by attention to bodily responses. These effects might crucially interact with arousal levels. Sympathetic nervous system activation affecting memory build-up might be the decisive factor influencing retrospective time judgments. Our data substantially extend former research findings underscoring the relevance of interoception for the effects of emotional states on subjective time experience.     

Does Seeing Ice Really Feel Cold? Visual-Thermal Interaction under an Illusory Body-Ownership

Although visual information seems to affect thermal perception (e.g. red color is associated with heat), previous studies have failed to demonstrate the interaction between visual and thermal senses. However, it has been reported that humans feel an illusory thermal sensation in conjunction with an apparently-thermal visual stimulus placed on a prosthetic hand in the rubber hand illusion (RHI) wherein an individual feels that a prosthetic (rubber) hand belongs to him/her. This study tests the possibility that the ownership of the body surface on which a visual stimulus is placed enhances the likelihood of a visual-thermal interaction. We orthogonally manipulated three variables: induced hand-ownership, visually-presented thermal information, and tactically-presented physical thermal information. Results indicated that the sight of an apparently-thermal object on a rubber hand that is illusorily perceived as one''s own hand affects thermal judgments about the object physically touching this hand. This effect was not observed without the RHI. The importance of ownership of a body part that is touched by the visual object on the visual-thermal interaction is discussed.     

Body Conscious? Interoceptive Awareness,Measured by Heartbeat Perception,Is Negatively Correlated with Self-Objectification

Background

‘Self-objectification’ is the tendency to experience one''s body principally as an object, to be evaluated for its appearance rather than for its effectiveness. Within objectification theory, it has been proposed that self-objectification accounts for the poorer interoceptive awareness observed in women, as measured by heartbeat perception. Our study is, we believe, the first specifically to test this relationship.

Methodology/Principal Findings

Using a well-validated and reliable heartbeat perception task, we measured interoceptive awareness in women and compared this with their scores on the Self-Objectification Questionnaire, the Self-Consciousness Scale and the Body Consciousness Questionnaire. Interoceptive awareness was negatively correlated with self-objectification. Interoceptive awareness, public body consciousness and private body consciousness together explained 31% of the variance in self-objectification. However, private body consciousness was not significantly correlated with interoceptive awareness, which may explain the many nonsignificant results in self-objectification studies that have used private body consciousness as a measure of body awareness.

Conclusions/Significance

We propose interoceptive awareness, assessed by heartbeat perception, as a measure of body awareness in self-objectification studies. Our findings have implications for those clinical conditions, in women, which are characterised by self-objectification and low interoceptive awareness, such as eating disorders.     

The Human Touch: Skin Temperature during the Rubber Hand Illusion in Manual and Automated Stroking Procedures

A difference in skin temperature between the hands has been identified as a physiological correlate of the rubber hand illusion (RHI). The RHI is an illusion of body ownership, where participants perceive body ownership over a rubber hand if they see it being stroked in synchrony with their own occluded hand. The current study set out to replicate this result, i.e., psychologically induced cooling of the stimulated hand using an automated stroking paradigm, where stimulation was delivered by a robot arm (PHANToM^TM force-feedback device). After we found no evidence for hand cooling in two experiments using this automated procedure, we reverted to a manual stroking paradigm, which is closer to the one employed in the study that first produced this effect. With this procedure, we observed a relative cooling of the stimulated hand in both the experimental and the control condition. The subjective experience of ownership, as rated by the participants, by contrast, was strictly linked to synchronous stroking in all three experiments. This implies that hand-cooling is not a strict correlate of the subjective feeling of hand ownership in the RHI. Factors associated with the differences between the two designs (differences in pressure of tactile stimulation, presence of another person) that were thus far considered irrelevant to the RHI appear to play a role in bringing about this temperature effect.     

Decreased Peripheral and Central Responses to Acupuncture Stimulation following Modification of Body Ownership

Acupuncture stimulation increases local blood flow around the site of stimulation and induces signal changes in brain regions related to the body matrix. The rubber hand illusion (RHI) is an experimental paradigm that manipulates important aspects of bodily self-awareness. The present study aimed to investigate how modifications of body ownership using the RHI affect local blood flow and cerebral responses during acupuncture needle stimulation. During the RHI, acupuncture needle stimulation was applied to the real left hand while measuring blood microcirculation with a LASER Doppler imager (Experiment 1, N = 28) and concurrent brain signal changes using functional magnetic resonance imaging (fMRI; Experiment 2, N = 17). When the body ownership of participants was altered by the RHI, acupuncture stimulation resulted in a significantly lower increase in local blood flow (Experiment 1), and significantly less brain activation was detected in the right insula (Experiment 2). This study found changes in both local blood flow and brain responses during acupuncture needle stimulation following modification of body ownership. These findings suggest that physiological responses during acupuncture stimulation can be influenced by the modification of body ownership.     

Being Barbie: the size of one's own body determines the perceived size of the world

A classical question in philosophy and psychology is if the sense of one's body influences how one visually perceives the world. Several theoreticians have suggested that our own body serves as a fundamental reference in visual perception of sizes and distances, although compelling experimental evidence for this hypothesis is lacking. In contrast, modern textbooks typically explain the perception of object size and distance by the combination of information from different visual cues. Here, we describe full body illusions in which subjects experience the ownership of a doll's body (80 cm or 30 cm) and a giant's body (400 cm) and use these as tools to demonstrate that the size of one's sensed own body directly influences the perception of object size and distance. These effects were quantified in ten separate experiments with complementary verbal, questionnaire, manual, walking, and physiological measures. When participants experienced the tiny body as their own, they perceived objects to be larger and farther away, and when they experienced the large-body illusion, they perceived objects to be smaller and nearer. Importantly, despite identical retinal input, this "body size effect" was greater when the participants experienced a sense of ownership of the artificial bodies compared to a control condition in which ownership was disrupted. These findings are fundamentally important as they suggest a causal relationship between the representations of body space and external space. Thus, our own body size affects how we perceive the world.     

Rubber Hand Illusion Reduces Discomfort Caused by Cold Stimulus

There is a growing interest in body-ownership disruptions and their consequences for subjective experiences such as tactile sensations or pain. Here, we investigated the effect of the rubber hand illusion (RHI) on the perceived discomfort caused by cold stimulus applied to the real hand. The results showed reduced discomfort to cold reflected in behavioural and subjective measures. The stronger the illusion, the later the cold temperature became unpleasant and the less intense the experience was rated. We discuss the link between thermoception and body ownership as well as possible theoretical and methodological implications for studies on pain experience under RHI.     

Closing the Gap between the Inside and the Outside: Interoceptive Sensitivity and Social Distances

Humans’ ability to represent their body state from within through interoception has been proposed to predict different aspects of human cognition and behaviour. We focused on the possible contribution of interoceptive sensitivity to social behaviour as mediated by adaptive modulation of autonomic response. We, thus, investigated whether interoceptive sensitivity to one''s heartbeat predicts participants'' autonomic response at different social distances. We measured respiratory sinus arrhythmia (RSA) during either a Social or a Non-social task. In the Social task each participant viewed an experimenter performing a caress-like movement at different distances from their hand. In the Non-social task a metal stick was moved at the same distances from the participant''s hand. We found a positive association between interoceptive sensitivity and autonomic response only for the social setting. Moreover, only good heartbeat perceivers showed higher autonomic response 1) in the social compared to the non-social setting, 2) specifically, when the experimenter''s hand was moving at boundary of their peripersonal space (20 cm from the participant''s hand). Our findings suggest that interoceptive sensitivity might contribute to interindividual differences concerning social attitudes and interpersonal space representation via recruitment of different adaptive autonomic response strategies.     

The Sense of the Body in Individuals with Spinal Cord Injury

Increasing evidence suggests that the basic foundations of the self lie in the brain systems that represent the body. Specific sensorimotor stimulation has been shown to alter the bodily self. However, little is known about how disconnection of the brain from the body affects the phenomenological sense of the body and the self. Spinal cord injury (SCI) patients who exhibit massively reduced somatomotor processes below the lesion in the absence of brain damage are suitable for testing the influence of body signals on two important components of the self–the sense of disembodiment and body ownership. We recruited 30 SCI patients and 16 healthy participants, and evaluated the following parameters: (i) depersonalization symptoms, using the Cambridge Depersonalization Scale (CDS), and (ii) measures of body ownership, as quantified by the rubber hand illusion (RHI) paradigm. We found higher CDS scores in SCI patients, which show increased detachment from their body and internal bodily sensations and decreasing global body ownership with higher lesion level. The RHI paradigm reveals no alterations in the illusory ownership of the hand between SCI patients and controls. Yet, there was no typical proprioceptive drift in SCI patients with intact tactile sensation on the hand, which might be related to cortical reorganization in these patients. These results suggest that disconnection of somatomotor inputs to the brain due to spinal cord lesions resulted in a disturbed sense of an embodied self. Furthermore, plasticity-related cortical changes might influence the dynamics of the bodily self.     

The role of self-touch in somatosensory and body representation disorders after stroke

Somatosensory impairments occur in about half of the cases of stroke. These impairments range from primary deficits in tactile detection and the perception of features, to higher order impairments in haptic object recognition and bodily experience. In this paper, we review the influence of active- and self-touch on somatosensory impairments after stroke. Studies have shown that self-touch improves tactile detection in patients with primary tactile deficits. A small number of studies concerned with the effect of self-touch on bodily experience in healthy individuals have demonstrated that self-touch influences the structural representation of one's own body. In order to better understand the effect of self-touch on body representations, we present an informal study of a stroke patient with somatoparaphrenia and misoplegia. The role of self-touch on body ownership was investigated by asking the patient to stroke the impaired left hand and foreign hands. The patient reported ownership and a change in affect over all presented hands through self-touch. The time it took to accomplish ownership varied, based on the resemblance of the foreign hand to the patient's own hand. Our findings suggest that self-touch can modulate impairments in body ownership and affect, perhaps by helping to reinstate the representation of the body.     

The Importance of Perceptual Experience in the Esthetic Appreciation of the Body

Several studies suggest that sociocultural models conveying extreme thinness as the widespread ideal of beauty exert an important influence on the perceptual and emotional representation of body image. The psychological mechanisms underlying such environmental influences, however, are unclear. Here, we utilized a perceptual adaptation paradigm to investigate how perceptual experience modulates body esthetic appreciation. We found that the liking judgments of round bodies increased or decreased after brief exposure to round or thin bodies, respectively. No change occurred in the liking judgments of thin bodies. The results suggest that perceptual experience may shape our esthetic appreciation to favor more familiar round body figures. Importantly, individuals with more deficits in interoceptive awareness were less prone to increase their liking ratings of round bodies after exposure, suggesting a specific risk factor for the susceptibility to the influence of the extreme thin vs. round body ideals of beauty portrayed by the media.     

Losing One's Hand: Visual-Proprioceptive Conflict Affects Touch Perception

Background

While the sense of bodily ownership has now been widely investigated through the rubber hand illusion (RHI), very little is known about the sense of disownership. It has been hypothesized that the RHI also affects the ownership feelings towards the participant''s own hand, as if the rubber hand replaced the participant''s actual hand. Somatosensory changes observed in the participants'' hand while experiencing the RHI have been taken as evidence for disownership of their real hand. Here we propose a theoretical framework to disambiguate whether such somatosensory changes are to be ascribed to the disownership of the real hand or rather to the anomalous visuo-proprioceptive conflict experienced by the participant during the RHI.

Methodology/Principal Findings

In experiment 1, reaction times (RTs) to tactile stimuli delivered to the participants'' hand slowed down following the establishment of the RHI. In experiment 2, the misalignment of visual and proprioceptive inputs was obtained via prismatic displacement, a situation in which ownership of the seen hand was doubtless. This condition slowed down the participants'' tactile RTs. Thus, similar effects on touch perception emerged following RHI and prismatic displacement. Both manipulations also induced a proprioceptive drift, toward the fake hand in the first experiment and toward the visual position of the participants'' hand in the second experiment.

Conclusions/Significance

These findings reveal that somatosensory alterations in the experimental hand resulting from the RHI result from cross-modal mismatch between the seen and felt position of the hand. As such, they are not necessarily a signature of disownership.     

“I Feel Contaminated in My Fake Hand”: Obsessive-Compulsive-Disorder like Disgust Sensations Arise from Dummy during Rubber Hand Illusion

Despite its theoretical and clinical interest, there are no experimental studies exploring obsessive-compulsive disorder (OCD)-like disgust sensations through using somatosensory illusions. Such illusions provide important clues to the nature and limits of multisensory integration and how the brain constructs body image; and may potentially inform novel therapies. One such effect is the rubber hand illusion (RHI) in which tactile sensations are referred to a rubber hand; if the experimenter simultaneously strokes a subject’s occluded hand together with a visible fake hand, the subject starts experiencing the touch sensations as arising from the dummy. In this study, we explore whether OCD-like disgust may result from contamination of a dummy hand during the RHI; suggesting a possible integration of somatosensory and limbic inputs in the construction of body image. We predicted that participants would experience sensations of disgust, when placing a disgust stimulus (fake feces, vomit or blood) on the dummy hand after establishing the RHI. We found that 9 out of 11 participants experienced greater disgust during the synchronous condition (real hidden hand and fake hand are stroked in synchrony) compared to the asynchronous control condition (real hidden hand and fake hand are stroked in asynchrony); and on average such disgust was significantly greater during the synchronous condition compared to the asynchronous control condition, Z = 2.7, p = .008. These results argue against a strictly hierarchical modular approach to brain function and suggest that a four-way multisensory interaction occurs between vision, touch, proprioception on the one hand and primal emotions like disgust on the other. These findings may inform novel clinical approaches for OCD; that is, contaminating a dummy during the RHI could possibly be used as part of an in-vivo exposure-intervention for OCD.     

Anteroposterior somatotopy of innocuous cooling activation focus in human dorsal posterior insular cortex

Prior data indicate that graded activation by innocuous thermal stimuli occurs in the dorsal posterior insular (dpIns) cortex of humans, rather than the parietal somatosensory regions traditionally thought necessary for discriminative somatic sensations. We hypothesized that if the dpIns subserves the haptic capacity of localization in addition to discrimination, then it should be somatotopically organized. Using functional magnetic resonance imaging to detect activation in the dpIns by graded cooling stimuli applied to the hand and neck, we found unimodal foci arranged in an anteroposterior somatotopographic pattern, consistent with participation of the dpIns in localization as well as discrimination. This gradient is orthogonal to the mediolateral somatotopy of parietal somatosensory regions, which supports the fundamental conceptual differentiation of the interoceptive somatic representation in the dpIns from the parietal exteroceptive representations. These data also support the suggestion that the poststroke central pain syndrome associated with lesions of the dpIns is a thermoregulatory dysfunction. Finally, another focus of strongly graded activation, which we interpret to represent thermoregulatory behavioral motivation elicited by dynamic cooling, was observed in the dorsal medial cortex.     

Interoception across modalities: on the relationship between cardiac awareness and the sensitivity for gastric functions

The individual sensitivity for ones internal bodily signals ("interoceptive awareness") has been shown to be of relevance for a broad range of cognitive and affective functions. Interoceptive awareness has been primarily assessed via measuring the sensitivity for ones cardiac signals ("cardiac awareness") which can be non-invasively measured by heartbeat perception tasks. It is an open question whether cardiac awareness is related to the sensitivity for other bodily, visceral functions. This study investigated the relationship between cardiac awareness and the sensitivity for gastric functions in healthy female persons by using non-invasive methods. Heartbeat perception as a measure for cardiac awareness was assessed by a heartbeat tracking task and gastric sensitivity was assessed by a water load test. Gastric myoelectrical activity was measured by electrogastrography (EGG) and subjective feelings of fullness, valence, arousal and nausea were assessed. The results show that cardiac awareness was inversely correlated with ingested water volume and with normogastric activity after water load. However, persons with good and poor cardiac awareness did not differ in their subjective ratings of fullness, nausea and affective feelings after drinking. This suggests that good heartbeat perceivers ingested less water because they subjectively felt more intense signals of fullness during this lower amount of water intake compared to poor heartbeat perceivers who ingested more water until feeling the same signs of fullness. These findings demonstrate that cardiac awareness is related to greater sensitivity for gastric functions, suggesting that there is a general sensitivity for interoceptive processes across the gastric and cardiac modality.     

Owning an Overweight or Underweight Body: Distinguishing the Physical,Experienced and Virtual Body

Our bodies are the most intimately familiar objects we encounter in our perceptual environment. Virtual reality provides a unique method to allow us to experience having a very different body from our own, thereby providing a valuable method to explore the plasticity of body representation. In this paper, we show that women can experience ownership over a whole virtual body that is considerably smaller or larger than their physical body. In order to gain a better understanding of the mechanisms underlying body ownership, we use an embodiment questionnaire, and introduce two new behavioral response measures: an affordance estimation task (indirect measure of body size) and a body size estimation task (direct measure of body size). Interestingly, after viewing the virtual body from first person perspective, both the affordance and the body size estimation tasks indicate a change in the perception of the size of the participant''s experienced body. The change is biased by the size of the virtual body (overweight or underweight). Another novel aspect of our study is that we distinguish between the physical, experienced and virtual bodies, by asking participants to provide affordance and body size estimations for each of the three bodies separately. This methodological point is important for virtual reality experiments investigating body ownership of a virtual body, because it offers a better understanding of which cues (e.g. visual, proprioceptive, memory, or a combination thereof) influence body perception, and whether the impact of these cues can vary between different setups.     

Interplay of Agency and Ownership: The Intentional Binding and Rubber Hand Illusion Paradigm Combined

The sense of agency (SoA) refers to the phenomenal experience of initiating and controlling an action, whereas the sense of ownership (SoO) describes the feeling of myness an agent experiences towards his or her own body parts. SoA has been investigated with intentional binding paradigms, and the sense of ownership (SoO) with the rubber-hand illusion (RHI). We investigated the relationship between SoA and SoO by incorporating intentional binding into the RHI. Explicit and implicit measures of agency (SoA-questionnaire, intentional binding) and ownership (SoO-questionnaire, proprioceptive drift) were used. Artificial hand position (congruent/incongruent) and mode of agent (self-agent/other-agent) were systematically varied. Reported SoO varied mainly with position (higher in congruent conditions), but also with agent (higher in self-agent conditions). Reported SoA was modulated by agent (higher in self-agent conditions), and moderately by position (higher in congruent conditions). Implicit and explicit agency measures were not significantly correlated. Finally, intentional binding tended to be stronger in self-generated than observed voluntary actions. Results provide further evidence for a partial double dissociation between SoA and SoO, empirically distinct agency levels, and moderate intentional binding differences between self-generated and observed voluntary actions.