Interoceptive Ingredients of Body Ownership: Affective Touch and Cardiac Awareness in the Rubber Hand Illusion

This document is the Accepted Manuscript version of the following article: Laura Crucianelli, Charlotte Krahe, Paul M. Jenkinson, Aikaterini (Katerina) Fotopoulou, 'Interoceptive Ingredients of Body Ownership: Affective Touch and Cardiac Awareness in the Rubber Hand Illusion', Cortex, first published online 1 May 2017, available at doi: https://doi.org/10.1016/j.cortex.2017.04.018. © 2017 Elsevier Ltd. All rights reserved.The sense of body ownership represents a fundamental aspect of bodily self-consciousness. Using multisensory integration paradigms, recent studies have shown that both exteroceptive and interoceptive information contribute to our sense of body ownership. Interoception refers to the physiological sense of the condition of the body, including afferent signals that originate inside the body and outside the body. However, it remains unclear whether individual sensitivity to interoceptive modalities is unitary or differs between modalities. It is also unclear whether the effect of interoceptive information on body ownership is caused by exteroceptive ‘visual capture’ of these modalities, or by bottom-up processing of interoceptive information. This study aimed to test these questions in two separate samples. In the first experiment (N = 76), we examined the relationship between two different interoceptive modalities, namely cardiac awareness based on a heartbeat counting task, and affective touch perception based on stimulation of a specialized C tactile (CT) afferent system. This is an interoceptive modality of affective and social significance. In a second experiment (N = 63), we explored whether ‘off-line’ trait interoceptive sensitivity based on a heartbeat counting task would modulate the extent to which CT affective touch influences the multisensory process during the rubber hand illusion (RHI). We found that affective touch enhanced the subjective experience of body ownership during the RHI. Nevertheless, interoceptive sensitivity, as measured by a heartbeat counting task, did not modulate this effect, nor did it relate to the perception of ownership or of CT-optimal affective touch more generally. By contrast, this trait measure of interoceptive sensitivity appeared most relevant when the multisensory context of interoception was ambiguous, suggesting that the perception of interoceptive signals and their effects on body ownership may depend on individual abilities to regulate the balance of interoception and exteroception in given contexts.Peer reviewedFinal Accepted Versio

The role of the skin in interoception : a neglected organ?

In the past two decades, interoception has received increasing attention in the fields of psychology and cognitive science, as well as neuroscience and physiology. A plethora of studies adopted the perception of cardiac signals as a proxy for interoception. However, recent findings have cast doubt to the methodological and intrinsic validity of the tasks used thus far. Therefore, there is an ongoing effort to improve the existing cardiac interoceptive tasks and to identify novel channels to target the perception of the physiological state of the body. Amid such scientific abundancy, one could question whether the field has been partially neglecting one of our widest organs in terms of dimensions and functions, the skin. According to some views grounded on anatomical and physiological evidence, skin-mediated signals such as affective touch, pain, and temperature have been re-defined as interoceptive. Nevertheless, there is no agreement at this regard. Here, we discuss some of the anatomical, physiological, and experimental arguments supporting the scientific study of interoception by means of skin-mediated signals. We argue that more attention should be paid to the skin as a sensory organ that monitors the bodily physiological state, and further propose thermosensation as a particularly attractive model of skin-mediated interoception.European Research Council under the European Union’s horizon 2020 research and innovation programme (SELF-UNITY)Marie Skłodowska-Curie Intra-European Individual Fellowship (HOMEOTHERMIC SELF)Accepte

Bodily Pleasure and the Self: Experimental, Pharmacological and Clinical Studies on Affective Touch

In the last decade, neuroscience and psychology alike have paid increasing attention to the study of affective touch, which refers to the emotional and motivational facets of tactile sensation. Some aspects of affective touch have been linked to a neurophysiologically specialised system, namely the C tactile (CT) system. While the role of this system for affiliation, social bonding and communication of emotions have been investigated, less is known about the potential role of affective touch in the awareness of the body as our own, i.e. as belonging to our psychological ‘self’. This thesis attempted to contribute to the knowledge on affective touch and its relation to body awareness, by exploring the potential role of this modality to the way we perceive and make sense of our body as our own. Specifically, this work aimed to advance the current state of knowledge by investigating: 1) the effect of affective touch on the sense of body ownership, which is a fundamental aspect of body awareness; 2) the relation between interoceptive modalities, originating both internally (i.e. cardiac awareness) and peripherally (i.e. affective touch), and exteroception in body awareness; 3) the effect of intranasal oxytocin on the perception of affective touch and bodily awareness; 4) the perception and social modulation of affective touch in psychiatric patients who show difficulties in body awareness, namely patients with Anorexia Nervosa, and 5) the modulating role of self-other distinction and of self-other relation in the perception of affective touch and body awareness. In a first experiment (N = 52) the rubber hand illusion paradigm was used to investigate the role played by CT-optimal, affective touch in the sense of body ownership. The results showed that slow, pleasant touch enhanced the experience of embodiment in comparison to faster, neutral touch, suggesting that affective touch might uniquely contribute to the sense of body ownership. The following study (N = 75), used a similar methodology to test whether interoceptive sensitivity as measured by a heartbeat counting task would modulate the extent to which affective touch influences the multisensory process taking place during the rubber hand illusion. The results could not confirm a systematic relation between interoceptive sensitivity and the perception of affective touch, nor its influence on body ownership. The next study (N = 41) included a double-blind, placebo-controlled, randomised, cross-over design testing the effect of intranasal oxytocin on the perception of affective touch and body ownership, as measured by means of the rubber hand illusion. There was no evidence supporting the hypothesis that intranasal oxytocin could influence the CT system as tested in this study. The next study (N = 55) applied some of the above methodologies to investigate the perception of CT-optimal touch in patients with anorexia nervosa and its emotional modulation by top-down factors. The results confirmed the hypothesis that people with anorexia nervosa show a reduced perception of affective touch compared to healthy controls, but its perception was not influenced by top-down affective modulation, in the sense that both patients and healthy controls perceived touch as more pleasant when presented concurrently with positive facial expressions compared to neutral and negative faces. Finally, the last two studies (N = 76 and 35 healthy volunteers, respectively) focused on the relationship between affective touch and body awareness in the context of social cognition. These studies used both online and offline social modulation paradigms to investigate the role of self-other distinction and of self-other relation in the perception of affective touch. The results showed that positive top-down social information can enhance the perceived pleasure of tactile stimulation. Taken together, these studies point to the central role of affective touch in body awareness and social cognition. Finally, they also pave the way for future studies examining the role of disruptions of the CT system in the development of neuropsychiatric impairments of body awareness and social cognition

Visuo-thermal congruency modulates the sense of body ownership

Thermosensation has been redefined as an interoceptive modality that provides information about the homeostatic state of the body. However, the contribution of thermosensory signals to the sense of body ownership remains unclear. Across two rubber hand illusion (RHI) experiments (N = 73), we manipulated the visuo-thermal congruency between the felt and seen temperature, on the real and rubber hand respectively. We measured the subjectively experienced RHI, the perceived hand location and temperature of touch, and monitored skin temperature. We found that visuo-thermal incongruencies between the seen and felt touch reduced the subjective and behavioural RHI experience (Experiment 1). Visuo-thermal incongruencies also gave rise to a visuo-thermal illusion effect, but only when the rubber hand was placed in a plausible position (Experiment 2) and when considering individual differences in interoceptive sensibility. Thus, thermosensation contributes to the sense of body ownership by a mechanism of dynamic integration of visual and thermosensory signals.Göran Gustafsson FoundationSwedish Research CouncilEuropean Research Council under the European Union’s horizon 2020 research and innovation programme (SELF-UNITY)Marie Skłodowska-Curie Intra-European Individual Fellowship (HOMEOTHERMIC SELF)Accepte

Limits of cross-modal plasticity? Short-term visual deprivation does not enhance cardiac interoception, thermosensation, or tactile spatial acuity

In the present study, we investigated the effect of short-term visual deprivation on discriminative touch, cardiac interoception, and thermosensation by asking 64 healthy volunteers to perform four behavioral tasks. The experimental group contained 32 subjects who were blindfolded and kept in complete darkness for 110 minutes, while the control group consisted of 32 volunteers who were not blindfolded but were otherwise kept under identical experimental conditions. Both groups performed the required tasks three times: before and directly after deprivation (or control) and after an additional washout period of 40 minutes, in which all participants were exposed to normal light conditions. Our results showed that short- term visual deprivation had no effect on any of the senses tested. This finding suggests that short-term visual deprivation does not modulate basic bodily senses and extends this principle beyond tactile processing to the interoceptive modalities of cardiac and thermal sensations.Swedish Research Council, 2017-03135Marie Skłodowska-Curie Intra-European Individual Fellowship, 891175Accepte

Interoception as independent cardiac, thermosensory, nociceptive, and affective touch perceptual submodalities

Interoception includes signals from inner organs and thin afferents in the skin, providing information about the body’s physiological state. However, the functional relationships between interoceptive submodalities are unclear, and thermosensation as skin-based interoception has rarely been considered. We used five tasks to examine the relationships among cardiac awareness, thermosensation, affective touch, and nociception. Thermosensation was probed with a classic temperature detection task and the new dynamic thermal matching task, where participants matched perceived moving thermal stimuli in a range of colder/warmer stimuli around thermoneutrality. We also examined differences between hairy and non-hairy skin and found superior perception of dynamic temperature and static cooling on hairy skin. Notably, no significant correlations were observed across interoceptive submodality accuracies (except for cold and pain perception in the palm), which indicates that interoception at perceptual levels should be conceptualised as a set of relatively independent processes and abilities rather than a single construct.Göran Gustafsson foundationSwedish Research CouncilEuropean Research Council under the European Union’s horizon 2020 research and innovation programme (SELF-UNITY)Marie Skłodowska-Curie Intra-European Individual Fellowship (HOMEOTHERMIC SELF)Accepte

Reading the mind in the touch: Neurophysiological specificity in the communication of emotions by touch

Copyright © 2017 The Authors. Published by Elsevier Ltd.. All rights reserved.Touch is central to interpersonal interactions. Touch conveys specific emotions about the touch provider, but it is not clear whether this is a purely socially learned function or whether it has neurophysiological specificity. In two experiments with healthy participants (N = 76 and 61) and one neuropsychological single case study, we investigated whether a type of touch characterised by peripheral and central neurophysiological specificity, namely the C tactile (CT) system, can communicate specific emotions and mental states. We examined the specificity of emotions elicited by touch delivered at CT-optimal (3 cm/s) and CT-suboptimal (18 cm/s) velocities (Experiment 1) at different body sites which contain (forearm) vs. do not contain (palm of the hand) CT fibres (Experiment 2). Blindfolded participants were touched without any contextual cues, and were asked to identify the touch provider's emotion and intention. Overall, CT-optimal touch (slow, gentle touch on the forearm) was significantly more likely than other types of touch to convey arousal, lust or desire. Affiliative emotions such as love and related intentions such as social support were instead reliably elicited by gentle touch, irrespective of CT-optimality, suggesting that other top-down factors contribute to these aspects of tactile social communication. To explore the neural basis of this communication, we also tested this paradigm in a stroke patient with right perisylvian damage, including the posterior insular cortex, which is considered as the primary cortical target of CT afferents, but excluding temporal cortex involvement that has been linked to more affiliative aspects of CT-optimal touch. His performance suggested an impairment in ‘reading’ emotions based on CT-optimal touch. Taken together, our results suggest that the CT system can add specificity to emotional and social communication, particularly with regards to feelings of desire and arousal. On the basis of these findings, we speculate that its primary functional role may be to enhance the ‘sensual salience’ of tactile interactions.Peer reviewedFinal Published versio

Subcortical contributions to the sense of body ownership

The sense of body ownership (i.e., the feeling that our body or its parts belong to us) plays a key role in bodily self-consciousness and is believed to stem from multisensory integration. The development of experimental paradigms that allow the controlled manipulation of body ownership in laboratory settings, such as the rubber hand illusion, provide an effective tool to investigate the malleability of the sense of body ownership and the boundaries distinguishing self and other. Neuroimaging studies on body ownership converge on the involvement of several cortical regions, including the premotor cortex and posterior parietal cortex. However, relatively less attention has been paid to subcortical structures that may also contribute to body ownership perception, such as the cerebellum and putamen. Here, on the basis of neuroimaging and neuropsychological observations, we provide an overview of relevant subcortical regions and consider their potential role in generating and maintaining a sense of ownership over the body. We also suggest novel avenues for future research targeting the role of subcortical regions in making sense of the body as our own

Editorial : When the body feels like mine : constructing and deconstructing the sense of body ownership through the lifespan

Marie Skłodowska-Curie Intra-European Individual Fellowship, 891175Israeli Science Foundation, 1169/17National Institute of Mental Health, R01MH 102272Accepte

A Multisensory Perspective on the Role of the Amygdala in Body Ownership

A sense of ownership over one's own body is essential for effective interaction with the world: acting upon objects or communicating with others relies on distinguishing between the parts of the world that constitute our self, and the parts of the world that do not. The sense of body ownership is frequently associated with activity in the ventral premotor cortex, intraparietal sulcus, and insula (Grivaz et al., 2017), and is believed to stem from multisensory integration (Ehrsson, 2012): congruent sensory signals are combined to provide a feeling of bodily self that is distinct from the surrounding environment. This is emphasized by the rubber hand illusion (RHI), in which synchronous, but not asynchronous, stroking of a rubber hand and the real hand (which is hidden from view) can induce a sense of ownership over the false limb (Botvinick and Cohen, 1998)