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

Developmental Perspectives on Interpersonal Affective Touch

In the last decade, philosophy, neuroscience and psychology alike have paid increasing attention to the study of interpersonal 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 widely investigated, only recently researchers have started to focus on the potential role of interpersonal affective touch in acquiring awareness of the body as our own, i.e. as belonging to our psychological ‘self’. We review and discuss recent developmental and adult findings, pointing to the central role of interpersonal affective touch in body awareness and social cognition in health and disorders. We propose that interpersonal affective touch, as an interoceptive modality invested of a social nature, can uniquely contribute to the ongoing debate in philosophy about the primacy of the relational nature of the minimal self

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

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

Restoring awareness: a review of rehabilitation in anosognosia for hemiplegia

Disturbances in body awareness offer important insights into neurocognitive processes involved in the construction of the bodily self. This review will focus on a specific disorder of awareness, namely, anosognosia for hemiplegia (AHP), or the denial of motor deficits contralateral to a brain lesion. Recently some progress has been made towards the management and rehabilitation of AHP, however to date no evidence-based treatment exists. Firstly, recent research on AHP will be reviewed, with the aim of providing an overview of the etiology, clinical presentation and assessment of the syndrome, as well as the major neurological and neuropsychological explanations. This article will then focus on recent advances in the management and rehabilitation of AHP, using a case study example of intervention-based (i.e. video replay) motor awareness recovery (Fotopoulou, Rudd, Holmes & Kopelman, 2009). Finally, a dynamic theoretical model of the multifaceted nature of anosognosia, using a predictive coding framework, will be proposed and future directions for research will also be discussed

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

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

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

Embodied Precision : Intranasal Oxytocin Modulates Multisensory Integration

© 2018 Massachusetts Institute of Technology.Multisensory integration processes are fundamental to our sense of self as embodied beings. Bodily illusions, such as the rubber hand illusion (RHI) and the size-weight illusion (SWI), allow us to investigate how the brain resolves conflicting multisensory evidence during perceptual inference in relation to different facets of body representation. In the RHI, synchronous tactile stimulation of a participant's hidden hand and a visible rubber hand creates illusory body ownership; in the SWI, the perceived size of the body can modulate the estimated weight of external objects. According to Bayesian models, such illusions arise as an attempt to explain the causes of multisensory perception and may reflect the attenuation of somatosensory precision, which is required to resolve perceptual hypotheses about conflicting multisensory input. Recent hypotheses propose that the precision of sensorimotor representations is determined by modulators of synaptic gain, like dopamine, acetylcholine, and oxytocin. However, these neuromodulatory hypotheses have not been tested in the context of embodied multisensory integration. The present, double-blind, placebo-controlled, crossover study ( N = 41 healthy volunteers) aimed to investigate the effect of intranasal oxytocin (IN-OT) on multisensory integration processes, tested by means of the RHI and the SWI. Results showed that IN-OT enhanced the subjective feeling of ownership in the RHI, only when synchronous tactile stimulation was involved. Furthermore, IN-OT increased an embodied version of the SWI (quantified as estimation error during a weight estimation task). These findings suggest that oxytocin might modulate processes of visuotactile multisensory integration by increasing the precision of top-down signals against bottom-up sensory input.Peer reviewedFinal Accepted Versio

Identifying with the Beautiful: Facial attractiveness effects on unisensory and multisensory self-other distinction

People tend to evaluate their own traits and abilities favourably and such favourable self-perceptions extend to attractiveness. However, the exact mechanism underlying this self-enhancement bias remains unclear and one possibility could be the identification with attractive others through blurring of self-other boundaries. Across two experiments, we used the enfacement illusion to investigate the effect of the attractiveness of others in the multisensory perception of the self. In a first experiment (N=35), participants were stroked on the cheek while looking at an attractive vs. non-attractive face being stroked on the cheek in synchrony or asynchrony. In the second experiment (N=35), two new faces were used and spatial incοngruency was introduced as a control condition. The results showed that increased ratings of attractiveness of an unfamiliar face lead to blurring of self-other boundaries, allowing the identification of our psychological self with another's physical self, and specifically their face, and this seems to be unrelated to perceived own attractiveness. The effect of facial attractiveness on face ownership showed dissociable mechanisms, with multisensory integration modulating the effect on similarity but not identification, an effect that may be purely based on vision. Overall, our findings suggest that others’ attractiveness may lead to positive distortions of the self, identifying with the more rather than less attractive others. This research provides a psychophysical starting point for studying the impact of others' attractiveness on how we perceive the self, which can be particularly important for individuals with malleable, embodied self-other boundaries and body image disturbances