Elsevier

Cortex

Volume 104, July 2018, Pages 180-192
Cortex

Special issue: Research report
Interoceptive ingredients of body ownership: Affective touch and cardiac awareness in the rubber hand illusion

https://doi.org/10.1016/j.cortex.2017.04.018Get rights and content

Abstract

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.

Introduction

The sense of body ownership represents a fundamental aspect of the psychological self (Gallagher, 2000). We usually take the ability to identify our body as our own for granted, but empirical research in the past few decades has shown that the sense of body ownership relies on our cognitive ability to combine information about the body originating from different sensory modalities (Tsakiris & Haggard, 2005). More specifically, the integration of different sensory modalities (i.e., multisensory integration) can be defined as the combination or synergy of information originating from two or more sensory channels, leading to unitary, yet not necessarily more accurate percepts than unisensory information (Guest & Spence, 2003; see Maravita et al., 2003, Stein and Stanford, 2008, for reviews).

One of the most widely used multisensory integration paradigms is the Rubber Hand Illusion (RHI, Botvinick & Cohen, 1998). In its classic version, the illusion relies on synchronous tactile stimulation of a visible rubber hand and of the participant's hidden hand, after which participants typically experience subjective feelings of ownership for the rubber hand (“it feels like the rubber hand is my own hand”) and they may perceive the position of their own hand as shifted towards that of the rubber hand (Botvinick & Cohen, 1998). These effects do not occur when the touch is asynchronous and hence are typically explained by a three-way weighted interaction between vision, touch, and proprioception: vision of tactile stimulation on the rubber hand ‘captures’ the tactile sensation on the participant's own hand, and this visual capture results in a mislocalisation of the felt location of one's own hand towards the spatial location of the visual percept, and corresponding changes in subjective ownership ratings. These bottom-up multisensory integration effects are subject to a number of top-down influences (Tsakiris et al., 2011, for review; see also Ferri, Ardizzi, Ambrosecchia, & Gallese, 2013). Recently, the relation between the two has been modelled according to Bayesian predictive coding schemes, emphasising that perception as a whole is not stimulus-driven, but rather an active process of instantiating neural contexts that allow for the enhanced or attenuated processing of forthcoming sensory events based on preexisting expectations (Friston, 2010). Specifically, the RHI is explained as the attenuation of the weighting of ascending, proprioceptive signals about the actual position of the participant's own arm in order to accept the more plausible (even if illusory) perceptual hypothesis that it is one's own body that receives synchronous tactile and visual information, rather than the alternative hypothesis that another body evokes tactile sensations (Apps and Tsakiris, 2013, Zeller et al., 2014). Moreover, the experience of owning a rubber hand during the RHI can cause a drop in temperature of the participant's own hand (Moseley et al., 2008), suggesting a down regulation not only of proprioception, but possibly also of the physiological state of one's own arm (see also Longo, Schüür, Kammers, Tsakiris, & Haggard, 2008). However, as subsequent studies have failed to replicate this temperature and other related findings regarding the downregulation of sensations from the participants' arm (Guterstam et al., 2011, Rohde et al., 2013, Schütz-Bosbach et al., 2009), further investigations of this measure and the physiological condition of participant's own arm are needed.

However, it is only in the last five years that a handful of studies have explored the role of interoception in multisensory integration and body ownership. This is especially relevant as according to a recent re-classification of the senses, interoception refers to information about the physiological condition of the body, involving sensations from within the body (e.g., relating to cardiac and respiratory functions or digestion) but also from the outside (e.g., temperature, itch, pain, and pleasure from sensual touch) conveyed by a specialised afferent pathway (Craig, 2002). Moreover, interoception is uniquely related to the generation of bodily feelings, informing the organism about its bodily needs (Craig, 2009, Seth, 2013). As such, the impact of interoception is thought to extend beyond homeostatic regulation, and to relate to self-awareness (Craig, 2009, Critchley et al., 2004, Damasio, 1994).

Interoceptive sensitivity refers to paradigms that quantify individual differences in behavioural performance, such as the Heartbeat Counting Task (Schandry, 1981), which entails participants silently counting their own heartbeat in specified time windows without taking their pulse or feeling their chest (see Garfinkel, Seth, Barrett, Suzuky, & Chritcley, 2015, for a broader discussion on such tasks and their relation to other subjective or metacognitive measures of interoceptive awareness). Tsakiris, Tajadura-Jiménez, and Costantini (2011) showed that individual differences in cardiac interoceptive sensitivity can affect the RHI. In particular, participants with low interoceptive sensitivity, as measured by an ‘off-line’ (i.e., administered prior to and independently of the RHI task) heartbeat counting task, reported a greater subjective experience of ownership for the rubber hand compared to people with high interoceptive sensitivity. Moreover, ‘off-line’ interoceptive sensitivity seems to predict behavioural and autonomic measures of temporary change in body ownership, namely increased proprioceptive drift and a drop in skin temperature of the real hand (Tsakiris et al., 2011). These studies suggest that individuals who can perceive their own interceptive signals with greater accuracy are less susceptible to the down-regulating effects of multisensory integration on both proprioception and the physiological state of one's own body.

However, the relationship between interoception and body representation has been investigated also in the context of the virtual body illusion (Aspell et al., 2013) and virtual RHI (Suzuki, Garfinkel, Critchley, & Seth, 2013). In both studies, visual feedback of participants' own heartbeat was provided ‘on-line’ (i.e., during the virtual reality tasks) by means of a flashing virtual body or hand in synchrony or out-of-synchrony with the participants' own heartbeats, with the synchronous condition increasing self-identification with the virtual body (Aspell et al., 2013) and embodiment of the rubber hand (Suzuki et al., 2013), respectively. Thus, somewhat contrary to the findings of Tsakiris and colleagues, when interoceptive signals are artificially provided also in the visual domain, vision seems capable of ‘capturing’ interoception, leading to enhanced down regulation of proprioception as in the classic RHI paradigm. Nevertheless, it remains unclear whether individuals with greater ‘off-line’ interoceptive sensitivity would be less susceptible to these visual effects, given their greater ability to perceive cardiac signals ‘from within’, or on the contrary, whether they would be more susceptible to these effects, given their ability to better regulate how much attention they attribute to interoception based on context (see Ainley et al., 2016, Decety and Fotopoulou, 2015, Fotopoulou, 2015, for the wider theoretical context of this hypothesis). To our knowledge, no study has assessed the relationship between ‘on-line’ and ‘off-line’ interoception during the RHI across different interoceptive modalities.

Importantly, the above studies on the role of interoception in body ownership have almost exclusively examined cardiac awareness. As there are currently only a handful of studies on whether sensitivity to cardiac signals predicts interoceptive sensitivity across other modalities (e.g., Herbert et al., 2012, Weiss et al., 2014; but see Garfinkel et al., 2016, Werner et al., 2009), the results of such studies cannot easily be generalised to all interoceptive modalities. Moreover, the ecological validity of providing ‘on-line’ visual or auditory feedback of interoceptive modalities that are not habitually experienced via such exteroceptive modalities (e.g., heartbeat related flashing of virtual bodies or hands) may be low, particularly in the context of multisensory integration tasks. By contrast, interoceptive modalities such as cutaneous pain or affective touch, whose stimuli are habitually located outside the body, can be manipulated ‘on-line’ with greater ecological validity.

In particular, a type of sensory pleasure on the skin is thought to be coded by specialised, unmyelinated C tactile (CT) afferents, which maximally respond to low-pressure, slow, caress-like tactile stimulation delivered at velocities between 1 and 10 cm/sec (Löken, Wessberg, Morrison, McGlone, & Olausson, 2009). These fibres are present only in the hairy skin of the body, and their activation linearly correlates with subjective reports of pleasantness (Löken et al., 2009). The discovery of a phylogenetically new primate lamina I spinothalamocortical pathway that conveys signals from small-diameter primary afferents from most tissues of the body, has led to some neuroscientists proposing a reclassification of the senses and an expansion of the term interoception. Specifically, CT afferents might take a distinct ascending pathway from the periphery to the posterior insular cortex (Olausson et al., 2002, Morrison et al., 2011; but see Gazzola et al., 2012 for evidence about concurrent activations of primary somatosensory cortices). Thus, key sensations from the body as such pain, itch, temperature and affective touch have been re-classified as interoceptive feelings and clearly separated from other discriminatory, exteroceptive sensations, such as non-affective touch. While several researchers continue to use the term interoception in its classic meaning, in this manuscript we define interoception according to this new reclassification which we think offers an important new perspective on homeostatic and affective regulation (Craig, 2002, Fotopoulou and Tsakiris, 2017, Gentsch et al., 2016).

Slow, caress-like touch activates both the CT system and other tactile modalities; in contrast, fast touch does not activate the CT afferents system to the same degree. Hence, comparing these two velocities is a way to make inferences about the involvement of the CT system in the perception of touch and the body more generally. In addition to this specialised, bottom-up interoceptive pathway, humans appear to be able to perceive slow, gentle touch as more pleasant than faster touch by vision alone and presumably due to top-down, learned processes (Gentsch et al., 2015, Morrison et al., 2011). Thus, manipulating the affective properties of touch in both felt and seen modalities in paradigms such as the RHI is both easier and more ecologically valid than using virtual cardiac signals, and may be better suited to characterise the relationship between multisensory integration, interoceptive sensitivity and the physiological regulation of body parts during the RHI.

Indeed, recent studies have found that affective touch can modulate the sense of body ownership in the RHI. In particular, slow, caress-like touch that activates CT afferents optimally can enhance the experience of owning a rubber hand more than fast, emotionally neutral touch that does not cause optimal CT activation (Crucianelli et al., 2013, Lloyd et al., 2013, Van Stralen et al., 2014). Additionally, Lloyd et al. (2013) showed that slow/CT-optimal touch enhanced the subjective embodiment of the rubber hand also in the condition when touch was applied to glabrous (non-hairy) skin, known to lack CT afferents (Vallbo, Olausson, & Wessberg, 1999). This finding suggests that the observed enhancing effect of affective touch in the RHI could be driven, at least partly, by top-down, learned expectations of sensory pleasure conveyed by the ‘seen’ slow touch on the rubber hand (Gentsch et al., 2015, Morrison et al., 2011), in the same manner as the virtual cardiac signals led to increased illusory ownership.

Moreover, in this setting, one could test whether individuals with higher versus lower interoceptive sensitivity, as measured by ‘off-line’ heartbeat perception accuracy, would either be less susceptible to the effects of affective touch on the RHI (as they would be more aware of the CT-related felt pleasure on their own hand, which should reduce the visual capture of touch in the RHI), or on the contrary, would be more susceptible to the illusion, given their greater capacity to regulate the perceptual (attentional) weighting they allocate to interoception depending on contextual factors (see Ainley et al., 2016, Decety and Fotopoulou, 2015, Fotopoulou, 2015, Krahé et al., 2013). The first hypothesis in turn assumes that cardiac awareness and CT-optimal affective touch perception will be related, so that individuals with greater cardiac awareness will also be more sensitive to perceiving the difference between CT-optimal and CT-suboptimal touch.

This study aimed to test these two hypotheses, and their relation, in two separate experiments. In addition, we aimed to test in an exploratory manner the relation between synchronicity and tactile pleasantness. Synchronous touch in the context of the RHI should be perceived as more pleasant, given its predictability (Joffily & Coricelli, 2013), but to our knowledge no study has examined the relation between the combined effects of synchronicity, CT-optimality and cardiac sensitivity on tactile pleasure.

Section snippets

Participants

Seventy-six women, aged 18 and over (M = 22.07, SD = 2.75), were recruited via the University of Hertfordshire research participation system. Participants received course credit or £5 for participating. Exclusion criteria included: being left handed or having a personal history of neurological or psychiatric disorders. The study was approved by an institutional ethics committee and conducted in accordance with the Declaration of Helsinki.

Design and statistical analysis

This experiment aimed to explore the role of individual

Participants

Sixty-nine right-handed women participated in the experiment in exchange for University credit or a £6 financial compensation. Six participants were later excluded from the analysis because we could not verify that they followed the experimental instruction correctly (i.e., they seemed to use the rating scale in an inverse manner). Thus, the final sample comprised 63 participants with a mean age of 24.03 years (SD = 6.48). Institutional ethical approval was obtained and the experiment was

Discussion of experiment 2 and general discussion

The aim of this second experiment was to investigate for the first time the interplay between different interoceptive modalities, namely cardiac awareness and affective touch, in body ownership. In particular, it sought to explore whether interoceptive sensitivity would modulate the extent to which affective touch influences the multisensory process taking place during the rubber hand illusion and leading to changes in various measures of ownership and sensory pleasure.

The results confirmed our

Conclusion

In conclusion, this study found that CT-optimal affective touch, an interoceptive modality of affective and social significance, 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

Funding

This work was funded by a European Research Council (ERC) Starting Investigator Award for the project ‘The Bodily Self’ grant number 313755 to A.F. and a University of Hertfordshire scholarship to L.C.

Acknowledgements

We are very grateful to Elizabeth Kolawole, Lauren Pearson and Maria Niedernhuber for their help with recruitment and testing. No conflicts of interest were reported.

References (58)

  • S. Schütz-Bosbach et al.

    Roughness perception during the rubber hand illusion

    Brain and Cognition

    (2009)
  • A.K. Seth

    Interoceptive inference, emotion and the embodied self

    Trends in Cognitive Sciences

    (2013)
  • K. Suzuki et al.

    Multisensory integration across exteroceptive and interoceptive domains modulates self-experience in the rubber-hand illusion

    Neuropsychologia

    (2013)
  • H.E. Van Stralen et al.

    Affective touch modulates the rubber hand illusion

    Cognition

    (2014)
  • Z. Abdulkarim et al.

    No causal link between changes in hand position sense and feeling of limb ownership in the rubber hand illusion

    Attention Perception & Psychophysics

    (2016)
  • R. Ackerley et al.

    Human C-Tactile afferents are tuned to the temperature of a skin-stroking caress

    The Journal of Neuroscience

    (2014)
  • V. Ainley et al.

    ‘Bodily precision’: A predictive coding account of individual differences in interoceptive accuracy

    Philosophical Transactions of the Royal Society B

    (2016)
  • M.A.J. Apps et al.

    The free energy self: A predictive coding account of self-recognition

    Neuroscience and Biobehavioral Reviews

    (2013)
  • J.E. Aspell et al.

    Turning body and self inside out: Visualized heartbeats alter bodily self-consciousness and tactile perception

    Psychological Science

    (2013)
  • M. Botvinick et al.

    Rubber hands ‘feel’ touch that eyes see

    Nature

    (1998)
  • A.D. Craig

    How do you feel? Interoception: The sense of the physiological condition of the body

    Nature Reviews Neuroscience

    (2002)
  • A.D. Craig

    How do you feel-now? The anterior insula and human awareness

    Nature Reviews Neuroscience

    (2009)
  • H.D. Critchley et al.

    Neural systems supporting interoceptive awareness

    Nature Neuroscience

    (2004)
  • L. Crucianelli et al.

    Bodily pleasure matters: Velocity of touch modulates body ownership during the rubber hand illusion

    Frontiers in Psychology

    (2013)
  • A.R. Damasio

    Descartes' error: Emotion, reason, and the human brain

    (1994)
  • J. Decety et al.

    Why empathy has a beneficial impact on others in medicine: Unifying theories

    Frontiers in Behavioural Neuroscience

    (2015)
  • F. Ferri et al.

    Closing the gap between the inside and the outside: Interoceptive sensitivity and social distances

    PLoS One

    (2013)
  • A. Fotopoulou

    Beyond the reward principle: Consciousness as precision seeking

    Neuropsychoanalysis

    (2015)
  • A. Fotopoulou et al.

    Mentalizing homeostasis: The social origins of interoceptive inference

    Neuropsychoanalysis

    (2017)
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