Absence of reliable physiological signature of illusory body ownership revealed by fine-grained autonomic measurement during the rubber hand illusion.

Hugo D Critchley,Jamie Ward,Vanessa Botan,Jane Elizabeth Aspell

doi:10.1371/journal.pone.0237282

Hugo D Critchley, Jamie Ward + Show 2 more

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https://doi.org/10.1371/journal.pone.0237282

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Abstract

The neural representation of a 'biological self' is linked theoretically to the control of bodily physiology. In an influential model, selfhood relates to internal agency and higher-order interoceptive representation, inferred from the predicted impact of efferent autonomic nervous activity on afferent viscerosensory feedback. Here we tested if an altered representation of physical self (illusory embodiment of an artificial hand) is accompanied by sustained shifts in autonomic activity. Participants (N = 37) underwent procedures for induction of the rubber hand illusion (synchronous stroking of own unseen hand and observed stroking of artificial hand) and a control condition (asychronous stroking). We recorded electrocardiography, electrodermal activity, and a non-invasive measure of multiunit skin sympathetic nerve activity (SKNA) from the chest. We compared these autonomic indices between task conditions, and between individuals who did and did not experience the illusion. Bayes factors quantified the strength of evidence for and against null hypotheses. Observed proprioceptive drift and subjective reports confirmed the efficacy of the synchronous (vs asynchronous) condition in inducing illusory hand ownership. Stringent discriminant analysis classified 24/37 individuals as experiencing the rubber hand illusion. Surprisingly, heart rate, heart rate variability, electrodermal activity, and SKNA measures revealed no autonomic differences between synchronous vs asynchronous conditions, nor between individuals who did or did not experience the rubber hand illusion. Bayes factors indicated substantial evidence for no physiological differences. In contrast to earlier reports, our autonomic data show the absence of a reliable change in physiological state during the rubber hand illusion. More encompassing perturbations of self-experience, for example in full body illusions, may nevertheless be coupled to, or facilitated by, changes in efferent autonomic activity and afferent viscerosensory feedback. Our findings suggest that such changes in bodily physiology are not sustained as an obligatory component of the rubber hand illusion.

Highlights

The representation of the body’s physiological state and physical boundaries is argued to be fundamental to self-perception and awareness
The dependence of the experience of body ownership on dynamic coherence across senses is illustrated by the rubber hand illusion, induced through correspondence between somatosensory stimulation and visual feedback: An artificial ‘rubber’ hand is placed in front of a participant and seen to be stroked
Proprioceptive drift was greater in the synchronous condition (M = 26.0 mm, SD = 5.46) than in the asynchronous condition (M = 4.6mm, SD = 3.67), t(36) = 3.097, p = 0.004, 95% CI [7.38, 35.41], d = 7.56, BH (0,1) = 0.123, there is moderate evidence for H1

Summary

Introduction

The representation of the body’s physiological state and physical boundaries is argued to be fundamental to self-perception and awareness. This representation is built upon the integration of sensory information across modalities with expectations and predictions regarding what our body should be doing [1,2,3,4]. The dependence of the experience of body ownership on dynamic coherence across senses is illustrated by the rubber hand illusion, induced through correspondence between somatosensory stimulation and visual feedback: An artificial ‘rubber’ hand is placed in front of a participant and seen to be stroked. Less subjective measures of the illusion include ‘proprioceptive drift’, where the judged location of the participant’s own hand shifts to be nearer the rubber hand. Even despite the relative consistency across studies of exaggerated reactivity to threats to an embodied rubber hand [8], these effects may be more nuanced, in some cases relating more to physical contact than threat [9,10]

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