Balancing body ownership: Visual capture of proprioception and affectivity during vestibular stimulation

Abstract

The experience of our body as our own (i.e. body ownership) involves integrating different sensory signals according to their contextual relevance (i.e. multisensory integration). Until recently, most studies of multisensory integration and body ownership concerned only vision, touch and proprioception; the role of other modalities, such as the vestibular system and interoception, has been neglected and remains poorly understood. In particular, no study to date has directly explored the combined effect of vestibular and interoceptive signals on body ownership. Here, we investigated for the first time how Galvanic Vestibular Stimulation (left, right, sham), tactile affectivity (a reclassified interoceptive modality manipulated by applying touch at C-tactile optimal versus non-optimal velocities), and their combination, influence proprioceptive and subjective measures of body ownership during a rubber hand illusion paradigm with healthy participants (N = 26). Our results show that vestibular stimulation (left GVS) significantly increased proprioceptive drift towards the rubber hand during mere visual exposure to the rubber hand. Moreover, it also enhanced participants' proprioceptive drift towards the rubber hand during manipulations of synchronicity and affective touch. These findings suggest that the vestibular system influences multisensory integration, possibly by re-weighting both the two-way relationship between proprioception and vision, as well as the three-way relationship between proprioception, vision and affective touch. We discuss these findings in relation to current predictive coding models of multisensory integration and body ownership.

Keywords: Affective touch; Bodily self; Body ownership; Multisensory integration; Vestibular stimulation.

Fig. 1

A) Timeline of one prototypical GVS block. At the beginning of each of the three GVS blocks (either LGVS, RGVS or Sham), participants undertook the visual capture condition, with measures taken before and after stimulation (see B for details of this condition and its measurements). Subsequently, one of the four stroking conditions (see C for further details) was conducted in a randomised order, with measures again taken before and after stimulation. B) Timeline of the visual capture condition. Before the visual capture condition started participants performed a proprioceptive judgement (pre-GVS measurement). Immediately afterwards, the vestibular or sham stimulation commenced for 2 min during which participants sat with their eyes open. During the last 15 s of vestibular or sham stimulation, the experimenter opened the box lid and instructed the participant to look at the rubber hand until told otherwise. After 120 s (total) stimulation the lid was closed and participants immediately performed a second proprioceptive judgement and completed the embodiment questionnaire (post-GVS measurements). C) Timeline of the stroking conditions. Each of the four stroking conditions (synchronous slow touch, synchronous fast touch, asynchronous slow touch and asynchronous fast touch) followed the same structure. Participants made an initial (pre-GVS measurement) proprioceptive judgement, followed immediately by vestibular or sham stimulation and concurrent tactile stimulation (i.e. stroking of both the participant and rubber hand's forearm) for 120 s, during which participants looked continuously at the rubber hand. A second proprioceptive judgement and embodiment questionnaire was completed immediately following completion of the 120 s concurrent vestibular / tactile stimulation (post-GVS measurements).

Fig. 2

Participants sat in front of the table, facing the box, and were asked to insert their left hand into the left compartment of the box, while the rubber hand was positioned in the compartment on the right, aligned with participant's left shoulder. Both the participant's and rubber hand's left index fingers were located on the corresponding marked spots. A) While the box was open, participants were asked to look inside and observe the rubber hand. In particular, during the stroking conditions, participants were instructed to follow the brush while it was stroking the rubber hand's forearm. B) Before and after each condition, with the box closed and covered by a black carton, participants had to perform a proprioceptive judgement (see Section 2.4).

Fig. 3

GVS effects during Visual Capture on Proprioceptive drift. A) Mean values of the proprioceptive drift measured in cm in the LGVS and in the RGVS; B) Mean values of the proprioceptive drift measured in cm in (LGVS+RGVS)/2 and Sham obtained during visual capture conditions. *= p < 0.01; Solid line=median; Black dot= mean; Whiskers: upper whisker = min(max(x), Q_3 + 1.5* IQR); lower whisker = max(min(x), Q_1 – 1.5* IQR).

Fig. 4

A) Mean values of the proprioceptive drift measured in cm in the LGVS and in the RGVS; B) Mean values of the proprioceptive drift measured in cm in (LGVS+RGVS)/2 and Sham obtained during the stroking conditions of the rubber hand illusion. SST= synchronous slow touch; SFT= synchronous fast touch; AST= asynchronous slow touch; AFT= asynchronous fast touch. * = p < 0.01; Solid line=median; Black dot= mean; Whiskers: upper whisker = min(max(x), Q_3 + 1.5* IQR); lower whisker = max(min(x), Q_1 – 1.5* IQR).