The importance of synchrony and temporal order of visual and tactile input for illusory limb ownership experiences - an FMRI study applying virtual reality

Abstract

In the so-called rubber hand illusion, synchronous visuotactile stimulation of a visible rubber hand together with one's own hidden hand elicits ownership experiences for the artificial limb. Recently, advanced virtual reality setups were developed to induce a virtual hand illusion (VHI). Here, we present functional imaging data from a sample of 25 healthy participants using a new device to induce the VHI in the environment of a magnetic resonance imaging (MRI) system. In order to evaluate the neuronal robustness of the illusion, we varied the degree of synchrony between visual and tactile events in five steps: in two conditions, the tactile stimulation was applied prior to visual stimulation (asynchrony of -300 ms or -600 ms), whereas in another two conditions, the tactile stimulation was applied after visual stimulation (asynchrony of +300 ms or +600 ms). In the fifth condition, tactile and visual stimulation was applied synchronously. On a subjective level, the VHI was successfully induced by synchronous visuotactile stimulation. Asynchronies between visual and tactile input of ±300 ms did not significantly diminish the vividness of illusion, whereas asynchronies of ±600 ms did. The temporal order of visual and tactile stimulation had no effect on VHI vividness. Conjunction analyses of functional MRI data across all conditions revealed significant activation in bilateral ventral premotor cortex (PMv). Further characteristic activation patterns included bilateral activity in the motion-sensitive medial superior temporal area as well as in the bilateral Rolandic operculum, suggesting their involvement in the processing of bodily awareness through the integration of visual and tactile events. A comparison of the VHI-inducing conditions with asynchronous control conditions of ±600 ms yielded significant PMv activity only contralateral to the stimulation site. These results underline the temporal limits of the induction of limb ownership related to multisensory body-related input.

Figure 1. Setup of the virtual hand illusion.

a) participant's view of the virtual reality environment, including the virtual limb and the stimulating rod at its starting position, b) the same view and rod at its end position touching the virtual finger, c) close-up picture of the pneumatic tactor, d) pneumatic tactor, attached to the participants' left index finger, e) participant lying on the table connected with the magnetic resonance imaging scanner. The participant has given written informed consent, as outlined in the PLOS consent form, to publication of her photograph.

Figure 2. Design of the study.

Displayed is the tactile stimulation in relation to the visual event for each condition. The 0 condition reflects the visuotactile stimulation in synchrony. Negative signs indicate the temporal delay (in milliseconds, ms), meaning that the tactile stimulation was applied prior to the visual stimulation; positive signs indicate that the tactile stimulation was applied after the visual stimulation.

Figure 3. Illusion vividness ratings.

a) Depicted are the virtual hand illusion (VHI) intensity ratings for each item in each condition. Items # 1–3 represent targets indicating ownership over the virtual hand, and items # 4–9 represent distractors. The number at the base of each target item bar indicates the number of non-responders (i.e., responses  = 0; only given for target items). Asterisks indicate significant differences between the synchronous and distinctly asynchronous conditions (Bonferroni-corrected p-values on item level). Note that there were only significant results for the target items. There were no significant differences between the synchronous and slightly asynchronous conditions for any item.Error bars indicate standard error; b) For illustrative purposes, the ratings of participants who responded minimally (participant # 1–5) or maximally (participant # 21–25) to illusion induction are depicted, arranged according to the proneness to perceive the VHI in the 0 condition (VHI vividness score). Colors indicate the conditions. The 0 condition reflects the visuotactile stimulation in synchrony. Negative signs indicate the temporal delay (in milliseconds), which means that the tactile stimulation was applied prior to the visual stimulation; positive signs indicate that the tactile stimulation was applied after the visual stimulation.

Figure 4. Results for the conjunction analysis.

a) whole brain analysis (p<.05, FWE-corrected); the number above each slice indicates the height (z-coordinate in Montreal Neurological Institute [MNI] space); b) analysis for bilateral ventral premotor cortex using regions of interest (p<.005, uncorrected); given is the y-coordinate of the slices of peak activity (in MNI space). MOG =  middle occipital gyrus; MTG =  middle temporal gyrus; S2+ =  secondary somatosensory cortex plus its vicinity; PG =  precentral gyrus. Color bars indicate t-values.