The rubber hand illusion in microgravity and water immersion.

Our body has evolved in terrestrial gravity and altered gravitational conditions may affect the sense of body ownership (SBO). By means of the rubber hand illusion (RHI), we investigated the SBO during water immersion and parabolic flights, where unconventional gravity is experienced. Our results show that unconventional gravity conditions remodulate the relative weights of visual, proprioceptive, and vestibular inputs favoring vision, thus inducing an increased RHI susceptibility.

We evolved on Earth, and our bodies have constantly been exposed to earthly gravity (1 g); hence, it has been suggested that the gravitational input significantly contributes to building a coherent sense of body ownership (SBO)[1], i.e., the feeling that different body parts belong to one’s own body[2]. Reports from subjects exposed to altered gravity conditions show various illusory body perceptions yielding errors in body localization, body acceleration, and body configuration[3-5]. The present work aims to investigate whether and to what extent experimental procedures simulating altered gravity conditions, such as microgravity (a condition in which people or objects appear to be weightless) and water immersion (a condition used to simulate zero gravity), can affect SBO. To manipulate SBO, we employed the well-known rubber hand illusion[6] (RHI) paradigm, where individuals watch a lifelike rubber hand being touched while their own hand, hidden from view, is touched synchronously. Our brain solves the multisensory conflict between the felt touch of one’s own hand and the vision of a touched rubber hand by incorporating the artificial hand, which is perceived as a part of the own body (i.e., embodied)[7-9].

In order to modulate the gravitational input, the RHI was administered in two unconventional gravitational environments: (1) a parabolic flight (Parabolic flight experiment), in a campaign organized by the European Space Agency (ESA); and (2) immersion in water in a swimming pool (Swimming pool experiment). Both experimental contexts expose the nervous system to altered gravity conditions (see below), during which any difference in objective (a shift in the perceived position of the real hand) and subjective (the reported SBO over the rubber hand) measurements of the RHI may inform us of a gravity-dependent effect on the multisensory integration process subtending the SBO. In particular, we predict that the reduced gravitational pull will lead to an attenuated SBO, which, in turn, will increase the susceptibility to the RHI (i.e., embodiment of the fake hand). In the Parabolic flight experiment (sample: n = 5), the RHI was induced in short (12 s)[10] stimulation sessions performed during both microgravity (0 g) and normal gravity (1 g) phases of each parabola (Fig. 1a). During parabolic flights, microgravity resembles 0 g and lasts about 20–25 s, whereas, in between parabolas, the aircraft flies in 1 g conditions (see Methods and Supplementary Information for the details about the acceleration). The feeling of weightlessness occurs when the airplane is in free fall only because in this condition, the aircraft’s speed and trajectory cancel out gravitational acceleration[11]. In the Swimming pool experiment (sample: n = 19), the RHI was performed during water immersion (Fig. 1c) and, as a baseline condition, out of the water on the ground (Fig. 1b). The water immersion condition was used for simulating zero gravity[12] since it can influence body posture[13], alter the habitual relationship between muscle activation and limb position[14], and change the innervations of muscle spindles[15]. In both experiments, objective (proprioceptive drift) and subjective (embodiment questionnaire) RHI measures were collected after both synchronous (wherein the RHI generally occurs) and asynchronous (wherein the RHI generally does not occur, i.e., control condition) visuo-tactile stimulations of the real and the fake hands (see details in Methods and Fig. 1).

Fig. 1

Experimental settings.

Upper panel (a): Parabolic flight experiment. Participants underwent the RHI procedure during a parabolic flight: in normal gravity (1 g, in red) during steady horizontal flight, and in microgravity (0 g, in blue). The tactile stimulation was delivered via a fully automated system assembled ad hoc for the experiment. Lower panel (b, c): Swimming pool experiment. Participants underwent the RHI both in an ordinary laboratory (on ground condition, in orange, b) and in a private swimming pool (water immersion condition, in green, c). For graphical purposes, the coat used to cover the right shoulder and arm of participants in both experiments is not shown in the figure.

The results were the following: the proprioceptive drift (i.e., the shift of the felt position of one’s own hand toward the rubber hand), was modulated by the altered gravitational input in both experiments (see statistical details in Fig. 2b, h). In particular, during parabolic flights, a greater proprioceptive drift was found in microgravity as compared to normal gravity in both synchronous and asynchronous conditions (Fig. 2c). In the Swimming pool experiment, significant differences in the proprioceptive drift between synchronous and asynchronous conditions were found in both gravity environments (Fig. 2g, i), but, crucially, greater proprioceptive drift values were observed only after the synchronous stimulation in water immersion as compared to the ground condition (Fig. 2i). As for the embodiment questionnaire (i.e., the subjective feeling of embodying the rubber hand), a gravity-induced modulation was present in the Parabolic flight experiment only (Fig. 2e). Notably, in both experiments, the typical greater illusory experience during the synchronous than asynchronous stimulation was found irrespective of the gravity conditions (Fig. 2d, j). However, only in the Parabolic flight experiment, higher embodiment ratings were reported in microgravity relative to normal gravity in both asynchronous and synchronous stimulation, even if this latter comparison does not reach the significance level (Fig. 2l).

Fig. 2

Results.

Upper panel (a–f): Parabolic flight experiment. Lower panel (g–l): Swimming pool experiment. Error bars represent standard errors of the means. Dots represent single-subject values, i.e., the mean of each participant’s judgment in each condition. °tendency toward statistical significance; *p < 0.05; ***p < 0.001. Values are normalized in z scores.

In both experiments, altered gravity conditions (i.e., 0 g in the Parabolic flight experiment; water immersion in the Swimming pool experiment) led to a modulation of the perceived hand location, with an increased shift of the own hand position, hidden from view, toward the (visible) rubber hand. These results show that the less reliable proprioceptive inputs experienced in the gravity experimental manipulations enhance the RHI susceptibility when considering the proprioceptive drift measure after the synchronous stimulation. We propose that these results can be accounted for within the Bayesian causal inference theories of multisensory integration, which have been suggested to regulate SBO and its manipulations[9,16-18]. Individuals use probabilistic representations of their surroundings and their own body that take into account information about sensory uncertainty to infer the causal structure of sensory signals and optimally process them to create a clear perceptual distinction between the self and the nonself[16]. Therefore, when people are presented with two stimuli from different modalities, they initially infer whether these have the same origin (i.e., cause) or not, and then they combine their information according to these beliefs[19]. In the case of the RHI, the causal inference principle predicts that the rubber hand should be perceived as part of the participant’s own body if a common cause is inferred for the visual, tactile, and proprioceptive signals, meaning that when the real hand is not visible, the rubber hand might be inferred as the source of the tactile and the proprioceptive inputs[16]. In our experiments, the lack of reliable proprioceptive information (a key element for SBO to arise) caused by gravity experimental manipulations may have decreased, or even abolished, the discrepancy between sensory inputs, leading to a stronger fusion of visual and somatosensory impressions (not affected by altered gravity). As a consequence, the brain, through a probabilistic computational process, inferred that visual and tactile inputs might arise from the same source. In other words, it assumed that the rubber hand was the common cause of vision and somatosensation by dynamically taking into account all available sensory evidence given their relative reliability and prior information.

Moreover, we found additional effects only in the Parabolic flight experiment, where not only proprioception (affected during both microgravity[20] and water immersion[21]), but also the vestibular system is perturbed[22,23]. Indeed, our vestibular system, which evolved to optimally work on ground in a 1 g environment, provides us with erroneous or disorienting information in microgravity conditions, where proprioceptive and vestibular signals[24] become unreliable sources of information. Firstly, results show a modulation after the asynchronous (control) condition, with an increased shift toward the rubber hand and higher embodiment ratings, in microgravity than in normal gravity. This increased SBO found during the asynchronous (generally assumed to be the control) stimulation might suggest that the multisensory integration time-window is extended during microgravity. Namely, the 0 g condition, in which proprioceptive and vestibular cues are greatly attenuated, would extend the time-window in which multisensory integration occurs, inducing a stronger illusory experience even during asynchronous tactile and visual stimulations. Accordingly, it has been shown that peripheral sensory loss in vestibular-deficient patients can alter multisensory integration by reducing the ability to temporally combine sensory cues appropriately[25,26] and making patients more susceptible to experimental manipulations of the visual inputs[27]. Secondly, results show enhanced subjective embodiment experience after the synchronous stimulation. These findings are in line with studies demonstrating a link between vestibular signals and body ownership[28,29], and in particular, with the results of previous research proving increased subjective ratings of embodiment during the RHI after galvanic vestibular stimulation[30] (although controversial results have been reported[31,32]). Explicit SBO is a complex and multifactorial experience and, as such, to be altered, it requires the modulation of converging multisensory information coming from our body. Accordingly, previous evidence shows that during parabolic flights, reduced intrinsic connectivity[11] occurs in the temporoparietal junction, which is thought to contribute to the integration of vestibular, visual, and proprioceptive inputs[33].

In summary, our results suggest that altered gravity conditions modulate the SBO, with stronger illusory embodiment of the rubber hand occurring during microgravity—where both vestibular and proprioceptive inputs are weakened—than during water immersion—where proprioception only is attenuated. Taken together, these findings contribute new evidence to our understanding of the neurocognitive mechanisms subtending our experience of the self as a unitary body. Internal brain models of multisensory integration should consider the fundamental yet neglected role of gravitational input in shaping SBO, thus increasing our understanding of the cognitive alterations experienced by astronauts during spaceflight missions.

Methods

Participants

Overall, 25 healthy volunteers with normal or corrected-to normal vision participated in the study (14 males; mean age: 27.3 ± 3.6; years of education: 17.2 ± 1.4). Six participants (3 males; mean age: 31.6.5 ± 3.4; years of education: 17.8 ± 0.4) took part in the Parabolic flight experiment, and 19 participants (11 males; mean age: 29.5 ± 3.45; years of education: 25.8 ± 2.3) took part in the Swimming pool experiment. Since a participant of the Parabolic flight experiment got sick during the flight, he was excluded from the analysis; therefore the sample of the Parabolic flight experiment resulted in five participants (2 males; mean age: 32 ± 3.7; years of education: 17.8 ± 0.4). All the participants of the Parabolic flight experiment had flown before on parabolic flights (i.e., they all underwent at least 31 parabolas before taking part to the present study). All participants were right-handed, as assessed with the Edinburgh Handedness Inventory[34], naïve to the experimental procedure and gave their written informed consent to take part to the study. None of them had a history of neurological, major medical, or psychiatric disorders. The study was approved by the local ethics committee of the University of Turin (prot. n. 153210), by the ESA medical board, and by the Centre Hospitalier Universitaire de Caen, (Caen, France). All clinical investigations have been conducted according to the principles expressed in the Declaration of Helsinki.

Table 1

Embodiment questionnaire (Botvinick and Cohen[6]).

1. It seemed as though the touch I felt was caused by the paintbrush touching the rubber hand

2. It seemed as if I were sensing the touch of the paintbrush in the location where I saw the rubber hand touched

3. I felt as if the rubber hand were my hand

4. It felt as if my hand were drifting toward the left/right (toward the rubber hand)

5. It seemed as if the touch I was feeling came from somewhere between my own hand and the rubber hand

6. It felt as if my hand were turning “rubbery”

The questionnaire consists of six selected statements (1–3 target questions, 4–6 control questions) from a previous study (Botvinick and Cohen[6]). Participants were asked to evaluate the vividness of their experience of ownership over the rubber hand using a 7-point Likert scale, by rating their agreement/disagreement with each item (–3 = strong disagreement; +3 = strong agreement; 0 = neither agreement nor disagreement).