Elsevier

Neuropsychologia

Volume 107, December 2017, Pages 41-47
Neuropsychologia

Movements and body ownership: Evidence from the rubber hand illusion after mechanical limb immobilization

https://doi.org/10.1016/j.neuropsychologia.2017.11.004Get rights and content

Highlights

  • We examined whether preventing limb movements for one week affects body ownership.

  • We measured RHI and physiological indexes before and after immobilization.

  • Immobilization induced stronger illusion which was correlated to motor threshold.

  • Results show that movements act upon body ownership.

Abstract

There is no consensus on whether, and to what extent, actions contribute to constructing awareness of one's own body. Here we investigated at both physiological and behavioral level whether a prolonged limb immobilization affects body ownership. We tested a group of healthy participants, whose left-hand movements were prevented by a cast for one week, and a control group without any movement restriction. In both groups, we measured the strength of the rubber hand illusion (i.e., proprioceptive shift and questionnaire on ownership) and the physiological parameters known to be modulated by short-term arm immobilization (i.e., resting motor threshold, motor evoked potentials and force parameters) before and after the week of immobilization. Our results showed stronger illusory effects on the immobilized hand on both behavioral indexes and weaker illusory effects on the non-immobilized hand on the questionnaire. Additionally, the increased proprioceptive shift was positively correlated to the motor threshold of the contralateral hemisphere. Our findings show at both behavioral and physiological level that altering those movement-related signals which constantly stem from our own body parts, modulates the experience of those body parts as mine. This, in turn, supports the view of a direct role of actions in the developing and maintaining a coherent body ownership.

Introduction

Converging evidence in cognitive neuroscience shows that the sense of body ownership (i.e., the conscious experience of the body as one's own; Blanke et al., 2015; Gallagher, 2000) is a plastic neurocognitive construct. Indeed, it can be selectively altered by stroke-induced brain damages (Bottini et al., 2009, Fossataro et al., 2016, Gandola et al., 2012, Jenkinson et al., 2013, Pia et al., 2014a, Pia et al., 2016, Pia et al., 2014b, Piedimonte et al., 2016, Vallar and Ronchi, 2009) or by ad-hoc experimental manipulations in healthy participants (Burin et al., 2017, Costantini and Haggard, 2007, Lenggenhager et al., 2007, Longo et al., 2008, Slater et al., 2010, Tsakiris et al., 2011). In this latter case, a well-established paradigm is the Rubber Hand Illusion (hereinafter RHI) first reported by Botvinick and Cohen (1998). In this experimental manipulation, the participants’ left (or right) hand is positioned on a table, out of view. Then, a rubber hand is located medially to the participant's hand. When the experimenter strokes for a few minutes both hands in synchrony (but not in asynchrony), participants experience a feeling of ownership over the rubber hand. Such phenomenon is demonstrated both behaviorally (i.e., mislocalization of the own hand toward the fake hand and/or subjective rating of ownership) and physiologically (e.g., skin conductance responses: Armel and Ramachandran, 2003; Ehrsson et al., 2007; homeostatic regulation: Moseley et al., 2008; motor evoked potentials: Della Gatta et al., 2016).

The RHI is thought to arise because the initial conflict between vision of the rubber hand and tactile/proprioceptive representation of the own hand is resolved by the embodiment of the rubber hand within the participant's own body representation (Botvinick, 2004, Makin et al., 2008). This, in turn, suggests that a key property for the emergence of a coherent sense of body ownership is the integration of multisensory signals that constantly reach the human body (i.e. visual, tactile and proprioceptive stimuli). Nonetheless, multisensory integration occurs not only in static conditions but also during actions. Indeed, we experience that our body belongs to us also when we move (“I know that this moving hand is mine”). Under these circumstances, further signals add to touch, vision and proprioception such as those coming from skin/joint receptors and muscles spindles. Moreover, during willed actions also centrally generated motor commands (i.e., efferent signals) are produced which, in turn, give rise to a forward model of sensory predictions. In order to examine whether these extra signals contribute to the construction of the feeling of body ownership, some studies modified the original RHI paradigm comparing passive and/or active movements conditions with static conditions (Dummer et al., 2009, Kalckert and Ehrsson, 2012, Kalckert and Ehrsson, 2014, Kammers et al., 2009, Longo and Haggard, 2009, Riemer et al., 2013, Tsakiris et al., 2006, Walsh et al., 2011). Overall, this literature reported contrasting findings with respect to whether or not movement-related signals modulate the sense of body ownership. Indeed, some of them demonstrated that body ownership decreases when we move (Walsh et al., 2011), others found no differences in terms of body ownership between movement and no-movement conditions (Kalckert and Ehrsson, 2012, Kalckert and Ehrsson, 2014), and others more that it increases (Dummer et al., 2009, Riemer et al., 2013, Tsakiris et al., 2006).

At present, whether and to what extent actions contribute to the emergence of body ownership is still a matter of debate. In order to answer this question, here we investigated at both behavioral and physiological level whether body ownership is affected by preventing the possibility of making movements. Specifically, we examined whether a prolonged immobilization of one arm, obtained by means of a cast, alters the RHI. First, we checked whether mere seeing the cast and/or just experiencing a sudden movement restriction affects body ownership. Hence, we compared RHI measures before (hereinafter T0) and immediately after (hereinafter T1) having positioned the cast. In the same first session (at T0), we also recorded motor-related physiological measures (resting motor threshold, motor evoked potentials and force parameters) known to represent plastic reactions to immobilization (Avanzino et al., 2011, Avanzino et al., 2014, Burianova et al., 2016, Facchini et al., 2002, Furlan et al., 2016, Kaneko et al., 2003, Zanette et al., 2004). Secondly, RHI measures obtained immediately after the immobilization (T1) were compared with those after one week of complete immobilization, as well as physiological parameters (hereinafter T2). We hypothesized that if motor-related signals contribute to the emergence of body ownership, the immobilized hand should display an increased strength of the RHI as well as a correlation with physiological parameters subserving immobilization. Additionally, since it is known that unilateral motor deficits can induce an overuse of the healthy arm in order to keep on accomplishing habitual actions (Sato et al., 2005, Sato et al., 1999) and since this increases corticospinal excitability (Avanzino et al., 2011), we hypothesized a decreased strength of the RHI effects (i.e., a more rigid sense of body ownership) for the non-immobilized hand.

Section snippets

Participants

Forty right-handed (Oldfield, 1971) healthy participants (25 females, mean age = 22.4 years, SD = 2.9 years; mean educational level = 16.4 years, SD = 2.1 years) with no previous neurological/orthopedic diseases gave their written informed consent to participate in the study approved by the Bioethical Committee of University of Turin. In addition, we were able to assess a subset of fourteen participants for physiological measures (see below). None of them had a history of neurological,

Rubber hand illusion

Pre-proprioceptive judgment was subtracted from post-proprioceptive judgment and referred as proprioceptive drift (Tsakiris and Haggard, 2005). Then, in order to obtain the pure effect of the main synchronous stimulation, proprioceptive drift in the asynchronous condition was subtracted from proprioceptive drift in the synchronous condition and referred as proprioceptive shift (Abdulkarim and Ehrsson, 2016). Positive scores indicate higher values in synchronous condition, and so a relative

Rubber Hand Illusion

For proprioceptive shift (Fig. 2), the ANOVA yielded a significant three-ways interaction (F (2, 76) = 4.92, p = 0.01). Post-hoc comparisons showed that in the Experimental group at T2, the crucial condition for our purposes, the proprioceptive shift for the Left Hand (mean ± sd: 2.56 ± 2.33), that is the one immobilized for one week, was significantly higher with respect to both its own baseline at T0 (mean ± sd: 1.30 ± 3.05) and at T1 (mean ± sd: 0.65 ± 2.66) (p always < 0.05). By contrast,

Discussion

The aim of the present study was to investigate the effect of arm immobilization in building up a coherent sense of body ownership as indexed by the rubber hand illusion paradigm.

As first, we examined whether the mere vision of the cast and/or the sudden experience of being blocked affects body ownership (T0 vs. T1 comparison). Indeed, a plaster cast surrounding the hand is both a strong visual cue. Additionally, the cast immediately prevents movements. Consistently, previous literature

Acknowledgements

The authors would like to thank the participants involved in the study. This work has been funded by Talenti della Società Civile 2015 (Fondazione Goria and Fondazione Molo) scholarship to DB and by Miur grant [RBSI146V1D MIUR-SIR 2014] to FG.

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