Having a body versus moving your body: How agency structures body-ownership

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Abstract

We investigated how motor agency in the voluntary control of body movement influences body awareness. In the Rubber Hand Illusion (RHI), synchronous tactile stimulation of a rubber hand and the participant’s hand leads to a feeling of the rubber hand being incorporated in the participant’s own body. One quantifiable behavioural correlate of the illusion is an induced shift in the perceived location of the participant’s hand towards the rubber hand. Previous studies showed that the induced changes in body awareness are local and fragmented: the proprioceptive drift is largely restricted to the stimulated finger. In the present study, we investigated whether active and passive movements, rather than tactile stimulation, would lead to similarly fragmented body awareness. Participants watched a projected image of their hand under three conditions: active finger movement, passive finger movement, and tactile stimulation. Visual feedback was either synchronous or asynchronous with respect to stimulation of the hand. A significant overall RHI, defined as greater drifts following synchronous than asynchronous stimulation, was found in all cases. However, the distribution of the RHI across stimulated and non-stimulated fingers depended on the kind of stimulation. Localised proprioceptive drifts, specific to the stimulated finger, were found for tactile and passive stimulation. Conversely, during active movement of a single digit, the proprioceptive drifts were not localised to that digit, but were spread across the whole hand. Whereas a purely proprioceptive sense of body-ownership is local and fragmented, the motor sense of agency integrates distinct body-parts into a coherent, unified awareness of the body.

Introduction

The sense of one’s own body is a fundamental product of the human mind. However, it is hard to study experimentally, because the body is “always there” (James, 1890/1981) in the background of mental life. Body awareness is therefore difficult to isolate and study in a controlled way. In addition, the bodily self involves two aspects which are normally confounded. These are the sense of agency and the sense of body ownership (Gallagher, 2000a, Gallagher, 2000b). Agency is the sense of intending and executing actions, including the feeling of controlling one’s own body movements, and, through them, events in the external environment. Agency involves a strong efferent component, because centrally generated motor commands precede voluntary movement. Body ownership refers to the sense that one’s own body is the source of sensations. The sense of body ownership involves a strong afferent component, through the various peripheral signals that indicate the state of the body. Importantly, the sense of body ownership is present not only during voluntary actions, but also during passive experience. In contrast, only voluntary actions produce a sense of agency. This asymmetry suggests that agency and ownership should have different effects on awareness of the body (for a review see Tsakiris & Haggard, 2005b). In the present context, body awareness refers to proprioceptive awareness, that is, the conscious experience of the location of a specific body-part (e.g., a finger or a hand) in space.

This hypothesis could be tested by applying a controlled, experimental method of manipulating body awareness, during active movements and passive stimulation. The “Rubber Hand Illusion” (RHI) offers one such method. Watching a rubber hand being stroked synchronously with one’s own unseen hand causes the rubber hand to be attributed to one’s own body, to “feel like it’s my hand” (Botvinick & Cohen, 1998). Correlated visual and tactile input induces a changed awareness of one’s own body, resulting in the incorporation of the rubber hand. One consequence of the visuo-tactile correlation is that the proprioceptively perceived position of one’s own hand seems closer to the rubber hand than it really is (Botvinick & Cohen, 1998). The RHI can thus be used to alter body awareness. Incorporation of the rubber hand into the body can be measured quantitatively via this drift in proprioceptively perceived position (Tsakiris & Haggard, 2005a). In the present study, we compare the strength of RHI induced by active and passive movement, to investigate the contributions of agency and ownership to body awareness.

We previously showed (Tsakiris & Haggard, 2005a) that body-awareness in the RHI is partly fragmented. In one experiment, participants viewed a rubber hand being stroked by a paintbrush on either the index or the little finger. The participant was always stroked by a similar paintbrush on the same finger as the rubber hand was stroked, synchronously for the experimental conditions and asynchronously for the control conditions. After synchronous stimulation, the stimulated finger was perceived to be significantly closer to the rubber hand than it really was, whereas the unstimulated finger was not (see Experiment 3 in Tsakiris & Haggard, 2005a). This pattern was replicated in a second experiment, in which both fingers were stimulated, one synchronously and one asynchronously with respect to the rubber hand (see Experiment 4 in Tsakiris & Haggard, 2005a). Again, only the finger that was synchronously stimulated was perceived to be significantly closer to the rubber hand. This fragmented pattern of localised proprioceptive drifts suggests that the sense of body ownership can be generated quite locally for individual stimulated body-parts. At the same time, a sense of the body as a coherent whole exists, both in everyday experience and in RHI experiments. For example, we showed that stroking the participant’s left hand while observing a right rubber hand being stroked did not induce any proprioceptive drift (Tsakiris & Haggard, 2005a). Therefore, self-attribution of the rubber hand to one’s own body arises as an interaction between bottom-up processes of visuo-tactile stimulation and top-down representations of a coherent body-scheme.

Where might the coherence of the body scheme originate in the brain? Is it primarily the effect of sensory or motor processing? The different principles of somatotopic organisation (Penfield & Boldrey, 1937) of the motor and sensory homunculus offer one approach to this question (see also de Vignemont, Tsakiris, & Haggard, 2005). The receptive field of neurons in primary somatosensory cortex (SI) corresponds to a small well-defined skin area. Neuroimaging studies show an orderly, segregated representation in human SI (Blankenburg, Ruben, Meyer, Schwiemann, & Villringer, 2003). We suggest that the fragmented quality of body awareness measured in RHI experiments may reflect discrete somatotopic coding in S1. Conversely, representations of different body parts strongly overlap in the primary motor cortex (M1). It seems that MI is organised for representing muscle groups and movement synergies rather than individual muscles (Lemon, 1988). Control of single finger movement recruits a population of neurons distributed throughout MI, rather than a discrete group based on somatotopic organisation (Schieber & Hibbard, 1993). These findings are consistent with the hierarchical control of synergies within the motor system. A task-level motor command (e.g., to grip an object) is expanded to produce synergic activation of muscles throughout the hand. Thus, in action, multiple body parts are controlled as an integrated whole.

Recent fMRI studies of overlap for activations evoked by different movements (Hlustik et al., 2001, Sanes et al., 1995) confirmed this difference between motor and sensory somatotopy: “the somatotopy in SI is more discrete and segregated, in contrast to the more integrated and overlapping somatotopy in MI” (Hlustik et al., 2001, p. 319) . If so, we might expect a less fragmented, more coherent version of the RHI for active (i.e. self-generated) movements than for purely sensory stimulation. For example, active movement of a single digit should produce general proprioceptive drifts for the whole hand, and not the localised proprioceptive drifts found after tactile stimulation.

We therefore compared the spread of the RHI from a stimulated finger to other fingers, after inducing RHI by three different kinds of stimulation. Participants viewed a video-projected image of their hand, while they were actively or passively moving either their index or little finger. The active movement was self-generated, whereas the passive movement was externally generated by the experimenter without any voluntary control by the participants. Comparing these conditions allowed us to disentangle agency and body-ownership. We assume that participants acquire a sense of owning the projected hand in both active and passive conditions. However, they acquire a sense of agency over the projected hand in the active condition only. A third tactile stimulation condition was included for comparison with previous studies. The video-projected hand was viewed either on-line (synchronous) or after a computer-controlled delay (asynchronous). Participants judged the proprioceptively perceived location of the index or little finger.

We predicted that synchronous vision of both active and passive movements would induce a drift in the proprioceptively perceived location of the participant’s finger, by analogy to previous tactile stimulation (i.e., larger proprioceptive drifts after synchronous than after asynchronous stimulation). We further predicted that the passive and tactile RHI would be localised to the stimulated finger, whereas in active RHI the perceived location of both the moved and unmoved fingers would drift to an equivalent extent. We hypothesised that efferent motor commands would be necessary for this spreading effect of RHI in the action condition: agency would facilitate the integration and coherence of body awareness.

Section snippets

Experimental design, methods, and participants

The experimental design was 3 × 2 × 2 × 2 factorial. Factor (i) had three blocked and counterbalanced levels: (a) tactile stimulation on a single finger by means of a paintbrush, (b) passive movement of a single finger generated by the experimenter, and (c) active movement of a single finger. Other factors were (ii) the delay in the projection of the hand image (synchronous or asynchronous), (iii) the finger stimulated (index vs. little), and (iv) the finger whose position the participant judged

Results

A baseline pre-test judgment of hand position was obtained prior to stimulation/movement of the hand and a post-test judgment was obtained after the stimulation/movement. The pre-test baseline judgments were subtracted from the post-test judgments prior to analysis for each trial. We use the term “proprioceptive drift” for this change in the perceived position of the hand due to stimulation. Positive proprioceptive drifts represent a mislocalisation towards the projected hand image. Table 1

Discussion

We compared the influence of agency and sensory afference on body-awareness using a version of the RHI. In particular, we used a quantitative measurement of the RHI, namely a drift in the proprioceptively sensed position of one’s own hand towards the rubber hand, to investigate the way efferent information influences the perception of one’s own body. First, we showed that the manipulation of the video-projection of one’s own hand induces a similar effect to the original RHI. Specifically,

Acknowledgments

The authors thank Richard Thomas for assistance and Chris Frith for his helpful comments. This work was partly supported by ESRC grant R00023946 to PH and by ESRC grant PTA-026-27-0889 to MT.

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