The body-related afferent signals that subserve body ownership (“this body is mine”) might have a key role in human sense of agency (“this action is due to my own will”); body ownership helps building up motor consciousness

The Role of Body-Related Afferent Signals in Human Sense of Agency. Maria Pyasik, Tiziano Furlanetto, Lorenzo Pia. Journal of Experimental Neuroscience, May 16, 2019. https://doi.org/10.1177/1179069519849907

Abstract: At present, most of the neurocognitive models of human sense of agency (ie, “this action is due to my own will”) have been traditionally rooted in a variety of internal efferent signals arising within the motor system. However, recent neuroscientific evidence has suggested that also the body-related afferent signals that subserve body ownership (ie, “this body is mine”) might have a key role in this process. Accordingly, in the present review paper, we briefly examined the literature investigating how and to what extent body ownership contributes to building up human motor consciousness. Evidence suggests that, if required by the context, body ownership per se can act on agency attribution (ie, independently from efferent signals). Hence, a unitary and coherent subjective experience of willed actions (ie, “this willed action is being realized by my own body”) requires both awareness of being an agent and of owning the body.

Keywords: Bodily self, body ownership, sense of agency, afferent signals, efferent signals

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When we achieve willed actions, we do not feel as though those acts simply happen to us, we strongly sense to be in charge. Such subjective experience of authorship is known as sense of agency.1 In other words, we are aware of intending, initiating, and controlling our volitional movements (so-called “body agency”),2 as well as their consequences in the external world (“external agency”),2 and this awareness is vital for survival. Indeed, perceiving to be an agent allows distinguishing actions that are self-generated from those that are generated by others. This, in turn, contributes to the key signature of human nature, that is, the phenomenological experience of self-consciousness.3

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It is worth emphasizing, however, that whenever we successfully achieve volitional actions, we feel not only being in control of our movements and their consequences but also that those movements are being executed through our own body (body agency). For instance, if I am thirsty and I quickly get a glass of water, I experience that my own body is moving toward the glass. In the absence of any movement, such an embodied and enduring sense of being aware of our own body, termed body ownership,16 is known to be rooted in multisensory integration. In other words, it arises whenever the body-related afferent sensory signals (ie, visual, tactile, proprioceptive, kinesthetic, auditory, etc) that constantly reach our body are integrated in both spatial and temporal terms. For example, if someone else caresses my arm, I experience that body part as my own because I see and I feel the touches at the same time and in the same place. All in all, the stronger the spatiotemporal congruency among these signals, the higher the feeling of body ownership.17–20 It is thought that in the human brain, body ownership is underpinned by the activity of a network including premotor areas, the occipitotemporal cortex, the primary/secondary somatosensory areas, and the anterior insula.18,21–23

Capitalizing on the above-mentioned considerations, it follows that the coherence, the richness, and the completeness of human subjective experience of being the agent of a given voluntary action necessarily requires both awareness of controlling the actions and awareness of owning the body that achieves them. However, whether, how, and to what extent body ownership has a role in building up such experiences is an issue that only very recently has come to the forefront of the scientific investigations. For these reasons, in this article, we aimed at reviewing all studies that, in one way or another, investigated the possible role of body ownership in building up the sense of agency over the body movements.

[...] In summary, this first set of studies showed that if an external object that is perceived as part of one’s own body moves together with the participant’s body, an illusory sense of agency over the movements of that object arises. This does not happen if the moving external object is not perceived as part of one’s own body.

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Another evidence came from a study employing the full-body illusion showing that when a virtual embodied avatar was walking repeatedly along a route, while the participant remained still, an illusion of walking occurred.40 This did not happen when the avatar was not embodied. It is also worth noting that highly automated actions, as walking, are thought to prime the movements and intentions to move in advance. In summary, this second set of studies showed that, if participants’ motor representations (eg, motor intentions, motor imagery or motor plan) match the movements of an external object perceived as part of one’s own body, an illusion of agency arises. This does not happen if the moving external object is not perceived as part of one’s own body.

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To sum up, here we reviewed evidence supporting the idea that body ownership does have a role in human sense of agency, specifically body agency. The review shows that being aware of one’s own body has a role per se in building and maintaining the sense of agency, namely it can act on agency attribution in the absence of any efferent signals, such as motor intentions and feedforward predictions, and causes preceding effects and so on. First, it is worth noticing that giving any role to body ownership is not trivial but, rather, consistent with human nature. Indeed, our actions are achieved mainly through the physical body,50 and the body is a prerequisite for any successful interaction with the environment.51 Indeed, it is already known that body ownership affects motor control, allowing to estimate limb positions,52 to tune motor commands,53 and to adjust errors.54 Hence, discovering its role also within motor consciousness would not be surprising. Here, we suggest that the signals that give rise to body ownership might have a key role in sense of agency by acting on agency attribution in the absence of any efferent signals. How is it possible to reconcile in a concrete manner this idea with the current neurocognitive model of the sense of agency? As already mentioned, the classical motor control model of sense of agency states that the experience of being an agent arises from the comparison between predicted and actual outcomes.4,7-10 This, in turn, means that action preparation is a necessary condition to have any experience of being an agent. We put forward the idea that under some circumstances, only seeing the own body moving would be enough to activate the neurocognitive processes subserving action preparation. At this point, the feeling of agency over that specific given act would be triggered. Such a process could be exemplified by the inference: “since this is my body part, any action performed by it would be intended by me.” Furthermore, in dynamic conditions, that is when we actually achieve the willed actions, body ownership would provide additional signals to the efferent motor-related signals and would contribute to the subjective experience of being an agent. Within this view, sense of agency is conceived as a very flexible neurocognitive mechanism. Indeed, it is rooted in the dynamic and optimal integration among efferent and afferent signals. Any given source of information would be weighted according to the specificity of the context and the actual availability of signals.55

We have to emphasize that the present review did not aim to investigate the interactions between human body ownership and sense of agency but, rather, it focused on the role of the former in the construction of the latter. Therefore, this article cannot provide an exhaustive picture of the complex interplay between the two senses, and future studies in this direction should allow gaining key hints to understand human bodily self-consciousness.