Body ownership determines the attenuation of self-generated tactile sensations

Abstract

Self-perception depends on the brain's abilities to differentiate our body from the environment and to distinguish between the sensations generated as a consequence of voluntary movement and those arising from events in the external world. The first process refers to the sense of ownership of our body and relies on the dynamic integration of multisensory (afferent) signals. The second process depends on internal forward models that use (efferent) information from our motor commands to predict and attenuate the sensory consequences of our movements. However, the relationship between body ownership and sensory attenuation driven by the forward models remains unknown. To address this issue, we combined the rubber hand illusion, which allows experimental manipulation of body ownership, and the force-matching paradigm, which allows psychophysical quantification of somatosensory attenuation. We found that a rubber right hand pressing on the left index finger produced somatosensory attenuation but only when the model hand felt like one's own (illusory selftouch); reversely, the attenuation that was expected to occur during actual self-touch with the real hands was reduced when the participants simultaneously experienced ownership of a rubber right hand that was placed at a distance from their left hand. These results demonstrate that the sense of body ownership determines somatosensory attenuation. From a theoretical perspective, our results are important because they suggest that body ownership updates the internal representation of body state that provides the input to the forward model generating sensory predictions during voluntary action.sensory attenuation | body ownership | forward models | state estimation | predictive motor control T he distinction between self and nonself is fundamental for all biological organisms. External signals constitute potential threats and must be clearly distinguished from self-related signals. Imagine, for example, how dangerous it would be if you could not distinguish between a spider crawling up your neck and your own fingers scratching the same part of the skin. The central nervous system has therefore developed mechanisms to distinguish between self-related signals and non-self-related signals. Two neural mechanisms are considered particularly important for this differentiation. First, the integration of signals from different sensory modalities (e.g., vision, touch, proprioception; multisensory integration) leads to the formation of a central representation of one's own body in space (1, 2). Sensory information attributed to this representation is experienced as originating from one's own body (sense of body ownership). Second, when we actively move our body, the brain predicts the sensory consequences of the movements by using internal copies of the voluntary motor commands (efference copy) (3-5). This allows the central nervous system to disambiguate self-produced sensations from sensations arising from external causes. However, the relationship between these two basic self-...

Sensorimotor conflicts induce somatic passivity and louden quiet voices in healthy listeners

“…A well-known example is the sensory attenuation of self-generated touch: touches produced by oneself are perceived as weaker compared to externally produced ones, even if applied with the same intensity [17][18][19] . Moreover, sensorimotor conflicts accompanying self-generated touches can abolish self-attenuation and thus alter the associated tactile perceptions 4,20,21 .…”

Welcoming back my arm: Affective touch increases body ownership following right hemisphere stroke

“…Traditionally, self-generated touch has been associated with attenuation of the resulting tactile stimulation, leading to the well-known phenomenon that we cannot tickle ourselves (Blakemore et al, 1998a). Recent work in healthy subjects further shows how body ownership influences this sensory attenuation during the rubber hand illusion (Kilteni and Ehrsson, 2017). However, other research highlights the enhancing effect of selftouch on sensory perception (see Valentini et al, 2008;Ackerley et al, 2012), including in patients with right hemisphere stroke (White et al, 2010) and those with disturbed body ownership (see van Stralen et al, 2011).…”

Functional connectivity between the cerebellum and somatosensory areas implements the attenuation of self-generated touch

“…To address the abovementioned issues, here we combined functional magnetic resonance 142 imaging (fMRI) with a force-matching psychophysics task and utilized a larger sample of 143 participants than those used in earlier studies. In addition to merely contrasting self-generated 144 touch and externally generated touch, we further took advantage of previous observations that 145 not all self-generated touches are attenuated to the same extent but mainly those that 146 correspond to direct self-touch where the two body parts in question are perceived to be in 147 physical contact (Kilteni and Ehrsson, 2017b). For example, in the force-matching task, when 148 the participants reproduce the externally generated forces by moving a joystick that controls 149 the force output on their finger instead of directly pressing their index finger against their 150 other finger, they show no attenuation of their self-generated forces (Shergill et al, 2003;151 Wolpe et al, 2016; Kilteni and Ehrsson, 2017a).…”

“…To identify connectivity changes that were specific to somatosensory attenuation, we used as 427 a second-level covariate the participants' attenuation index as extracted from the force-428 matching task. For each participant we calculated the difference between the mean force 429 he/she exerted in the condition of interest and the force that he/she exerted in a reference 430 condition, similar to our previous study (Kilteni and Ehrsson, 2017b). Specifically, to 431 investigate connectivity increases in the self-generated touch condition compared to the 432 externally generated touch condition (Movement 0cm -by-Touch 0cm interaction), we used the 433 difference between the mean matched force in the press 0cm condition and the mean matched 434 force in the slider condition.…”