Causal Inference of Body Ownership in the Posterior Parietal Cortex

Abstract

How do we come to sense that a hand in view belongs to our own body or not? Previous studies have suggested that the integration of vision and somatosensation in the frontoparietal areas plays a critical role in the sense of body ownership (i.e., the multisensory perception of limbs and body parts as our own). However, little is known about how these areas implement the multisensory integration process at the computational level and whether activity predicts illusion elicitation in individual participants on a trial-by-trial basis. To address these questions, we used functional magnetic resonance imaging and a rubber hand illusion-detection task and fitted the registered neural responses to a Bayesian causal inference model of body ownership. Thirty healthy human participants (male and female) performed 12 s trials with varying degrees of asynchronously delivered visual and tactile stimuli of a rubber hand (in view) and a (hidden) real hand. After the 12 s period, participants had to judge whether the rubber hand felt like their own. As hypothesized, activity in the premotor and posterior parietal cortices was related to illusion elicitation at the level of individual participants and trials. Importantly, activity in the posterior parietal cortex fit the predicted probability of illusion emergence of the Bayesian causal inference model based on each participant's behavioral response profile. Our findings suggest an important role for the posterior parietal cortex in implementing Bayesian causal inference of body ownership and reveal how trial-by-trial variations in neural signatures of multisensory integration relate to the elicitation of the rubber hand illusion. SIGNIFICANCE STATEMENT How does the brain create a coherent perceptual experience of one's own body based on information from the different senses? We examined how the likelihood of eliciting a classical bodily illusion that depends on vision and touch—the rubber hand illusion—is related to neural activity measured by functional magnetic resonance imaging. We found that trial-by-trial variations in the neural signal in the posterior parietal cortex, a well known center for sensory integration, fitted a statistical function that describes how likely it is that the brain infers that a rubber hand is one's own given the available visual and tactile evidence. Thus, probabilistic analysis of sensory information in the parietal lobe underlies our unitary sense of bodily self.

Quantifying body ownership information processing and perceptual bias in the rubber hand illusion

“…Thus, the present results demonstrate that even small spatial changes within peripersonal space influence the strength of the illusion both in terms of sensitivity and bias. Again, this fits with a more continuous and probabilistic understanding of how spatial congruence influences the RHI, as opposed to a "fixed rule" with a distinct boundary, similar to the temporal rule as discussed above 24,39,110 .…”

“…We have recently scanned the RHI under a psychophysics detection task and found that activity in the premotor and posterior parietal cortices was related to illusion elicitation at the level of individual participants and trials. Moreover, activity in the posterior parietal cortex followed a Bayesian causal inference model's predicted probability of illusion emergence 110 . Thus, multisensory combination versus segregation performed by multisensory neuronal populations within frontoparietal circuits may implement the critical neuronal computations underlying the current findings of body ownership sensitivity and perceptual biases.…”

“…SDT thus allowed us to characterise the systematic relationship between the subjective judgement about illusory hand ownership and its sensory information patterns. The RHI might be particularly suitable for SDT analysis, because an extensive previous literature has established the critical role of visuo-tactile synchrony and asynchrony in the emergence of the illusion (for a recent review, see Ehrsson 11 ), and we have a good theoretical understanding of why this is so within the theoretical framework of multisensory perception, both at the level of computational processes 37,41,106,110 and neural mechanisms 28,[53][54][55]106,111,112 .…”

No reduction in corticospinal excitability during the rubber hand illusion

“…It is also important for the field of body representation to examine the robustness of this effect since it has theoretical implications for models of body ownership. A negative result would be similarly interesting because it would be in line with more parsimonious multisensory models of the RHI and body ownership that do not include motor processes or the primary motor cortex as a critical structure (Chancel, Iriye, & Ehrsson, 2022;Ehrsson, 2020;Fang et al, 2019;Guterstam et al, 2019;Kilteni et al, 2015;Samad, Chung, & Shams, 2015). Notably, Karabanov et al (2017) did not observe a reduction in corticospinal excitability as a consequence of the RHI, though they had a smaller sample size than della Gatta et al ( 2016) and used a slightly different paradigm (a moving version of the RHI).…”

“…One possibility is that they are simply a side effect of increased inhibitory output to the motor cortex from posterior parietal regions involved in multisensory body perception (Casula et al, 2022). Such an inhibitory influence could arise in some individuals purely from the strong structural and functional connectivity between the motor cortex and posterior parietal regions, the latter playing an important role in both motor control (Rizzolatti & Luppino, 2001) and multisensory integration during the RHI (Chancel et al, 2022;Ehrsson et al, 2004). One must be cautious in interpreting changes in corticospinal excitability in functional terms (Bestmann & Krakauer, 2015).…”