Neural Substrates of Body Ownership and Agency during Voluntary Movement

Abstract

Body ownership and the sense of agency are two central aspects of bodily self-consciousness. While multiple neuroimaging studies have investigated the neural correlates of body ownership and agency separately, few studies have investigated the relationship between these two aspects during voluntary movement when such experiences naturally combine. By eliciting the moving rubber hand illusion with active or passive finger movements during functional magnetic resonance imaging, we isolated activations reflecting the sense of body ownership and agency, respectively, as well as their interaction, and assessed their overlap and anatomical segregation. We found that perceived hand ownership was associated with activity in premotor, posterior parietal and cerebellar regions, whereas the sense of agency over the hand’s movements was related to activity in the dorsal premotor cortex and superior temporal cortex. Moreover, one section of the dorsal premotor cortex showed overlapping activity for ownership and agency, and somatosensory cortical activity reflected the interaction of ownership and agency with higher activity when both agency and ownership were experienced. We further found that activations previously attributed to agency in the left insular cortex and right temporoparietal junction reflected the synchrony or asynchrony of visuo-proprioceptive stimuli rather than agency. Collectively, these results reveal the neural bases of agency and ownership during voluntary movement. Although the neural representations of these two experiences are largely distinct, there are interactions and functional neuroanatomical overlap during their combination, which has bearing on theories on bodily self-consciousness.

Synchronous motor imagery and visual feedback of finger movement elicit the moving rubber hand illusion, at least in illusion-susceptible individuals

“…Thus, we could not examine whether individual differences in the vividness of motor imagery were related to the strength of the imagery-induced illusion. Third, the moving rubber hand illusion in the current experiment appears to be weaker (ownership rating + 0.44 in the real synchronous condition) than in the previous studies (in the range from + 1 to + 2) (Abdulkarim et al 2023 ; Caspar et al 2015 ; Kalckert and Ehrsson 2012 , 2014 ). This difference could relate to fewer individuals being susceptible to the illusion in the current group due to random variation or to differences in the experimental setups and procedures, such as potentially less synchronized seen and felt finger movements between the self-paced finger movements and the robot’s steady rhythm compared with Kalckert’s mechanical connection between the two fingers that ensured near-perfect synchrony throughout the trials.…”

“…That motor imagery coupled with arbitrarily sensory feedback that matches learned sensorimotor associations can lead to a sense of agency is supported by BCI research (Braun et al 2016 ; Nierula et al 2021 ), presumably reflecting the flexibility with which the mind can link intentions with outcomes through learning, internal models and cognitive postdictive processes (Caspar et al 2015 ; Synofzik et al 2008 , 2013 ). However, the current study suggests that motor imagery can elicit agency over a moving limb that feels like one’s own, which presumably taps into the most basic form of agency that involves the sense of control of one’s own bodily movement based on sensorimotor processes (Abdulkarim et al 2023 ; Farrer et al 2013 ; Frith et al 2000 ).…”

“…Moreover, psychophysics and modeling approaches could be used to clarify the computational basis of the imagery effect on the rubber hand illusion (Chancel et al 2022 ). It would also be interesting to investigate the neural mechanisms of the imagery-induced moving rubber hand illusion to determine whether it is associated with patterns of ownership-related activation in the premotor cortex, posterior parietal cortex and cerebellum similar to those of the veridical illusion (Abdulkarim et al 2023 ). The possibility that the imagery-induced version of the rubber hand illusion may engage similar frontoparietal processes related to the sense of body ownership as the veridical version of the illusion would be in line with an EEG study that found that hand mental motor imagery and illusory limb ownership have similar electrophysiological correlates (modulation of the mu band of rhythmic electrical activity) in frontoparietal regions (Evans and Blanke 2013 ).…”

“…Kalckert and Ehrsson ( 2012 ) found that synchrony between the felt movements of one’s hidden real index finger and the seen finger movements of a wooden model hand wearing a rubber glove elicited subjective feelings of rubber hand ownership coupled with a significant drift in the perceived location of one’s real hand (hidden from view) toward the seen rubber hand, which is characteristic of successful rubber hand illusion induction (‘proprioceptive drift; Botvinick and Cohen 1998 ; Tsakiris and Haggard 2005 ). Asynchronous seen and felt movements abolish the illusion according to temporal congruence principles similar to those of the classic rubber hand illusion (Dummer et al 2009 ; Ismail and Shimada 2016 ; Kalckert and Ehrsson 2012 ), as does introducing a substantial spatial incongruence between the orientations of the rubber hand and the real hand (Abdulkarim et al 2023 ; Kalckert and Ehrsson 2012 , 2014 ). Thus, illusory body ownership of the moving rubber hand depends on multisensory integration of visual, kinesthetic and proprioceptive signals.…”

No reduction in motor‐evoked potential amplitude during the rubber hand illusion

“…One view holds that somatosensory feedback from movement contributes to body ownership (only) through multisensory integration with visual and other types of sensory feedback (Kalckert & Ehrsson, 2012, 2014. Others claim that the feeling of being in control of the movement (sense of agency) influences body ownership (Tsakiris et al, 2006), for example, through efferent information from motor commands influencing visuoproprioceptive integration of hand signals (Abdulkarim et al, 2023). Others still have argued for a functional reciprocal relationship between body ownership and the motor system, whereby reduced capacity for movement, either through paralysis, limb immobilization, or non-invasive neurostimulation, can alter susceptibility to body ownership illusions (Burin et al, 2015(Burin et al, , 2017Fossataro et al, 2018).…”