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Contribution of interaction force to the sense of hand ownership and the sense of hand agency.

ABSTRACT: When performing willed actions, we have the unified and coherent experience of owning and controlling our body. Body ownership is believed to emerge from the integration of coherent multisensory signals, while agency is believed to emerge from the coherence between predicted and perceived outcomes of actions. As a consequence, body ownership and agency can both be modulated by multisensory conflicts. The contribution of active movement generation to ownership and agency has not been parametrically explored. Here, we investigated the contribution of interaction force between the agent and the environment to the sense of hand ownership (SO) and the sense of hand agency (SA). By combining robotics and virtual reality, we manipulated the sensorimotor and visual information during immersive scenarios to induce and quantify altered states of SO and SA. First, we demonstrated that SO and SA could be successfully manipulated by our experimental paradigms. Second, we showed that interaction force strongly contributes to SA, but to a lesser extent to SO. Finally, we showed that SO and SA interact beyond their common multisensory basis. Our results, based on two independent studies, provide a direct link between sensorimotor interactions and subjective body experience and demonstrate a new dissociation between SO and SA.

SUBMITTER: Akselrod M

PROVIDER: S-EPMC8433290 | biostudies-literature | 2021 Sep

REPOSITORIES: biostudies-literature

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Contribution of interaction force to the sense of hand ownership and the sense of hand agency.

Akselrod Michel M Vigaru Bogdan B Duenas Julio J Martuzzi Roberto R Sulzer James J Serino Andrea A Blanke Olaf O Gassert Roger R

Scientific reports 20210910 1

When performing willed actions, we have the unified and coherent experience of owning and controlling our body. Body ownership is believed to emerge from the integration of coherent multisensory signals, while agency is believed to emerge from the coherence between predicted and perceived outcomes of actions. As a consequence, body ownership and agency can both be modulated by multisensory conflicts. The contribution of active movement generation to ownership and agency has not been parametrical ...[more]

PMID: 34508126

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Project description:Traumatic experiences have been linked to the development of altered states of consciousness affecting bodily perception, including alterations in body ownership and in sense of agency, the conscious experience of the body as one's own and under voluntary control. Severe psychological trauma and prolonged distress may lead to posttraumatic stress disorder (PTSD). Together, symptoms of derealization and, related specifically to the sense of body ownership and agency, of depersonalization (where parts of the body or the entire body itself is perceived as detached and out of control), constitute the dissociative subtype (PTSD+DS). In this study, we explored the Rubber Hand Illusion, an experimental paradigm utilized to manipulate sense of body ownership in PTSD (n = 4) and PTSD+DS (n = 6) as compared to healthy controls (n = 7). Perceived finger location and self-report questionnaires were used as behavioral and subjective measures of the illusion, respectively. In addition, the correlation between the illusion's effect and sense of agency as a continuous feeling of controlling one's own body movements was explored. Here, a lower illusion effect was observed in the PTSD as compared to the control group after synchronous stimulation for both the proprioceptive drift and subjectively perceived illusion. Moreover, by both proprioceptive drift and by subjective ratings, the PTSD+DS group showed a response characterized by high variance, ranging from a very strong to a very weak effect of the illusion. Finally, sense of agency showed a trend toward a negative correlation with the strength of the illusion as subjectively perceived by participants with PTSD and PTSD+DS. These findings suggest individuals with PTSD may, at times, maintain a rigid representation of the body as an avoidance strategy, with top-down cognitive processes weakening the impact of manipulation of body ownership. By contrast, the response elicited in PTSD+DS appeared to be driven by either an increased vulnerability to manipulation of embodiment or by a dominant top-down cognitive representation of the body, with disruption of multisensory integration processes likely in both cases. Taken together, these findings further our understanding of bodily consciousness in PTSD and its dissociative subtype and highlight the supportive role played by sense of agency for the maintenance of body ownership.

Project description:The appearance of the self-body influences the feeling that one's body belongs to oneself, that is, a sense of ownership (SoO) and pain perception. This can be identified by measuring the SoO and pain thresholds after performing the rubber hand illusion (RHI) with an injured rubber hand. The generation of SoO is thought to be caused by multisensory integration of bottom-up factors (vision, proprioceptive, and touch), and by top-down factors, such as the context effect. The appearance is one of the context effects which may become more effective when used simultaneously with other context effects (e.g., verbal suggestion). However, in the RHI, when appearance and other context effects are used simultaneously, the effect is unclear. In this study, we attempted to identify the influence of verbal suggestion on the SoO and heat pain threshold (HPT). As a preliminary step, in Experiment 1, the "normal" rubber hand and "penetrated nail" as injured rubber hand were used to clarify the context effect with appearance alone during RHI (synchronous/asynchronous), which was conducted within-subjects. In Experiment 2, we only used the "penetrated nail" rubber hand to clarify the context effect with verbal suggestion and appearance during RHI. We randomly classified participants into two suggestion groups ("fear" and "no-fear"). The RHI (synchronous/asynchronous) was conducted for each group. In each experiment, the effect of each condition was assessed by subjective measures of SoO, such as questionnaire, and objective measures of SoO, such as proprioceptive drift and electrodermal activity. Following RHI in each condition, HPT was measured. The main finding was that, in the synchronous condition, the "penetrated nail" appearance with "fear" verbal suggestion modulated questionnaire and HPT, but not electrodermal activity. We conclude that the context-included multisensory integration affected the subjective factors because it contains a higher cognitive process by verbal suggestion.

Project description:BACKGROUND:Several daily living activities require people to coordinate the motion and the force produced by both arms, using their position sense and sense of effort. However, to date, the interaction in bimanual tasks has not been extensively investigated. METHODS:We focused on bimanual tasks where subjects were required: (Experiment 1) to move their hands until reaching the same position - equal hand position implied identical arm configurations in joint space - under different loading conditions;(Experiment 2) to produce the same amount of isometric force by pushing upward, with their hands placed in symmetric or asymmetric positions. The arm motions and forces required for accomplishing these tasks were in the vertical direction. We enrolled a healthy population of 20 subjects for Experiment 1 and 25 for Experiment 2. Our primary outcome was the systematic difference between the two hands at the end of each trial in terms of position for Experiment 1 and force for Experiment 2. In both experiments using repeated measure ANOVA we evaluated the effect of each specific condition, namely loading in the former case and hand configuration in the latter. RESULTS:In the first experiment, the difference between the hands' positions was greater when they were concurrently loaded with different weights. Conversely, in the second experiment, when subjects were asked to exert equal forces with both arms, the systematic difference between left and right force was not influenced by symmetric or asymmetric arm configurations, but by the position of the left hand, regardless of the right hand position. The performance was better when the left hand was in the higher position. CONCLUSIONS:The experiments report the reciprocal interaction between position sense and sense of effort inbimanual tasks performed by healthy subjects. Apart for the intrinsic interest for a better understanding of basic sensorimotor processes, the results are also relevant to clinical applications, for defining functional evaluation and rehabilitative protocols for people with neurological diseases or conditions that impair the ability to sense and control concurrently position and force.

Dataset Information

Contribution of interaction force to the sense of hand ownership and the sense of hand agency.

Publications

Contribution of interaction force to the sense of hand ownership and the sense of hand agency.

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