Body ownership alterations emerge from proprioceptive impairment and frontoparietal network damage

Presented During:

Thursday, June 27, 2024: 11:30 AM - 12:45 PM
COEX  
Room: Grand Ballroom 104-105  

Poster No:

2083 

Submission Type:

Abstract Submission 

Authors:

Giulio Mastria1, Tommaso Bertoni2, Henri Perrin3, Nikita Akulenko2, Gaia Risso4, Michel Akselrod2, Eleonora Guanziroli5, Franco Molteni5, Patric Hagmann6, Michela Bassolino4, Andrea Serino2

Institutions:

1Geneva University Hospitaal, Geneva, Geneva, 2CHUV-UNIL, Lausanne, Vaud, 3CHUV, Lausanne, Vaud, 4HES-SO Valais-Wallis, Sion, Valais, 5Valduce Hospital, Costa Masnaga, Lecco, 6Department of Radiology, Lausanne University Hospital and University of Lausanne (CHUV-UNIL), Lausanne, Switzerland

First Author:

Giulio Mastria  
Geneva University Hospitaal
Geneva, Geneva

Co-Author(s):

Tommaso Bertoni  
CHUV-UNIL
Lausanne, Vaud
Henri Perrin  
CHUV
Lausanne, Vaud
Nikita Akulenko  
CHUV-UNIL
Lausanne, Vaud
Gaia Risso  
HES-SO Valais-Wallis
Sion, Valais
Michel Akselrod  
CHUV-UNIL
Lausanne, Vaud
Eleonora Guanziroli  
Valduce Hospital
Costa Masnaga, Lecco
Franco Molteni  
Valduce Hospital
Costa Masnaga, Lecco
Patric Hagmann  
Department of Radiology, Lausanne University Hospital and University of Lausanne (CHUV-UNIL)
Lausanne, Switzerland
Michela Bassolino  
HES-SO Valais-Wallis
Sion, Valais
Andrea Serino  
CHUV-UNIL
Lausanne, Vaud

Introduction:

The sense of body ownership refers to the feeling that our body belong to us and it plays a crucial role in our perception of our body's position and movement. Alterations in the sense of ownership for the contralesional upper limb are relatively common in the acute phase after cerebral stroke, with patients experiencing difficulties in self-attributing the affected limb, visually perceived, or persistently denying ownership of it (i.e., somatoparaphrenia). Our understanding of the pathophysiological mechanisms underlying these alterations is still poor, limiting the development of effective neurorehabilitative approaches.
Body ownership shares its neural substrate with multisensory integration processes and motor control. According to most accepted accounts, sensorimotor and multisensory integration deficits are key factors determining body ownership alterations in stroke patients; however experimental evidence supporting this view is scarce.

Methods:

We used a virtual reality reaching task implementing a varying visuo-motor rotation, thus introducing a mismatch in visuo-proprioceptive cues about hand's position during movement execution. We studied the weight attributed to the virtual hand in guiding reaching movements and used it as an implicit proxy of body ownership, which was also assessed by subjective ratings. We modelled body ownership as the product of an online Bayesian inference process, wherein the brain infers ownership over the virtual hand based on the degree of congruency between visual and proprioceptive inputs, influencing the extent of visual adjustments applied to reaching movements. We then performed network based lesion analysis in order to investigate the neural source of body ownership alterations in stroke patients.

Results:

We found that stroke patients exhibit an increased tendency to perceive ownership for an incongruent virtual hand and to incorporate it into their motor planning when performing movements with the affected limb, compared to both the intact limb and to a group of age-matched healthy controls. Importantly, this tendency also correlated with diminished ownership for a congruent virtual hand, simulating patient's actual limb. This constitutes novel, quantitative evidence that pathological alterations in subjective body experience affect visuo-proprioceptive sensorimotor loops underlying motor control. The Bayesian inference model effectively explained these alterations as stemming from proprioceptive deficits, reducing the ability to detect visuo-proprioceptive disparities. Finally, through the analysis of brain lesions, we further linked body ownership deficit to alterations in connectivity within the frontoparietal network, affecting connections between the intraparietal sulcus and the supramarginal gyrus with the premotor and dorsolateral prefrontal cortex. This indicates that, besides somatosensory deficits, alterations in body ownership and underlying sensorimotor loops may be attributed to a specific impairment in multisensory integration processes.

Conclusions:

This paper provides, for the first time, a quantitative model explaining how somatosensory loss and multisensory integration deficits contribute to body ownership alterations in stroke patients. Moreover, it sheds light on the link between patients' subjective bodily experience and closed-loop motor control. These findings have great relevance for neurorehabilitation: some of the current neurorehabilitation strategies (e.g., prism adaptation, mirror therapy) are based on the manipulation of multisensory feedback, but we have limited knowledge about how the interaction between sensory modalities during functional tasks might affect the efficacy of the intervention. Our framework may be used to predict the capability of a lesioned brain to process and combine multisensory information, supporting body ownership and motor control, and may allow adapting the neurorehabilitation strategy accordingly.

Modeling and Analysis Methods:

Bayesian Modeling 2

Motor Behavior:

Visuo-Motor Functions 1

Perception, Attention and Motor Behavior:

Perception: Multisensory and Crossmodal

Keywords:

Computational Neuroscience
MRI
Neurological
STRUCTURAL MRI
Tractography
WHITE MATTER IMAGING - DTI, HARDI, DSI, ETC
Other - Stroke

1|2Indicates the priority used for review
Supporting Image: Figure1.png
   ·Results of the visuo-proprioceptive reaching task
Supporting Image: Figure2.png
   ·Unisensory and multisensory contributions to body ownership alterations in stroke patients
 

Provide references using author date format

Bertoni T, Mastria G, Akulenko N, et al. The self and the Bayesian brain: testing probabilistic models of body ownership through a self-localization task. Cortex. July 2023. doi:10.1016/j.cortex.2023.06.019

Fang W, Li J, Qi G, Li S, Sigman M, Wang L. Statistical inference of body representation in the macaque brain. PNAS. 2019;116(40):20151-20157. doi:10.1073/pnas.1902334116

Blanke O, Slater M, Serino A. Behavioral, Neural, and Computational Principles of Bodily Self- Consciousness. Neuron. 2015;88(1):145-166. doi:10.1016/j.neuron.2015.09.029