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Research Articles, Behavioral/Cognitive

Neural substrates of body ownership and agency during voluntary movement

Z Abdulkarim, A Guterstam, Z Hayatou and HH Ehrsson
Journal of Neuroscience 17 February 2023, JN-RM-1492-22; DOI: https://doi.org/10.1523/JNEUROSCI.1492-22.2023
Z Abdulkarim
1Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
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A Guterstam
2Department of Clinical Neuroscience, Karolinska Institutet, Stockholm, Sweden
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Z Hayatou
3Université Paris-Saclay, CNRS, Institut Des Neurosciences Paris-Saclay, 91190 Gif-sur-Yvette, France
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HH Ehrsson
1Department of Neuroscience, Karolinska Institutet, Stockholm, Sweden
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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.

Footnotes

  • The authors have no conflicts of interest to declare.

  • Zakaryah Abdulkarim was funded by a PhD student grant from the Karolinska Institutet (Clinical Scientist Training Programme). Henrik Ehrsson and project costs were supported by funding from the Swedish Research Council, The Göran Gustafsson Foundation and the European Research Council under the European Union’s horizon 2020 research and innovation programme. Arvid Guterstam was supported by the Wenner-Gren Foundations and the Swedish Brain Foundation. We thank Martti Mercurio for help with the experimental setups and the staff at the Karolinska University Hospital Solna’s MR-center for support with the fMRI. We thank Konstantina Kilteni for valuable input during the analysis of the fMRI data.

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Neural substrates of body ownership and agency during voluntary movement
Z Abdulkarim, A Guterstam, Z Hayatou, HH Ehrsson
Journal of Neuroscience 17 February 2023, JN-RM-1492-22; DOI: 10.1523/JNEUROSCI.1492-22.2023

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Neural substrates of body ownership and agency during voluntary movement
Z Abdulkarim, A Guterstam, Z Hayatou, HH Ehrsson
Journal of Neuroscience 17 February 2023, JN-RM-1492-22; DOI: 10.1523/JNEUROSCI.1492-22.2023
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