A fronto-insular-parietal network for the sense of body ownership

Abstract

Neuropsychological disturbances in the sense of limb ownership provide unique opportunities to study the neurocognitive basis of body ownership. Previous small sample studies that showed discrete cortical lesions cannot explain why multisensory, affective, and cognitive manipulations alter disownership symptoms. We tested the novel hypothesis that disturbances in the sense of limb ownership would be associated not only with discrete cortical lesions but also with disconnections of white-matter tracts supporting specific functional networks. We drew on an advanced lesion-analysis and Bayesian statistics approach in 49 right-hemisphere patients (23 with and 26 without limb disownership). Our results reveal that disturbances in the sense of ownership are associated with lesions in the supramarginal gyrus and disconnections of a fronto-insular-parietal network, involving the frontal-insular and frontal inferior longitudinal tracts, confirming previous disconnection hypotheses. Together with previous behavioral and neuroanatomical results, these findings lead us to propose that the sense of body ownership involves the convergence of bottom-up, multisensory integration, and top-down monitoring of sensory salience based on contextual demands.

Disconnections in personal neglect

“…Firstly, to the best of our knowledge, our sample of patients is currently the largest of any used for the neuroanatomical investigation of PN correlates. Secondly, this is the first study on PN that investigates the white matter via a tractography procedure (although indirect) and does not simply rely on lesion mapping processes that focus on discrete cortical lesions and modular accounts that fail to explain the neural correlates of complex syndromes (Bartolomeo et al 2007 ; Doricchi et al 2008 ; Pacella et al 2019 ; Monai et al 2020 ; Moro et al 2022 ). Furthermore, the neuroanatomical analysis controls for the impact of clinical variables other than PN.…”

“…Crucially, the PN network does not overlap with the network associated with other body representation disorders, such as a disturbed sensation of body ownership (i.e. asomatognosia and somatoparaphrenia) which involves a fronto-insular–parietal network (Moro et al 2022 ), or anosognosia for hemiplegia, which involves the premotor loop, the ventral attentional system and the limbic system (Pacella et al 2019 ). Thus, the sense of bodily self is probably widespread across complex multiple networks.…”

“…The clinical MRI or CT neuroimaging data were available for all of the patients. Their clinical and anatomical data had been described in two previous studies which focused on the neural correlates and diagnosis of anosognosia for hemiplegia (Pacella et al 2019 ; Moro et al 2021 ) and disorders in the sense of body ownership (Moro et al 2022 ) and the data are shown in Table 1 . As the data were collected from two different stroke recovery units, we took into account the neurological and neuropsychological tests that were most commonly administered to all of the patients in the centres and investigated the symptoms which are more frequently associated with PN (i.e.…”

“…Comb and Razor/Compact), the two subtests are highly correlated (McIntosh et al 2000 ; Beschin and Robertson 1997 ) and several previous studies have used only one subtest (e.g. Moro et al 2022 ; Moro and Besharati 2021 ; Pacella et al 2019 ; D’Imperio et al 2017a , b ; Caggiano et al 2020 ). The choice of the Comb subtest guarantees the possibility of using the same task for both males and females and to exclude any effects of sensory deficits (as the upper part of the face has bilateral innervation).…”

“…The hypothesis at the basis of the present study is that PN is a disconnection syndrome which is not associated with discrete grey matter lesions, but instead involves a right hemisphere network of cortical and subcortical structures contributing to body representation. Related disconnection hypotheses have been recently supported in other syndromes, such as spatial neglect (Thiebaut de Schotten et al 2005 ), anosognosia for hemiplegia (Pacella et al 2019 ; Monai et al 2020 ) and disorders in the sensations of body ownership (Moro et al 2022 ). Previous neuroanatomical data on PN correlates also support this hypothesis, since they suggest a role played by multimodal areas (i.e.…”