Motor versus body awareness: Voxel-based lesion analysis in anosognosia for hemiplegia and somatoparaphrenia following right hemisphere stroke

Abstract

Anosognosia for hemiplegia (AHP) is informative about the neurocognitive basis of motor awareness. However, it is frequently associated with concomitant symptoms, such as hemispatial neglect and disturbances in the sense of body ownership (DSO). Although double dissociations between these symptoms have been reported, there is ongoing debate about whether they are manifestations of independent abnormalities, or a single neurocognitive deficit.We aimed to investigate the specificity of lesions associated with AHP by surpassing four, existing methodological limitations: (a) recruit a relatively large sample of patients (total N = 70) in a multi-centre study; (b) identify lesions associated with AHP in grey and white matter using voxel-based methods; (c) take into account the duration of AHP and concomitant neglect symptoms; and (d) compare lesions against a control hemiplegic group , patients suffering from AHP and DSO, and a few, rare patients with selective DSO. Results indicated that acute AHP is associated with a wide network, mainly including: (1) the Rolandic operculum, (2) the insula and (3) the superior temporal gyri. Subcortically, damage mainly involved the basal ganglia and white matter, mostly the superior corona radiate, arcuate fasciculus and the ventral part of the superior longitudinal fasciculus. Persistent symptoms were linked with wider damage involving fronto-temporal cortex and long white matter tracts. A shift in the latero-medial direction (mainly involving the basal ganglia and surrounding white matter) emerged when DSO was taken accounted for. These results suggest that while bodily awareness is processed by areas widely distributed across the brain, intact subcortical structures and white matter tracts may be necessary to support basic feelings of owning and controlling contralateral body parts. An accurate and 'up-to-date' awareness of our motor abilities, however, may rely also on intact processing in cortical areas which presumably allow higher-order inferences about the current state of the body. Reviewer #1: The authors investigated the neuronal basis for anosognosia (AHP) and related disorders (body awareness and spatial neglect). The authors report a 70-strong study cohort, which they separate into different groups for their analysis and claim a different neuronal pattern for the acute and chronic stages of anosognosia. Whilst this study is well-written and strong neuropsychologically, the imaging analysis and in particular its interpretation lack substance. The anatomical regions described most the time do not match with the figures provided and therefore the conclusion of the current manuscript are not supported by the neuroimaging findings. The authors need to work on this aspect before publication should be considered. Motor Versus Body General comments1. The introduction is very well written and leads nicely to the research hypotheses. However, given the limited publications available on the neuronal basis of anosognosia the authors should make an effort to include a ...

Welcoming back my arm: Affective touch increases body ownership following right hemisphere stroke

“…However, our exploratory VLSM using less restrictive criteria revealed that lesions in the insula and corpus callosum, and, resulted in significantly less increase in body ownership following other-affective touch. These findings are consistent with the proposed role of the insula in body awareness, as well as the importance of white matter tracts in self-awareness (Pacella et al, 2019) and body ownership (Moro et al, 2016;Martinaud et al, 2017) and warrant further study.…”

Anosognosia for Hemiplegia as a tripartite disconnection syndrome

“…The regression computed on the lesion sites ( Figure 1a ) indicated the involvement of grey matter structures previously associated with AHP (15), such as the insula (anterior long gyrus, t = 4.89; p = 0.002), the temporal pole (t = 4.77; p = 0.003), and the striatum (t = 4.68; p = 0.003) as well as a very large involvement of white matter (t = 4.98; p = 0.002). The second regression on white matter maps of disconnection ( Figure 1b ) revealed a significant contribution of the cingulum (t = 3.85; p = 0.008), the third branch of the superior longitudinal fasciculus (SLF III; t = 4.30; p = 0.003), and connections to the pre-supplementary motor area (preSMA; t = 3.37; p = 0.013), such as the frontal aslant and the fronto-striatal connections.…”

Building the bodily self‐awareness: Evidence for the convergence between interoceptive and exteroceptive information in a multilevel kernel density analysis study

“…Its damage or disconnection can lead to USN (see Chelazzi, Bisley, & Bartolomeo, ) but also to the so‐called “out‐of‐body experience,” a situation in which patients perceive themselves as observing their body from an extracorporeal perspective (Blanke, Landis, Spinelli, & Seeck, ). Also, lesions or structural alterations to insular regions have been associated with both body ownership and interoceptive disorders (ereda, Ghika, Maeder, & Bogousslavsky, ; Ibañez et al, ; Karnath, ; Moro et al, ; Ronchi et al, 2015; Salvato, Mercurio, Sberna, Paulesu, & Bottini, ).…”

“…Also, lesions or structural alterations to insular regions have been associated with both body ownership and interoceptive disorders (ereda, Ghika, Maeder, & Bogousslavsky, 2002;Ibañez et al, 2010;Karnath, 2005;Moro et al, 2016;Ronchi et al, 2015;Salvato, Mercurio, Sberna, Paulesu, & Bottini, 2018).…”