Neural Basis of Limb Ownership in Individuals with Body Integrity Identity Disorder

Abstract

Our body feels like it is ours. However, individuals with body integrity identity disorder (BIID) lack this feeling of ownership for distinct limbs and desire amputation of perfectly healthy body parts. This extremely rare condition provides us with an opportunity to study the neural basis underlying the feeling of limb ownership, since these individuals have a feeling of disownership for a limb in the absence of apparent brain damage. Here we directly compared brain activation between limbs that do and do not feel as part of the body using functional MRI during separate tactile stimulation and motor execution experiments. In comparison to matched controls, individuals with BIID showed heightened responsivity of a large somatosensory network including the parietal cortex and right insula during tactile stimulation, regardless of whether the stimulated leg felt owned or alienated. Importantly, activity in the ventral premotor cortex depended on the feeling of ownership and was reduced during stimulation of the alienated compared to the owned leg. In contrast, no significant differences between groups were observed during the performance of motor actions. These results suggest that altered somatosensory processing in the premotor cortex is associated with the feeling of disownership in BIID, which may be related to altered integration of somatosensory and proprioceptive information.

Structural and functional hyperconnectivity within the sensorimotor system in xenomelia

“…(11) The undirected, weighted 116 × 116‐node connectivity matrices were then subjected to a network‐based statistical analysis (see below). We also investigated a smaller and more xenomelia‐specific network with 28 nodes (see below), the brain regions of which were derived from previous empirical neuroimaging findings in xenomelia (Hänggi et al., 2016; Hilti et al., 2013; van Dijk et al., 2013). …”

“…Sixteen nodes were derived from the eight clusters showing reduced cortical thickness or surface area in xenomelia compared with control men (Hilti et al., 2013). The 28‐node xenomelia‐specific network investigated in this study encompasses these 16 nodes in addition to the thalamus, caudate nucleus, putamen, and pallidum (Hänggi et al., 2016) as well as the ventral and dorsal premotor cortex (Blom et al., 2016; van Dijk et al., 2013). The eight subcortical nodes (bilateral thalamus, caudate nucleus, putamen, and pallidum) based on probability maps were derived from the Harvard–Oxford subcortical structural atlas (http://fsl.fmrib.ox.ac.uk/fsl/fslwiki/Atlases), whereas the remaining 20 nodes of the xenomelia‐specific 28‐node networks were spherical in nature and constructed using the MNI coordinates with a radius of 3 mm and 6 mm for the functional and structural analysis, respectively.…”

“…(2013) and the subcortical structures thalamus, caudate nucleus, putamen and pallidum were derived from another independent brain atlas.…”

“…Individuals suffering from xenomelia typically report that their unwanted limb does not belong to their body and that they would feel “more complete” after its removal (Blanke, Morgenthaler, Brugger, & Overney, 2009). While it is hard to empathize with these feelings and inferences, extensive psychiatric examination of persons with xenomelia revealed a normal mental status and especially the absence of any psychotic disorder (First, 2005; Hilti et al., 2013; van Dijk et al., 2013). A recent review (Brugger, Lenggenhager, & Giummarra, 2013) covering telephone‐ and internet‐based interview studies in well over 100 persons with the disorder summarized the main findings: (1) The majority of affected persons are men (>90%); (2) there is an association of the disorder with nonheterosexuality, and a frequently accompanying symptom involves the erotic attraction by amputees; (3) adverse feelings linked to the unaccepted limb were usually noted in early childhood or adolescence; and (4) unaccepted limbs involve more frequently the lower limbs (>80%) and, in unilateral cases, there is a marked asymmetry in favor of left‐sided limbs (66%–80%; First, 2005; Hilti et al., 2013; Johnson, Liew, & Aziz‐Zadeh, 2011).…”

“…A whole‐brain connectome as well as region–of‐interest (ROI) approach have been applied to the DTI and rsfMRI data using advanced network‐based statistic tools. For the definition of the network nodes, we applied the commonly used automated anatomical labeling (AAL) ROI atlas (Tzourio‐Mazoyer et al., 2002) consisting of 116 different brain regions covering the whole cerebrum, cerebellum, and subcortical structures (whole‐brain connectome approach), but we also constructed a xenomelia‐specific network comprised by brain regions formerly shown to be anatomically altered in xenomelia compared with control men (Hänggi, Bellwald, & Brugger, 2016; Hilti et al., 2013) or differentially activated in different conditions in participants with xenomelia (van Dijk et al., 2013; ROI approach). We expected to find differences in structural and functional connectivity between subjects suffering from xenomelia and control men in brain regions belonging to the sensorimotor system and in the insula.…”