Structural and functional hyperconnectivity within the sensorimotor system in xenomelia

Abstract

IntroductionXenomelia is a rare condition characterized by the persistent and compulsive desire for the amputation of one or more physically healthy limbs. We highlight the neurological underpinnings of xenomelia by assessing structural and functional connectivity by means of whole‐brain connectome and network analyses of regions previously implicated in empirical research in this condition.MethodsWe compared structural and functional connectivity between 13 xenomelic men with matched controls using diffusion tensor imaging combined with fiber tractography and resting state functional magnetic resonance imaging. Altered connectivity in xenomelia within the sensorimotor system has been predicted.ResultsWe found subnetworks showing structural and functional hyperconnectivity in xenomelia compared with controls. These subnetworks were lateralized to the right hemisphere and mainly comprised by nodes belonging to the sensorimotor system. In the connectome analyses, the paracentral lobule, supplementary motor area, postcentral gyrus, basal ganglia, and the cerebellum were hyperconnected to each other, whereas in the xenomelia‐specific network analyses, hyperconnected nodes have been found in the superior parietal lobule, primary and secondary somatosensory cortex, premotor cortex, basal ganglia, thalamus, and insula.ConclusionsOur study provides empirical evidence of structural and functional hyperconnectivity within the sensorimotor system including those regions that are core for the reconstruction of a coherent body image. Aberrant connectivity is a common response to focal neurological damage. As exemplified here, it may affect different brain regions differentially. Due to the small sample size, our findings must be interpreted cautiously and future studies are needed to elucidate potential associations between hyperconnectivity and limb disownership reported in xenomelia.

Experimentally induced limb-disownership in mixed reality

“…Although these results may seem somewhat contradictory, they can be reconciled, if we assume the effect of stimulation in both the RHI and ReHI is relevant to inducing disownership over one's own limb. The underlying mechanism of this effect could on the one hand relate to a localized change in multisensory processing (Lira et al, 2018), body-specific integration (Convento et al, 2018;Tsakiris et al, 2008), or a re-weighting of sensory information over body-representation in the parietal lobe, or on the other hand a change in functionally connected regions such as the primary or secondary somatosensory cortex (Hänggi et al, 2017), where structural and functional hyper-connectivity have been reported in individuals with Xenomelia. This explanation is necessarily speculative but could further be investigated using neuroimaging alongside the ReHI paradigm.…”

“…the feeling of estrangement for their own limb. Both Somatoparaphrenia and Xenomelia have been suggested to relate to alterations in multisensory bodily areas in the predominantly righthemispheric posterior parietal areas (Hilti et al, 2013;McGeoch et al, 2011;Rode et al, 1992) as well as structural and functional hyper-connectivity within the sensorimotor system (Hänggi et al, 2017). As a consequence, both syndromes predominantly affect the left side of the body.…”

Mental rotation of feet in individuals with Body Integrity Identity Disorder, lower-limb amputees, and normally-limbed controls

“…Individuals with this condition, particularly those who desire amputation of a limb, describe themselves as "overcomplete" and as though the limb does not belong to them, experiencing a sense of (non-delusional) disownership over the body part. While research is scant on this subject, it has been growing in recent years [3][4][5][6][7]. The condition manifests before adolescence, usually affects males, and the desire to amputate/paralyze is usually directed towards the lower limbs [2,8].…”

“…[10]), recent imaging studies suggest that there are structural and functional alterations to brain areas that contribute to maintaining a coherent representation of the body (particularly within the sensorimotor system). These areas generally refer to frontal, parietal, and insular areas, but have extended to the thalamus, basal ganglia, and cerebellum as well [3,7,[10][11][12]. For instance, the premotor cortex (PMC) plays a critical role in integrating multisensory information about the body (e.g.…”

Effects of observing normal and abnormal goal‐directed hand movements on somatosensory cortical activation

“…The ~20 Hz activity of MI exhibited more suppression in the observation of normal than abnormal hand movements, suggesting that observing graceful, smooth hand actions induces stronger MI activities. As motor or premotor cortex has structural/functional neural connections with primary somatosensory cortices of the same (Pavlides et al ., ; Shinoura et al ., ) and opposite (Unrath et al ., ) sides, as well as secondary somatosensory cortices (Rocca et al ., ; Hanggi et al ., ), it is postulated that the modifications of observation of normal and abnormal hand movements could also be found in the somatosensory processing.…”