Structural and functional hyperconnectivity within the sensorimotor system in xenomelia

Abstract

Introduction: Xenomelia 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.

Methods: We 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.

Results: We 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.

Conclusions: Our 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.

Keywords: body integrity identity disorder; diffusion tensor imaging; limb amputation; resting state functional magnetic resonance imaging; sensorymotor system; structural and functional hyperconnectivity.

Figure 1

Increased structural connectivity in xenomelia. Shown are the results of the 116‐node network analysis. Two different solutions (sensitivity thresholds) are represented, one solution with many connections (a: p = .019, corrected for multiple comparisons) and one with less connections (b: p = .039, corrected for multiple comparisons). Blue circles represent nodes of the sensorimotor system, whereas turquoise circles represent all other nodes. The nodes are presented in Montreal neurological institute (MNI) space using the centroids of the regions of interest of the automated anatomical labeling (AAL) atlas. Red lines represent the white matter connections showing enhanced structural connectivity in xenomelia compared with control men

Figure 2

Increased structural connectivity in xenomelia. Shown are the results of the 28‐node xenomelia‐specific network analysis. Blue circles represent nodes of the sensorimotor system and the insula. These nodes were derived from three different xenomelia studies (Hänggi et al., 2016; Hilti et al., 2013; van Dijk et al., 2013). The nodes are presented in Montreal neurological institute (MNI) space using the centroids of the regions of interest derived from the above mentioned studies. Red lines represent the white matter connections showing enhanced structural connectivity in xenomelia compared with healthy control men. Note that this subnetwork was statistically significant only on a trend level (p = .087, corrected for multiple comparisons)

Figure 3

Increased functional connectivity in xenomelia. Shown are the results of the 116‐node network analysis. Two different solutions (sensitivity thresholds) are represented, one solution with many connections (a: p = .037, corrected for multiple comparisons) and one with less connections (b: p = .022, corrected for multiple comparisons). Blue circles represent nodes of the sensorimotor system, whereas turquoise circles represent all other nodes. The nodes are presented in Montreal neurological institute (MNI) space using the centroids of the regions of interest of the automated anatomical labeling (AAL) atlas. Red lines connect the nodes (brain regions) showing enhanced functional connectivity in xenomelia compared with healthy control men

Figure 4

Increased functional connectivity within the structurally hyperconnected subnetwork. Shown are the results of the 116‐node functional network analysis restricted to the connections that already showed structural hyperconnectivity (see solution 1 in Figure 1 and Table 2). Blue circles represent nodes of the sensorimotor system, whereas turquoise circles represent all other nodes. The nodes are presented in Montreal neurological institute (MNI) space using the centroids of the regions of interest of the automated anatomical labeling (AAL) atlas. Red lines connect the nodes (brain regions) showing enhanced functional connectivity (p = .035, corrected for multiple comparisons) in xenomelia compared with healthy control men