The hidden side of body integrity dysphoria: aberrant limbic responses to dynamic touch

Abstract

Body integrity dysphoria (BID) is a brain-based disorder characterized by a persistent, obsessing and disturbing desire for the amputation of healthy limbs. Importantly, individuals with BID are adamant about which specific body segment they wish to have amputated and the exact level at which the amputation should occur. The condition has been linked to altered resting-state brain functional connectivity and task-based activity at the level of somatosensory cortices. However, the inevitable distress associated with the condition has not been explained by current neurophysiological data. In this functional MRI (fMRI) study, we studied individuals with a lifelong desire for the amputation of their left leg using a dynamic somatosensory stimulation paradigm. We identified and marked the desired line of amputation on the BID individuals' left leg and a corresponding point on their right leg. We measured brain activations in response to stimulation of the lower limbs while participants were instructed to focus on the tactile sensations and detect when the stimulation crossed the line of the desired amputation. Compared with healthy controls focusing on the same segments of their legs, individuals with BID showed higher neural activations specifically for the stimulation of their left leg in a large cortical and subcortical neural network primarily associated with rewarding and pain stimuli. Some of these hyperactivations were particularly marked immediately after the stimulation had passed over the line of the desired amputation. When the stimulation crossed the desired point of amputation, there were also increased activations in the premotor cortices and the anterior cingulum, a sign of premotor attentional arousal. Our data show a pathological relationship between altered neural representations of the body map and the brain reward system, connecting BID to the visceral brain for the first time.

Keywords: body integrity dysphoria; body ownership; fMRI; tactile stimulation; xenomelia.

Graphical Abstract

Figure 1

fMRI results: topography of the stimulation. (A) Full factorial ANOVA (N = 23). Brain regions showing a significant group-by-side interaction, with increased activations recorded in individuals with BID, particularly in response to the stimulation of the left leg (independently from the part of the leg). (B) Full factorial ANOVA (N = 23). Plot of the haemodynamic response recorded in the local maxima of the displayed clusters: anterior cingulum, [4, 16, 18], Z-score: 4.69, (P < 0.001 at peak level, P < 05 family-wise error corrected at cluster level); thalamus [−4, −22, 2], Z-score: 4.60, (P < 0.001 at peak level, P < 0.05 family-wise error corrected at cluster level). (C) Scatterplot of the correlation analysis (N = 9) between the haemodynamic response and BID individuals’ score at the Zurich Xenomelia Scale (erotic attraction subscale; min = 1; max = 6): anterior cingulum, [4, 16, 18], Pearson’s coefficients: 0.54; thalamus [−4, −22, 2], Pearson’s coefficients: 0.57. Each data point represents a BID individual’s BOLD response plotted against the corresponding score on the subscale.

Figure 2

fMRI results: direction of the stimulation. (A) Full factorial ANOVA (N = 23). Brain regions showing a significant group-by-side interaction, with increased activations recorded in individuals with BID, particularly in response to the stimulation of the left leg (independently from the part of the leg). (B) Full factorial ANOVA (N = 23). Plot of the haemodynamic response recorded in the local maxima of the displayed cluster: periaqueductal grey [4, −30, −16]; Z-score: 4.30 (P < 0.001 at peak level, P < 0.05 family-wise error corrected at cluster level). (C) Scatterplot of the correlation analysis (N = 9) between the BID individuals’ haemodynamic response and their score at the Zurich Xenomelia Scale (pure amputation desire subscale; min = 1; max = 6): periaqueductal grey, [4, −30, −16], Spearman’s coefficient: 0.5. Each data point represents a BID individual’s BOLD response plotted against the corresponding score on the subscale.

Figure 3

fMRI results: amputation line. (A) Full factorial ANOVA (N = 23). Brain regions showing a significant group-by-side interaction, with increased activations recorded in individuals with BID, particularly in response to the stimulation of the desired point of amputation (independently from the direction). (B) Full factorial ANOVA (N = 23). Plot of the haemodynamic response recorded in the local maxima of the displayed clusters: middle cingulum [16, 22, 33], Z-score: 5.21, (P < 0.001 at peak level, P < 05 family-wise error corrected at cluster level); precentral gyrus [56, 6, 42], Z-score: 4.75, (P < 0.001 at peak level, P < 0.05 family-wise error corrected at cluster level). (C) Scatterplot of the correlation analysis (N = 9) between the BID individuals’ haemodynamic response and their score at the Zurich Xenomelia Scale (erotic attraction subscale; min = 1; max = 6): middle cingulum [16, 22, 33], Pearson’s coefficient = 0.43; precentral gyrus [56, 6, 42], Pearson’s coefficient = 0.17. Each data point represents a BID individual’s BOLD response plotted against the corresponding score on the subscale.