Enhanced processing of aversive stimuli on embodied artificial limbs by the human amygdala

Abstract

Body perception has been extensively investigated, with one particular focus being the integration of vision and touch within a neuronal body representation. Previous studies have implicated a distributed network comprising the extrastriate body area (EBA), posterior parietal cortex (PPC) and ventral premotor cortex (PMv) during illusory self-attribution of a rubber hand. Here, we set up an fMRI paradigm in virtual reality (VR) to study whether and how the self-attribution of (artificial) body parts is altered if these body parts are somehow threatened. Participants (N = 30) saw a spider (aversive stimulus) or a toy-car (neutral stimulus) moving along a 3D-rendered virtual forearm positioned like their real forearm, while tactile stimulation was applied on the real arm in the same (congruent) or opposite (incongruent) direction. We found that the PPC was more activated during congruent stimulation; higher visual areas and the anterior insula (aIns) showed increased activation during aversive stimulus presentation; and the amygdala was more strongly activated for aversive stimuli when there was stronger multisensory integration of body-related information (interaction of aversiveness and congruency). Together, these findings suggest an enhanced processing of aversive stimuli within the amygdala when they represent a bodily threat.

Figure 1

(a) Image of the virtual environment seen by the participants. Only the right-eye view is shown. Stimuli used for aversive (spider) and neutral (car) conditions. The red fixation dot at the center of the forearm blinked briefly during attentional control trials. (b) Details of the set-up inside the MRI room. Five pairs of surface-adhesive electrodes were positioned on the lateral side of the right forearm, from the wrist to the elbow, to enable five stimulation sites. The right arm was placed horizontally on top of the participant’s chest using pillows, fist closed. The left hand was holding the response button box with the arm along the body. The head was slightly tilted in the direction of the chest within the head coil (approx. 20°–30°). Stereoscopic goggles were attached to the participant’s forehead and the head coil (not shown) with Velcro strips to minimize motion.

Figure 2

(a) Congruent versus incongruent visual-tactile stimulation produced significant activation differences in the left SPL (area 7A; p < 0.05, FWE corrected on the cluster level). (b) Aversive versus neutral stimuli showed significant activation differences in left aIns (area Id7; p < 0.001, uncorrected), and left and right middle temporal area (LOC/hMT+/V5), left and right V1, and right fusiform gyrus (p < 0.05, FWE corrected on the cluster level). (c) Interaction congruency × aversiveness revealed activations in right amygdala (area SF; p < 0.001, uncorrected). Here, activations within anatomical masks of the bilateral amygdala and insula (SPM Anatomy Toolbox) are shown. Mean contrast estimates of peak activations for both regions are plotted; error bars represent standard error.