Attenuated sensitivity to the emotions of others by insular lesion

Abstract

The insular cortex has been considered to be the neural base of visceral sensation for many years. Previous studies in psychology and cognitive neuroscience have accumulated evidence indicating that interoception is an essential factor in the subjective feeling of emotion. Recent neuroimaging studies have demonstrated that anterior insular cortex activation is associated with accessing interoceptive information and underpinning the subjective experience of emotional state. Only a small number of studies have focused on the influence of insular damage on emotion processing and interoceptive awareness. Moreover, disparate hypotheses have been proposed for the alteration of emotion processing by insular lesions. Some studies show that insular lesions yield an inability for understanding and representing disgust exclusively, but other studies suggest that such lesions modulate arousal and valence judgments for both positive and negative emotions. In this study, we examined the alteration in emotion recognition in three right insular and adjacent area damaged cases with well-preserved higher cognitive function. Participants performed an experimental task using morphed photos that ranged between neutral and emotional facial expressions (i.e., anger, sadness, disgust, and happiness). Recognition rates of particular emotions were calculated to measure emotional sensitivity. In addition, they performed heartbeat perception task for measuring interoceptive accuracy. The cases identified emotions that have high arousal level (e.g., anger) as less aroused emotions (e.g., sadness) and a case showed remarkably low interoceptive accuracy. The current results show that insular lesions lead to attenuated emotional sensitivity across emotions, rather than category-specific impairments such as to disgust. Despite the small number of cases, our findings suggest that the insular cortex modulates recognition of emotional saliency and mediates interoceptive and emotional awareness.

Keywords: arousal level; facial expression; heartbeat perception task; insula; interoceptive accuracy.

FIGURE 1

Transverse magnetic resonance imaging with FLAIR acquisition of the brains of the cases. Left sides of images correspond to the right side of the brain. (A) Case A, (B) Case B, and (C) Case C.

FIGURE 2

The stimuli used in the task (A) and outline of a trial (B). (A) Morphed continua photos ranging between neutral (stimulus 1) and 100% of each facial expression (stimulus 10), i.e., angry. (B) A stimulus was followed by a judgment about whether the stimulus elicited an emotion. If participants responded “yes,” options were presented and they were asked to choose the most appropriate emotion category.

FIGURE 3

Numbers of responses for happiness (blue), sadness (red), disgust (green), and anger (purple) for each stimulus. (A) Case A, (B) Case B, and (C) Case C. Red arrows show the place where the thresholds of cases appeared, and yellow arrows show the averaged thresholds of healthy participants.