Enhanced Positive Emotional Reactivity Undermines Empathy in Behavioral Variant Frontotemporal Dementia

Abstract

Behavioral variant frontotemporal dementia (bvFTD) is a neurodegenerative disease characterized by profound changes in emotions and empathy. Although most patients with bvFTD become less sensitive to negative emotional cues, some patients become more sensitive to positive emotional stimuli. We investigated whether dysregulated positive emotions in bvFTD undermine empathy by making it difficult for patients to share (emotional empathy), recognize (cognitive empathy), and respond (real-world empathy) to emotions in others. Fifty-one participants (26 patients with bvFTD and 25 healthy controls) viewed photographs of neutral, positive, negative, and self-conscious emotional faces and then identified the emotions displayed in the photographs. We used facial electromyography to measure automatic, sub-visible activity in two facial muscles during the task: Zygomaticus major (ZM), which is active during positive emotional reactions (i.e., smiling), and Corrugator supercilii (CS), which is active during negative emotional reactions (i.e., frowning). Participants rated their baseline positive and negative emotional experience before the task, and informants rated participants' real-world empathic behavior on the Interpersonal Reactivity Index. The majority of participants also underwent structural magnetic resonance imaging. A mixed effects model found a significant diagnosis X trial interaction: patients with bvFTD showed greater ZM reactivity to neutral, negative (disgust and surprise), self-conscious (proud), and positive (happy) faces than healthy controls. There was no main effect of diagnosis or diagnosis X trial interaction on CS reactivity. Compared to healthy controls, patients with bvFTD had impaired emotion recognition. Multiple regression analyses revealed that greater ZM reactivity predicted worse negative emotion recognition and worse real-world empathy. At baseline, positive emotional experience was higher in bvFTD than healthy controls and also predicted worse negative emotion recognition. Voxel-based morphometry analyses found that smaller volume in the thalamus, midcingulate cortex, posterior insula, anterior temporal pole, amygdala, precentral gyrus, and inferior frontal gyrus-structures that support emotion generation, interoception, and emotion regulation-was associated with greater ZM reactivity in bvFTD. These findings suggest that dysregulated positive emotional reactivity may relate to reduced empathy in bvFTD by making patients less likely to tune their reactions to the social context and to share, recognize, and respond to others' feelings and needs.

Keywords: dysregulation; emotion recognition; empathy; facial electromyography; frontotemporal dementia; positive emotion.

Figure 1

On the left, we show an example of the images that participants viewed during a baseline and a trial. The emotional faces were selected from the UC Davis Set of Emotions Expressions (50); the disgust face from that stimuli set is shown here for illustrative purposes. On the right, we show EMG reactivity scores for one patient with bvFTD and one healthy control (HC) from the disgust trial. Reactivity scores for zygomaticus major (ZM) and corrugator supercilli (CS) were calculated by subtracting mean activity during the last 2 s of the baseline from each 100 ms window during the first 5 s of the trial. Peak muscle reactivity was identified for each participant using the maximum change score during the 5 s trial (circled).

Figure 2

Greater total zygomaticus major (ZM) peak reactivity across trials correlated with lower empathic concern and perspective-taking on the Interpersonal Reactivity Index (IRI), a measure of real-world empathy that was completed by informants in a subset of participants (7 patients with bvFTD, 9 HC). bvFTD, behavioral variant frontotemporal dementia; HC, healthy controls.

Figure 3

(A) T-score maps of brain areas in which patients with bvFTD have smaller gray matter volume compared to healthy controls, controlling for age, sex, and total intracranial volume (hot; p_FWE < 0.05). The patient group had smaller volume in the anterior cingulate, insula, striatum, and amygdala, among other regions. (B) The mask for our VBM analysis in red. (C) An overlay of both (A,B).

Figure 4

(A) T-score maps of brain areas in which smaller gray matter volume was associated with greater zygomaticus major reactivity in bvFTD. We examined whether there was a zygomaticus major X diagnosis interaction on gray matter volume (controlling for the main effects of total zygomaticus major peak reactivity across all trials and diagnosis as well as additional nuisance covariates: CDR-Box and total intracranial volume). Smaller volume (Max T-score = 5.33) in the bilateral thalamus, bilateral midcingulate cortex, bilateral precentral gyri, left anterior temporal pole, right amygdala, right posterior insula, and bilateral inferior frontal gyrus was associated with greater zygomaticus major reactivity across all trials in bvFTD (blue; p < 0.005). Clusters in the bilateral thalamus and right midcingulate cortex survived family wise error correction (cyan; p_FWE < 0.05). Color bars indicate the T-scores. (B) T-score maps of brain areas in which patients with bvFTD have smaller gray matter volume compared to healthy controls (hot; p_FWE < 0.05) with an overlay of T-score maps of brain areas in which smaller gray matter volume was associated with greater zygomaticus major reactivity in bvFTD (cyan; p_FWE < 0.05).