Heightened emotional contagion in mild cognitive impairment and Alzheimer's disease is associated with temporal lobe degeneration

Abstract

Emotional changes are common in mild cognitive impairment (MCI) and Alzheimer's disease (AD). Intrinsic connectivity imaging studies suggest that default mode network degradation in AD is accompanied by the release of an emotion-relevant salience network. We investigated whether emotional contagion, an evolutionarily conserved affect-sharing mechanism, is higher in MCI and AD secondary to biological alterations in neural networks that support emotion. We measured emotional contagion in 237 participants (111 healthy controls, 62 patients with MCI, and 64 patients with AD) with the Interpersonal Reactivity Index Personal Distress subscale. Depressive symptoms were evaluated with the Geriatric Depression Scale. Participants underwent structural MRI, and voxel-based morphometry was used to relate whole-brain maps to emotional contagion. Analyses of covariance found significantly higher emotional contagion at each stage of disease progression [controls < MCI (P < 0.01) and MCI < AD (P < 0.001)]. Depressive symptoms were also higher in patients compared with controls [controls < MCI (P < 0.01) and controls < AD (P < 0.0001)]. Higher emotional contagion (but not depressive symptoms) was associated with smaller volume in right inferior, middle, and superior temporal gyri (PFWE < 0.05); right temporal pole, anterior hippocampus, parahippocampal gyrus; and left middle temporal gyrus (all P < 0.001, uncorrected). These findings suggest that in MCI and AD, neurodegeneration of temporal lobe structures important for affective signal detection and emotion inhibition are associated with up-regulation of emotion-generating mechanisms. Emotional contagion, a quantifiable index of empathic reactivity that is present in other species, may be a useful tool with which to study emotional alterations in animal models of AD.

Keywords: affective resonance; empathy; simulation; social behavior.

Fig. 1.

Emotional contagion and depressive symptoms in MCI and AD are higher than in healthy controls (CTL). (A) Raw emotional contagion (IRI Personal Distress subscale) and (B) depressive symptom (GDS) scores for the CTL (n = 111), MCI (n = 62), and AD (n= 64) groups. Komogorov-Smirnov tests of normalcy indicated that there was a normal distribution of emotional contagion scores in MCI (P > 0.05) and AD (P > 0.05). (C) Emotional contagion and (D) depressive symptoms, adjusted for age and education and stratified by sex, were higher in patients than in healthy controls. Significant main effects of diagnosis are denoted by *P < 0.01, **P < 0.001, and ***P < 0.0001. Error bars represent SEMs.

Fig. 2.

T-score maps of brain areas for which smaller volume is associated with higher emotional contagion (IRI Personal Distress subscale score) when controlling for age, education, sex, diagnosis, field strength, and total intracranial volume (n = 237). Smaller volume in right inferior, middle temporal, and superior temporal gyri was associated with higher emotional contagion after correction for type 1 error (P_FWE < 0.05). At less stringent statistical thresholds, smaller volume in left middle temporal gyrus, right temporal pole, right anterior hippocampus, and right parahippocampal gyrus were also associated with higher emotional contagion (P < 0.001, uncorrected). Color bars represent T scores (hot, P_FWE < 0.05 according to study-specific permutation analysis; blue, P < 0.001, uncorrected; T > 3.13 and cluster size > 150 mm³). Results are overlaid on a DARTEL-derived template of 50 older healthy controls.