Neuroanatomical Correlates of Recognizing Face Expressions in Mild Stages of Alzheimer's Disease.

Laurie-Anne Sapey-Triomphe,Jean-Michel Dorey,Alzheimer’s Disease Neuroimaging Initiative ,Alexander Hammers,Catherine Padovan,Marie-Anne Hénaff,Isabelle Rouch,Rolf A Heckemann,Nawele Boublay,Pierre Krolak-Salmon

doi:10.1371/journal.pone.0143586

Abstract

Early Alzheimer’s disease can involve social disinvestment, possibly as a consequence of impairment of nonverbal communication skills. This study explores whether patients with Alzheimer’s disease at the mild cognitive impairment or mild dementia stage have impaired recognition of emotions in facial expressions, and describes neuroanatomical correlates of emotion processing impairment. As part of the ongoing PACO study (personality, Alzheimer’s disease and behaviour), 39 patients with Alzheimer’s disease at the mild cognitive impairment or mild dementia stage and 39 matched controls completed tests involving discrimination of four basic emotions—happiness, fear, anger, and disgust—on photographs of faces. In patients, automatic volumetry of 83 brain regions was performed on structural magnetic resonance images using MAPER (multi-atlas propagation with enhanced registration). From the literature, we identified for each of the four basic emotions one brain region thought to be primarily associated with the function of recognizing that emotion. We hypothesized that the volume of each of these regions would be correlated with subjects’ performance in recognizing the associated emotion. Patients showed deficits of basic emotion recognition, and these impairments were correlated with the volumes of the expected regions of interest. Unexpectedly, most of these correlations were negative: better emotional facial recognition was associated with lower brain volume. In particular, recognition of fear was negatively correlated with the volume of amygdala, disgust with pallidum, and happiness with fusiform gyrus. Recognition impairment in mild stages of Alzheimer’s disease for a given emotion was thus associated with less visible atrophy of functionally responsible brain structures within the patient group. Possible explanations for this counterintuitive result include neuroinflammation, regional β-amyloid deposition, or transient overcompensation during early stages of Alzheimer’s disease.

Highlights

Interpersonal communication relies on verbal conversation, and on non-verbal cues such as facial emotional expressions
Only a few studies [3, 7,8,9,10] investigated this ability at early stages corresponding to mild cognitive impairment (MCI) or prodromal and mild dementia stages of Alzheimer’s disease (AD)
As early atrophy occurs in brain regions crucial for emotion processing, it might be linked to social disinvestment and behavioural symptoms, early social cognition impairment, and emotion recognition impairment

Summary

Introduction

Interpersonal communication relies on verbal conversation, and on non-verbal cues such as facial emotional expressions. Interpreting facial expressions is crucial to recognition of the mental state of others and to successful social interaction. AD is characterized at the early stages by an episodic memory decline, but other cognitive domains, like executive function and social cognition, may be impaired [3, 4]. Only a few studies [3, 7,8,9,10] investigated this ability at early stages corresponding to mild cognitive impairment (MCI) or prodromal and mild dementia stages of AD. AD at the MCI or mild dementia stage is characterized by episodic memory impairment, cognitive decline to various degrees, and entorhinal cortex and hippocampal atrophy [12], as well as amygdala atrophy [13, 14]. As early atrophy occurs in brain regions crucial for emotion processing, it might be linked to social disinvestment and behavioural symptoms, early social cognition impairment, and emotion recognition impairment

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