Behavioral and neural correlates of visual emotion discrimination and empathy in mild cognitive impairment

•Orbitofrontal atrophy and executive deficits are associated with lack of EEF in MCI.•MCI patients lack emotional enhancement effect specifically for facial stimuli.•Lower cognitive empathy in MCI is associated with fusiform and cerebellar atrophy.•Reduced interpersonal functioning is independent from implicit emotional deficits.•Implicit and explicit measures of empathy in Mild Cognitive Impairments.

Emotional and social cognitive deficits were investigated in a group of 24 individuals with mild cognitive impairment (MCI) and 24 healthy controls. Empathic and visual emotional responses were collected, analyzed and correlated to brain structural imaging data by means of: (i) a pictorial matching-to-sample task with facial and non-facial stimuli; (ii) self-reported questionnaires for cognitive and affective emotional components, and alexithymia; (iii) in-depth assessment of cognitive functions. Results indicated that visual processing of faces in MCI individuals did not benefit from fearful emotional content which in healthy controls facilitates stimulus’ recognition (emotional enhancement effect). This implicit visuo-emotional disorder was specific for the faces, did not generalize to other categories, and did not correlate to explicit measures of empathy. Thus, our main finding indicates that in MCI individuals, deficits in visual recognition of facial emotions may arise already in the earliest stages of memorization, during the visual encoding of facial emotions. Voxel-based morphometry revealed its association with atrophy in frontal and occipito-temporal regions, mostly involving the anterior medial prefrontal cortex (P < 0.05, multiple-comparison correction). Neural evidences were corroborated by clinical scores showing significant correlation between reduction of Emotion Enhancement Effect and deficits in frontal/executive functions. Crucially, the disorder did not appear to be related to the number of impaired cognitive domains (single or multiple-domain MCI) but rather to the involvement of frontal brain networks and frontal/executive functions. This suggests that in prodromal stages of dementia, frontal symptoms may represent a significant signal of emotional recognition disorders.