The cortical processing of facial emotional expression is associated with social cognition skills and executive functioning: A preliminary study

Abstract

Several lines of experimental evidence support an association between facial processing and social cognition, but no direct link between cortical markers of facial processing and complex cognitive processes has been reported until now. In the current study, we tested the hypothesis that cortical electrophysiological markers for the processing of facial emotion are associated with individual differences in executive and social cognition skills. We tested for correlations between the amplitude of event-related potentials (N170) in a dual valence task and participants’ scores on three neuropsychological assessments (general neuropsychology, executive functioning, and social cognition). N170 was modulated by the stimulus type (face versus word) and the valence of faces (positive versus negative). The neural source of N170 was estimated to be the fusiform gyrus. Robust correlations were found between neuropsychological markers and measures of facial processing. Social cognition skills (as measured by three tests: the Reading the Mind in the Eyes test, the Faux Pas test, and the Iowa Gambling Task) correlated with cortical measures of emotional discrimination. Executive functioning ability also correlated with the cortical discrimination of complex emotional stimuli. Our findings suggest that the cortical processing of facial emotional expression is associated with social cognition skills.

Introduction

Faces are among the most important visual stimuli for humans [17]. In the current study, we tested the hypothesis that cortical electrophysiological markers of the processing of facial emotion are associated with individual differences in complex social cognition skills. Face processing is critically important for many aspects of social interaction (see reviews [17], [27]). Impairments in facial processing may be central to abnormal social cognition [15]. Furthermore, facial emotion processing has shown positive associations with information processing speed, executive function and working memory [18]. Indeed, Bruce and Young [4] have postulated that facial processing is related to high-level cognitive processes. This relationship would be explained by a higher order cognitive process in which the structural representation of the face is associated with semantic and cognitive information. Thus, facial processing may be also associated with important aspects of cognitive processing such as executive functions. Existing studies of healthy participants [11], [12], participants with autism spectrum disorders [5], and participants with frontotemporal dementia [7] all suggest that facial processing is required for and related to different high-level social cognition skills. However, a possible association between the cortical markers of facial processing and neuropsychological markers of social cognition has not yet been proposed.

We measured cortical markers of face processing with an early event-related potential (ERP) component, referred to as the N170. This component shows a negative peak at approximately 140–200 ms post-stimulus involved in the processing of faces [23]. The N170 component is sensitive to stimulus type (facial or other) [13], [16], [22] and is affected by emotional valence [3], [29]. Moreover, the N170 amplitude can be modulated by interference [8] (e.g., two stimuli with opposing valences). Studies of brain topography have localized the source of the N170 to the fusiform gyrus (FG) [25]. The current study used a modified version of the dual valence task (DVT) [14], [30] design with healthy participants. In the DVT, faces, words or simultaneous face–word stimuli are presented. Participants are asked to classify the stimuli according to their emotional valence. In order to relate cortical markers of face processing to social cognition and executive functions, a set of neuropsychological tests was included.

The most commonly used social cognition tasks test emotional inference, high level theory of mind processing and affective decision making. We hypothesised that the N170 would be associated with each of these three levels of social processing. First, we proposed emotional N170 would be associated with basic theory of mind (ToM), as measured by the Reading the Mind in the Eyes test (RMET) [2] because mental inference is determined by facial emotional content. Second, we expect the Faux Pas test [FPT], another ToM task, would be mediated by emotional and executive functions because the FPT involves dealing with a high number of cognitive and affective components [1]. Third, we proposed that decision making assessments with the Iowa Gambling Task [IGT] (especially the first of five blocks) would be associated with cortical emotional processing. Only the first block of the IGT can be consistently associated with ambiguity and influenced by emotional heuristics [6].

Based on these hypotheses, we predicted that higher performance on the social cognition tasks would correlate with greater discrimination of facial emotional valence and stimulus type as shown by the amplitude of the N170 component. Our second prediction was that higher performance on tasks of executive function would be associated with greater discrimination of emotional valence as shown by the amplitude of the N170 in response to simultaneous (face–word) stimuli.