How Negative Social Bias Affects Memory for Faces: An Electrical Neuroimaging Study

RESEARCH ARTICLE How Negative Social Bias Affects Memory for Faces: An Electrical Neuroimaging Study Alice Mado Proverbio1*, Francesca La Mastra1, Alberto Zani2 1 NeuroMi - Milan Center for Neuroscience, Dept. of Psychology, University of Milano-Bicocca, Milan, Italy, 2 Institute of Bioimaging and Molecular Physiology, IBFM-CNR, Milan, Italy * a11111 OPEN ACCESS Citation: Proverbio AM, La Mastra F, Zani A (2016) How Negative Social Bias Affects Memory for Faces: An Electrical Neuroimaging Study. PLoS ONE 11(9): e0162671. doi:10.1371/journal. pone.0162671 Editor: Peter James Hills, Bournemouth University, UNITED KINGDOM Received: February 27, 2015 Accepted: August 28, 2016 Published: September 21, 2016 Copyright: © 2016 Proverbio et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The authors confirm that all data underlying the findings are fully available without restriction. However, data containing participant information cannot be deposited to a public repository and shared, according to our ethical approval granted by the Ethics Committee of University of Milano-Bicocca. Data are confidential and will be available upon request. Interested researchers and readers can contact the corresponding author () of the manuscript to request access to the data. Abstract During social interactions, we make inferences about people’s personal characteristics based on their appearance. These inferences form a potential prejudice that can positively or negatively bias our interaction with them. Not much is known about the effects of negative bias on face perception and the ability to recognize people faces. This ability was investigated by recording event-related potentials (ERPs) from 128 sites in 16 volunteers. In the first session (encoding), they viewed 200 faces associated with a short fictional story that described anecdotal positive or negative characteristics about each person. In the second session (recognition), they underwent an old/new memory test, in which they had to distinguish 100 new faces from the previously shown faces. ERP data relative to the encoding phase showed a larger anterior negativity in response to negatively (vs. positively) biased faces, indicating an additional processing of faces with unpleasant social traits. In the recognition task, ERPs recorded in response to new faces elicited a larger FN400 than to old faces, and to positive than negative faces. Additionally, old faces elicited a larger Old-New parietal response than new faces, in the form of an enlarged late positive (LPC) component. An inverse solution SwLORETA (450–550 ms) indicated that remembering old faces was associated with the activation of right superior frontal gyrus (SFG), left medial temporal gyrus, and right fusiform gyrus. Only negatively connoted faces strongly activated the limbic and parahippocampal areas and the left SFG. A dissociation was found between familiarity (modulated by negative bias) and recollection (distinguishing old from new faces). Introduction Prejudice is a type of "premature judgment" of subjects of which we have no direct, complete and sufficient knowledge. Allport [1] described the prejudice as a feeling, positive or negative, relative to a person or a thing before direct experience or that is not based on the person or thing. Prejudice formation is considered to be an adaptive cognitive process that helps the human mind to process information through the help of categories. After these categories have been created, prejudice inevitably arises. We know that people’s social traits are inferred on the basis of their appearance and that this judgment activates a potential bias able to influence PLOS ONE | DOI:10.1371/journal.pone.0162671 September 21, 2016 1 / 18 Memory for Faces: The Effect of Prejudice Funding: This work was supported by the 9928 2013-ATE-0037 grant from University of MilanoBicocca. Competing Interests: The authors have declared that no competing interests exist. social interactions. At this regard a social context network model (SCNM), a fronto-insulartemporal network has been proposed by Ibáñez and Manes [2], as being responsible for processing social contextual effects, able to update the context and use it to make predictions and consolidate context-target associative learning. Indeed many studies have extensively shown the role of contextual and social factors in in stimulus recognition (e.g., [3]). However, not much is known about the impact of these biases on specific aspects of human cognition, such as memory processes. While walking through the streets of our city, we encounter hundreds of people, and although we will easily forget some of them, others remain etched in our memory. Why are some faces remembered better than others? A strong indicator of how and when a face is remembered is face typicality [4]. Unusual faces with atypical features are better remembered than more typical faces [5], even if less attractive. Another component that affects facial memory is perceived trustworthiness. Some studies suggest that faces perceived as the most untrustworthy are remembered significantly more than those perceived as reliable [6]. However, in these experiments, characters were perceived as unreliable only on the basis of perceptual appearance. In a study manipulating social traits, Mealey and colleagues [7] associated a face with some fictional personal traits (irrelevant history, history of unreliability, history of cheating) of the person depicted in the photograph. A week later, the experimental subjects were presented the old as well as new faces, and the task was to recognize which one had been previously encountered. The results showed a higher percentage of recognition of persons described as crooks in the learning phase. Generally, negative emotionally-valenced stimuli are remembered better than positive or neutral stimuli. For example, Ochsner [8] reported better performance in an old/new task for faces with a negative facial expression vs. a positive or a neutral face, whereas another study [9], in which both faces and scenes were used as experimental stimuli, showed that greater recognition of stimuli with negative valence occurred compared to those with neutral valence. The reason for this advantage might be due to stronger memory traces for aversive stimuli that might involve associations with amygdala and limbic structures. Indeed, investigations of emotion’s impact on memory have shown that emotion enhances memory [10–12] and that this enhancement is associated with increased engagement of amygdala, hippocampus, parahippocampus, and medial temporal lobe regions [13]. The enhanced activity in these areas has been observed during both encoding [14–17] and retrieval [18–20]. However, a di (...truncated)