Elsevier

Cortex

Volume 134, January 2021, Pages 52-64
Cortex

Research Report
Attention is prioritised for proximate and approaching fearful faces

https://doi.org/10.1016/j.cortex.2020.10.011Get rights and content

Abstract

Attention is an important function that allows us to selectively enhance the processing of relevant stimuli in our environment. Fittingly, a number of studies have revealed that potentially threatening/fearful stimuli capture attention more efficiently. Interestingly, in separate fMRI studies, threatening stimuli situated close to viewers were found to enhance brain activity in fear-relevant areas more than stimuli that were further away. Despite these observations, few studies have examined the effect of personal distance on attentional capture by emotional stimuli. Using electroencephalography (EEG), the current investigation addressed this question by investigating attentional capture of emotional faces that were either looming/receding, or were situated at different distances from the viewer. In Experiment 1, participants carried out an incidental task while looming or receding fearful and neutral faces were presented bilaterally. A significant lateralised N170 and N2pc were found for a looming upright fearful face, however no significant components were found for a looming upright neutral face or inverted fearful and neutral faces. In Experiment 2, participants made gender judgements of emotional faces that appeared on a screen situated within or beyond peripersonal space (respectively 50 cm or 120 cm). Although response times did not differ, significantly more errors were made when faces appeared in near as opposed to far space. Importantly, ERPs revealed a significant N2pc for fearful faces presented in peripersonal distance, compared to the far distance. Our findings show that personal distance markedly affects neural responses to emotional stimuli, with increased attention towards fearful upright faces that appear in close distance.

Introduction

Attention is an important cognitive process that allows the prioritisation of specific stimuli in our environment for further evaluation. This is particularly relevant when stimuli warn of potential danger, for example in detecting the presence of a potential predator in the environment.

In the field of face processing, electrophysiological evidence with EEG has shown that the visual system prioritizes attention towards fearful faces compared to other expressions (Holmes, Green, & Vuilleumier, 2005; Santesso et al., 2008), in particular using a component linked to attention termed the N2pc. The N2pc, characterized as a larger negativity appearing over electrodes contralateral to the side of the attended stimulus compared to ipsilateral electrodes, occurs approx. 200–320 msec post stimulus onset at posterior scalp sites and has been found to reflect selective attention (Holmes, Bradley, Nielsen, & Mogg, 2009; Kiss, Van Velzen, & Eimer, 2008). Eimer and Kiss (2007) investigated how attention, as indexed by this N2pc component, was influenced by a task-irrelevant fearful face presented among other, non-threatening neutral expressions. Even though participants were asked to respond to a luminance change at the centre and to ignore the surrounding faces, an N2pc was observed in response to a fearful face surrounded by neutral other faces. By contrast, there was no N2pc towards a neutral face among fearful faces, indicating that attention is prioritised towards a potentially threatening face. Corroborating this interpretation, behavioural studies have revealed that RTs were faster when detecting a fearful face in visual search or in a dot probe task (Armony & Dolan, 2002; Carlson & Reinke, 2008; Pourtois, Grandjean, Sander, & Vuilleumier, 2004).

Other studies reported that fearful faces can also modulate the N170, a component thought to reflect face processing. The N170 is a bilateral negative deflection, usually predominant over the right hemisphere, that appears about 170 msec after the presentation of a face compared to other non-face stimuli (Bentin, Allison, Puce, Perez, & McCarthy, 1996; Eimer, 2000a; Rossion, Joyce, Cottrell, & Tarr, 2003). Furthermore, when faces are presented bilaterally rather than centrally, this component can be observed as a larger negativity contralateral to the relevant face (lateralised N170; Burra & Kerzel, 2019; Towler & Eimer, 2015; Towler, Kelly, & Eimer, 2016). In one study, fearful faces were found to modulate the amplitude of the N170, with a larger negativity for fearful faces in comparison to other emotional expressions (Blau, Maurer, Tottenham, & McCandliss, 2007). It has been suggested that this effect may result from an enhancement of the visual response due to feedback projections from the amygdala to associative visual areas (Vuilleumier, Richardson, Armony, Driver, & Dolan, 2004).

A distinct and less explored topic is the effect of personal distance on neurophysiological responses. A small number of fMRI studies have demonstrated that fearful/threatening stimuli activate fear-related areas more markedly when they appear to be situated physically closer to the viewer (Coker-Appiah et al., 2013; Mobbs et al., 2010). For instance, Mobbs et al. (2010) measured brain activity while participants were shown a simulated spider that appeared either at a far distance, or close to the participant's foot. When the spider was closer, an increased activation was observed, particularly in the amygdala. Other investigations have shown that when irrelevant stimuli (e.g., meaningless shapes) appear close to the participant, they are attended more rapidly than when they appear at a greater distance (Chen, Weidner, Vossel, Weiss, & Fink, 2012; Kasai, Morotomi, Katayama, & Kumada, 2003). By contrast, in humans, damage to the amygdala appears to disrupt the processing of personal space. Indeed, Kennedy, Glascher, Tyszka, and Adolphs (2009) studied a patient with bilateral damage to this structure and observed a loss of the sense of personal space in this individual.

These observations open the possibility that distance (physical or perceived) can modulate the processing and attentional capture of fearful faces, effects that would be reflected on the N170 and the N2pc. To our knowledge, this has yet to be investigated with the use of EEG or combining distances with emotional faces. EEG measures have extensively demonstrated good temporal resolution and have revealed the neural timing of events associated with both face processing (N170 component) and attention (the N2pc component) (Burra & Kerzel, 2019; Eimer & Kiss, 2007). We therefore used EEG in this study to determine the neural dynamics associated with the encoding and attentional capture of fearful faces, as indexed by the lateralised N170 and N2pc components, in particular to determine how proximity modulates these processes.

In the first experiment, we reasoned that if attention was biased towards fearful faces that potentially entered peripersonal space, this would be reflected in a larger N2pc to approaching (looming) fearful face compared to receding fearful faces, or control stimuli, which were looming neutral and inverted faces. However, another possibility could be that fearful faces attract attention regardless of looming or receding motion, which would produce an N2pc to upright fearful faces in general.

Section snippets

Experiment 1

In Experiment 1, participants completed a task at the centre of the screen by responding to changes of a letter ‘H’ into an odd or even number. Participants were instructed to ignore all looming and receding faces that appeared on the screen on either side of the fixation letter task. Simultaneously, a fearful and a neutral face appeared bilaterally, one of which dynamically increased in size (‘looming’), while the other decreased in size (‘receding’). As a control, inverted fearful and neutral

Experiment 2

The second experiment examined whether the distance of the faces affected the electrophysiological markers of face processing (N170) and attention (N2pc). Fearful and neutral faces were presented bilaterally on a screen that was situated either 50 cm away (within reaching distance) or at 120 cm (beyond reaching distance). Contrary to experiment 1 where faces were entirely irrelevant to the task, experiment 2 required faces to be attended by asking them to compare the two stimuli for gender

General discussion

The two experiments carried out here aimed to determine whether attentional capture of fearful faces is modulated by viewing distance, such that emotional faces might attract attention more strongly when the stimuli are presented within peri-personal space (reaching distance) than when they are situated beyond, in extrapersonal space. To our knowledge, this is the first electrophysiological study to show such an effect, reflected in a larger N2pc to fearful faces in peripersonal space than in

CRediT author statement

Aimee Martin: Conceptualization, Methodology, Software, Formal analysis, Investigation, Writing - Original Draft, Writing - Review & Editing, Visualization.

Stefanie I Becker: Conceptualization, Methodology, Resources, Writing - Review & Editing, Supervision.

Alan J Pegna: Conceptualization, Methodology, Resources, Writing - Review & Editing, Supervision.

Open practices

The study in this article earned Open Materials and Open Data badges for transparent practices. Materials and data for the study are available at https://osf.io/zg89x/?view_only=e7e32fca399046fbbbb8965d0bcf1267.

Acknowledgements

This research was funded by an Australian Research Council, DP170102559, and an ARC Future Fellowship awarded to Stefanie I. Becker, FT130101282. Aimee Martin was supported by the Australian Government Research Training Program Scholarship.

References (51)

  • C. Jacques et al.

    Early electrophysiological responses to multiple face orientations correlate with individual discrimination performance in humans

    Neuroimage

    (2007)
  • T. Kasai et al.

    Attending to a location in three-dimensional space modulates early ERPs

    Cognitive Brain Research

    (2003)
  • T. Marzi et al.

    Interplay between familiarity and orientation in face processing: An ERP study

    International Journal of Psychophysiology

    (2007)
  • A.J. Pegna et al.

    Electrophysiological evidence for early non- conscious processing of fearful facial expressions

    International Journal of Psychophysiology

    (2008)
  • B. Rossion et al.

    Early lateralization and orientation for face, word, and object processing in the visual cortex

    Neuroimage

    (2003)
  • D.L. Santesso et al.

    Electrophysiological correlates of spatial orienting towards angry faces: A source localization study

    Neuropsychologia

    (2008)
  • J. Towler et al.

    Early stages of perceptual face processing are confined to the contralateral hemisphere: Evidence from the N170 component

    Cortex; a Journal Devoted To the Study of the Nervous System and Behavior

    (2015)
  • M. Allen et al.

    Raincloud plots: A multi-platform tool for robust data visualization [version 1; peer review: 2 approved]

    Wellcome Open Research

    (2019)
  • S. Bentin et al.

    Electrophysiological studies of face perception in humans

    Journal of Cognitive Neuroscience

    (1996)
  • A. Berti et al.

    When far becomes near: Remapping of space by tool use

    Journal of Cognitive Neuroscience

    (2000)
  • V.C. Blau et al.

    The face-specific N170 component is modulated by emotional facial expression

    Behavioral and Brain Functions: BBF

    (2007)
  • N. Burra et al.

    Task demands modulate effects of threatening faces on early perceptual encoding

    Frontiers in Psychology

    (2019)
  • J.M. Carlson et al.

    Masked fearful faces modulate the orienting of covert spatial attention

    Emotion

    (2008)
  • Q. Chen et al.

    Neural mechanisms of attentional reorienting in three-dimensional space

    The Journal of Neuroscience

    (2012)
  • D.S. Coker-Appiah et al.

    Looming animate and inanimate threats: The response of the amygdala and periaqueductal grey

    Social Neuroscience

    (2013)
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