Research ReportAttention is prioritised for proximate and approaching fearful faces
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.
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