Inhibition of Return Is Modulated by Negative Stimuli: Evidence from Subliminal Perception

ORIGINAL RESEARCH published: 20 June 2017 doi: 10.3389/fpsyg.2017.01012 Inhibition of Return Is Modulated by Negative Stimuli: Evidence from Subliminal Perception Fada Pan *, Xiaogang Wu, Li Zhang and Yuhong Ou Department of Applied Psychology, School of Education Science, Nantong University, Nantong, China Edited by: Richard A. Abrams, Washington University in St. Louis, United States Reviewed by: Elisa Martín-Arévalo, INSERM-U1028 - CRNS UMR5292 Centre de Recherche en Neurosciences de Lyon, France John J. McDonald, Simon Fraser University, Canada *Correspondence: Fada Pan Specialty section: This article was submitted to Cognition, a section of the journal Frontiers in Psychology Received: 20 March 2017 Accepted: 01 June 2017 Published: 20 June 2017 Citation: Pan F, Wu X, Zhang L and Ou Y (2017) Inhibition of Return Is Modulated by Negative Stimuli: Evidence from Subliminal Perception. Front. Psychol. 8:1012. doi: 10.3389/fpsyg.2017.01012 Inhibition of return (IOR) is considered as a “blindness mechanism” that emotional stimuli have no impact on it. Most previous studies suggested that IOR was not modulated by emotional cues. However, one key question they ignored was that only supraliminal presentation of emotional stimuli was used in their experiments. The present experiment is aimed at exploring the possible interaction between the IOR effect and subliminal emotional process. We manipulated three different kinds of valence strength of negative stimuli (high negative, HN; moderate negative, MN; low negative, LN) which were presented under the subliminal perception level and an event-related potentials (ERPs) recording was adopted. The results showed that, compared to MN and HN, the IOR effect triggered by peripheral cues was more significant for LN with aspects of behavioral and electrophysiological data (a reduction P1 effect, more negative on cued trials than on uncued trials for both early posterior Nd and Nd components). This indicated that IOR can be modulated by emotionally relevant stimuli. The automatic processing that was triggered by subliminally negative stimuli of peripheral cues had an influence on the shifting of spatial attention that was triggered by IOR. These two mechanisms may occur in the perceptual stage simultaneously. Keywords: inhibition of return, negative stimuli, subliminal perception, event-related potentials, emotional processing INTRODUCTION The limited processing capacity of the visual system makes attention select the most valuable information when our visual environment is rich. Moreover, the rapid and efficient attention to stimuli relating to the development or survival of individuals may have a crucial influence on flexible and adaptive behavior, especially for the threatening information. Inhibition of return (IOR) is widely considered as a “foraging facilitation” which contributes to adaptive behavior (Wang and Klein, 2010). Posner and Cohen (1984) first found this phenomenon using a non-predictive cue-target paradigm, combining peripheral cue with the peripheral target. Reaction times are usually faster at the uncued location (cue and target appeared at different positions) than at the cued location when SOA (stimulus onset asynchrony) is more than about 300 ms. The common interpretation is that, by inhibiting attention return to the inspected locations, IOR encourages attention to orient to novel locations. Consequently, the improved efficiency of visual search reflects flexible and adaptive cognitive process (Klein, 2000; Ivanoff and Taylor, 2006). The current experiment is aimed at investigating how the IOR effect will be affected when attention is attracted by biological stimuli (i.e., negative events) during the spatially visual search. Frontiers in Psychology | www.frontiersin.org 1 June 2017 | Volume 8 | Article 1012 Pan et al. Negative Stimuli Modulated IOR sensory/perceptual ERP components (P1: perceptual; N1, Nd: late-perceptual) (Zhang and Zhang, 2007; Prime and Jolicoeur, 2009; Satel et al., 2014). Those three components are mostly used to investigate IOR effect regardless of types of tasks, time courses or theories, and there is no signal electrophysiological marker for the IOR effect so far (Martín-Arévalo et al., 2015). When researchers use a non-predictive cueing paradigm to investigate the relation between the IOR effect and emotion processing, peripheral cues will trigger the exogenous attentional capture. A bottom-up selective response to potential relevant stimuli is raised from this exogenous capture of attention (Hopfinger and West, 2006). Thus, the IOR effect may mainly reflect the perceptual process of visual search and represents a bottom-up reflexive behavior (Stoyanova et al., 2007; Sapir et al., 2014). One question is that the present time of biologically relevant stimuli in previous literature is hardly less than 200 ms, indicating supraliminal perception. The supraliminal and subliminal visual processes of emotional stimuli have different neural pathways and response characteristics (Bernat et al., 2001). The supraliminal process of emotional stimuli is subject to top-down attentional control (Yamasaki et al., 2002). Thus, this may reflect that the supraliminal perception of emotional stimuli and reflexive IOR may occur in the different stages, leading to no interaction between them. One rational hypothesis of attentional bias should propose that, if attention is captured more easily by biologically relevant stimuli than less relevant stimuli appearing at the cued location, the magnitude of IOR effect will be reduced or eliminated. However, this hypothesis does not fit well with previously experimental results. Whether emotional, neutral faces or spiders are presented at the peripheral cueing locations, the magnitude of IOR effect have no conspicuous difference under all cue conditions (Stoyanova et al., 2007; Lange et al., 2008; Hu et al., 2014), indicating that IOR is blind to emotion stimuli. Another special central cue-target paradigm presented supraliminal emotion cues at the center of the screen found that the attentional system tended to inhibit irrelevant negative emotion but not inhibit irrelevant positive emotion (Chao, 2010). However, researchers recently replicated Chao’s experiment and their reanalysis indicated slower responses to negative facial expressions than positive ones regardless of the preceding cue (Poliakoff et al., 2015). Thus, they thought that orienting in the emotional domain could not be measured by using a cue-target task. On the other hand, manipulation of emotional targets is also used to investigate attentional capture. These studies found the modulation of IOR effect relating with schematic sadly face only in the left visual field (Baijal and Srinivasan, 2011), anxiety induced by threatening context (Rutherford and Raymond, 2010) and schizophrenic patients (Hu et al., 2014, experiment 2). Based on above studies, it seems that IOR is not modulated by e (...truncated)