Elsevier

Brain Research

Volume 1589, 17 November 2014, Pages 37-44
Brain Research

Research Report
Eye gaze triggers reflexive attention shifts: Evidence from lateralised ERPs

https://doi.org/10.1016/j.brainres.2014.09.029Get rights and content

Highlights

  • The study explored ERP technique in spatial cuing task combined with visual search.

  • In the task, targets were defined by feature conjunctions.

  • Reflexive attention shifts were triggered by eye gazes.

  • Lateralized ERPs EDAN, ADAN, N2pc and SPCN were found.

Abstract

Social cues, such as another individual׳s eye gaze, provide valuable information regarding the actions and intentions of others. Previous studies have suggested that seeing another׳s gaze automatically orients one׳s attention in the gaze direction. In this event-related potential (ERP) study, a spatial cuing paradigm was combined with a visual search task in which targets were defined by feature conjunctions in order to eliminate effects of target/distractor salience. Participants viewed centrally presented faces with neutral expressions in which eyes looked to the left or right. The participants׳ task was to identify a target object (with or without gap) defined by a combination of shape and orientation, which appeared in either the same (cued) or the opposite (uncued) location as the direction of the eye gaze. There was behavioural evidence of a gaze congruency effect, as reaction times (RTs) were faster when the eyes looked towards the target rather than away from the location of the target. The ERP data indicated the presence of significant gaze-congruent early directing attention negativity (EDAN) and anterior directing attention negativity (ADAN), reflecting attention shifts to the cued location in advance of the target presentation. ERP data did not show evidence of later orienting of attention triggered by gaze cues in the late attention-directing attention positivity (LDAP) at posterior sites. The results disclosed the neural response during reflexive attention shifting triggered by gazes and ascertained the relationship among EDAN, ADAN, LDAP and gaze-elicited attention shifts. After the presentation of the target array without salient stimuli, the presence of the N2-posterior-contralateral (N2pc) in the cued trials and the absence in the uncued trials further supported that attention had been directed to the possible target location prior to the target onset. The ERPs in response to the target array also extend our understanding of the neural response that orients spatial attention by providing valuable information about the temporal dynamics without the influence of salience.

Introduction

Selective attention is considered to be a central component of cognitive functioning. Research has been extensively conducted on attention shifts triggered by various visual stimuli, such as eye gazes, arrows, gestures, colour cues, numerical cues and peripheral squares (Brignani et al., 2009, Kasten and Navon, 2008, Sato et al., 2009, Ranzini et al., 2009). Reaction time (RT) is commonly used in the studies, and results indicate that people respond faster to targets in a cued location than other locationsthis is the cuing effect (Driver et al., 1999, Farroni et al., 2003, Friesen and Kingstone, 1998, Friesen et al., 2004, Hietanen and Leppänen, 2003, Hood et al., 1998, Langton and Bruce, 1999, Feng et al., 2011, Friesen et al., 2005). Some studies focus on the ERP activities evoked by the targets and demonstrate that the early visual P1 and N1 components are enhanced for targets at the cued location (Schuller and Rossion, 2001, Schuller and Rossion, 2004, Schuller and Rossion, 2005, Hietanen et al., 2008, Brignani et al., 2009, Feng et al., 2011).

Reflexive deployments of covert attention have been studied extensively using uninformative spatial cuing paradigms. Several studies have concerned the brain activities after the cue presentation and before the target onset. If attention is shifted before the target presentation, there are related neural processes during the cue–target interval. The previous studies using a symbolic cuing task demonstrated that centrally presented symbolic cues elicited the early directing attention negativity (EDAN) at posterior electrodes between approximately 200 and 400 ms post-cue and the anterior directing attention negativity (ADAN) at frontal and central sites between 300 and 500 ms post-cue and the posterior late attention-directing attention positivity (LDAP) that starts approximately 500 ms post-cue, and these components have been suggested to reflect attention shifts (Harter et al., 1989, Hopf and Mangun, 2000, Hietanen et al., 2008). Some previous symbolic cuing tasks demonstrated LDAP effects during the cue–target interval (Harter et al., 1989, Hopf and Mangun, 2000) whereas some have not (Talsma et al., 2005, Yamaguchi et al., 1994, Nobre et al., 2000). The absence of an LDAP in these studies was considered most likely due to the use of short cue–stimulus intervals (stimulus onset asynchrony (SOA) between the cue and target was not more than 800 ms) (Talsma et al., 2005, Hietanen et al., 2008).

Eye gaze represents a special stimulus with a great social and biological relevance. The ability to discriminate gaze direction, already evident early in life, is essential for the development of more complex socially relevant tasks, such as joint and shared attention (Rigato and Farroni, 2013). The ERP studies with gaze cues have also produced mixed results. A previous ERP study using non-predictive arrows or simple pictures of gazes as cues found the presence of EDAN effects with arrows but not with eye-gaze cues (Hietanen et al., 2008). In contrast, a later study using uninformative gaze cues and an SOA of 800 ms found EDAN and ADAN effects but no LDAP (Li et al., 2010). There are no consistent findings concerning the ERPs during attention shifts triggered by gaze. In the present study, human faces with averted eyes were used as the cue to further examine the lateralised ERP activities relating to attention shifting evoked by eye gaze. The SOA in this study was 1000 ms, which was selected based on previous studies (Hopf and Mangun, 2000, Harter et al., 1989).

Besides investigating the effect of eye gaze on EDAN, ADAN, and LDAP in the time window between eye gaze and target onset, the present study investigated the N2pc (N2-posterior-contralateral – see Luck and Hillyard, 1994, Woodman and Luck, 1999) elicited by the onset of the target. After the presentation of targets, we focused on the N2pc, a recent ERP index of attention shifts over space (Woodman et al., 2009, Eimer and Kiss, 2008, Eimer and Kiss, 2010, Eimer et al., 2009, Hickey et al., 2006, Galfano et al., 2011). The N2pc is a lateralised ERP component, which typically starts approximately 180 ms post-target onset and lasts approximately 100 ms and is maximal at the posterior electrode sites contralateral to an attended item (Luck et al., 1994). The N2pc is believed to reflect visual–spatial attention mechanisms that separate relevant and irrelevant perceptual information in bilateral, multi-element search arrays. The present study concerned the lateralised ERP component, N2pc, and thus a single, lateralised target object was not suitable. This study combined the spatial cuing paradigm with visual search task. Furthermore, previous studies used bilateral, single targets (Driver et al., 1999, Farroni et al., 2003, Friesen and Kingstone, 1998, Friesen et al., 2004, Friesen et al., 2005, Hietanen and Leppänen, 2003, Hood et al., 1998, Langton and Bruce, 1999, Feng et al., 2011, Galfano et al., 2011) or target arrays containing targets defined by a singleton feature (Kiss et al., 2008) which are pop-out and salient and may automatically and spontaneously capture an observer׳s attention (Yantis and Jonides, 1984, Kiss et al., 2008, Hickey et al., 2010). While in the present study participants were presented a mixed-feature search task, in which the search display contained a less-salient target and distractors defined by feature conjunctions, and thus attention shifts triggered by gaze could be examined without the bottom-up effect of target/distractor salience on attention shifts. In addition, previous studies always used one pair of eyes as the cue stimuli. The present study also aimed to examine whether eye gazes could trigger attention shifts in the context of the other pair of gazes presented, which would be a scenario more similar to real life.

Section snippets

Behavioural performance

Behavioural performance (reaction time, accuracy) was analysed with repeated measures ANOVAs for the factors target side (left vs. right), cue type (face 1, face 2) and cue congruency (cued vs. uncued). Statistical analysis revealed a significant main effect of cue congruency on RT [F(1,14)=13·0, p<0.01, partial η2=0·48]. As expected, shorter RTs were produced in cued (1258·47±338·25 ms) than in uncued trials (1339·47±377·28 ms). No other main effects [F(1,14)=1·09, 3·64, ps>0·05] or interactions

Discussion

Consistent with the results of previous gaze-cuing studies (e.g., Driver et al., 1999, Farroni et al., 2003, Friesen and Kingstone, 1998, Friesen et al., 2004, Friesen et al., 2005, Hietanen and Leppänen, 2003, Hood et al., 1998, Langton and Bruce, 1999, Feng et al., 2011), this study combining gaze-cuing procedures with visual search demonstrated that participants responded faster to the targets that appeared at the cued locations than the uncued locations, i.e., cuing effects were observed

Participants

Fifteen healthy, right-handed students (7 females, age range 18–25 years, mean 22·6 years) took part in the experiment. All had normal or corrected-to-normal visual acuity. The study was approved by the local ethics committee, and informed consent from participants was obtained prior to the beginning of the experiment.

Procedure and stimuli

Fig. 3 illustrates the structure of every experimental trial as well as the arrangement of the stimuli. The experiment was controlled by E-Prime software (E-Prime 1·1, Psychology

Acknowledgments

This research was supported by the National Basic Research Programme of China (No. 2011CB711001) and National Natural Science Foundation of China (No. 31271083) to Xuemin Zhang.

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