Investigating hemispheric lateralization of reflexive attention to gaze and arrow cues
Highlights
► Hemispheric differences in attentional orienting by eye-gaze cues. ► Right hemispheric dominance in reflexive attentional orienting triggered by eyegaze cues. ► The mechanisms triggering attentional orienting after arrows and gaze cues are differently lateralized in the brain.
Introduction
Several studies have provided evidence supporting the notion that gaze acts as a special attention cue that reflexively triggers attentional shifts (e.g., Driver et al., 1999, Friesen et al., 2004; for a review, see Frischen, Bayliss, & Tipper, 2007). These studies applied a spatial cueing paradigm, first introduced by Posner (1980) and reviewed by Friesen and Kingstone (1998). In this paradigm, a drawing/photograph of a face looking to the left or right is presented in the center of the screen. The participant is required to respond to a target that might appear either at the looked-at (valid) or at the opposite location (invalid). Quicker reaction times for validly cued targets are thought to indicate an allocation of attention to the looked-at location (i.e. gaze cueing effect). This effect occurs even when the gaze direction is not predictive of the subsequent target location and the time interval between the presentation of the cue and the target is short (around 100 ms; Friesen and Kingstone, 2003, Langton and Bruce, 1999, Ristic et al., 2002) and even when participants are told to expect targets at the opposite location (see, e.g., Driver et al., 1999). These behavioral evidences have been taken as evidences of reflexive orienting to gaze direction. Contrary to the notion that gaze is a special attentional cue, many studies have provided behavioral evidence for similar shifts of attention when arrows instead of eye-gaze are used as cues (Hommel et al., 2001, Ristic et al., 2002, Tipples, 2002, Tipples, 2008). For example, participants are quicker to respond to targets appearing congruently to the arrow direction (arrow cueing effect) even when it is not predictive of the subsequent target location and the target appears very quickly after the cue onset (around 100 ms; Bayliss et al., 2005, Tipples, 2002).
An initial comparison between gaze and arrow cues has shown that eye-gaze cues are more resistant to voluntary control (Friesen et al., 2004). In particular, Friesen et al. (2004) used a so-called counter-predictive cueing paradigm (the target was more likely to appear in the location opposite the one indicated by the cue) and showed that attention shifts to the cued locations were only observed when eye-gaze were used as cues. In contrast, when counter-predictive cueing was tested with arrows, participants’ attention did not shift to the cued locations. However, in a more recent study using the same counterpredictive paradigm as that of Friesen et al., 2004, Tipples, 2008 found that both eye and arrow cues produce similar reflexive shifts of attention, while Guzzon, Brignani, Miniussi, and Marzi (2010; Experiment 1) observed an early top-down control of attention (from 100 ms) with both central cues.
Although many studies have not shown robust behavioral differences between gaze and arrow cues, it is possible that the underlying neural architecture are differently engaged. However, again, electrophysiological and neuroimaging studies have generally yielded mixed results concerning brain activity dissociations between gaze and arrow cueing conditions. While some studies reported similar activation for social and nonsocial cues in frontoparietal regions (Brignani et al., 2009, Greene et al., 2009, Sato et al., 2009, Tipper et al., 2008), other studies found a different cortical activation during social cueing compared to nonsocial cueing, including greater activity in bilateral extrastriate cortices (Engell et al., 2010, Greene et al., 2009, Hietanen et al., 2006, Tipper et al., 2008) right ventral regions (Tipper et al., 2008) as well as in the right STS (Kingstone, Tipper, Ristic, & Ngan, 2004).
In addition, some neuropsychological studies have suggested that there are distinct neural systems for gaze and arrow cueing (Akiyama et al., 2006, Kingstone et al., 2000, Ristic et al., 2002).1 For instance, a study with split-brain patients has shown that the reflexive gaze-cueing effect is lateralized to the right hemisphere, which is specialized for face processing (Kingstone et al., 2000). This laterality effect was not found in a later study using non-predictive arrows cues, in which the same split-brain patient showed no lateralization of reflexive orienting, with the cueing effect occurring in both hemispheres (Ristic et al., 2002). Furthermore, Akiyama and colleagues (2006) found that a patient with focal lesion in her right superior temporal gyrus showed no gaze-cueing effect, but preserved orienting to non-predictive arrow cues.
Taken together, these neuropsychological findings are consistent with the idea that reflexive orienting to arrow cues is subserved by brain mechanisms that are shared between the two hemispheres, whereas reflexive orienting to gaze cues is subserved by lateralized brain mechanisms involved in face/gaze processing (e.g., Friesen and Kingstone, 2003, Kingstone et al., 2004). However, in light of natural variations in the gaze-cueing effect across individuals and the unavailability of prelesional data, these findings must be interpreted with some caution and can hardly be extended to the general population.
To our knowledge, only one behavioral experiment has directly compared the hemispheric lateralization of gaze and arrow cueing effects in normal adults (Greene & Zaidel, 2011). In particular, the authors found a right hemisphere bias for attentional orienting induced by gaze cue, but not for attentional orienting induced by nonsocial stimuli (arrow cues and peripheral cues). However, in our opinion in this study the lateralization of the attentional orienting was manipulated in a way that made difficult the interpretation of the results. First, gaze and arrow cues were presented in the right or left Visual Hemifield (VHF), and the target-stimuli were presented in the upper or lower hemispace of the same VHF. For this reason, cues were 100% informative with regard to the VHF location of the stimulus target, although they were uninformative about the top–bottom location of the target within the same VHF. As underlined by the authors themselves, this experimental choice could have induced a mix of automatic (uninformative regard to up-down location of the stimulus) and controlled (informative regard the VHF) orienting. Furthermore, such lateralized presentation of the cue stimuli (gaze and arrow) makes it potentially difficult to disambiguate the effects of the processing of the lateralized cue stimuli from the effects of the attentional orienting induced by those stimuli. For example, Birmingham and Kingstone (2009) argue that the right hemisphere is more activated by biologically relevant face and gaze stimuli than it is by biologically irrelevant arrow stimuli. By presenting the cue stimuli centrally, the effects of possible hemispheric differences in processing those stimuli can be eliminated.
Therefore, in the current study we used a central (instead of a peripheral) presentation of cue stimuli (gaze an arrow) in an attempt to investigate the hemispheric lateralization of the attentional shifts induced by arrow and gaze cues, rather than the processing of the cues themselves. Following the neuropsychology data indicating that orienting to gaze cues is subserved by right lateralized brain mechanisms involved in face/gaze processing (e.g., Friesen and Kingstone, 2003, Kingstone et al., 2004), we hypothesized that gaze cueing effects would occur for targets presented in the left visual field. Such hemispheric lateralization was predicted not to be present when the spatial cue was an arrow as neuropsychological data showed no lateralization of reflexive orienting to arrow cues, with the arrow cueing effect occurring in both hemispheres (Ristic et al., 2002).
Section snippets
Participants
Forty-eight university students (40 females and eight males; mean age 23 ± 2.6 years) signed an informed consent before participating as volunteers in the study. The local ethical committee approved the study. All participants were right-handed, with a hand preference equal or greater than 85%, as assessed by means of a lateral preference questionnaire (Salmaso & Longoni, 1985), had normal or corrected-to-normal vision, and were unaware of the purpose of the experiment.
Apparatus
Stimuli were presented on a
Results
Mean response times, standard deviations and error rates are shown in Table 1. RTs faster than 200 ms or slower than 1200 ms (1% of the trials), as well as incorrect responses (7% of the trials), were excluded from the RT analysis. The ANOVA showed that the main effect of Validity reached significance (F1,47 = 16.39; p < .001; partial η2 = 0.26), with faster responses for valid than invalid trials (494 ms vs. 504 ms). The effect of VHF was significant (F1,47 = 7.08; p < .01; partial η2 = 0.13), showing faster
Discussion
The comparison between eye-gaze and arrow cueing effects has been used to evaluate the cognitive mechanisms of social attention (for a review, see Birmingham & Kingstone, 2009). Despite the extensive research on the orienting effects induced by gaze and arrow cues, subtle or no behavioral differences have been observed between the two types of cues. Therefore, the usual findings observed in these behavioral studies seem to run counter the intuition that considers eyes as unique, special
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